Color-Flow Doppler Echocardiography and Myocardial Strain Imaging
Number: 0008
Table Of Contents
PolicyApplicable CPT / HCPCS / ICD-10 Codes
Background
References
Policy
Scope of Policy
This Clinical Policy Bulletin addresses color-flow doppler echocardiography and myocardial strain imaging with echocardiography.
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Medical Necessity
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Color-flow Doppler echocardiography
Aetna considers color-flow Doppler echocardiography in adults medically necessary for the following indications:
- During excision of left atrial mass;
- Evaluation of angina;
- Evaluation of aortic diseases;
- Evaluation of aortocoronary bypass grafts;
- Evaluation of atrial fibrillation/flutter;
- Evaluation of cardiac function after the Fontan procedure;
- Evaluation of cardiac tamponade;
- Evaluation of cardiomyopathy (including hypertrophic cardiomyopathy (formerly known as idiopathic hypertrophic subaortic stenosis);
- Evaluation of congestive heart failure;
- Evaluation of dyspnea (shortness of breath);
- Evaluation of heart murmur;
- Evaluation of pericardial effusion;
- Evaluation of prosthetic valves;
- Evaluation of pulmonary hypertension;
- Evaluation of septal defects;
- Evaluation of site of left-to-right or right-to-left shunts;
- Evaluation of valvular diseases (including mitral regurgitation and severity of valve stenosis);
- Monitoring of individuals after repair of tetralogy of Fallot;
- Monitoring of individuals receiving cardiotoxic chemotherapy; or
- Status post an episode of ventricular tachycardia.
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Myocardial strain imaging
Aetna considers myocardial strain imaging medically necessary (unless otherwise stated) in adults when any of the following criteria are met:
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For initial evaluation of left ventricular hypertrophy (LVH), in addition to the primary echocardiogram, when there is documentation of both of the following:
- Unclear etiology; and
- Concern for infiltrative cardiomyopathy; or
- For heart transplant evaluation and surveillance per transplant protocol; or
- In addition to the primary echocardiogram, for individuals receiving therapy with cardiotoxic agents for any of the following:
- Initial evaluation prior to treatment with either medications that could result in cardiotoxicity/heart failure or radiation that could result in cardiotoxicity/heart failure; or
- Re-evaluation of an individual previously or currently undergoing therapy if an echocardiogram shows a new abnormality; or
- Re-evaluation of an individual undergoing therapy every 3 months or with worsening symptoms; or
- Initial post-treatment evaluation 3-12 months after completion of treatment; or
- Periodic surveillance for medium- and high-risk survivors.
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Myocardial strain imaging is considered not medically necessary for evaluating kidney or liver transplant candidacy.
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Experimental, Investigational, or Unproven
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Color-flow Doppler
Aetna considers color-flow Doppler echocardiography in adults experimental, investigational, or unproven for all other indications (e.g., to guide catheter ablation in ventricular tachycardia) because its effectiveness for these indications has not been established.
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Myocardial strain imaging
Aetna considers myocardial strain imaging experimental, investigational, or unproven for all other indications, including the following (not an all-inclusive list), because its effectiveness for these indications has not been established:
- In addition to primary echocardiogram for risk stratification in asymptomatic adults with repaired tetralogy of Fallot,
- In children with an atrial septal defect (ASD),
- To assess risk or directing asymptomatic management strategies in children.
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Related Policies
Background
Color-Flow Doppler Echocardiography
Color-flow Doppler echocardiography is an advanced cardiac ultrasound technique that overlays color-coded blood flow information onto a two-dimensional echocardiographic image, allowing real-time visualization of flow direction and velocity within the heart and great vessels. This method is used for a variety of indications, including during the excision of left atrial masses, evaluation of angina, assessment of aortic diseases, and examination of aortocoronary bypass grafts. It is also used for evaluating atrial fibrillation/flutter, cardiac function following the Fontan procedure, cardiac tamponade, and cardiomyopathy, including hypertrophic cardiomyopathy. Additionally, it is widely used in the evaluation of congestive heart failure, dyspnea (shortness of breath), heart murmurs, pericardial effusion, prosthetic valves, pulmonary hypertension, septal defects, and the sites of left-to-right or right-to-left shunts. Furthermore, color-flow Doppler echocardiography is important for assessing valvular diseases, such as mitral regurgitation and the severity of valve stenosis, as well as for monitoring individuals after the repair of tetralogy of Fallot, those receiving cardiotoxic chemotherapy, and patients status post an episode of ventricular tachycardia.
Echocardiography is usually performed by placing a transducer over the chest. In transesophageal echocardiography, however, the transducer is placed at the tip of an endoscope that is inserted into the esophagus (Beers and Berkow, 1999). Even smaller transducers can be placed on intravascular catheters, permitting intravascular recordings of vessel anatomy and blood flow.
Two-dimensional (or cross-sectional) echocardiography is the dominant echocardiographic technique (Beers and Berkow, 1999; Gottdiener et al, 2004). It uses pulsed, reflected ultrasound to provide spatially correct real time tomographic images of the heart, which are recorded on videotape and resemble cine-angiograms. Two-dimensional (2D) echocardiography provides information about the cardiac chamber size, wall thickness, global and regional systolic function, and valvular and vascular structures. B-mode imaging refers to cross-sectional 2-D images displayed without motion, and provides detail of static structures.
M-mode (or motion-mode) echocardiography creates a continuous 1-D graphic display, and is useful for measuring single dimensions of walls and chambers of the heart, which can be used to estimate chamber volumes and left ventricular mass (Beers and Berkow, 1999; Gottdiener et al, 2004). M-mode echocardiography is performed by directing a stationary pulsed ultrasound beam at some portion of the heart.
The Doppler technique uses reflections from moving red blood cells to characterize blood flow (Beers and Berkow, 1999; Gottdiener et al, 2004). Spectral Doppler echocardiography uses ultrasound to record the velocity, direction, and type of blood flow in the cardiovascular system. The spectral Doppler signal is displayed on a strip chart recorder or videotape.
Stress echocardiography uses any combination of the above echocardiography modalities, before and during (or shortly after) a physical or pharmacological stress intervention (Beers and Berkow, 1999; Gottdiener et al, 2004). Most commonly, a treadmill or exercise bicycle is used for stress echocardiography. In patients who are unable to exercise, stress testing can be performed with pharmacological agents, such as dobutamine, that increased myocardial oxygen demand, or vasodilators that produce coronary steal. These tests have utility primarily in the detection of myocardial ischemia and viability.
Contrast echocardiography is an M-mode or 2-D echocardiographic examination during which contrast agents are administered via venous injection (Beers and Berkow, 1999; Gottdiener et al, 2004). Venous contrast injections are used to enhance left ventricular endocardial borders and Doppler signals and to assess myocardial perfusion.
Color Doppler echocardiography is essentially 2-D Doppler echocardiography with flow encoded in color to show its direction (red is toward and blue is away from the transducer) (Beers and Berkow, 1999; Gottdiener et al, 2004). In color flow mapping, blood flow velocity is measured along each sector line of a 2-D echocardiographic image and is displayed as color coded pixels. Color flow Doppler is most useful for assessing valves for regurgitation and stenosis, detecting the presence of intracardiac shunts, and imaging blood flow in the heart.
Evidence-based guidelines from the American College of Cardiology, American Heart Association, and American Society of Echocardiography (Antman et al, 2003) outlined the accepted capabilities for Doppler echocardiography in the adult patient. Specific indications were classified as relating to "anatomy-pathology" or to "function", and each potential indication was rated from "most helpful" to "not useful."
Among indications related to anatomy-pathology, color Doppler was rated as most helpful for evaluating septal defects (Antman et al, 2003). Color Doppler was considered not useful for all other indications related to anatomy-pathology: evaluation of chamber size, thickness of walls, relation of chambers, early closure of mitral valve, systolic anterior motion of mitral valve, left ventricular mass, left ventricular masses (tumor, clot, vegetation), masses in atria and right ventricle, anatomic valvular pathology, and pericardial effusion.
Among functional indications, color Doppler was considered most useful for evaluating the site of right-to-left and left-to-right shunts (Antman et al, 2003). Color Doppler was also considered useful for evaluating severity of valve stenosis and valve regurgitation and evaluation of prosthetic valves. Color Doppler was also considered to be of some use in evaluating aortic diseases. Color Doppler was considered not useful for assessment of global left ventricular systolic function (ejection fraction), evaluation of regional wall motion, measurement of right ventricular and pulmonary artery systolic pressures, measurement of left ventricular filling pressure, measurement of stroke volume and cardiac output, assessment of left ventricular diastolic function, and identifying ischemia and viable myocardium with exercise or pharmacological stress.
Nishimura et al (2011) examined the significance of measurement of stenosis by aliasing coronary flow (the MOSAIC method) for the detection of proximal left coronary stenosis in patients with unstable angina (UA) by means of transthoracic Doppler echocardiography. Patients (n = 107) with UA were evaluated. Proximal left coronary flow was sought in the short axis at the aortic root level using color Doppler guidance. When detected coronary flow showed color aliasing, the color velocity range was gradually increased until color aliasing nearly disappeared. Then, the color baseline was shifted until the color flow showed "isovelocity". Proximal coronary flow was detected in 86 (80.4 %) of 107 patients. In these 86 patients, an optimal cut-off value of isovelocity greater than or equal to 47.5 cm/second predicted significant coronary stenosis (percent diameter stenosis greater than or equal to 70 %) of the proximal left anterior descending (American Heart Association segment 6) or left main coronary artery with a sensitivity of 88 %, specificity of 97 %, positive predictive value of 98 %, and negative predictive value of 86 %. In all 107 patients, the same cut-off value predicted significant coronary stenosis with a sensitivity of 78 %, specificity of 98 %, positive predictive value of 98 %, and negative predictive value of 81 %. The authors concluded that the MOSAIC method may play a complementary role in expeditious risk stratification and decision making in patients with UA.
