|Year : 2023 | Volume
| Issue : 2 | Page : 128-136
Left Ventricular Strain in Systemic Diseases
Department of Non-Invasive Cardiology, Suraksha Diagnostics Private Limited, Kolkata, West Bengal, India
|Date of Submission||16-Mar-2023|
|Date of Decision||15-Apr-2023|
|Date of Acceptance||27-Apr-2023|
|Date of Web Publication||15-Jun-2023|
Dr. Aniruddha De
Department of Non-Invasive Cardiology, Suraksha Diagnostics Private Limited, Kolkata, West Bengal
Source of Support: None, Conflict of Interest: None
Systemic diseases consist of various pathological conditions with a wide range of symptoms, often with progressive clinical worsening. Cardiac involvement is not uncommon in many of these conditions. Subclinical myocardial dysfunction is the common manifestation during the early stages of the disease and recognition of early myocardial dysfunction is very important for diagnosis and future prognosis. Left ventricular ejection fraction (LVEF) is considered less sensitive to detect early LV myocardial dysfunction. Strain imaging, performed using speckle-tracking echocardiography (STE), has emerged as a robust tool for detecting early subclinical myocardial dysfunction. The longitudinal muscle fibres are predominantly found in the sub-endocardium and are more susceptible to damage since the sub-endocardium is comparatively less perfused. Hence, longitudinal strain is impaired early in the course of the disease and helps in detecting subtle cardiac involvement in various systemic diseases. Global longitudinal strain, which is the average longitudinal strain of all the LV myocardial segments, is currently the most useful strain parameter for this purpose.
Keywords: Global longitudinal strain, left ventricle, systemic diseases
|How to cite this article:|
De A. Left Ventricular Strain in Systemic Diseases. J Indian Acad Echocardiogr Cardiovasc Imaging 2023;7:128-36
| Introduction|| |
Systemic diseases are a broad category of pathological conditions, which are frequently autoimmune, and are characterized by systemic involvement, a wide range of symptoms, and in many cases, progressive clinical worsening. Cardiac involvement may occur in many of these conditions and can present in several different ways. Myocardial dysfunction is one of the most common manifestations and may often be subclinical, at least during the early stages of the disease. Recognition of such myocardial dysfunction may have diagnostic, prognostic, and therapeutic implications.
Left ventricular ejection fraction (LVEF) is the traditional echocardiographic measure used for assessing LV systolic function. However, it is now well-recognized that LVEF is not sufficiently sensitive to detect early stages of LV myocardial dysfunction. It also has suboptimal measurement reproducibility. Strain imaging, performed using speckle-tracking echocardiography (STE), overcomes these limitations and has emerged as a useful tool for detecting subclinical myocardial dysfunction in a wide variety of clinical conditions.
STE has changed echocardiography from a subjective image interpretation to an objective diagnostic tool. By accurately measuring the movement of acoustic speckles in serial images, myocardial deformation can be easily quantified. Strain is the percentage change in the length of the myocardium relative to its original length and can be evaluated in longitudinal, circumferential, or radial planes. When tied to a timeframe, the strain rate can be calculated as a unit-less metric of the deformational change. The myofibers in the LV wall are distributed in a complex manner. The longitudinal fibers are typically found in the sub-endocardium and are more vulnerable to damage since the subendocardium is comparatively less perfused. Hence, longitudinal strain is usually the earliest to get impaired when cardiac involvement occurs in systemic diseases. Accordingly, global longitudinal strain (GLS), the average longitudinal strain of all the LV myocardial segments, is the most useful strain parameter for clinical purposes. In addition, GLS is easy to obtain, quick, and highly reproducible [Figure 1].
|Figure 1: Bull's eye plot of left ventricular global longitudinal strain in a normal individual|
Click here to view
| Speckle-Tracking Echocardiography in Immune-Mediated Diseases|| |
Autoimmune diseases encompass a wide range of chronic illnesses that can affect one or more target organs or systems and negatively impact the quality of life. Genetic causes, gender variances, environmental influences, pathophysiological aberrations, and specific sub-phenotypes that are characterized by autoimmune reiteration are among the common instruments behind these illnesses.
The most predominant autoimmune arthropathy at present is rheumatoid arthritis (RA). In affluent nations, the overall incidence varies from 0.5% to 1.0%. Numerous studies have shown that RA patients are more likely to experience fatal and nonfatal cardiovascular (CV) events than the general population.,, The life expectancy of RA patients is 3–10 years less than that of the general population, and CV mortality is an important contributor. CV disease is known to develop early and more frequently in patients with RA and accounts for about 50% of all deaths in them. Strain imaging is useful for detecting cardiac involvement in RA. In a study using STE for LV and right ventricular (RV) longitudinal strain measurement, it was shown that patients with active RA had lower strain values than those in remission. The GLS remained low even in the remission phase when compared with the controls. Conventional echocardiographic measurements, however, were ineffective in differentiating between the groups of people with active RA, those who were in remission, and controls. Only late diastolic dysfunction in heart failure could be detected by it. In a different cross-sectional study involving 37 RA patients, STE was used to compare those with early and advanced disease (2.8 ± 1.2 years vs. 14.6 ± 6.8 years, respectively). Patients with CV comorbidities such as diabetes mellitus, hypertension, and others were not included in this study. It was found that the patients with advanced disease had much lower longitudinal strain values. However, the circumferential strain was comparable between the two groups [Figure 2].
