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 Table of Contents  
Year : 2021  |  Volume : 5  |  Issue : 1  |  Page : 10-15

Strain Reversus: A Diagnostic Regional Myocardial Left Ventricular Longitudinal Strain Pattern in Tuberculous Constrictive Pericarditis on Two-Dimensional Speckle Tracking Echocardiography

1 Department of Cardiology, Lokmanya Tilak Municipal Medical College and General Hospital, Mumbai, Maharashtra, India
2 Department of Cardiology, Cardiology Clinic and Jupiter Hospital, Thane, Maharashtra, India

Date of Submission13-Aug-2020
Date of Decision11-Oct-2020
Date of Acceptance14-Oct-2020
Date of Web Publication27-Feb-2021

Correspondence Address:
Dr. Milind S Phadke
Department of Cardiology, Lokmanya Tilak Municipal Medical College and General Hospital, Dr. Babasaheb Ambedkar Road, Sion (West), Mumbai - 400 022, Maharashtra
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jiae.jiae_43_20

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Background: Tuberculous constrictive pericarditis (CP) is a chronic inflammatory disease by Mycobacterium tuberculosis affecting the pericardium, occurring mainly in developing nations. The aim of this study was to evaluate left atrial (LA) and left ventricular (LV) myocardial mechanics in tuberculous CP using standard two-dimensional (2D) echocardiography and speckle tracking echocardiography (STE). Methods: A prospective observational echocardiographic study of 30 subjects was performed: 15 patients with tuberculous CP and 15 controls. 2D echocardiography, color Doppler imaging, and tissue Doppler imaging (TDI) were performed along with STE to evaluate the LV and LA mechanics. Results: We found that the global circumferential strain (GCS, P = 0.002) and the global longitudinal strain (P = 0.02) were significantly reduced in patients with CP compared with controls. The longitudinal lateral wall strain was significantly reduced (P = 0.001) in CP patients, whereas longitudinal septal strain was not reduced significantly (P = 0.18) in CP patients compared with controls. The longitudinal lateral strain was significantly reduced as compared to the longitudinal septal strain (P = 0.001) within the CP group (strain reversus). Annulus reversus (medial early diastolic mitral annular velocity [e'] > lateral e') by TDI was observed in 11 cases out of 15 in tuberculous CP group, whereas strain reversus (septal strain > lateral strain) was seen in all cases of CP group. The LA reservoir strain showed a statistically significant reduction in CP patients (P = 0.001) compared to controls. Conclusions: “Strain reversus” and reduced GCS are characteristic imaging findings on STE in patients with tuberculous CP and may provide an additional parameter to conventional echocardiography in the diagnosis of tuberculous CP.

Keywords: Global circumferential strain, global longitudinal strain, left atrial reservoir strain, speckle tracking echocardiography, strain reversus, tuberculous constrictive pericarditis

How to cite this article:
Deshpande MS, Phadke MS, Bhatia VP, Mankame PR, Burkule NJ, Khan MT, Mahajan AU, Nathani PJ. Strain Reversus: A Diagnostic Regional Myocardial Left Ventricular Longitudinal Strain Pattern in Tuberculous Constrictive Pericarditis on Two-Dimensional Speckle Tracking Echocardiography. J Indian Acad Echocardiogr Cardiovasc Imaging 2021;5:10-5

How to cite this URL:
Deshpande MS, Phadke MS, Bhatia VP, Mankame PR, Burkule NJ, Khan MT, Mahajan AU, Nathani PJ. Strain Reversus: A Diagnostic Regional Myocardial Left Ventricular Longitudinal Strain Pattern in Tuberculous Constrictive Pericarditis on Two-Dimensional Speckle Tracking Echocardiography. J Indian Acad Echocardiogr Cardiovasc Imaging [serial online] 2021 [cited 2021 Oct 17];5:10-5. Available from: https://www.jiaecho.org/text.asp?2021/5/1/10/310494