The American College of Radiology's Expert Panel on Cardiovascular Imaging (Ho et al, 2011) states that echocardiography using color flow Doppler is essential for evaluating blood flow as seen across an atrial defect or a ventricular septal defect or across a valve. Assessment of the valves (sclerosis, fusion, estimation of valve gradients) and determination of right ventricular systolic pressure can usually be achieved.
An UpToDate review on "Catheter ablation for ventricular arrhythmias" (Ganz, 2012) states that "[i]ntracardiac echocardiography (ICE) with 2D and Doppler color flow imaging may be useful to guide mapping and ablation catheters and monitor morphologic changes after ablation". The reference cited was the study by Ren et al (2002) that comprised only 4 patients with ventricular tachycardia. Thus, there is currently insufficient evidence to support the use of color-flow Doppler echocardiography during ventricular tachycardia ablation.
An UpToDate review on “Principles of Doppler echocardiography” (Manning, 2013) states that “Color flow imaging is typically used in the screening and assessment of regurgitant flows. It is also useful in the assessment of intracardiac shunts (e.g., atrial and ventricular septal defects) and pulmonary vein flow, and to assist in continuous wave Doppler alignment for tricuspid regurgitation velocities”.
Echocardiography for Evaluation of Pericardial Effusion and Cardiac Tamponade
Miranda and Oh (2017) stated that effusive-constrictive pericarditis (ECP) corresponds to the coexistence of a hemodynamically significant pericardial effusion and decreased pericardial compliance. The hallmark of ECP is the persistence of elevated right atrial pressure post-pericardiocentesis. The prevalence of ECP appeared higher in tuberculous pericarditis and lower in idiopathic cases. The diagnosis of ECP is traditionally based on invasive hemodynamics but the presence of echocardiographic features of constrictive pericarditis post-peri-cardiocentesisis can also identify ECP. Data on the prognosis and optimal treatment of ECP are still limited. Anti-inflammatory agents should be the 1st-line of treatment. Pericardiectomy should be reserved for refractory cases.
Chalikias et al (2017) examined the prognostic value of echocardiographic tissue imaging markers in predicting tamponade among patients with large malignant pericardial effusion compared to routinely used echocardiographic signs. A total of 96 consecutive patients with large malignant pericardial effusion, not in clinical cardiac tamponade, underwent an echocardiographic examination and were prospectively assessed for 1 month. Clinically evident cardiac tamponade was considered as the study end-point. The prognostic performance of tricuspid valve annular plane systolic excursion (TAPSE) and peak systolic annular velocity at the lateral margin of the tricuspid valve annulus (STV ) was assessed and compared to routinely used imaging signs. During follow-up, 37 patients (39 %) developed clinically evident cardiac tamponade. TAPSE (area under the curve [AUC] 0.958) and STV (AUC 0.948) had excellent predictive accuracy for tamponade. Multi-variate analysis showed that TAPSE (hazard ratio [HR] 3.03; 95 % confidence interval [CI]: 1.60 to 5.73, p = 0.001) and STV (HR 1.17; 95 % C: 1.05 to 1.29, p = 0.005) remained independent significant predictors of cardiac tamponade. Re-classification analysis and decision curve analysis showed additive prognostic value and adjunct clinical benefit of these markers when added to a recently published triage pericardiocentesis score. The authors concluded that echocardiographic tissue imaging markers such as TAPSE and STV are characterized by an excellent prognostic ability for development of cardiac tamponade and better prognostic value compared to routine echocardiographic signs in patients with large malignant pericardial effusion. Incorporating these markers to a recent triage pericardiocentesis score resulted in additional prognostic value and increased clinical benefit.
Honasoge and Dubbs (2018) noted that one of the most common causes of pericardial effusion in the Western world is malignancy. Emergency physicians must maintain vigilance in suspecting pericardial effusion and tamponade in patients with known or suspected malignancy who present with tachycardia, dyspnea, and hypotension. Diagnosis can be expedited by key physical examination, electrocardiogram, and sonographic findings. Unstable or crashing patients with tamponade must undergo emergent pericardiocentesis for removal of fluid and pressure to restore cardiac output.
Miranda et al (2019) reviewed 2D and Doppler findings in patients diagnosed with ECP and compared these to patients with cardiac tamponade and patients with surgically-proven constrictive pericarditis (CP). These researchers identified 22 patients diagnosed with ECP at Mayo Clinic, MN between 2002 and 2016 who had persistent elevation of jugular venous pressure post-pericardiocentesis. They compared them to 30 patients with CP and 30 patients with cardiac tamponade who had normalization of venous pressure post-pericardiocentesis. All patients were in sinus rhythm. Mean age was 57 ± 18 years in the ECP group; 36 % were women. Most ECP and cardiac tamponade cases were idiopathic (41 % and 33 %, respectively). Prior to pericardiocentesis, medial and lateral e' velocities were higher in ECP compared with tamponade; both ECP and tamponade patients had markedly decreased hepatic vein diastolic forward flow velocities. Inspiratory and expiratory mitral E/A ratios were higher in ECP compared with tamponade, but lower than those observed in CP. Post-pericardiocentesis, hepatic vein diastolic forward flow velocities increased in both ECP and tamponade. Hepatic vein diastolic reversal velocities decreased in tamponade but were unchanged in ECP. During median follow-up of 481 days, 3 patients required pericardiectomy for CP; they were all in the ECP group (14 % of ECP cases). The authors concluded that ECP may have unique echo-Doppler features that distinguish it from both CP and tamponade. These researchers stated that these findings suggested that ECP could be diagnosed by echocardiography even prior to pericardiocentesis; ECP appeared to have a good prognosis, particularly in patients presenting acutely.
An UpToDate review on “Cardiac tamponade” (Hoit, 2020) states that “Echocardiography -- Although cardiac tamponade is a clinical diagnosis, two-dimensional and Doppler echocardiography play major roles in the identification of pericardial effusion and in assessing its hemodynamic significance. The use of echocardiography for the evaluation of all patients with suspected pericardial disease was highly recommended by a 2003 task force of the American College of Cardiology (ACC), the American Heart Association (AHA), and the American Society of Echocardiography (ASE). The 2015 European Society of Cardiology (ESC) Guidelines recommend echocardiography as the initial imaging technique to assess the hemodynamic impact of a pericardial effusion and a judicious clinical evaluation that includes echocardiographic findings to guide the timing of pericardiocentesis. In patients who do not have cardiac tamponade on initial assessment, but in whom the suspicion is high, repeat echocardiography during clinical follow-up may be appropriate to detect early signs of developing cardiac tamponade in the presence of large or rapidly accumulating effusions … Following either percutaneous or surgical drainage of a pericardial effusion in a patient with cardiac tamponade, the patient should be monitored with continuous telemetry and frequent vital signs for at least 24 to 48 hours. Subsequent monitoring with two-dimensional and Doppler echocardiography prior to discharge from the hospital is warranted to confirm adequate fluid removal and to detect possible recurrent fluid accumulation”.
Echocardiography During Excision of Left Atrial Mass
Smith et al (1991) described the case of an asymptomatic patient who was discovered to have a large right atrial myxoma by transthoracic echocardiography. Pre-operative considerations included the possibility of satellite lesions, left atrial origin, and a question of tricuspid valve involvement. Subsequent operative transesophageal echocardiography demonstrated single-stalk attachment in the right atrial septal wall and no satellite lesions. Doppler and color flow examination immediately following tumor removal aided in the decision not to perform tricuspid annuloplasty as there was no significant tricuspid regurgitation. The authors concluded that the combined use of transthoracic and transesophageal echocardiography with Doppler and color flow imaging aids in the pre-operative and intra-operative diagnosis and surgical management of right atrial tumors.
Tekin et al (2019) stated that the treatment of atrial-extension Wilms’ tumor thrombus is surgical excision after chemotherapy. Atriotomy with cardiovascular by-pass is the one of the most common method for this procedure. These investigators presented a case of Wilms’ tumor with a tumor thrombus extending into the right atrium totally excised with retro-hepatic cavatomy. A 3.5 year-old girl was admitted with the symptom of dysuria. The examinations revealed a mass consistent with Wilms’ tumor in the middle and lower poles of the left kidney. Doppler ultrasound (US) and echocardiographic examinations showed a tumor thrombus extending into the right atrium and some pulmonary nodules which were interpreted to be metastasis. Wilms’ tumor was histopathologically diagnosed by an open biopsy. After 3 courses of chemotherapy, imaging studies revealed that the atrial extension of the tumor thrombus persisted. The tumor thrombus was found to be fibrotic on the magnetic resonance imaging (MRI) scan of the patient; thus, nephron-ureterectomy along with the excision of the tumor thrombus from the inferior vena cava was carried out with intra-operative continuous trans-esophageal echocardiography (TEE). The suprarenal and retro-hepatic vena cava were exposed by dissecting and ligating all short hepatic veins and completely mobilizing the right lobe of the liver. The thrombus was dissected out via vertical cavatomy at the retro-hepatic level. TEE confirmed complete removal of the thrombus from the atrium; vena cava was then repaired. There was no need for a blood transfusion, or cardiovascular by-pass (CBP) during the operation. Total exposure of the retro-hepatic and sub-diaphragmatic vena cava using transplantation techniques was an effective method for the excision of a tumor thrombus without sternotomy, atriotomy and CBP, avoiding possible intra- and post-operative complications in selected cases of Wilms’ tumor with intra-atrial thrombus extension. The case emphasized the importance of multi-disciplinary communication and collaboration.