|Figure 2: Bull's eye plot of left ventricular global longitudinal strain in a patient with rheumatoid arthritis|
Click here to view
Graves' disease is an autoimmune thyroid disorder and a major cause of hyperthyroidism. Thyroid hormones have several undesirable effects on the CV system through a variety of direct and indirect insults. They raise heart rate, cardiac contractility, systolic and mean pulmonary artery pressures, cardiac output, and myocardial oxygen consumption while lowering systemic vascular resistance and diastolic pressure. If not treated early, any of these hemodynamic changes in the CV system can cause heart failure, arrhythmias, and systemic and pulmonary arterial hypertension. CV involvement in Graves' disease can lead to substantial morbidity and mortality. LV GLS reduction has been observed in Graves' disease, which persists despite therapy and thyroid hormone correction. This is most likely owing to the autoimmune component of the disease, as GLS values are associated with tissue inhibitors of metalloproteinase-1, which is crucial for cardiac remodeling. STE can detect subclinical cardiomyopathy and ophthalmopathy because both are impacted by the same mechanism. Failure to return to normal GLS levels after achieving euthyroid status indicates hyperthyroidism caused by Graves' disease.
Rheumatic heart disease
Rheumatic heart disease has no direct effect on myocardial function in advanced stages. Pancarditis in acute rheumatic fever, on the other hand, can induce permanent modest myocardial impairment, which can be diagnosed by monitoring GLS. Strain is found to be lowered in acute rheumatic fever despite normal LVEF and the absence of a valve defect.
Systemic lupus erythematosus
Cardiac involvement is common in systemic lupus erythematosus (SLE), and all cardiac structures, including the pericardium, myocardium, endocardium, conduction tissues, and coronary circulatory system, can be involved. Immunological complexes produced by specific antibodies such as anti-double-stranded deoxyribonucleic acid antibodies, anti-smooth muscle antibody, and antibodies to other self-antigens have been demonstrated in cardiac tissues in patients with SLE indicating immune-mediating mechanisms underlying cardiac injury. Since SLE has significant systemic manifestations, impairment of the CV system often gets overlooked during the early stages due to inconspicuous symptoms or subtle clinical indicators. Early recognition of cardiac involvement is crucial because controlling further progression becomes increasingly difficult as the disease advances. Up to 63% of patients with SLE were found to have myocardial damage in an autopsy series., Myocarditis is the most common manifestation of myocardial injury in SLE and can present with obscure and unusual clinical symptoms. It can present clinically as dyspnea, chest uneasiness not related to exertion, dependent edema, fever, sweating, orthopnea, paroxysmal nocturnal dyspnea, nausea, anorexia, vomiting, and palpitations. SLE patients with myocardial involvement also have increased evidence of atherosclerosis, which further increases their risk of CV morbidity and mortality., Traditional echocardiographic and laboratory tests are unable to identify the early evidence of cardiac involvement. STE may be helpful for this purpose and several studies have revealed diminished RV and LV GLS in SLE, especially in juvenile SLE. In addition, serial strain imaging may also be useful to track the response to treatment, [Figure 3].
|Figure 3: Bull's eye plot of left ventricular global longitudinal strain in a patient with systemic lupus erythematosus|
Click here to view
Clinical signs of systemic sclerosis (SSc) include localized or diffuse thickening and fibrosis of the skin as well as systemic illnesses affecting the digestive system, heart, and lungs. The pathological characteristics of this disease include extensive vascular disease, collagen growth, and fibrosis of the afflicted tissue. SSc frequently affects the heart. Almost every region of the heart may experience collagen growth and fibrosis in SSc and clinical symptoms manifest accordingly. Myocardial fibrosis, which can appear as patchy fibrosis, localized degeneration, or necrosis, is a common manifestation of cardiac involvement in SSc. Vasospasm, inadequate vasodilation, localized ischemia, and inflammation are all associated with cardiac fibrosis. Myocardial fibrosis, in turn, can lead to myocardial ischemia, hypertrophy, and ventricular diastolic dysfunction. Apart from the direct myocardial involvement, SSc may affect the heart indirectly also. In fact, pulmonary hypertension and subsequent RV dysfunction are the major cardiac complications in SSc and the foremost reason for morbidity and mortality.
