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Year : 2022  |  Volume : 32  |  Issue : 2  |  Page : 107-111

Abnormal longitudinal strain reduction of basal left ventricular segments in patients recovered of COVID-19

Private Center of Cardiology, Tucuman, Argentina, South America

Date of Submission15-Dec-2020
Date of Decision05-Feb-2022
Date of Acceptance14-Mar-2022
Date of Web Publication17-Aug-2022

Correspondence Address:
Aldo Prado
Virgen De La Merced 550, Tucumán
South America
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jcecho.jcecho_138_20

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Background: The Severe acute respiratory syndrome coronavirus 2, is the pathogen that causes COVID-19. Cardiovascular (CV) involvement during this infection, has been related to adverse outcomes. Interestingly, some patients may remain symptomatic beyond the first 14 days of disease diagnosis. Although a particular reduction on left ventricular (LV) global longitudinal strain (GLS) in basal segments has been recently described in patients hospitalized with diagnosis of COVID-19, the correlation of these findings with the persistence of symptoms has not been determined. Objectives: The objective of this study is to describe echocardiographic findings in patients recovered from COVID-19 and to determine its association with persistent dyspnea. Methods: Seventy-six patients were analyzed. Forty-six were asymptomatic (group N°1) and 30 referred persistent dyspnea at the time of examination (group N°2), and a cohort of 25 healthy individuals was included as a control group. Total LV GLS, average basal LV GLS, and average mid-apical LV GLS were assessed. Basal-mid-apical index (BMAI) was calculated. A difference in BMAI bigger than 15% between both groups was stablished as cutoff point. Results: Nonsignificative differences on standard echocardiographic measurements were found between the analyzed groups. When compared to the control group, there was nonsignificative reduction on basal LV GLS values in patients with persistent dyspnea. However, BMAI values were bigger than 15% in 70% of patients from group N°2 but in none of the patients from the control group (P = 0.0002). Conclusions: This new index allowed to identify an abnormal relation in LV GLS values between basal and medium-apical segments among patients recovered from COVID-19 and persistent dyspnea.

Keywords: Echocardiography, SARS-CoV-2, strain, subclinical dysfunction

How to cite this article:
Cotella JI, Hasbani J, Hasbani E, Prado A. Abnormal longitudinal strain reduction of basal left ventricular segments in patients recovered of COVID-19. J Cardiovasc Echography 2022;32:107-11

How to cite this URL:
Cotella JI, Hasbani J, Hasbani E, Prado A. Abnormal longitudinal strain reduction of basal left ventricular segments in patients recovered of COVID-19. J Cardiovasc Echography [serial online] 2022 [cited 2022 Sep 29];32:107-11. Available from: https://www.jcecho.org/text.asp?2022/32/2/107/353851

  Background Top

SARS-CoV-2 has generated a huge impact worldwide, especially due to a remarkable increase on morbidity and mortality associated with it. Despite pulmonary involvement has been reported as the most severe and frequent presentation of the COVID-19, multiorgan and cardiovascular (CV) damage have been recently described, having a major role in the prognosis of these patients.[1],[2],[3]

Furthermore, the dosage of serum biomarkers as brain natriuretic peptide and troponins, as well as certain echocardiographic and cardiac magnetic resonance (CMR) findings, have been used to determine the presence of myocardial involvement in these individuals.[2],[4],[5],[6] Although standard echocardiographic techniques and measurements (such as left ventricular ejection fraction [LVEF], left ventricular [LV] volumes, and LV diameters) may allow physicians to assess myocardial involvement in advanced stages of the disease, these may remain normal in subclinical stages. Is in these scenarios, where LV global longitudinal strain (GLS) assessment has shown to be useful as a method for early detection of myocardial involvement in a wide spectrum of CV pathologies.[3],[7],[8],[9]

It has been recently described a reduction in GLS values in LV basal segments among patients hospitalized with SARS-CoV-2 infection, showing a clear association with biomarkers levels increase and worsen prognosis.[6],[10]

Interestingly, despite the high number of patients recovered from COVID-19, an important number of these individuals might still refer to the presence of chest pain or persistent dyspnea, after the initial phase of the disease. The presence of an association between the persistence of symptoms and specific quantitative parameters provided by noninvasive imaging tools, might impact the way we evaluate these patients in our daily clinical practice.

The goal of this study was to identify the presence of abnormal echocardiographic findings among these patients (including LV GLS) and to determine whether there was a correlation with persistent dyspnea at the time of evaluation.