Furthermore, an UpToDate review on “Echocardiographic evaluation of the atria and appendages” (Forster, 2021) states that “Although the left atrium and even the left atrial appendage can be imaged with transthoracic echocardiography, transesophageal echocardiography (TEE) permits detailed examination of most of the left atrium, including excellent views of the left atrial appendage. TEE is the preferred approach for the detection of thrombi in the left atrium and appendage, given it is far more sensitive than transthoracic echocardiograph”.
Echocardiography for Evaluation of Cardiac Function After the Fontan Procedure
Vitarelli et al (2005) noted that there is evidence that "inappropriate hypertrophy" of the single left ventricle, which occurs as a result of acute preload reduction, leads to adverse consequences on ventricular function. However, a systematic study of the capability of tissue Doppler imaging (TDI) to examine systolic and diastolic ventricular functions after the Fontan procedure is still missing. In a prospective study, a total of 24 post-operative patients aged 12 to 33 years were assessed with two-dimensional (2D) echocardiography equipped with TDI capabilities; 19 age-matched normal subjects were selected as controls. Good-quality echoes for the measurement of ejection fractions (EFs) were available in 21 patients; 10 patients (group 1) had systolic dysfunction (EF less than 50 %), and 11 patients (group 2) had normal systolic function. Peak systolic and diastolic wall velocities were acquired from the 2-chamber view in the myocardia and mitral annulus. Compared with controls, the Fontan patients had a significantly reduced peak systolic velocity at wall and annulus sites. A linear correlation existed between EF and systolic myocardial velocity from the annular sites. Group 1 patients had lower wall velocities and lower annulus velocities both in systole and diastole. Group 2 patients had preserved systolic velocities but decreased regional and annular early diastolic velocities, suggesting impaired filling. Multiple correlation analysis showed a relation between peak early diastolic mitral velocity and ventricular EF, mean mitral annular motion at systole, mass/volume ratio, and the number of years post-Fontan revision. The authors concluded that myocardial velocities recorded after the Fontan operation provided insight into systolic and diastolic ventricular functions. The peak systolic mitral annular velocity correlated well with the ventricular EF. The peak early diastolic velocity and the ratio between the early and late diastolic mitral annular velocity were reduced and reflected diastolic dysfunction even in the presence of normal systolic EF.
Stines et al (2011) stated that atrial function is increasingly being recognized as a significant factor in overall cardiac function in adults. Limited studies evaluating atrial properties exist in the pediatric congenital heart disease population. These researchers examined atrial properties in patients with single ventricle physiology after Fontan completion and compared these values with normal control patients. Echocardiography was carried out in patients with single ventricular physiology and in control patients; tissue Doppler and blood flow measurements were obtained. Atrial fraction and atrial electromechanical values were calculated. Differences were assessed with 1-way analysis of variance. Post-hoc comparisons were carried out with Tukey adjustment; p < 0.05 was considered significant. No significant difference was present in age or heart rate between single ventricle and control patients. The single right ventricle tricuspid valve A wave (52.6 ± 14.5 versus 36.7 ± 10.4 cm/s) and atrial fraction (39.2 ± 6.2 versus 32.7 ± 7.7%) were significantly higher, and the E/A ratio (1.4 + 0.3 versus 1.8 + 0.4), tricuspid valve E/A velocity-time integral (1.6 + 0.4 versus 2.2 + 0.7 cm), and late diastolic annular value (5.3 + 1.5 versus 8.7 + 1.4 cm/s) were significantly lower compared with the controls. The single left ventricle late diastolic annular velocity (4.2 + 1.0 versus 6.7 + 1.3 cm/s) was significantly lower and atrial fraction was significantly higher compared with the controls (37.7 ± 12.5 % versus 29.8 ± 4.3 %). There were no significant differences in atrial electromechanical measurements between groups; however, the single right ventricle patients tended to have increased atrial dyssynchrony compared with controls. The authors concluded that patients with single ventricle physiology after Fontan completion had differences in atrial properties when compared with normal controls. These researchers stated that these differences may have important implications in their long-term outcomes; further studies are needed to determine the clinical significance of these findings.
Rios et al (2017) noted that quantitative echocardiographic measurements of single ventricular (SV) function have not been incorporated into routine clinical practice. These investigators instituted a clinical protocol, which included quantitative measurements of SV deformation (global circumferential and longitudinal strain and strain rate), standard deviation of time to peak systolic strain, myocardial performance index (MPI), dP/dT from an atrioventricular valve regurgitant jet, and superior mesenteric artery resistance index, for all patients with a history of Fontan procedure undergoing echocardiography. All measures were performed real time during clinically indicated studies and were included in clinical reports. A total of 100 consecutive patients (mean age of 11.95 ± 6.8 years, range of 17 months to 31.3 years) completed the protocol between September 1, 2014 to April 29, 2015. Deformation measures were completed in 100 % of the studies, MPI in 93 %, dP/dT in 55 %, and superior mesenteric artery Doppler in 82 %. The studies were reviewed to evaluate for efficiency in completing the protocol. The average time for image acquisition was 27.4 ± 8.8 mins (range of 10 to 62 mins). The average time to perform deformation measures was 10.8 ± 5.5 mins (range of 5 to 35 mins) and time from beginning of imaging to report completion was 53.4 ± 13.7 mins (range of 27 to 107 mins). There was excellent inter-observer reliability when deformation indices were blindly repeated. Patients with a single left ventricle had significantly higher circumferential strain and strain rate, longitudinal strain and strain rate, and dP/dT compared to a single right ventricle. There were no differences in quantitative indices of ventricular function between patients of less than 10 years versus of greater than 10 years post-Fontan. The authors concluded that advanced quantitative assessment of SV function post-Fontan can be consistently and efficiently performed real time during clinically indicated echocardiography with excellent reliability.
Margossian et al (2016) noted that patients with functional single ventricles after the Fontan procedure have abnormal cardiac mechanics. These researchers determined factors that influence diastolic function and described associations of diastolic function with current clinical status. Echocardiograms were obtained as part of the Pediatric Heart Network Fontan Cross-Sectional Study. Diastolic function grade (DFG) was assessed as normal (grade 0), impaired relaxation (grade 1), pseudonymization (grade 2), or restrictive (grade 3). Studies were also classified dichotomously (restrictive pattern present or absent). Relationships between DFG and pre-Fontan variables (e.g., ventricular morphology, age at Fontan, history of volume-unloading surgery) and current status (e.g., systolic function, valvar regurgitation, exercise performance) were examined. DFG was calculable in 326 of 546 subjects (60 %) (mean age of 11.7 ± 3.3 years). Overall, 32 % of patients had grade 0, 9 % grade 1, 37 % grade 2, and 22 % grade 3 diastolic function. Although there was no association between ventricular morphology and DFG, there was an association between ventricular morphology and E', which was lowest in those with right ventricular morphology (p < 0.001); this association remained significant when using Z scores adjusted for age (p < 0.001). DFG was associated with achieving maximal effort on exercise testing (p = 0.004); the majority (64 %) of those not achieving maximal effort had DFG 2 or 3. No additional significant associations of DFG with laboratory or clinical measures were identified. The authors concluded that assessment of diastolic function by current algorithms resulted in a high percentage of patients with abnormal DFG; however, few clinically or statistically significant associations were found. This may imply a lack of impact of abnormal diastolic function on clinical outcomes in this cohort, or it may indicate that the methodology may not be applicable to pediatric patients with functional single ventricles.
Michel et al (2016) stated that accurate assessment of ventricular function is particularly important in children with hypoplastic left heart syndrome (HLHS) after completion of the total cavo-pulmonary connection (TCPC). For this purpose, 2D speckle tracking (2DST) is a promising technique as it does not depend on the angle of insonation or the geometry of the ventricle. These researchers examined changes in systolic and diastolic right ventricular (RV) function within a 5-year follow-up period of HLHS patients after Fontan palliation using conventional and 2DST echocardiography. RV fractional area change (RVFAC), tricuspid annular plane systolic excursion (TAPSE), E/A, E/e' and 2DST parameters [global longitudinal peak systolic strain (GS) and strain rate (GSRs), global strain rate in early (GSRe) and late (GSRa) diastole] of 40 HLHS patients were compared at 1.6 and at 5.1 years after TCPC. RVFAC, E/A, E/e' and GS did not change, whereas TAPSE (13.7 ± 3.2 versus 10.5 ± 2.4 mm/m(2), p < 0.001), GSRs (-1.56 ± 0.28 versus -1.35 ± 0.31 1/s, p < 0.001), GSRe (2.22 ± 0.49 versus 1.96 ± 0.44 1/s, p = 0.004) and GSRa (1.19 ± 0.39 versus 0.92 ± 0.39 1/s, p < 0.001) decreased significantly. Systolic and diastolic RV function parameters of HLHS patients decreased from 1.6 to 5.1 years after TCPC in these patients. The authors concluded that changes in global strain rate parameters may be signaling early RV dysfunction that is not detectable by traditional echocardiography; further study is needed to verify this and to examine if these changes are clinically relevant.