  Introduction Top

Constrictive pericarditis (CP) represents the end-stage manifestation of a chronic inflammatory process affecting the pericardium, leading to the development of fibrosis, calcification, and adhesion of parietal and visceral pericardium.[1] In developing countries, tuberculosis remains the most common cause of CP.[2] When pericardial adhesions are present, the normal independent motion of visceral and parietal pericardium is lost and tethering occurs.[3] The demonstration of this pericardial tethering by 2-dimensional (2D) echocardiography can be difficult. Myocardial strain imaging is a valuable addition to visual impression or tissue Doppler imaging (TDI). Global circumferential strain (GCS) is classically reduced in CP due to peripheral tethering of pericardium, and global longitudinal strain (GLS) is usually normal in these patients.[4],[5] Left ventricle (LV) can demonstrate diminished negative peak systolic strain in the lateral free wall as compared to septal peak systolic strain, a phenomenon which has been described as “strain reversus.”[4] It is known that abnormalities of the left atrium (LA) are associated with diastolic dysfunction of the LV and impaired LV filling; however, the pathophysiology of the LA dysfunction in patients with CP is not completely understood. The aims of this study were (1) to evaluate LA and LV myocardial mechanics in patients with tuberculous CP using speckle tracking echocardiography (STE), (2) to identify the prevalence and utility of characteristic regional and global patterns of LV and LA myocardial mechanics and (3) to compare the prevalence and utility of STE values and indices with the conventional 2D echo, spectral Doppler, TDI values and indices (e.g., LA volume index [LAVI], and early diastolic transmitral flow velocity/early diastolic mitral annular velocity [E/e'] ratio, and annulus reversus). To the best of our knowledge, this is the first study to assess these echocardiographic parameters in tuberculous CP.

  Methods Top

Study population and design

This was a single-center prospective observational study conducted at a tertiary care hospital over one year period (January 1, 2019, to December 31, 2019), and all patients presenting to the hospital with tuberculous CP during this period were included in the study. Patients with any other etiology for reduced LV and LA strain including dilated cardiomyopathy, coronary artery disease with regional wall motion abnormalities, atrial fibrillation, and structural heart disease were excluded from the study. None of the case group had comorbidities such as diabetes and hypertension. Patients with poor transthoracic echo window were also excluded. Posttreatment and follow-up patients of tuberculous CP were excluded from this study, and only de novo patients were selected for inclusion. After application of the inclusion and exclusion criteria, a total of 15 patients with tuberculous CP were included in this study. Echocardiographic images of 15 healthy subjects who were matched for age, sex, and ejection fraction (EF) were selected as controls. Standard 2D echocardiography and Doppler studies along with TDI was done for baseline LVEF, and for demonstration, all the classical echocardiographic findings of CP. The diagnosis of tuberculosis was confirmed either by sputum microscopy, pericardial fluid microscopy, or accessory diagnostic features of tuberculosis on high-resolution computed tomography of the thorax (such as necrotic lymph nodes, pericardial thickening, pulmonary cavities, and bronchiolitis). Institutional ethics committee approval was obtained and informed consent was taken from each participant.

Echocardiographic methods

All patients underwent standard echocardiographic examination using a 1–5 MHz X5-1 2D transducer by a Philips EPIQ 7C ultrasound machine (Philips Healthcare, Andover, MA 01810, USA). All 2D and strain echocardiography studies were performed by a single operator with 10 years' experience in 2D echocardiography on the same machine to avoid interobserver and interdevice variability and discrepancies in the techniques. A standard 2D echocardiographic examination, color Doppler studies, and TDI was done and the quantitative analysis of heart was performed according to the societal recommendations. It included calculations of LA dimensions, LV end diastolic diameter, LV end systolic diameter, EF by Simpson's method, demonstration of pericardial thickening [Figure 1]a, septal bounce, inferior vena cava (IVC) dilatation [Figure 1]b and collapsibility, exaggerated respiratory variation of atrioventricular (AV) valve inflow velocities [Figure 1]c, and increased hepatic Doppler flow reversal [Figure 1]d during expiration which all were used to reasonably confirm the presence of constrictive physiology. The peak early diastolic mitral annular velocities (e') were assessed by pulsed wave tissue Doppler at the septal and lateral mitral annulus and the presence of annulus reversus, i.e., medial e' > lateral e' [Figure 2]a and [Figure 2]b, was demonstrated. We calculated the mean LAVI by biplane area length method divided by the body surface area (BSA).[6] LA size was measured at the end-ventricular systole (maximum LA size). In the area-length formula, the length was measured in both the four- and two-chamber views, and the shortest of these two length (L) measurements was used in the formula. LA area was measured by planimetry in both four-chamber (A1) and two-chamber views (A2), and LAVI was calculated using the formula:
Figure 1: Two-dimensional echocardiography, color Doppler imaging, and tissue Doppler imaging findings in constrictive pericarditis. (a) Parasternal long-axis view showing pericardial thickening (green arrow). (b) Mitral valve in-flow velocity showing significant respiratory variation in inspiration (orange arrow) and expiration (green arrow). (c) Subcostal view showing congested inferior vena cava (orange arrow). (d) Hepatic vein diastolic reversal with expiration. Orange arrow indicating reverse flow and green arrow indicating forward flow