Recognition of early cardiac involvement in SSc is difficult as the LVEF is rarely reduced during the early stages. Cardiac magnetic resonance (CMR) imaging is regarded as the gold standard for identifying mild myocardial fibrosis, whereas strain imaging can also identify early myocardial dysfunction. In one study, 22 SSc patients with normal LVEF and a mean duration since diagnosis of 5.4 ± 4.6 years were compared with 22 sex- and age-matched healthy volunteers. LV GLS was found to be significantly reduced in the SSc group. This was mainly due to reduced strain in the basal segments, whereas strain values in the mid and apical segments did not differ much. There are several other studies which have shown that STE-based strain imaging may be helpful for cardiac risk stratification and early initiation of cardioprotective medications in SSc.,,,
| Speckle-Tracking Echocardiography in Infiltrative Diseases|| |
Clinically, thalassemia is classified into two major groups based on the patient's necessity for blood transfusion. Patients with transfusion-dependent thalassemia commonly present with severe anemia during childhood, requiring life-long transfusion therapy. Nontransfusion-dependent thalassemia patients, on the other hand, characteristically present with mild-to-moderate anemia in late childhood or early adulthood, needing only occasional or short-course routine transfusions in particular clinical contexts. CV disease is still the principal cause of death in both groups of patients, accounting for 71% of all deaths., Iron overload, induced by frequent blood transfusions, hemolysis, increased intestinal absorption, and a lack of iron excretion mechanism, are the primary mechanisms responsible for myocardial injury in these patients. Contractility is hampered by iron deposition in the myocytes through the activation of L-Type calcium channels brought on by iron overload.
Patients with thalassemia should have regular clinical examinations and appropriate investigations to gauge their overall functional capacity because cardiac problems can go unnoticed for long. T2* CMR is the current modality of choice for assessing myocardial and hepatic iron load. STE offers a relatively cheap and widely available alternative to CMR for the detection of subclinical cardiac dysfunction in thalassemia. As iron deposition is mostly concentrated in the subepicardium, LV circumferential strain is frequently decreased. However, LV GLS is also decreased due to chronic hypoxia, which often affects the subendocardium. Because the half-life of deposited iron is 14 months, serial echocardiographic follow-up of these individuals allows risk categorization and timely institution of the chelation therapy. However, STE may not be able to detect acute cardiac dysfunction resulting from severe iron excess as well as the impact of ongoing treatment,, [Figure 4].
|Figure 4: Bull's eye plot of left ventricular global longitudinal strain in a patient with thalassemia on chelation|
Click here to view
Cardiac amyloidosis is one of the common causes of restricted cardiomyopathy. However, it is often missed, and hence, a high index of suspicion is needed. Imaging is essential for diagnosing cardiac amyloidosis. The extracellular deposition of insoluble amyloid proteins is the distinctive feature of amyloidosis, which is a systemic infiltrative disease. There are two main forms of amyloidosis that involve the heart. Amyloid light chain amyloidosis, which affects more than ten persons per million annually, occurs due to the deposition of monoclonal immunoglobulins. The deposition of either a normal or mutant form of the transthyretin protein results in the other kind of cardiac amyloidosis known as amyloid transthyretin amyloidosis. Echocardiography is commonly the first pointer and is important for identifying and establishing the diagnosis of cardiac amyloidosis. It typically reveals thick-walled ventricles with bi-atrial enlargement. There is often thickening of the valve leaflets and the interatrial septum also. The myocardium usually has altered echotexture. The LV is not dilated, and until late in the course of the disease, LVEF remains preserved. However, diastolic dysfunction is always present, and typically, the grade of diastolic dysfunction advances quickly. Pericardial and pleural effusions are frequent.
Two-dimensional STE is very valuable in diagnosing cardiac amyloidosis and its prognostication. As mentioned above, LVEF remains preserved in cardiac amyloidosis, at least during the early stages; however, subclinical LV systolic dysfunction is widely prevalent. More importantly, there is a characteristic LV apical sparing of longitudinal strain in cardiac amyloidosis, which helps to differentiate it from other conditions associated with LV hypertrophy. It produces the so-called “cherry-on-top” pattern in the bull's eye plot of the LV longitudinal strain. It can also be assessed quantitatively by measuring the ratio of the average apical longitudinal strain to the average strain of basal and mid-LV segments. A ratio of >1 has been shown to have 93% sensitivity and 82% specificity for differentiating cardiac amyloidosis from other causes of LV hypertrophy. It also has significant prognostic value. In one study, a cutoff value of 1.9 of the relative regional strain ratio was found to be associated with a greater requirement for heart transplantation and mortality, [Figure 5].