Furthermore, an UpToDate review on “Overview of the management and prognosis of patients with Fontan circulation” (Johnson and Connolly, 2021) states that “Echocardiography may identify systemic ventricular dysfunction. This is typically assessed using a combination of qualitative and quantitative measures. Changes in ventricular function should prompt consideration for further evaluation (e.g., catheterization or advanced imaging) and addition of heart failure therapies. Atrioventricular and semilunar valve disease are also assessed routinely by TTE, and the presence of severe valve disease may prompt further intervention. Intracardiac thrombus is sought routinely, especially those with arrhythmias and/or atrio-pulmonary Fontan procedure with associated right atrial dilation. Aortic dilation may be noted in select patient populations following Fontan procedure. Echocardiography with Doppler and other imaging modalities may identify obstruction at any point in the Fontan circuit. If suspected, cardiac catheterization will be required to confirm and determine best treatment options. Since echocardiography and other imaging may miss Fontan obstruction, cardiac catheterization is the diagnostic test of choice when obstruction is suspected”.
Echocardiography for Monitoring of Patients After Repair of Tetralogy of Fallot
An UpToDate review on “Management and outcome of tetralogy of Fallot” (Doyle et al, 2021) states that “Echocardiography is recommended annually until the age of 10 years and every 2 years through adulthood. The focus of echocardiography monitoring is to:
- Detect the presence and size of any residual septal defects
- Determine the severity of pulmonary insufficiency
- Determine if there is persistent RVOT obstruction, and if present, ascertain the severity and the site of obstruction
- Assess RV and left ventricular size, function, and wall motion
- Detect any aortic root dilation and/or aortic valve insufficiency.
Echocardiography for Status Post an Episode of Ventricular Tachycardia
Morgera et al (1985) noted that in order to examine the anatomic substrate of “idiopathic” ventricular tachycardia (VT), a total of 10 patients with chronic recurrent VT and no apparent sign of heart disease underwent an echocardiographic, hemodynamic and histologic study (5 men, 5 women: mean age of 40 +/- 11 years). In the patients with a left bundle branch block morphology of VT (7 cases), 4 showed findings compatible with an arrhythmogenic right ventricular (RV) dysplasia or a RV cardiomyopathy. In the other 3 all examinations were normal with the exception of endomyocardial biopsy, which showed slight non-specific changes in 2. Of the remaining 3 cases (characterized by a right bundle branch block morphology of VT or by the presence of polymorphic VT, 1 had histologic evidence of myocarditis while another developed dilated cardiomyopathy. Macroscopic and/or microscopic ventricular abnormalities were frequently found in patients with VT that appeared idiopathic. In these cases, myocardial disease was frequently progressive, despite optimal control of VT.
Mehta et al (1989) examined the RV by multiple biopsies and detailed echocardiographic evaluation, including measurement of cavity dimensions at the level of the inflow, body and outflow tract, in 27 patients with RV tachycardia who had no clinical evidence of an underlying morphologic abnormality; 9 (33 %) patients had abnormal biopsy results, with a quantifiable increase in interstitial fibrosis. Abnormal echocardiograms, defined as an increase in greater than or equal to 2 dimensions of the RV cavity or wall motion abnormalities or both, were observed in 9 patients. There was a strong association between abnormal myocardial histology and abnormal RV echocardiograms (p < 0.001). An abnormal echocardiogram was 94 % specific and 80 % sensitive for an abnormal biopsy. The findings of echocardiography and biopsy were correlated with the electrocardiographic features of the tachycardia. Evidence of RV disease was observed in all 6 patients with superior frontal plane axis of clinical tachycardia as compared with 4 of 21 with inferior axis (p < 0.001); thus, 2-dimensional (2D) echocardiography is a sensitive means of diagnosing RV disease in patients with non-ischemic tachycardias of left bundle branch block morphology. The authors concluded that a superior frontal plane axis of ventricular tachycardia in this group strongly suggested RV disease, whereas an inferior frontal plane axis was frequently not associated with any morphologic or histologic abnormality of the RV.
The American College of Cardiology/American Heart Association’s guidelines on “The clinical application of echocardiography” (Cheitlin et al, 1997) stated that “In the setting of arrhythmias, the utility of echocardiography lies primarily in the identification of associated heart disease, the knowledge of which will influence treatment of the arrhythmia or provide prognostic information. In this regard, echocardiographic examination is frequently performed to assess patients with atrial fibrillation or flutter, reentrant tachycardias, ventricular tachycardia, or ventricular fibrillation. Echocardiography detects an underlying cardiac disorder in approximately 10 % of patients with atrial fibrillation who have no other clinically suspected cardiac disease and in 60 % of those with equivocal indicators of other heart disease. Ventricular arrhythmias of RV origin should alert the physician to a diagnosis of RV abnormalities, including RV dysplasia, while ventricular tachycardias of LV origin are frequently associated with reduced LV function”. Adult patients with congenital heart disease (CHD) are seen by the cardiologist because they develop arrhythmias (including ventricular tachycardia, atrial flutter, or atrial fibrillation) that may result in syncope or sudden death; 2D Doppler echocardiography is employed in the adult patient with CHD.
Myocardial Strain Imaging
Myocardial strain imaging is an advanced echocardiographic technique that evaluates deformation (strain) of the myocardium rather than just its motion, providing a more sensitive measure of cardiac function. It quantifies how much the myocardial fibers shorten, lengthen, or thicken during the cardiac cycle, expressed as a percentage change from their original length. The most commonly assessed parameter is global longitudinal strain (GLS), which reflects longitudinal fiber shortening and is particularly useful for detecting subclinical left ventricular dysfunction before changes in ejection fraction occur. Strain imaging is typically performed using speckle-tracking echocardiography, which tracks natural acoustic markers within the myocardium on 2D images. Clinically, it is valuable in monitoring cardiotoxicity from chemotherapy and in assessing cardiomyopathies.
Myocardial Strain Imaging and Echocardiography for Monitoring of Patients Receiving Cardiotoxic Chemotherapy
Chemotherapy drugs that can cause irreversible toxicity include anthracyclines (daunorubicin, doxorubicin, epirubicin, idarubicin); alkylating agents (busulfan, carboplatin, carmustine, chlormethine, cisplatin, cyclophosphamide, mitomycin); taxanes (docetaxel, cabazitaxel, paclitaxel); topoisomerase inhibitors (etoposide, tretinoin, vinca alkaloids); and antimetabolites (cladribine, cytarabine, 5-FU). In addition, certain monoclonal antibodies (trastuzumab, bevacizumab) and tyrosine kinase inhibitors (e.g., lapatinib and sunitinib) have been associated with reversible cardiotoxicity (Thomas, 2017).
Thavendiranathan et al (2014) stated that the literature examining the utility of advanced echocardiographic techniques (such as deformation imaging) in the diagnosis and prognostication of patients receiving potentially cardiotoxic cancer therapy has involved relatively small trials in the research setting. In a systematic review of the current literature, these investigators described echocardiographic myocardial deformation parameters in 1,504 patients during or after cancer chemotherapy for 3 clinically-relevant scenarios. The systematic review was carried out following the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines using the Embase (1974 to November 2013) and Medline (1946 to November 2013) databases. All studies of early myocardial changes with chemotherapy demonstrated that alterations of myocardial deformation preceded significant change in left ventricular ejection fraction (LVEF) . Using tissue Doppler-based strain imaging, peak systolic longitudinal strain rate has most consistently detected early myocardial changes during therapy, whereas with speckle tracking echocardiography (STE), peak systolic global longitudinal strain (GLS) appeared to be the best measure. A 10 % to 15 % early reduction in GLS by STE during therapy appeared to be the most useful parameter for the prediction of cardiotoxicity, defined as a drop in LVEF or heart failure (HF). In late survivors of cancer, measures of global radial and circumferential strain are consistently abnormal, even in the context of normal LVEF, but their clinical value in predicting subsequent ventricular dysfunction or HF has not been explored. The authors concluded that the findings of this systematic review confirmed the value of echocardiographic myocardial deformation parameters for the early detection of myocardial changes and prediction of cardiotoxicity in patients receiving cancer therapy.
Mornoş et al. (2014) highlight that while anthracyclines are vital anticancer agents, their use is constrained by both acute and chronic cardiotoxicity, and current surveillance methods often fail to adequately detect myocardial disease. They propose that strain imaging may identify early myocardial dysfunction, with speckle analysis from three-dimensional (3D) echocardiography enhancing the assessment of left ventricular (LV) segmental and global deformation by minimizing speckle loss seen in traditional bidimensional strain analysis. The study evaluated 59 patients (mean age 51 ± 10 years) using echocardiography, troponin T (TnT), and N-terminal pro-brain natriuretic peptide before, and at 12 and 36 weeks after anthracycline treatment, measuring LV global longitudinal strain (3DGLS), global radial strain (3DGRS), and global circumferential strain (3DGCS) through 3D-strain imaging. The percentage changes from baseline to 12 weeks post-chemotherapy were calculated for all parameters. During follow-up, 13.5% of patients developed cardiotoxicity, with significant deterioration in isovolumic relaxation time, 3DGLS, 3DGCS, and 3DGRS, alongside elevated troponin levels at 12 weeks, all before any decline in LV ejection fraction. Univariate logistic regression identified cumulative anthracycline dose at 12 weeks, LVEF, 3DGLS, and TnT as predictors of subsequent cardiotoxicity, while multiple logistic regression revealed 3DGLS as the sole independent predictor (Odds ratio 1.09, p=0.04). The findings indicate that anthracycline therapy leads to early declines in 3DGLS, 3DGCS, and 3DGRS, with 3DGLS serving as a strong predictor for the future onset of anthracycline-induced cardiotoxicity.