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Figure 2: Tissue Doppler imaging showing annulus reversus (i.e early diastolic mitral annular velcoity [e'] at medial annulus greater than that at lateral mitral annulus) in a patient with constrictive pericarditis. (a) Tissue Doppler imaging measurement of lateral e' (orange arrow); (b) Measurement of medial e' (green arrow).

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LAVI = LA volume/BSA

where LA volume = 0.85 × A1 × A2/L [Figure 3].
Figure 3: Two-dimensional echocardiographic images showing calculation of left atrial volume by area–length method. (a) Apical four-chamber view showing area A1 (green arrow) and length L1 (orange arrow). (b) Apical two-chamber view showing area A2 (green arrow) and length L2 (orange arrow). The formula used for LA volume calculation is LA volume = 0.85 × A1 × A2/L. The shortest among L1 and L2 (i.e., L) is used in the formula

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The ratio of average peak early transmitral velocity (E) to e', i.e., the E/e' ratio, was also calculated – this ratio correlates with LV filling pressure. LV relaxation as measured by e' is relatively independent of filling pressures. The phenomena of annulus paradoxus, i.e., only a mild rise in E/e' ratio despite an evidence of elevated LV filling pressure as indicated by LAVI was looked for in tuberculous CP patients.[7]

2D STE was performed on the same machine and analyzed as per the standard protocols. The machine was well equipped with the commercially available software (aCMQ Cardiac Analysis, Philips) for the quantification of 2D-derived GLS, GCS, and LA reservoir strain. For LV GLS and GCS, standard 2D gray scale images of the LV were obtained from the apical two-, three-, and four-chamber views as well as the parasternal short-axis views at the basal, mid, and apical level. The software then automatically divided the entire circumference of the LV into equal segments and generated myocardial strain curves by frame-by-frame tracking of the natural acoustic markers throughout the cardiac cycle. From these curves, peak-systolic strain curves were recorded for each of the myocardial segments and averaged to derive a software calculated global value (GLS and GCS) which was used for the analysis.[8] By using dynamic 2D ultrasound, images of three cardiac cycles from apical four-chamber views were acquired and analyzed using customized software aCMQ Cardiac Analysis, Philips.

To evaluate the impact of CP on cardiac mechanics, the LV was divided into nonseptal (i.e., lateral longitudinal strain) and septal (i.e., septal longitudinal strain) regions. Septal longitudinal strain was calculated by averaging the six septal segments (system generated), and lateral longitudinal strain was determined by averaging the 12 nonseptal segments in the three long-axis views.[9] For LA reservoir strain, in the apical four-chamber and two-chamber views, the endocardial boundary of the LA was delineated manually, and then, the software automatically drew the epicardial boundary. The regions of interest were then manually adjusted to match the epicardial and endocardial boundaries. The automatically generated region of interest was divided into six segments, and a software generated curve of LA strain was derived with the highest point on the curve being taken as peak LA reservoir strain.[10] The reference values of LA strain were considered as discussed in the study by Nemes et al.[11]


Statistical analysis was performed using Statistical Package for the Social Sciences Version 20 (IBM, Chicago, Illinois, United States). Frequency tables were calculated. Paired sample's t-tests were used to analyze differences between CP group and control group. A P < 0.05 was considered statistically significant.