|Figure 5: Bull's eye plot of left ventricular global longitudinal strain in a patient with cardiac amyloidosis showing the characteristic 'cherry on top' appearance|
Click here to view
Cardiac involvement with evidence of ventricular arrhythmias, conduction disorders, and heart failure is found in 5% of sarcoidosis patients. Cardiac manifestations often can be the earliest sign of sarcoidosis. Since the majority of patients with the clinically obvious cardiac illness have limited extra-cardiac involvement and almost two-thirds have isolated cardiac sarcoidosis (CS), CV signs typically dominate over extra-cardiac signs. Asymptomatic cardiac involvement is found in around 20%–25% of cases with pulmonary or systemic sarcoidosis. The extent of LV systolic dysfunction seems to be the most important prognosticator in clinically apparent CS. The prognosis for CS is particularly poor, with a mortality rate of around 40% within 5 years. It starts with subclinical myocardial inflammation and progresses to fibrosis with ventricular remodeling, which causes arrhythmias, atrioventricular conduction block, and heart failure. GLS is frequently reduced in patients with CS, despite normal LVEF, and is recognized as an early and sensitive indicator of myocardial dysfunction.,, As a result, strain imaging may be utilized as a regular screening tool in suspected CS patients and serve as an alternative to other expensive modalities such as CMR and cardiac positron emission tomography scans. In one study, 23 patients with early CS with normal LVEF and no wall motion abnormalities were compared with 97 controls. A comprehensive strain assessment of the left and right ventricles was performed. The longitudinal strain values of both ventricles were meaningfully lower in patients with early CS as compared to the controls. The LV GLS value of -16.3% was found to be 82.2% sensitive and 81.2% specific, whereas an RV strain value of -19.9% was 88.1% sensitive and 86.7% specific for diagnosing CS. Heart failure and hospitalization have been shown to have a strong relationship with poor LV GLS (>−14%) [Figure 6].
|Figure 6: Bull's eye plot of left ventricular global longitudinal strain in a patient with cardiac sarcoidosis|
Click here to view
| Speckle-Tracking Echocardiography in Metabolic and Endocrine Diseases|| |
Obesity is a growing health concern worldwide. It is related to an elevated CV risk as a result of both obesity and accompanying medical disorders (e.g., hypertension, diabetes mellitus, insulin resistance, dyslipidemia, and sleep apnea syndrome). Obesity is a major provider of atherosclerosis and consequent coronary artery disease. Heart failure is another common manifestation. Anatomical and functional alterations of the heart due to obesity are the major reasons for heart failure. Altered myocardial configuration in obesity is also responsible for the increased incidence of atrial fibrillation and sudden cardiac death. Improved cardiac imaging techniques allow for the early diagnosis of abnormal cardiac anatomy and function in obese people. Impaired LV GLS is a useful marker of early myocardial dysfunction in these subjects [Figure 7].
|Figure 7: Bull's eye plot of left ventricular global longitudinal strain in an obese individual|
Click here to view
Diabetes mellitus is a chronic metabolic disease and is responsible for multi-organ dysfunction. It is one of the strongest risk factors for atherosclerosis and results in coronary, cerebrovascular, and peripheral arterial disease. Diabetes can also compromise cardiac function independent of coronary artery disease, eventually leading to heart failure. Interestingly, diabetes increases cardiomyocyte hypertrophy and cardiac inflammation in people with heart failure with preserved ejection fraction (EF) but lowers fibrosis and cardiomyocyte cell death in those with heart failure with reduced EF., Nonetheless, diabetes is linked to an increased risk of death, poor functional status, and hospitalization in both of these scenarios.
Impairment of GLS is common in diabetes and is directly related to the body-mass index and the degree and duration of diabetes., As a result, GLS can be used as a screening tool for subclinical myocardial impairment in both obese patients and those with diabetes. Type 2 diabetes is also linked to nonalcoholic fatty liver disease, and there is a definite link between the severity of fatty liver disease and decreased LV GLS. STE also revealed LV systolic dysfunction in children with type 1 diabetes, which corresponded to poor glycemic management [Figure 8].
|Figure 8: Bull's eye plot of left ventricular global longitudinal strain in a patient with diabetes mellitus|
Click here to view
Hypothyroidism causes significant CV alterations such as reduction in cardiac output, contractility, and heart rate and an increase in the peripheral vascular resistance. Hypothyroidism is characterized by a decrease in the oxygen and substrate utilization by all the major organ systems. As a result, the demands on cardiac output are reduced. In addition, hypothyroidism influences cardiac function directly through alterations in myocyte-specific gene expression. In both short- and long-term hypothyroidism, all measures of LV performance are compromised, resulting in a decrease in the cardiac output. There is also a decrease in the rate of ventricular diastolic relaxation, which in turn impairs compliance and diastolic filling. The cause of the decreased ventricular function is most likely multifaceted. Because these alterations are reversible with effective therapy, LV GLS is helpful in the management of hypothyroid-related myocardial dysfunction at an early stage and to monitor treatment effectiveness during the subsequent follow-up., It is advised to perform myocardial strain imaging at regular intervals since myocardial alterations require time to reverse when thyroid function has been restored, [Figure 9].