Venturelli et al (2018) stated that cardiotoxic effects of anthracycline therapy are a major cause of morbidity for childhood cancer survivors. In a retrospective study, these researchers examined the efficacy of tissue Doppler imaging (TDI) in the early detection of myocardial alterations in these patients. A total of 50 childhood cancer survivors (32 males and 18 females) who have been treated with anthracyclines was evaluated by standard and TDI echocardiographic examination of the basal and median region of the interventricular septum (IVSb, IVSm), of the left ventricular posterior wall (LVPWb, LVPWm), and of the mitral annulus; the results were compared with those obtained from a population of 50 healthy age-matched and sex-matched controls by using the Student t-test. The clinical and echocardiographic data of the 2 groups were compared also with the independent samples t-test. All data were expressed as mean ± standard deviation. A 2-tailed p-value of < 0.05 was considered statistically significant. Statistical analysis was performed using STATA 7.0. The case-control analysis showed statistically significant differences (p < 0,05) between the patients and the controls values. The systolic performance of the patients was normal (LVEF (p = 0,0029) and LVFS (p = 0,0002)). Statistically significant differences between patients and controls were found for diastolic function measurements obtained with PW Doppler such as IVRT (p = 0,0000), DT (p = 0,0041), E (p = 0,0000), A (p = 0,0458), even if E/A ratio was not altered. TDI analysis also showed significant differences between patients and controls in both LVPW and IVS (basal and middle segments); E/E' ratio and E'/A' ratio did not vary significantly. Linear Regression and multi-variate analysis showed that hematopoietic stem cell transplantation had the highest impact on the measurements. The authors concluded that the results showed a myocardial diastolic impairment with preserved EF. Since the median follow-up time of this cohort was 2 years, further evaluation is needed to better define the diastolic alterations. These investigators stated that TDI analysis showed high sensitivity for the detection of mild myocardial dysfunction; the implementation of this novel method as standard practice in the follow-up of selected childhood cancer survivors might help to achieve a better management of long-term complications of cardiotoxic chemotherapy.
McGregor et al (2021) noted that transthoracic echocardiography is the primary cardiac imaging modality for the detection of cancer therapeutics-related cardiac dysfunction (CTRCD) through evaluation of serial changes in LVEF. However, LVEF assessment by standard methods including 3D Echo has important limitations including the fact that reduction in LVEF occurs late in the process of CTRCD. In contrast, by detecting early myocardial change, myocardial strain or deformation imaging has evolved to be a preferred parameter for detecting CTRCD. Peak systolic GLS by STE has become an important pre-chemotherapy parameter that can independently predict subsequent adverse cardiac events as these abnormalities typically precede reduction in LVEF. While an absolute GLS measurement may be informative, a 10 % to 15 % early reduction in GLS by STE appeared to be the most useful prognosticator for cardiotoxicity while on therapy. These investigators presented a current systematic literature review of application of myocardial strain imaging in cancer patients performed following PRISMA guidelines using electronic databases from Medline, Embase, and SCOPUS Library from their inception until June 11, 2020. This review demonstrated the incremental value of myocardial deformation imaging over traditional LVEF in detection and its clinical implication in management of CTRCD.
Furthermore, an UpToDate review on “Cardiotoxicity of non-anthracycline cancer chemotherapy agents” (Floyd and Morgan, 2021) states that “Trabectedin is an alkaloid that is approved for use in soft tissue sarcomas after progression on an anthracycline. It has been associated with a low rate of cardiac toxicities, including congestive heart failure and rarely, cardiac arrest. The median time to development of grade 3 to 4 cardiotoxicity on trabectedin is 5.3 months. A baseline assessment of ejection fraction should be performed using echocardiogram or multi-gated acquisition (MUGA) prior to initiation of trabectedin and at 2- to 3-month intervals while treatment is continued. Trabectedin should be held for a decrease in ejection fraction below the lower limit of normal and permanently discontinued for symptomatic cardiomyopathy or for persistent left ventricular dysfunction that does not recover to the lower limit of normal within 3 weeks”.
The 2022 European Society of Cardiology (ESC) guidelines on cardio-oncology therapies recommend monitoring global longitudinal strain (GLS) every 3 months for patients undergoing various cardiotoxic therapies, as anti-HER2 treatments can lead to left ventricular dysfunction (LVD) in 15–20% of patients, potentially resulting in overt heart failure if surveillance is neglected, particularly in high- and very high-risk individuals. Surveillance of left ventricular (LV) function, utilizing both left ventricular ejection fraction (LVEF) and GLS, is advised prior to and every 3 months during HER2-targeted therapy. While no studies have established an optimal follow-up protocol for patients with multiple myeloma (MM) receiving proteasome inhibitors (PIs), a common approach includes visits every 3–6 months for ECG, complete blood tests (including natriuretic peptides and cardiac troponin), and echocardiography surveillance. A recent prospective study in relapsed MM patients highlighted the value of natriuretic peptides for risk stratification and managing cardiovascular morbidity during treatment. Cancer therapy-related cardiac dysfunction (CTRCD) can occur anytime from the first month of therapy to 2 years post-treatment, prompting recommendations for baseline transthoracic echocardiography (TTE) in patients at moderate to high risk of cancer therapy-related cardiovascular toxicity (CTR-CVT). For patients treated with cobimetinib/vemurafenib, ECG monitoring is recommended at 2 and 4 weeks after treatment initiation, followed by every 3 months thereafter.
Sperlongano et al. (2025) highlight the central role of transthoracic echocardiography in diagnosing and monitoring cancer therapy-related cardiac dysfunction, as it provides a reliable, non-invasive, and cost-effective means for early detection of myocardial damage and effective management of cardiotoxicity. Early identification and management of therapy-induced cardiotoxicity are vital to prevent cardiovascular complications without compromising treatment efficacy. Echocardiographic evaluation is essential in this context, offering a dependable method to monitor cardiac function and detect subclinical dysfunction. Notably, speckle-tracking derived global longitudinal strain (GLS) has emerged as a highly sensitive marker for early myocardial damage, often showing impairment before a decline in left ventricular ejection fraction (LVEF). Cancer therapies can negatively impact cardiac structure and function, leading to either asymptomatic dysfunction or symptomatic heart failure, collectively termed cancer therapy-related cardiac dysfunction (CTRCD). The latest definition of CTRCD, based on the 2022 IC-OS consensus statement, focuses on changes in LVEF, systolic dysfunction, and heart failure events. While LVEF, assessed by biplane Simpson’s method, remains the most commonly used parameter for identifying left ventricular dysfunction, it has limitations, including variability and hemodynamic load-dependence. When feasible, three-dimensional (3D) echocardiography is preferred for LVEF assessment due to its enhanced accuracy and reproducibility. In contemporary cardiology, GLS is recognized as a more sensitive and reproducible marker of myocardial dysfunction than LVEF, with strong evidence supporting its diagnostic and prognostic value in cancer patients. A relative GLS reduction greater than 15% from baseline is currently recommended as the threshold for diagnosing CTRCD, as it predicts significant future declines in LVEF. Although GLS measurements from 3D speckle-tracking echocardiography have shown added value over two-dimensional methods in detecting cardiotoxicity, their routine clinical use is limited by challenges such as the need for optimal acoustic windows, high-quality images, specialized training, and lack of standardization. Additionally, left ventricular myocardial work indices (MWIs), derived from strain parameters and non-invasive systolic blood pressure measurements, have shown promise in improving CTRCD diagnosis and prognosis. A decrease in the global work index, particularly in patients with minor GLS reductions but significant systolic blood pressure declines, may help identify those at higher risk for CTRCD. However, optimal thresholds for using GLS and MWIs sequentially require validation through large multicenter studies before clinical application. The 2022 ESC guidelines on cardio-oncology do not explicitly include left ventricular diastolic dysfunction as a criterion for diagnosing CTRCD or for initiating cardioprotective therapy, although traditional diastolic function indices may change during cancer treatment and could serve as early markers of subsequent systolic dysfunction, especially in patients receiving anthracyclines and/or trastuzumab. While the role of LV GLS in cardio-oncology is well established, the significance of left atrial (LA) strain, recently identified as a potential indicator of early diastolic dysfunction, remains less understood. The STRANO study found that LA strain impairment was significantly greater in patients who developed asymptomatic mild CTRCD, suggesting its potential as a valuable parameter in this context. Despite its limitations, echocardiography remains the primary imaging modality due to its availability, cost-effectiveness, and real-time functional assessment capabilities. Cardiac magnetic resonance (CMR) is considered the gold standard for assessing cardiac chamber volumes, myocardial mass, and contractile function, offering advanced tissue characterization and strain imaging. In cardio-oncology, CMR is typically used as a second-line diagnostic tool when echocardiography is suboptimal, particularly in patients with conditions that affect acoustic windows. Current guidelines recommend CMR for diagnosing and monitoring immune checkpoint inhibitor myocarditis and for detecting pericardial involvement due to its superior characterization capabilities. Additionally, computed tomography is the reference imaging modality for identifying pericardial calcifications, while cardiac computed tomography angiography (CCTA) is useful for detecting atherosclerotic cardiovascular disease, particularly in oncological patients who face increased bleeding risks. In the evolving field of cardio-oncology, transthoracic echocardiography remains a cornerstone for diagnosing and monitoring CTRCD. The integration of traditional echocardiographic parameters with advanced imaging techniques facilitates early detection of subclinical myocardial damage and enhances risk stratification for cancer patients. Further validation in larger prospective studies is necessary to establish the prognostic significance of novel ultrasound tools, including speckle-tracking and 3D echocardiography, and their therapeutic implications in cardio-oncology. Close collaboration between cardiologists and oncologists is essential to ensure that all cancer patients, especially those at high cardiovascular risk, receive optimal treatment while minimizing cardiotoxicity and initiating cardioprotective therapy when necessary.