  Results Top

The demographic and echocardiography characteristics are shown in [Table 1]. There were no significant differences in age and gender between patients with CP and controls. All the 15 cases in CP group had the classical findings on 2D echocardiography such as increased hepatic Doppler flow reversal during expiration, dilated IVC, septal bounce, and thickened pericardium. One of the patients in CP group had associated pericardial effusion. There were two cases of CP group with EF less than 45% by Simpson's biplanar method. Both subjects were of a young age (less than 35 years), and did not have any co-morbidities for coronary artery disease. Neither of them had any electrocardiography changes suggestive of coronary artery disease nor had dilated cardiac chambers to suggest any long-standing cardiomyopathy. Both had preserved LV wall thickness.
Table 1: Demographic and echocardiographic details of control group and constrictive pericarditis group

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In the CP group, the phenomenon of annulus reversus (medial e' value greater than lateral e' value) was seen in 11 out of 15 patients on TDI [Figure 2]a and [Figure 2]b but was absent in 4 out of 15 cases in whom lateral e' was greater than medial e' [Figure 4]a and [Figure 4]b. However, when assessed by strain imaging, strain reversus (i.e., lateral longitudinal strain reduced more than medial longitudinal strain) [Figure 4]c was seen in all 15 patients.
Figure 4: Tissue Doppler imaging and strain imaging findings in a patient with constrictive pericarditis showing a discrepancy between tissue Doppler imaging and strain imaging. (a),(b) The medial tissue Doppler imaging (green arrow) is not greater than lateral tissue Doppler imaging (orange arrow) indicating that annulus reversus is absent. Medial tissue Doppler imaging = 14 cm/s and lateral tissue Doppler imaging = 18 cm/s. (c) Echocardiography bulls eye map in the same patient showing regional variation with relative preservation of septal strain and reduction in the lateral strain (strain reversus)

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  Discussion Top

Tuberculous constrictive pericarditis

Tuberculosis is a granulomatous infectious disease caused by Mycobacterium tuberculosis prevalent worldwide, particularly common in parts of Asia and Sub-Saharan Africa.[8] Tuberculosis can affect the cardiovascular system in the form of both myocarditis and pericarditis. Long-standing pericarditis causes pericardial constriction due to chronic granulomatous pericardial inflammation, called CP. The thickened, fibrotic pericardium forms a noncompliant shell around the heart. This shell prevents the heart from expanding when blood enters it, thereby impairing the diastolic filling. Disuse atrophy of subepicardial myocardium is caused by gradual pericardial restriction. Penetration of the pathologic processes (including mycobacteria) to the myocardium may result in myocarditis and myocardial fibrosis, which is particularly more common in tuberculous CP.[12]

Echocardiography in tuberculous constrictive pericarditis

Conventional echocardiographic parameters such as EF and visual assessment of regional wall abnormalities may not be able to identify regional and global LV dysfunction in patients with CP due to the regional and localized nature of involvement. Previous studies show decreased GCS in CP patients compared with healthy controls, while GLS value show less reduction.[5],[9],[13],[14],[15],[16] It is postulated that tethering of pericardium in CP patients predominantly affects subepicardial function, thus altering LV circumferential mechanics more as compared to longitudinal mechanics.[5] Impaired GLS is associated with transmural myocardial injury. Our study showed a significant reduction in both GCS [Figure 5] and GLS [Figure 6] compared to the control population, which could be explained by tuberculous myocardial involvement in addition to changes in regional mechanics of the LV caused by pericardial tethering. The CP group had a relatively preserved EF by Simpson's biplanar method assessment, as compared to measurement of EF by strain imaging, indicating that 2D strain imaging could provide more comprehensive information about heart mechanics and be able to detect subclinical myocardial dysfunction at an earlier stage as compared with conventional imaging modalities in tuberculous CP.
Figure 5: Global circumferential strain by speckle tracking echocardiography. (a) Global circumferential strain bulls eye map in control/normal subject showing no regional variation (global circumferential strain = −27.5%). (b) Global circumferential strain bulls eye map in constrictive pericarditis patient showing marked reduction (global circumferential strain = −17.4%) as compared to normal