|Figure 9: Bull's eye plot of left ventricular global longitudinal strain in a patient with hypothyroidism|
Click here to view
| Speckle-Tracking Echocardiography in Viral Myocarditis|| |
Viral myocarditis can present with a wide spectrum of manifestations ranging from asymptomatic myocardial injury to frank cardiogenic shock and sudden cardiac death. Acute myocarditis may lead to dilated cardiomyopathy and sudden cardiac death in 9% and 12% of young adults, respectively. CMR imaging is a very useful tool for the diagnostic assessment of myocarditis but is not widely available and has many other practical challenges. Therefore, in practice, acute myocarditis is mostly diagnosed based on clinical symptoms, electrocardiogram (ECG), cardiac biomarkers, and echocardiography. However, a regular echocardiogram often fails to identify any major cardiac involvement in acute myocarditis. GLS can be of help in this scenario [Figure 10]. Many studies have shown the utility of GLS in diagnosing acute myocarditis. Furthermore, as confirmed by CMR in cases of acute myocarditis, GLS correlates proportionately with the amount of myocardial edema. Thus, it may be advisable to perform strain imaging on every patient in whom myocarditis is suspected.
|Figure 10: Bull's eye plot of left ventricular global longitudinal strain in a patient with viral myocarditis|
Click here to view
Approximately 15%–40% of patients with dengue fever show evidence of cardiac involvement., Like many viral infections, dengue can induce cardiac damage through direct invasion or an immunological response that results in myocardial inflammation. Dengue-related cardiac abnormalities are transitory and self-limiting and often manifest as subclinical myocarditis. Cardiac expression in dengue fever may vary from slight bradycardia to severe myocarditis. Cardiac rhythm irregularities are often observed during the acute phase of the illness and during recovery. Sinus and junctional bradycardia, varying degrees of atrioventricular block, and brief ventricular arrhythmias are the common cardiac rhythm disturbances observed. Conventional echocardiography is likely to miss the evidence of cardiac involvement in many of these cases. In one study, ECG was abnormal in 64.6% of the patients, while only 6% of the patients had structural abnormalities on echocardiography. However, based on the European Society of Cardiology criteria and strain analysis, 27.3% of patients were judged to have myocardial dysfunction. Reduced LV longitudinal (−16.4%) and circumferential (−15.7%) strains were observed in severe dengue infection. In another study involving patients with dengue hemorrhagic fever, the peak LV GLS was found to be significantly lower in the subendocardial region when compared to normal controls. The length of the hospital stay can also be predicted independently by subendocardial longitudinal strain [Figure 11].
|Figure 11: Bull's eye plot of left ventricular global longitudinal strain in a patient with dengue myocarditis|
Click here to view
Coronavirus disease 2019
Coronavirus disease 2019 (COVID-19) is known to cause systemic inflammation, multiorgan dysfunction, and life-threatening complications. Myocardial dysfunction, myocarditis, acute myocardial infarction, heart failure, arrhythmias, and venous thromboembolic manifestations are the common CV complications of COVID-19. Multiple mechanisms for cardiac injury have been proposed. First, high cytokine levels can damage a variety of organs, including vascular endothelium and cardiac myocytes. Second, cardiac injury may result from direct viral invasion, mediated through the angiotensin-converting enzyme 2 receptors present on the surface of the cardiac myocytes (apart from the alveolar cells). Finally, myocardial injury can also occur as a consequence of hypoxemia, tachycardia, and hypotension, which are commonly present in patients with severe COVID-19 illness. Preexisting cardiac illnesses further complicate the matter by increasing the likelihood of more severe COVID-19 illness.
Several studies have been conducted during the COVID-19 pandemic to investigate the utility of STE for diagnosing myocardial injury and for the risk stratification of these patients. LV GLS and the RV-free wall strain have been shown to be independent predictors of morbidity and mortality in COVID-19., STE also helps reduce interaction time between the echocardiographer and the patient while being fairly accurate in recognizing early myocardial dysfunction. It has also been used for diagnosing residual myocardial damage in patients convalescing from acute COVID-19 episodes. A recent study compared 472 patients with COVID-19 history (median time since COVID-19 – 12.0 weeks) with 100 age-matched controls. It was found that the LV systolic and diastolic functions were reduced in patients with prior COVID-19 illness. Those with a more severe first infection had more obvious LV dysfunction, and this dysfunction persisted even after the initial infection had been treated several months ago [Figure 12].
|Figure 12: Bull's eye plot of left ventricular global longitudinal strain in a patient with coronavirus disease myocarditis|
Click here to view
| Conclusion|| |
Cardiac involvement is common in several systemic diseases. In many of these conditions, the evidence of cardiac involvement is only subtle (at least during the initial stages) and may not be recognizable using conventional echocardiography. Strain imaging, with its ability to detect subclinical myocardial dysfunction, is potentially useful in this setting. LV GLS is the most robust strain parameter for this purpose. It is easy to obtain and is highly reproducible. It improves the sensitivity of echocardiography to detect early myocardial involvement in various systemic disorders. The pattern of strain impairment can also provide an etiological diagnosis in certain cases, such as cardiac amyloidosis. In addition, the strong relationship between LV GLS and clinical outcomes makes it a very good prognostic tool. However, more research is needed to determine the actual incremental value and cost-effectiveness of STE in various systemic disorders.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Silman AJ, Pearson JE. Epidemiology and genetics of rheumatoid arthritis. Arthritis Res 2002;4 Suppl 3:S265-72.