Myocardial Strain Imaging for Heart Transplant Evaluation and Surveillance
Tseng et al. (2018) investigated the challenges of noninvasive diagnosis of allograft rejection in heart transplant recipients, specifically evaluating the effectiveness of two-dimensional speckle-tracking echocardiography (2D-STE) in predicting severe rejection in patients with preserved left ventricular ejection fraction (LVEF). The study included adult heart transplant patients with LVEF greater than 55% who either had severe rejection (Rejection Grade ≥ 2R) or no rejection, as determined by biopsy, between 1997 and 2011 at the Mayo Clinic in Rochester, Minnesota. Transthoracic echocardiography was conducted within one month of the biopsy, and the researchers retrospectively analyzed left ventricular global longitudinal strain (GLS), global circumferential strain (GCS), and their respective strain rates (GLSR and GCSR). Among the 65 patients studied, 25 had severe rejection while 40 served as normal transplant controls, with both groups predominantly male (64% and 75%, respectively) and similar baseline clinical characteristics. Both groups exhibited normal LVEF (64.3% vs. 64.5%; P = .87), and all non-strain echocardiographic variables were comparable. However, strain analysis revealed a significantly increased early diastolic longitudinal strain rate (P = .02) and decreased GCS (P < .001) and GCSR (P = .02) in the rejection group compared to controls. The area under the receiver operating characteristic curve for GCS was 0.77, indicating that with a GCS cutoff of -17.60%, the sensitivity and specificity for detecting severe acute rejection were 81.8% and 68.4%, respectively. The findings suggest that 2D-STE may be a valuable tool for identifying severe transplant rejection in heart transplant patients with normal LVEF.
Ruiz Ortiz et al. (2020) explored the utility of tissue Doppler velocities in ruling out treatment-requiring acute cellular rejection (TR-ACR) within the framework of myocardial deformation analysis using speckle tracking echocardiography. The study involved serial echocardiograms conducted on 37 heart transplant recipients during their first year post-transplantation, performed within three hours of routine surveillance endomyocardial biopsies (EMB). The researchers examined the relationship between the sum of lateral mitral annulus systolic (s') and early diastolic (e') velocities, measured in absolute values by tissue Doppler echocardiography (s' + e'), and TR-ACR (defined as ACR grade ≥ 2R) through multivariate analysis that included traditional echocardiographic parameters and myocardial deformation metrics. A total of 251 pairs of EMB and echocardiogram examinations were analyzed, with 35 (14%) showing rejection grade ≥ 2R (TR-ACR). The findings indicated that s' + e' was independently associated with TR-ACR (OR 0.80, 95% CI 0.72-0.89, p < 0.0005), achieving a C statistic of 0.79 (95% CI 0.71-0.87, p < 0.0005) in ROC curve analysis. An s' + e' value of ≥ 23 cm/s, observed in 43% of the studies, demonstrated a negative predictive value of 98% for excluding TR-ACR. Additionally, in patients experiencing TR-ACR, s' + e' significantly decreased by -3.7 ± 3.3 cm/s (p = 0.003) compared to previous studies without this condition, while remaining consistent when rejection status was unchanged. A reduction in s' + e' of less than 2.7 cm/s from the prior echocardiogram yielded a 99% negative predictive value for ruling out TR-ACR. Overall, tissue Doppler velocities emerged as a valuable marker for excluding TR-ACR in this multivariate study that incorporated myocardial deformation variables.
Pergola and colleagues (2023) state that strain echocardiography demonstrates greater sensitivity and accuracy than conventional echocardiography alone, which is especially crucial in the early stages of acute cellular rejection when standard echocardiography may fail to detect certain pathological changes, such as pericardial effusion, wall thickening, or increased left ventricular (LV) mass. In contrast, strain echocardiography can reveal features like myocardial edema or fibrosis that often impact the sub-endocardial muscle fibers, leading to a decline in longitudinal graft function. In the context of heart transplantation (HT), a reduction in global longitudinal strain (GLS) shortly after transplantation or a lack of improvement in GLS between two weeks and three months post-transplant has been associated with poor outcomes, making GLS evaluation a valuable tool for risk stratification during the critical early post-transplant period, complementing traditional monitoring methods like right-heart catheterization and endomyocardial biopsies (EMBs). Notably, some HT patients may exhibit reduced GLS despite having normal or slightly reduced LV ejection fraction. The left atrium (LA) and right atrium (RA) play essential roles in regulating ventricular filling through their reservoir, conduit, and contractile functions. In HT recipients, atrial function is affected not only by ventricular dysfunction but also by surgical factors, as both atria are typically enlarged due to the connection of recipient and donor tissue. The bicaval technique, however, reconstructs the RA using only donor tissue, while the LA comprises a mix of donor and recipient tissue, resulting in smaller atrial sizes compared to the standard technique. Advanced strain echocardiography can assess atrial function in HT recipients, with studies indicating a significant reduction in atrial reservoir function linked to elevated pulmonary capillary wedge pressure (PCWP), LA enlargement, and impaired longitudinal right ventricular function. This decline is most pronounced with elevated filling pressures, and alterations in LA function throughout the cardiac cycle have been observed, regardless of the surgical technique. Peak LA strain correlates with worse LV systolic function, highlighting the importance of LA function in HT patients. Measurements of LA strain are derived from six atrial segments captured in both apical four-chamber and two-chamber views. The integration of novel echocardiographic parameters, such as strain imaging, with dobutamine stress echocardiography (DSE) has proven more accurate than visual assessments alone in diagnosing coronary artery disease (CAD) in non-transplant populations, suggesting that further studies using these techniques could enhance DSE's sensitivity in detecting early-stage cardiac allograft vasculopathy (CAV) and provide additional prognostic value. Although the evaluation of coronary flow reserve (CFR) to assess microvascular disease is not routinely performed in HT patients, previous studies indicate that reduced CFR is associated with major cardiovascular events in this population. HT patients with normal systolic function and no evidence of CAV may still experience coronary microvascular impairment due to structural remodeling and diminished vasodilatory capacity. New non-invasive techniques are being proposed and tested to minimize the need for invasive examinations in the follow-up of HT patients. Overall, advanced echocardiography techniques, including strain imaging and tissue Doppler imaging, enhance the assessment of cardiac function and can help identify abnormalities in HT patients, with GLS emerging as a promising early marker of cardiac allograft rejection.
The guidelines from the International Society for Heart and Lung Transplantation (ISHLT) regarding the care of heart transplant recipients (Velleca et al., 2023) advocate for the incorporation of myocardial strain imaging in the management of heart transplantation. Cardiac MRI (CMR) presents several potential benefits for diagnosing transplant rejection, utilizing techniques such as volumetric measurement, functional assessment including strain imaging, perfusion imaging, and tissue characterization methods like T1 and T2 mapping, extracellular volume (ECV) measurement, late gadolinium enhancement (LGE), and spectroscopy.
In a systematic review and meta-analysis, Xourgia et al. (2025) examined the management of immunosuppression following cardiac transplantation, emphasizing the need for active monitoring for acute cellular rejection (ACR), with endomyocardial biopsy (EMB) being the gold standard for surveillance. Due to the associated costs and potential complications of EMB, there is increasing interest in non-invasive screening methods. This study aimed to evaluate the effectiveness of speckle-tracking echocardiography as a screening tool for ACR. The researchers conducted a comprehensive search of PubMed (CENTRAL) and gray literature for studies that provided data on speckle tracking echocardiography in heart transplant patients experiencing ACR. The primary outcomes of the meta-analysis focused on left and right ventricular global longitudinal strain. Utilizing random effects models for their calculations, the authors pre-registered their meta-analysis with PROSPERO (CRD42024508654). By analyzing data from over 2,000 biopsies across 18 studies, they found that both left ventricular global longitudinal strain (LVGLS, MD -1.96, 95% CI -2.85 to -1.07, p < 0.0001) and right ventricular global longitudinal strain (RVGLS, MD -2.90, 95% CI -4.03 to -1.76, p < 0.00001) were significantly lower in patients without ACR. Additionally, the change in LVGLS from baseline over time was more pronounced in patients with ACR (MD -2.43, 95% CI -4.82 to -0.05, p = 0.045). These findings suggest that myocardial strain measured by speckle tracking echocardiography is impacted by ACR and could serve as a valuable tool for early detection of rejection, potentially reducing the need for routine EMB in the follow-up of heart transplant patients.
In a clinical consensus statement from the American Society of Echocardiography developed in collaboration with the European Association of Cardiovascular Imaging of the European Society of Cardiology, Thomas et al. (2025) outline several recommendations for the use of myocardial strain imaging in heart transplant patients. They emphasize that two-dimensional speckle-tracking echocardiography (2D-STE) is a valuable tool for assessing myocardial function, particularly in detecting early signs of dysfunction and rejection in heart transplant recipients. The consensus highlights the importance of measuring left ventricular global longitudinal strain (LVGLS) as a complementary parameter to traditional left ventricular ejection fraction (LVEF), especially in patients with preserved LVEF. It is recommended that LVGLS be reported as end-systolic strain and that the midwall/full-thickness approach be used for strain measurements to enhance reproducibility and accuracy. The document also advises against the use of radial strain due to its poor performance in clinical settings and underscores the need for consistent vendor-specific software for follow-up assessments. Overall, the consensus aims to guide clinicians in effectively utilizing strain imaging to improve patient outcomes in heart transplant care.