  Methods Top

We conducted a prospective study, including outpatients that were admitted for CV evaluation once COVID-19 infection had resolved. Patients with previous COVID-19 infection (positive SARS-CoV-2 swab testing according to the WHO guidelines), at least 14 days after they were diagnosed, that had good acoustic window a signed the informed consent, were included in this study. Those patients that had at least one of the following criteria were excluded: requirement of mechanical ventilation during COVID-19 hospitalization, and history or actual diagnosis of heart failure, COVID-19-related myocarditis, severe valve disease, atrial fibrillation, implanted pacemaker or cardio-defibrillator, chronic obstructive pulmonary disease or other pulmonary conditions, as well as the presence of obesity or actual tobacco use.

CV exam and medical records were performed to all included patients. Dyspnea severity was graded as mild, moderate, or severe, according to the level of effort needed for the symptom to onset. A complete echocardiographic study was performed (Vivid E9, General Electric Vingmed Ultrasound, Milwaukee, WI) and all measurements were acquired according to the ASE guidelines.[11] Images were obtained on parasternal long-axis, parasternal short-axis, and apical 4–3 and 2 chamber (A4C, A3C, and A2C, respectively) views. LVEF measurement was performed using the biplane Simpson method. Mitral Doppler assessment was performed using pulsed-wave Doppler on an A4C view, and E-wave peak, A-wave peak, deceleration time, and E/A ratio were measured. LV end-diastolic volume (LVEDV, ml), LV end-systolic volume (LVESV, ml), and LA volume (LA Vol, ml), were also assessed on A4C view. Right ventricular (RV) systolic function was assessed using the fractional area change method (RV). Tricuspid annular plane systolic excursion was measured on a dedicated RV focus view in A4C. Pulmonary artery systolic pressure was estimated by the measurement of the tricuspid regurgitation peak gradient associated with the right atrial estimated pressure. LV GLS measurement was performed on images obtained from A4C, A3C, and A2C views. Systolic time was calculated from the identification of aortic valve opening and closure, using continuous-wave Doppler through the aortic valve. Then, total LV GLS, and average GLS of basal and mid-apical segments, were obtained. Basal and mid-apical LV GLS average values were obtained through the summation of the strain values corresponding for each segment, divided by the total number of analyzed segments. Basal-mid-apical index (BMAI) was expressed as a percentage ratio obtained from the difference between the average GLS values of basal and mid-apical segments. This result was then divided by the total LV GLS value, and multiplied by 100, as expressed in the following formula: (Average Basal GLS-Average Mid-Apical GLS/Total LV GLS) × 100.

The study population was divided according to the presence of dyspnea at the time of admission, in two subgroups: those without persistent dyspnea (group N°1) and those with moderate and severe dyspnea (group N°2). A total of 25 healthy patients, without previous CV disease and without COVID-19 diagnosis, were selected as a control group.

Statistical analysis was performed using Mann–Whitney on continuous variables and X2 or Fisher on categorical variables. Reproducibility was determined through the random selection of 15 patients and its further analysis from a second observer. Statistical signification level was considered with a P < 0.05.

  Results Top

From 87 patients included, 11 were excluded for having suboptimal acoustic window or lack of data, remaining 76 patients as the final study population.

The average age was 49 years (min 17 and max 74), and 36 patients were female (48%). Forty-six patients were identified as group 1 and 30 as group 2. Nonsignificant differences on age, gender, blood pressure, heart rate, or body mass index were noted between these groups.

We did not find any significant differences between groups when conventional echocardiographic measurements for LV and RV function were used [Table 1]. Total LV GLS, average GLS of basal and mid-apical segments, and BMAI values are presented in [Table 2] [Figure 1].
Figure 1: Measurements of total LV GLS and average segmental values of LV GLS among the study population and control group. LV GLS = left ventricle global longitudinal strain, Basal LV GLS = Basal left ventricle global longitudinal strain, and Medium apical LV GLS = medium apical left ventricle global longitudinal strain

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Table 1: Echocardiographic findings in COVID-19-infected patients. Distribution according to the study population

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Table 2: Left ventricular global longitudinal strain values and segmental left ventricular global longitudinal strain in patients with persistent dyspnea (Group n=2), without dyspnea (Group n=1) and in the control group

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Twenty percent of patients from group N°2 and 17% of patients from group N°1, shown basal LV GLS below than-18%. Moreover, 63% of patients from group N°2 and 41% of patients from group N°1 showed basal LV GLS values lower than-20% [Figure 2].
Figure 2: Left ventricle global longitudinal strain Bulls-eye from four selected patients (a: control group; b-d: group 2). Different levels of basal left ventricle global longitudinal strain impairment can be observed

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Although these findings in both groups were statistically significant when compared with the healthy control group (P < 0.005), these differences were not statistically significant when compared between them (P = 0.124). We did not notice any statistically significant differences in the LV GLS basal/mid-apical ratio in none of the analyzed groups [Figure 3].
Figure 3: LV GLS analysis in the study groups and control groups. Box plot graphic of patients with persistent dyspnea (group N°2), without dyspnea (group N°1) and the control group. LV GLS = left ventricle global longitudinal strain, Basal LV GLS = Basal left ventricle global longitudinal strain, and Medium apical LV GLS = medium apical left ventricle global longitudinal strain

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Regarding the BMAI, 70% of the patients with persistent dyspnea had BMAI values higher than 15%. This finding was present only in 28% of those patients without persistent symptoms and in nobody from the control group (P < 0.0002). We observed that those patients with BMAI higher than 15%, had a 3-time fold risk (RR 2.9) to present persistent dyspnea when compared to those with BMAI below this cutoff point. The estimated sensitivity for BMAI to identify these patients was 0.7 and the specificity of 0.72 (PPV 0.62, NPV 0.79).