Wallberg-Jonsson S, Ohman ML, Dahlqvist SR. Cardiovascular morbidity and mortality in patients with seropositive rheumatoid arthritis in Northern Sweden. J Rheumatol 1997;24:445-51.
del Rincón ID, Williams K, Stern MP, Freeman GL, Escalante A. High incidence of cardiovascular events in a rheumatoid arthritis cohort not explained by traditional cardiac risk factors. Arthritis Rheum 2001;44:2737-45.
Solomon DH, Karlson EW, Rimm EB, Cannuscio CC, Mandl LA, Manson JE, et al.
Cardiovascular morbidity and mortality in women diagnosed with rheumatoid arthritis. Circulation 2003;107:1303-7.
Aviña-Zubieta JA, Choi HK, Sadatsafavi M, Etminan M, Esdaile JM, Lacaille D. Risk of cardiovascular mortality in patients with rheumatoid arthritis: A meta-analysis of observational studies. Arthritis Rheum 2008;59:1690-7.
Naseem M, Samir S, Ibrahim IK, Khedr L, Shahba AA. 2-D speckle-tracking assessment of left and right ventricular function in rheumatoid arthritis patients with and without disease activity. J Saudi Heart Assoc 2019;31:41-9.
Baktir AO, Sarli B, Cebicci MA, Saglam H, Dogan Y, Demirbaş M, et al.
Preclinical impairment of myocardial function in rheumatoid arthritis patients. Detection of myocardial strain by speckle tracking echocardiography. Herz 2015;40:669-74.
Duzen IV, Tabur S, Ozturk S, Savcilioglu MD, Alıc E, Yetisen M, et al.
Assessment of subclinical left ventricular dysfunction with speckle-tracking echocardiography in hyperthyroid and euthyroid Graves' disease and its correlation with serum TIMP-1. Acta Cardiol 2021;76:177-84.
Beaton A, Richards H, Ploutz M, Gaur L, Aliku T, Lwabi P, et al.
Cardiac strain findings in children with latent rheumatic heart disease detected by echocardiographic screening. Cardiol Young 2017;27:1180-5.
Aviña-Zubieta JA, To F, Vostretsova K, De Vera M, Sayre EC, Esdaile JM. Risk of myocardial infarction and stroke in newly diagnosed systemic lupus erythematosus: A general population-based study. Arthritis Care Res (Hoboken) 2017;69:849-56.
Pan SY, Tian HM, Zhu Y, Gu WJ, Zou H, Wu XQ, et al.
Cardiac damage in autoimmune diseases: Target organ involvement that cannot be ignored. Front Immunol 2022;13:1056400. Published online 2022 Nov 22.
Panchal L, Divate S, Vaideeswar P, Pandit SP. Cardiovascular involvement in systemic lupus erythematosus: An autopsy study of 27 patients in India. J Postgrad Med 2006;52:5-10.
] [Full text]
McMahon M, Hahn BH, Skaggs BJ. Systemic lupus erythematosus and cardiovascular disease: Prediction and potential for therapeutic intervention. Expert Rev Clin Immunol 2011;7:227-41.
Di Minno MN, Forte F, Tufano A, Buonauro A, Rossi FW, De Paulis A, et al.
Speckle tracking echocardiography in patients with systemic lupus erythematosus: A meta-analysis. Eur J Intern Med 2020;73:16-22.
Dedeoglu R, Şahin S, Koka A, Öztunç F, Adroviç A, Barut K, et al.
Evaluation of cardiac functions in juvenile systemic lupus erythematosus with two-dimensional speckle tracking echocardiography. Clin Rheumatol 2016;35:1967-75.
Kahan A, Coghlan G, McLaughlin V. Cardiac complications of systemic sclerosis. Rheumatology (Oxford) 2009;48 Suppl 3:iii45-8.
Rodríguez-Reyna TS, Morelos-Guzman M, Hernández-Reyes P, Montero-Duarte K, Martínez-Reyes C, Reyes-Utrera C, et al.
Assessment of myocardial fibrosis and microvascular damage in systemic sclerosis by magnetic resonance imaging and coronary angiotomography. Rheumatology (Oxford) 2015;54:647-54.
Cusmà Piccione M, Zito C, Bagnato G, Oreto G, Di Bella G, Bagnato G, et al.
Role of 2D strain in the early identification of left ventricular dysfunction and in the risk stratification of systemic sclerosis patients. Cardiovasc Ultrasound 2013;11:6.