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Figure 6: Global longitudinal strain by speckle tracking echocardiography. (a) Global longitudinal strain bulls eye map in control/normal subject showing no regional variation. (b) Global longitudinal strain bulls eye map in constrictive pericarditis patient showing marked regional variation with relative preservation of septal strain and reduction in the lateral strain

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The CP group had the lateral strain declined more as compared to septal strain. Perimyocardial adhesions and tethering at the LV free wall cause difference between septal and free wall strain. Many previous studies found similar results that strain was depressed in the LV anterolateral wall but preserved in the LV septal wall.[6],[9],[13],[16],[17] It was observed in our study that the phenomenon of annulus reversus (medial e' > lateral e') was seen only in 11 out of 15 cases whereas strain reversus (mean septal strain > mean lateral strain) was seen in all 15 cases in CP group. A potential explanation for the absence of annulus reversus and not of strain reversus in 4 out of 15 patients could be that the AV groove, where mitral e' is measured, was less affected by CP due to patchy nature of the disease. On the other hand, strain values which represent the function of entire free wall and septal wall were more affected explaining the presence of strain reversus in all 15 cases of CP. Although the sample size was small, this finding can have potentially significant implications if it can be reproduced in larger studies, namely that strain reversus could possibly be an additional and important parameter to annulus reversus in detecting changes in regional myocardial mechanics in CP patients.

In patients with CP, because of the pericardial restriction of the LV, the LA pressure rises to maintain adequate LV filling pressure, and the increased atrial wall tension causes dilatation of the chamber and stretching of the atrial myocardium. In our study, the LA reservoir strain was decreased in CP patients compared with the control group [Figure 7], indicating that the passive dilatation of LA was impaired during atrial filling phase. This was also supported by elevated LA volumes as measured by LAVI, found in the CP group. The E/e' ratio in our study was mildly (but statistically significantly) raised in CP compared with controls despite a chronically elevated LV filling pressures (indicated by high LAVI and altered LA reservoir strain) consistent with annulus paradoxus.[18]
Figure 7: Reservoir left atrial strain by speckle tracking echocardiography. (a) Left atrial strain in control subject showing normal curve (white dotted line) and normal peak left atrial strain (orange arrow). (b) Left atrial strain in constrictive pericarditis patient showing flattened curve (white dotted line) and abnormal peak left atrial strain (green arrow)

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Study limitations

Our study had a few limitations, including small sample size as a result of the rarity of the disease. Large-scale studies are needed to prove additional value of strain imaging in cases of CP. The clinical implication of reduced reservoir LA strain needs to be studied further. In future studies, a long-term and posttreatment follow-up and analysis of strain will be required to assess the prognostic value of strain imaging for tuberculous CP patients.

Implications for practice

To the best of our knowledge, there is no prior study in medical literature to assess STE-derived strain parameters in tuberculous CP. Comprehensive echocardiography is a readily available, cost-effective tool to assess patients with CP and can provide diagnostic and mechanistic information in these patients. Speckle tracking imaging in CP can be a complementary, additional parameter for the diagnosis and understanding the pathophysiology of CP better. It may also prove to be a convenient imaging modality for prognosis and recovery for posttreatment monitoring of patients with tuberculous CP.

  Conclusions Top

Regional myocardial STE helps in understanding myocardial mechanics in patients with CP and shows characteristic imaging findings which help in diagnosis of tuberculous CP. “Strain reversus” and reduced GCS are intriguing imaging findings on STE in patients with tuberculous CP. Strain imaging can be regarded complementary to conventional echocardiography in diagnosis of tuberculous CP and in some cases may prove to be of additional value in the assessment of global and regional myocardial mechanics in these patients.

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Conflicts of interest

There are no conflicts of interest.

  References Top

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7]

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