Interobserver correlation for LV GLS measurements showed high levels of agreement with a coefficient of correlation of 0.92 (95% confidence interval 0.87–0.95).

  Discussion Top

Since COVID-19 outbreak, greatest attention has been focused on mortality rates. Due to the broad spectrum of clinical presentations of this disease, the interest to identify factors related to worse prognosis among these patients has been a constant need.[12],[13] In this context, detection of myocardial involvement is paramount, as it has been reported in more than 12% of inpatients hospitalized for COVID-19 infection and in more than 50% of patients that were referred for imaging studies.[14],[15]

Differently to these reports, our study focused on the evaluation of recovered patients that did not have any prior or actual associated conditions. Despite these patients had none or scarce symptoms during the acute stage of the disease, 39% complained of severe persistent dyspnea beyond this period.

Dweck et al. reported CV findings (including LV and RV systolic dysfunction) in 46% of a cohort of previously healthy patients.[15] In our study, all the patients from the study group had normal echocardiographic measurements, without statistically significant differences in echocardiographic measurements when compared with the control group.

It has been largely described, that the speckle tracking technique and its application to GLS analysis, are particularly useful in subclinical scenarios, where the early recognition of myocardial involvement may have relevant prognostic implications.[16],[17] Contrary to recent reports,[6] we noticed that in our cohort, there was no significant reduction on total LV GLS nor on average basal segments (10.0% ± 2.9%).

Probably, the most interesting piece of information provided by our study is the proposal of a novel index that allowed us to analyze the reduction in GLS in LV basal segments in relation to those GLS values observed in medium-apical portions and total LV GLS. Although a basal to apical LV GLS gradient might be present in healthy patients as it was observed in our control group, BMAI values were never bigger than 5% in cohort of healthy patients.

Regarding this observation, we decided to set up the upper limit of normality for BMAI as 3 times higher than the value observed in healthy patients. Interestingly, with this cutoff point, 70% of patients with persistent dyspnea showed BMAI values higher than 15%, while none of the patients on the control group exhibited these values.

Several reasons have been proposed to explain this particular behavior of the GLS in the LV basal segments. It has been reported that these segments might be more stressful and sensitive to inflammatory processes, probably related to a higher concentration of ACE receptors in them.[18] Moreover, recent studies using CMR have reported fibrosis foci and areas of edema in basal and medium LV segments in COVID-19-infected patients.[19] However, it is difficult and potentially misleading to assume that only one single mechanism might be implied.

According to our findings, patients recovered from a SARS-CoV-2 infection, that remain symptomatic after the first 14 days of diagnosis, should be systematically studied using echocardiogram and particularly GLS analysis. BMAI values higher than 15% might be useful among patients with persistent dyspnea during follow, in whom subclinical myocardial involvement might account for these manifestations.

Limitations of this study are related to the small size of the study population, lack of serum biomarkers measurement, and lack of CMR studies to correlate our findings with. As it was not an objective of this study, patients were not followed-up, thus, we are not able to determine if our findings persisted or resolved throughout time.

Although our results about the BMAI are not sufficient to consider it as a risk factor for the persistence of symptoms in patients recovered from COVID-19, they might help to raise interest in developing future investigations about this subject.

  Conclusions Top

Through the proposal of this new index (BMAI), we have identified an abnormal LV GLS pattern based on the correlation between impaired basal segments and preserved medium and apical segments, among patients with persistent dyspnea beyond the 14 days of COVID-19 diagnosis. Further and extensive research is necessary to determine the prognostic impact of these findings.