Spethmann S, Dreger H, Schattke S, Riemekasten G, Borges AC, Baumann G, et al.
Two-dimensional speckle tracking of the left ventricle in patients with systemic sclerosis for an early detection of myocardial involvement. Eur Heart J Cardiovasc Imaging 2012;13:863-70.
Galanello R, Origa R. Beta-thalassemia. Orphanet J Rare Dis 2010;5:11.
Borgna-Pignatti C, Rugolotto S, De Stefano P, Piga A, Di Gregorio F, Gamberini MR, et al.
Survival and disease complications in thalassemia major. Ann N Y Acad Sci 1998;850:227-31.
Oudit GY, Trivieri MG, Khaper N, Liu PP, Backx PH. Role of L-type Ca2+channels in iron transport and iron-overload cardiomyopathy. J Mol Med (Berl) 2006;84:349-64.
Parsaee M, Saedi S, Joghataei P, Azarkeivan A, Alizadeh Sani Z. Value of speckle tracking echocardiography for detection of clinically silent left ventricular dysfunction in patients with β-thalassemia. Hematology 2017;22:554-8.
Di Odoardo LA, Giuditta M, Cassinerio E, Roghi A, Pedrotti P, Vicenzi M, et al.
Myocardial deformation in iron overload cardiomyopathy: Speckle tracking imaging in a beta-thalassemia major population. Intern Emerg Med 2017;12:799-809.
Anderson LJ, Westwood MA, Holden S, Davis B, Prescott E, Wonke B, et al.
Myocardial iron clearance during reversal of siderotic cardiomyopathy with intravenous desferrioxamine: A prospective study using T2* cardiovascular magnetic resonance. Br J Haematol 2004;127:348-55.
Liu D, Hu K, Nordbeck P, Ertl G, Störk S, Weidemann F. Longitudinal strain bull's eye plot patterns in patients with cardiomyopathy and concentric left ventricular hypertrophy. Eur J Med Res 2016;21:21.
Phelan D, Collier P, Thavendiranathan P, Popović ZB, Hanna M, Plana JC, et al.
Relative apical sparing of longitudinal strain using two-dimensional speckle-tracking echocardiography is both sensitive and specific for the diagnosis of cardiac amyloidosis. Heart 2012;98:1442-8.
Iskander J, Kelada P, Rashad L, Massoud D, Afdal P, Abdelmassih AF. Advanced echocardiography techniques: The future stethoscope of systemic diseases. Curr Probl Cardiol 2022;47:100847.
Barros-Gomes S, Williams B, Nhola LF, Grogan M, Maalouf JF, Dispenzieri A, et al.
Prognosis of light chain amyloidosis with preserved LVEF: Added value of 2D speckle-tracking echocardiography to the current prognostic staging system. JACC Cardiovasc Imaging 2017;10:398-407.
Birnie DH, Kandolin R, Nery PB, Kupari M. Cardiac manifestations of sarcoidosis: Diagnosis and management. Eur Heart J 2017;38:2663-70.
Ipek E, Demirelli S, Ermis E, Inci S. Sarcoidosis and the heart: A review of the literature. Intractable Rare Dis Res 2015;4:170-80.
Murtagh G, Laffin LJ, Patel KV, Patel AV, Bonham CA, Yu Z, et al.
Improved detection of myocardial damage in sarcoidosis using longitudinal strain in patients with preserved left ventricular ejection fraction. Echocardiography 2016;33:1344-52.
Di Stefano C, Bruno G, Arciniegas Calle MC, Acharya GA, Fussner LM, Ungprasert P, et al.
Diagnostic and predictive value of speckle tracking echocardiography in cardiac sarcoidosis. BMC Cardiovasc Disord 2020;20:21.
Joyce E, Ninaber MK, Katsanos S, Debonnaire P, Kamperidis V, Bax JJ, et al.
Subclinical left ventricular dysfunction by echocardiographic speckle-tracking strain analysis relates to outcome in sarcoidosis. Eur J Heart Fail 2015;17:51-62.
Quijano-Campos JC, Williams L, Agarwal S, Tweed K, Parker R, Lalvani A, et al.
CASPA (CArdiac Sarcoidosis in PApworth) improving the diagnosis of cardiac involvement in patients with pulmonary sarcoidosis: Protocol for a prospective observational cohort study. BMJ Open Respir Res 2020;7:e000608.
Doğduş M, Kılıç S, Vuruşkan E. Evaluation of subclinical left ventricular dysfunction in overweight people with 3D speckle-tracking echocardiography. Anatol J Cardiol 2019;21:180-6.
Conte L, Fabiani I, Barletta V, Bianchi C, Maria CA, Cucco C, et al.
Early detection of left ventricular dysfunction in diabetes mellitus patients with normal ejection fraction, stratified by BMI: A preliminary speckle tracking echocardiography study. J Cardiovasc Echogr 2013;23:73-80.
van Heerebeek L, Hamdani N, Handoko ML, Falcao-Pires I, Musters RJ, Kupreishvili K, et al.