Myocardial Strain Imaging and Atrial Septal Defect
Di Salvo et al. (2005) compared the value of strain and strain rate imaging in evaluating regional myocardial function to that of myocardial velocities. These investigators examined 10 patients late following successful percutaneous atrial septal defect (ASD) closure. Analysis was carried out for atrial longitudinal peak systolic velocity, strain, and strain rate from the mid-segment of the inter-atrial septum, in correspondence with the device, and from the lateral left atrial wall. Placing the sample volume in the middle part of the ASD occluder, a bulky non-contractile element passively moved by global heart motion, the new ultrasonic (US)-derived myocardial deformation indexes showed almost the absence of any deformations, whereas myocardial velocities failed to significantly discriminate between this non-contracting structure and the normal atrial wall.
Vitarelli et al. (2012) noted that real-time three-dimensional (3D) echocardiography allows clinicians to measure right ventricular (RV) end-diastolic volume irrespective of its shape. Tissue Doppler imaging (TDI) and speckle tracking imaging (STI) are new tools to evaluate myocardial function. These researchers examined RV function by 3D echocardiography and myocardial strain imaging in adult patients with ASD before and 6 months following transcatheter closure to examine the use of these new indexes in comparison with standard 2D and Doppler parameters. A total of 39 ASD patients and 39 healthy age- and sex-matched controls were studied using a commercially available cardiovascular US system. 2D-Doppler parameters of RV function (fractional area change, tricuspid annular plane systolic excursion, myocardial performance index) were calculated, and 3D RV volumes were also obtained. RV peak-systolic velocities, peak-systolic strain, and peak systolic and diastolic strain rate were measured in the basal, mid, and apical segments of the lateral and septal walls in the apical 4-chamber view by TDI and STI. In open ASD, RV ejection fraction (3D-RVEF) as well as global and regional RV longitudinal strain were significantly higher than in the control group and decreased significantly following closure. By multivariate analysis, 3D-RVEF, apical strain, and strain rate were independent predictors of functional class. ROC analysis showed 3D-RVEF and apical strain to be more sensitive predictors of unfavorable outcomes following defect closure compared to 2D-Doppler indexes. The authors concluded that 3D echocardiography and myocardial strain imaging provided useful insights into the quantitative assessment of RV function in ASD patients before and after closure.
In a retrospective study, Li et al. (2022) examined the role of right ventricular strain parameters (RVSP) quantified by cardiac magnetic resonance feature tracking (CMR-FT) in the early assessment of RV function in patients with pulmonary arterial hypertension associated with ASD (PAH-ASD). From September 2017 to May 2021, a total of 41 patients with PAH-ASD and 20 healthy controls were enrolled in this trial. All participants underwent CMR-FT, and right heart catheterization was performed in patients with PAH-ASD. The relationship between RVSP and RV functional parameters was subjected to correlation analysis, and intra-group correlation coefficient (ICC) and Bland-Altman plots were used to examine the consistency. Participants were divided into three groups: Group A (controls; n = 20), Group B (PAH-ASD, RVEF ≥ 45%; n = 14), and Group C (PAH-ASD, RVEF < 45%; n = 27). Compared with healthy controls, the RV global longitudinal strain (GLS) in Group B was significantly decreased (-19.68 ± 2.72% versus -25.21 ± 3.6%, p < 0.05). In RVEF-preserved PAH-ASD patients (Group B), compared with patients with GLS ≤ -20%, patients with GLS > -20% also had significantly elevated RV end-diastolic pressure (RVEDP) [8 (6.5 to 8.25) mmHg versus 4.5 ± 1.64 mmHg, p < 0.05]. RV GLS had a moderate-to-strong correlation with RVEF, RVESVi, RVEDVi, RVEDP, and NT-proBNP (p < 0.05). ICC and Bland-Altman plots revealed good intra-group and inter-group consistency in radial, circumferential, and longitudinal strains of RV. The authors concluded that it was feasible to quantify RV strain in patients with PAH-ASD by CMR-FT, and GLS was valuable for the early assessment of RV dysfunction in patients with PAH-ASD.
Wu et al. (2023) stated that non-invasive RV myocardial work (RVMW) determined by echocardiography is a novel indicator used to estimate RV systolic function. Currently, the feasibility of using RVMW has not been verified in assessing RV function in patients with ASD. In a single-center, proof-of-concept (POC) study, non-invasive RVMW was analyzed in 29 ASD patients (median age of 49 years; 21% male) and 29 age- and sex-matched individuals without cardiovascular disease. The ASD patients underwent echocardiography and right heart catheterization (RHC) within 24 hours. The RV global work index (RVGWI), RV global constructive work (RVGCW), and RV global wasted work (RVGWW) were significantly higher in the ASD patients than in the controls, while there was no significant difference in RV global work efficiency (RVGWE). RV global longitudinal strain (RV GLS), RVGWI, RVGCW, and RVGWW showed significant correlations with RHC-derived stroke volume (SV) and SV index. The RVGWI (area under receiver operating characteristic curve [AUC] = 0.895), RVGCW (AUC = 0.922), and RVGWW (AUC = 0.870) could be considered good predictors of ASD and were superior to RV GLS (AUC = 0.656). The authors concluded that RVGWI, RVGCW, and RVGWW were feasible indicators that evaluated RV systolic function and correlated with RHC-derived SV and SV index in patients with ASD. Non-invasive RVMW may predict RV systolic function and correlate with RHC-derived SV and SV index in patients with ASD, with possible prognostic implications. Moreover, these researchers stated that further studies are needed to verify the clinical role of non-invasive RVMW.
The authors stated that this study had several drawbacks. First, this trial was a single-center study. Second, the sample size of ASD patients included was small (n = 29). Third, non-invasive RVMW was not validated by radionuclide ventriculography or cardiovascular magnetic resonance. Fourth, RVMW was acquired by using a single-provider platform specifically designed for measuring LVMW. The RV GLS was calculated by measuring the strains of the inter-ventricular septum and RV free wall because of the irregular and complicated RV anatomy; thus, the RVMW derived by RV PSL was not as accurate as the LVMW derived by the LV pressure-strain loop. These researchers stated that non-invasive RVMW should be validated by invasive RV pressure-strain loop (RV-PSL) in the future.
Jiang et al. (2025) stated that the non-invasive RV-PSL represents a novel method for the quantitative assessment of RV myocardial function. Given that ASD is a prevalent congenital heart anomaly associated with RV volume overload, this study quantitatively examined the myocardial function of the right ventricle in ASD patients pre- and post-occlusion by non-invasive RV-PSL. This trial enrolled 36 patients diagnosed with secundum ASD and 30 healthy adults (control group). These researchers compared conventional RV echocardiographic parameters, RV strain, and myocardial work in the ASD group before occlusion, 2 days post-occlusion, and 3 months post-occlusion, with those in the control group. Prior to and 2 days following occlusion, the ASD group exhibited higher RV global work index (RVGWI), RV global wasted work (RVGWW), and RV global constructive work (RVGCW) compared to the control group (p < 0.05). Within the ASD group, post-occlusion, RVGWI, RVGCW, and RVGWW values were significantly reduced compared to pre-occlusion values (p < 0.001). In addition, RVGWI and RVGCW demonstrated a significant decrease 3 months following occlusion compared to 2 days post-occlusion (p < 0.05). Multivariate regression analysis identified ASD diameter and pulmonary artery systolic pressure (PASP) as independent predictors of RVGWI (β = 0.405, p < 0.001; β = 2.307, p = 0.037) and RVGCW (β = 0.350, p < 0.001; β = 1.967, p = 0.023). The authors concluded that non-invasive RV-PSL showed the alterations in RV myocardial function in ASD patients pre- and post-occlusion. The metrics of RV myocardial work (RVMW) offer a novel indicator for evaluating RV myocardial function in these patients. Moreover, ASD diameter and PASP emerge as independent determinants of RVGWI and RVGCW.
Furthermore, UpToDate reviews on “Isolated atrial septal defects (ASDs) in children: Classification, clinical features, and diagnosis” (Vick and Bezold, 2025a), and “Isolated atrial septal defects (ASDs) in children: Management and outcome” (Vick and Bezold, 2025b) do not mention myocardial strain imaging as a management tool.
Myocardial Strain Imaging and Kidney and Liver Transplant
The KDIGO clinical practice guideline on the evaluation and management of candidates for kidney transplantation does not include a recommendation for myocardial strain imaging (Chadban et al., 2020).