Ethical clearance

This study was approval by the ethical review committee of the Centro Privado de Cardiología. The study was conducted according to the guidelines of the Declaration of Helsinki. Informed consent was obtained from all subjects involved in the study.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

  References Top

Chen T, Wu D, Chen H, et al. Clinical characteristics of 113 deceased patients with coronavirus disease 2019: retrospective study. BMJ 2020;368:m1091.  Back to cited text no. 1
Shi S, Qin M, Shen B, et al. Association of Cardiac Injury With Mortality in Hospitalized Patients With COVID-19 in Wuhan, China. JAMA Cardiol 2020;5:802-10. doi: 10.1001/jamacardio.2020.0950.  Back to cited text no. 2
Baycan OF, Barman HA, Atici A, et al. Evaluation of biventricular function in patients with COVID-19 using speckle tracking echocardiography. Int J Cardiovasc Imaging 2020:1–10. doi: 10.1007/s10554-020-01968-5.  Back to cited text no. 3
Janus SE, Hajjari J, Karnib M, et al. Prognostic Value of Left Ventricular Global Longitudinal Strain in COVID-19. Am J Cardiol 2020.  Back to cited text no. 4
Stöbe S, Richter S, Seige M, Stehr S, Laufs U, Hagendorff A. Echocardiographic characteristics of patients with SARS-CoV-2 infection. Clin Res Cardiol 2020;109:1549-66. doi: 10.1007/s00392-020-01727-5.  Back to cited text no. 5
Erin Goerlich MD, Nisha A. Gilotra MD, et al. Prominent Longitudinal Strain Reduction of Basal Left Ventricular Segments in Patients with COVID-19. J Card Fail 2020;S1071-9164(20)31436-6.  Back to cited text no. 6
Potter E and Marwick TH. Assessment of Left Ventricular Function by Echocardiography: The Case for Routinely Adding Global Longitudinal Strain to Ejection Fraction. JACC Cardiovasc Imaging 2018;11:260-74.  Back to cited text no. 7
Leitman M, Lysyansky P, Sidenko S et al. Two-dimensional strain - a novel software for real-time quantitative echocardio- graphic assessment of myocardial function. J Am Soc Echocardi Ogr 2004;17:1021–9.  Back to cited text no. 8
Adamo L, Perry A, Novak E, et al. Abnormal global longitudinal strain predicts future deterioration of left ventricular function in heart failure patients with a recovered left ventricular ejection fraction. Circ Heart Fail 2017;10:e003788.  Back to cited text no. 9
Croft LB, Krishnamoorthy P, Ro R, et al. Abnormal left ventricular global longitudinal strain by speckle tracking echocardiography in COVID-19 patients. Future Cardiol 2020. doi: 10.2217/fca-2020-0121.  Back to cited text no. 10
Mitchell C, Rahko PS, Blauwet LA, et al. Guidelines for performing a comprehensive transthoracic echocardiographic examination in adults: recom-mendations from the American Society of Echocardiography. J Am Soc Echocardiogr 2019;32:1–64.  Back to cited text no. 11
Wang D, Hu B, Hu C, et al. Clinical Characteristics of 138 Hospitalized Patients With 2019 Novel Coronavirus-Infected Pneumonia in Wuhan, China. JAMA 2020;323:1061-9. doi: 10.1001/jama.2020.1585.  Back to cited text no. 12
Zhou F, Yu T, Du R, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: A retrospective cohort study. Lancet 2020;395:1054-62. doi: 10.1016/S0140-6736(20)30566-3. Epub 2020. Erratum in: Lancet 2020;395:1038. Erratum in: Lancet 2020;395:1038. PMID: 32171076; PMCID: PMC7270627.  Back to cited text no. 13
Agricola E, Beneduce A, Esposito A, et al. Heart and Lung Multimodality Imaging in COVID-19. JACC Cardiovasc Imaging 2020;13:1792-808. doi: 10.1016/j.jcmg.2020.05.017.  Back to cited text no. 14
Dweck MR, Bularga A, Hahn RT, et al. Global evaluation of echocardiography in patients with COVID-19. Eur Heart J Cardiovasc Imaging 2020;21:949-58. doi: 10.1093/ehjci/jeaa178.  Back to cited text no. 15
Chan J, Hanekom L, Wong C, Leano R, Cho GY, Marwick TH. Differentiation of subendocardial and transmural infarc- tion using two-dimensional strain rate imaging to assess short- axis and long-axis myocardial function. J Am Coll Cardiol 2006;48:6.  Back to cited text no. 16
Shah AM, Claggett B, Sweitzer NK, et al. Prognostic importance of impaired systolic function in heart failure with preserved ejection fraction and the impact of spironolactone. Circulation 2015;132:402-14.  Back to cited text no. 17
Sanfilippo F, Corredor C, Fletcher N, et al. Left ven-tricular systolic function evaluated by strain echocardiography and relationship with mortality in patients with severe sepsis or septic shock: A systematic review and meta-analysis. Crit Care 2018;22:183.  Back to cited text no. 18
Baycan OF, Barman HA, Atici A, et al. Evaluation of biventricular function in patients with COVID-19 using speckle tracking echocardiography. Int J Cardiovasc Imaging 2020:1–10. doi: 10.1007/s10554-020-01968-5.  Back to cited text no. 19


  [Figure 1], [Figure 2], [Figure 3]

  [Table 1], [Table 2]


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