Diastolic stiffness of the failing diabetic heart: Importance of fibrosis, advanced glycation end products, and myocyte resting tension. Circulation 2008;117:43-51.
MacDonald MR, Petrie MC, Varyani F, Ostergren J, Michelson EL, Young JB, et al.
Impact of diabetes on outcomes in patients with low and preserved ejection fraction heart failure: An analysis of the Candesartan in Heart failure: Assessment of Reduction in Mortality and morbidity (CHARM) programme. Eur Heart J 2008;29:1377-85.
Elgohary AA, Shalaby MA, Mahfouz RA, Mohamed MG. Effect of diabetic duration on left ventricular global longitudinal strain by speckle tracking imaging. Am J Cardiol 2017;119:e6.
Gray N, Picone G, Sloan F, Yashkin A. Relation between BMI and diabetes mellitus and its complications among US older adults. South Med J 2015;108:29-36.
Dong Y, Cui H, Sun L, Wang Y, Li Y, Chang W, et al.
Assessment of left ventricular function in type 2 diabetes mellitus patients with non-alcoholic fatty liver disease using three-dimensional speckle-tracking echocardiography. Anatol J Cardiol 2020;23:41-8.
Bakhoum SW, Habeeb HA, Elebrashy IN, Rizk MN.
Assessment of left ventricular function in young type 1 diabetes mellitus patients by two-dimensional speckle tracking echocardiography: Relation to duration and control of diabetes. Egypt Heart J 2016;68:217-25.
Chawda N, Jain S, Solanki B, Tejani V, Patel P, Sonkar C, et al.
A study of cardiovascular manifestations in hypothyroidism. Ser Endo Diab Met 2022;4:68-77.
Erdogan E, Akkaya M, Bacaksiz A, Tasal A, Ilhan M, Kul S, et al.
Electrocardiographic and echocardiographic evidence of myocardial impairment in patients with overt hypothyroidism. Ann Endocrinol (Paris) 2013;74:477-82.
Zito C, Longobardo L, Citro R, Galderisi M, Oreto L, Carerj ML, et al.
Ten years of 2D longitudinal strain for early myocardial dysfunction detection: A clinical overview. Biomed Res Int 2018;2018:8979407. eCollection 2018.
De Stefano L, Perez de Arenaza D, Yeyati EL, Pietrani M, Kohan A, Falconi M, et al.
Low rate of cardiovascular events in patients with acute myocarditis diagnosed by cardiovascular magnetic resonance. Cardiovasc Diagn Ther 2014;4:64-70.
Di Bella G, Gaeta M, Pingitore A, Oreto G, Zito C, Minutoli F, et al.
Myocardial deformation in acute myocarditis with normal left ventricular wall motion – A cardiac magnetic resonance and 2-dimensional strain echocardiographic study. Circ J 2010;74:1205-13.
Løgstrup BB, Nielsen JM, Kim WY, Poulsen SH. Myocardial oedema in acute myocarditis detected by echocardiographic 2D myocardial deformation analysis. Eur Heart J Cardiovasc Imaging 2016;17:1018-26.
Mansanguan C, Hanboonkunupakarn B, Muangnoicharoen S, Huntrup A, Poolcharoen A, Mansanguan S, et al.
Cardiac evaluation in adults with dengue virus infection by serial echocardiography. BMC Infect Dis 2021;21:940.
Gupta S, Gupta M, Kashyap JR, Arora SK. Early cardiovascular involvement in dengue fever: A prospective study with two-dimensional speckle tracking echocardiography. Trop Doct 2022;52:285-92.
Sengupta SP, Nugurwar A, Jaju R, Khandheria BK. Left ventricular myocardial performance in patients with dengue hemorrhagic fever and thrombocytopenia as assessed by two-dimensional speckle tracking echocardiography. Indian Heart J 2013;65:276-82.
Li Y, Li H, Zhu S, Xie Y, Wang B, He L, et al.
Prognostic value of right ventricular longitudinal strain in patients with COVID-19. JACC Cardiovasc Imaging 2020;13:2287-99.
Baycan OF, Barman HA, Atici A, Tatlisu A, Bolen F, Ergen P, et al.
Evaluation of biventricular function in patients with COVID-19 using speckle tracking echocardiography. Int J Cardiovasc Imaging 2021;37:135-44.
Kaminski A, Payne A, Roemer S, Ignatowski D, Khandheria BK. Answering to the call of critically Ill patients: Limiting sonographer exposure to COVID-19 with focused protocols. J Am Soc Echocardiogr 2020;33:902-3.
De A, Bansal M. Clinical profile and the extent of residual myocardial dysfunction among patients with previous coronavirus disease 2019. Int J Cardiovasc Imaging 2023;39:887-94.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10], [Figure 11], [Figure 12]