Cheng et al. (2022) examine the evaluation of coronary heart disease (CHD) risk in liver transplant (LTx) candidates, emphasizing the potential role of myocardial strain measurement. A multi-center study involving 5,296 LTx cases found that intraoperative cardiac arrest occurred in 3.7% of patients, leading to a significant intraoperative mortality rate of 32%. This underscores the need to identify patients at risk for perioperative death to enhance long-term outcomes. The approach to CHD screening varies widely among transplant programs; a 2021 survey indicated that 28% lacked standardized protocols, while 92% of those with protocols employed a risk-based strategy. The authors stress the importance of involving dedicated cardiology and anesthesia teams in CHD evaluations due to the complexities and high perioperative risks associated with LTx. They suggest that myocardial strain measurement via transthoracic echocardiography could be included in the initial assessment of asymptomatic candidates to evaluate cardiac function and detect issues like pulmonary hypertension; however, its routine use is not yet recommended pending further research. Additionally, the study highlights the limitations of current non-invasive functional assessments for CHD risk, noting that traditional stress testing may have low sensitivity and predictive value due to the unique physiological challenges faced by these patients. While cardiac magnetic resonance imaging offers excellent negative predictive value, its low sensitivity and high cost restrict its broader application. Ultimately, although myocardial strain measurement is acknowledged as a promising tool for assessing cardiac function in LTx candidates, further validation is needed for its integration into standard practice. A comprehensive, individualized approach to CHD risk stratification is advocated to address the specific challenges faced by these patients.
Myocardial Strain Imaging and Sarcoidosis
Barssoum et al. (2020) conducted a meta-analysis to assess the effectiveness of speckle tracking echocardiography (STE) in detecting cardiac sarcoidosis (CS) in its early stages. Traditional methods like electrocardiography and echocardiography have limited sensitivity for this purpose, while advanced imaging techniques such as cardiac magnetic resonance (CMR) and 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) face challenges related to cost and accessibility. The researchers reviewed English-language articles that reported left ventricular global longitudinal strain (LVGLS) or global circumferential strain (GCS) in patients with confirmed extra-cardiac sarcoidosis compared to healthy controls, excluding studies that focused solely on patients with probable or definite CS. Continuous data were analyzed as a standard mean difference (SMD), comparing the sarcoidosis group to healthy controls, using a random-effects model for all analyses and assessing heterogeneity with Q and I² statistics. The final analysis included nine studies with a total of 967 patients, revealing that LVGLS was significantly lower in the extra-cardiac sarcoidosis group compared to controls (SMD -3.98, 95% confidence interval [CI]: -5.32, -2.64, P < .001) and was also significantly lower in patients who experienced major cardiac events (MCE) (SMD -3.89, 95% CI -6.14, -1.64, P < .001). Similarly, GCS was significantly reduced in the extra-cardiac sarcoidosis group compared to controls (SMD -3.33, 95% CI -4.71, -1.95, P < .001). The study concluded that both LVGLS and GCS were significantly lower in patients with extra-cardiac sarcoidosis, even in the absence of cardiac symptoms, and that LVGLS correlates with MCEs in CS. The authors emphasized the need for further research to explore the role of STE in the early screening of CS.
Okafor et al. (2023) describe cardiac sarcoidosis (CS) as a rare inflammatory condition characterized by non-caseating granulomas in the myocardium. Recent studies indicate that 25-30% of patients with systemic sarcoidosis exhibit cardiac involvement, with detection rates rising due to advancements in cardiac imaging techniques. Late gadolinium enhancement cardiac magnetic resonance and 18-fluorodeoxyglucose positron emission tomography (FDG-PET) imaging have become preferred methods for diagnosing CS, surpassing the need for endomyocardial biopsy. Traditionally, echocardiography has served as a screening tool, identifying abnormalities that warrant further advanced imaging and assessing cardiac function. Indicators such as regional wall thinning or aneurysm formation in a noncoronary distribution may suggest granuloma infiltration, while thinning of the basal septum in patients with extracardiac sarcoidosis is highly specific for cardiac involvement. Additionally, abnormal myocardial echotexture and eccentric hypertrophy may indicate active myocardial inflammation. Right-ventricular involvement, evidenced by free-wall aneurysms, can resemble arrhythmogenic right-ventricular cardiomyopathy. The incorporation of myocardial strain has recently enhanced the sensitivity of echocardiography for diagnosing cardiac involvement. However, echocardiography has limitations in prognostication, with impaired left-ventricular (LV) ejection fraction and LV dilatation being the only established independent predictors of mortality. Further research is needed to investigate how advanced echocardiographic technologies can improve both the diagnostic sensitivity and prognostic capabilities of this modality in CS.
According to UpToDate, “Reduced global longitudinal strain is a feature that may be present in cardiac sarcoidosis with preserved ejection fraction, and reduction in longitudinal strain magnitude may vary inversely with LGE burden. Further studies are needed to evaluate the role of strain in screening for cardiac sarcoidosis" (Blankstein and Stewart, 2024).
Myocardial Strain Imaging and Tetralogy of Fallot
Fujiwara et al. (2022) conducted a prospective comparative study involving 22 adults with repaired Tetralogy of Fallot (rTOF) and 22 hemodynamically normal controls to evaluate the feasibility and clinical utility of right ventricular free-wall (RVFW) strain measured by two-dimensional speckle-tracking echocardiography (2D STE). The primary endpoint was to assess how well RVFW strain correlates with cardiac magnetic resonance (CMR)-derived measures of RV ejection fraction (RVEF) and pulmonary regurgitation fraction (PRF). The study found that RVFW longitudinal strain was significantly reduced in rTOF patients compared to controls (−19.6 vs. −24.7, p < 0.01), and RVFW strain correlated moderately with PRF (r = 0.44, p < 0.05) and RVEF (r = 0.57, p < 0.01). Notably, all rTOF patients exhibited more than moderate pulmonary regurgitation but were clinically near-asymptomatic. The intra-observer variability for RVFW strain was deemed acceptable, supporting the reproducibility of the method. The authors concluded that 2D STE is a feasible and complementary modality to CMR for assessing RV systolic function and PR severity in rTOF patients. However, limitations of the study include the small sample size, single-center design, and lack of longitudinal outcome data.
Vitarelli et al. (2023) conducted a prospective observational study involving 24 adult patients with repaired Tetralogy of Fallot (rTOF) and 24 matched controls to evaluate right ventricular (RV) performance, pulmonary artery (PA) elastic properties, and RV–PA coupling (RVPAC) using three-dimensional speckle-tracking echocardiography (3DSTE) and Doppler echocardiography. The primary endpoint was to assess the feasibility and clinical utility of 3DSTE-derived indices in evaluating exercise capacity and cardiovascular function. The study found that rTOF patients exhibited significantly impaired RV ejection fraction and strain, increased RV volumes, and reduced PA pulsatility and capacitance, along with elevated PA elastance compared to controls. Several 3DSTE-derived RVPAC ratios (e.g., 3DRVAS/RVESV, 3DRVAS/RVSP) demonstrated high sensitivity (88–91%) and specificity (79–81%) for identifying impaired exercise capacity. The authors concluded that 3DSTE is a feasible and clinically valuable modality for assessing RV function and RVPAC in rTOF patients. However, limitations of the study include the small sample size, single-center design, and lack of longitudinal follow-up, which may restrict generalizability and prognostic interpretation.
In the 2024 American Heart Association scientific statement by Geva et al., the authors provide a comprehensive review of long-term management strategies for right ventricular outflow tract (RVOT) dysfunction in patients with repaired Tetralogy of Fallot (rTOF), a population increasingly composed of adults due to improved early survival rates. The statement emphasizes the near-universal presence of RVOT dysfunction—manifesting as pulmonary stenosis, regurgitation, or both—and its role in precipitating electromechanical cardiomyopathy, arrhythmias, and premature death. While current surveillance heavily relies on volumetric and functional imaging via cardiovascular magnetic resonance (CMR), the authors highlight myocardial strain as a novel imaging biomarker with the potential to improve risk stratification. However, they do not recommend routine myocardial strain testing at this time, stating that “future work to further refine risk stratification in this population should explore novel imaging biomarkers such as myocardial strain.” This indicates that, while promising, myocardial strain remains investigational and has not yet been integrated into standard adult rTOF surveillance protocols. Limitations of current practice include reliance on observational data, a lack of randomized trials, and an incomplete understanding of the pathophysiological mechanisms linking imaging biomarkers to clinical outcomes.
Myocardial Straining Imaging for Assessing Risk in Asymptomatic Children
Myocardial strain imaging by echocardiography can detect subclinical myocardial dysfunction in HCM mutation carriers before left ventricular hypertrophy develops. However, there is little evidence on how strain abnormalities should guide management in asymptomatic, genotype-positive children, and more research is needed to clarify their prognostic value and impact on clinical decision-making.
The American Society of Echocardiography (Nagueh, et al., 2022) notes that although strain and other advanced imaging markers (e.g., crypts, segmental dysfunction) may be present before overt hypertrophy, there is insufficient evidence linking these abnormalities to subsequent pathological LVH or informing changes in management or surveillance intervals.
The ACC, in its 2024 guideline for the management of hypertrophic cardiomyopathy (Ommen, et al., 2024), does not specifically recommend routine myocardial strain imaging for genotype-positive, phenotype-negative children and adolescents with a family history of HCM. The guideline acknowledges that changes in myocardial strain and diastolic function can precede definitive hypertrophy, and family members with these abnormalities may warrant closer follow-up. However, it also states that the clinical significance of subclinical findings such as altered strain is unclear, and treatment decisions are not made based on these findings alone.
Appendix
Note on Documentation Requirements:
Physicians are reminded to bill the findings of the diagnostic test as the primary indication rather than the referring physician’s diagnosis, as indicated by Medicare’s Diagnostic Imaging Billing guidelines. These guidelines are available in the Medicare Claims Processing Manual, Chapter 13 - Radiology Services and Other Diagnostic Procedures (revised November 2016). This is also indicated in the ICD-9-CM Coding Guidelines, Section IV, Paragraph L.
References
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