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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 33  |  Issue : 1  |  Page : 138-151

Left ventricular functions in patients with beta-thalassemia major: a speckle tracking imaging study


1 Department of Pediatrics, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Cardiovascular Medicine, Faculty of Medicine, Menoufia University, Menoufia, Egypt
3 Department of Pediatric, Benha Specialized Children Hospital, Benha, Egypt

Date of Submission29-Nov-2016
Date of Decision31-Jan-2017
Date of Acceptance03-Feb-2017
Date of Web Publication25-Mar-2020

Correspondence Address:
Amir I Lashin
Sabry Abo Alam Street, Shebin El-Kom, Menoufia Governorate
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_639_16

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  Abstract 

Objectives
To assess left ventricular (LV) functions in patients with beta-thalassemia major (β-TM) on regular blood transfusion (without cardiac manifestations) by speckle tracking echocardiography and correlate the findings with serum ferritin levels of these patients.
Background
Patients with β-TM have extravasal hemolysis and ineffective erythropoiesis, resulting in severe anemia. Thus, they require regular blood transfusions, which results in iron overload. Patients with thalassemia absorb more iron than normal individuals. Iron overload results in iron deposition in a variety of parenchymal tissues including the heart leading to ventricular systolic and diastolic dysfunctions. Iron-mediated cardiomyopathy is the main cause of death in patients with thalassemia. Early detection of cardiac abnormalities is important as aggressive chelation therapy may improve prognosis in these patients.
Patients and methods
A total of 50 patients with β-TM on regular blood transfusion for more than or equal to 4 years and 25 sex-matched and age-matched controls were included. The laboratory parameters measured were blood hemoglobin and ferritin, which were measured 2 h before doing echocardiography with Doppler imaging and speckle tracking analysis.
Results
There were no significant differences in LV ejection fraction and fractional shortening between the groups by conventional echocardiography. However, by using speckle tracking echocardiography, systolic strain and strain rate of the LV walls were significantly lower in patients with thalassemia.
Conclusion
Patients with thalassemia have regional systolic dysfunction in the LV walls, even if they do not have overt heart failure. Strain imaging is more helpful than conventional echocardiography in early detection of LV systolic dysfunction in patients with thalassemia.

Keywords: beta-thalassemia major, speckle tracking echocardiography, strain and strain rate


How to cite this article:
Khattab AA, Elnoamany MF, Ahmed NF, Elian DM, Lashin AI. Left ventricular functions in patients with beta-thalassemia major: a speckle tracking imaging study. Menoufia Med J 2020;33:138-51

How to cite this URL:
Khattab AA, Elnoamany MF, Ahmed NF, Elian DM, Lashin AI. Left ventricular functions in patients with beta-thalassemia major: a speckle tracking imaging study. Menoufia Med J [serial online] 2020 [cited 2020 Aug 15];33:138-51. Available from: http://www.mmj.eg.net/text.asp?2020/33/1/138/281317




  Introduction Top


Beta-thalassemia major (β-TM) is a hemoglobinopathy that produces severe anemia owing to ineffective erythropoiesis[1]. In these patients, excessive iron exposure and secondary iron overload ensues primarily because of repeated blood transfusions as well as increased gastrointestinal iron absorption in the setting of ineffective erythropoiesis. A reduction in childhood mortality from infection and malnutrition coupled with increased use of chronic blood transfusions have led to a growing incidence of iron overload in patients with thalassemia. The early diagnosis of iron-overload cardiac involvements is important while the cardiac dysfunction is reversible, to initiate effective therapy before the onset of overt heart failure[2].

Patients with TM remain asymptomatic with normal left ventricular (LV) function for a long period of time. Early identification of ventricular dysfunction, before the appearance of symptoms, can alter the prognosis of these patients, because it reinforces the need to optimize the therapy with chelators[3].

The aim of our study is to assess LV functions in patients with β-TM (without cardiac manifestations) by speckle tracking echocardiography and correlate the findings with serum ferritin levels of these patients.


  Patients and Methods Top


The present study was carried out on children with β-TM on regular blood transfusion in Hematology Unit, Pediatric Department, Menoufia University Hospital, who met the inclusion criteria during the period from April 2015 to April 2016. The children included were 75 divided into two groups. Group 1 included 50 patients, comprising 22 girls and 28 boys. These children were receiving regular blood transfusion every 2–4 weeks and were on chelation therapy. Their ages ranged from 5 to 18 years (mean, 9.84 years). Group 2 included apparently healthy 25 children, age and sex matched, as a control group.

A child was eligible to be included in this test if he/she was a β-TM patient, 5 years or older, and on regular blood transfusion for more than 4 years.

The child was excluded if he/she was less than 5 years old; had history of chronic diseases, for example, diabetes mellitus, hypertension, renal failure, and rheumatic heart disease; had sustained atrial or ventricular arrhythmias; had congenital heart disease; had heart failure; had valvular disease; or had pulmonary hypertension.

A written consent was obtained from the parents on behalf of their children. The ethics committee of faculty of medicine, Menoufia University, approved this study.

All patients and controls were subjected to complete history taking with stress on age, sex, age at first blood transfusion, number of transfusions per month, onset of chelation therapy, compliance to chelation therapy, and type of chelation. Moreover, it included inquiry about splenectomy, consanguinity, and family history of beta-thalassemia.

All patients and controls were subjected to thorough clinical examination, stressing on weight, height, thalassemic features (in the form of large head, frontal and parietal bossing, depressed nasal bridge, and protruded maxilla), leg ulcers, presence of splenomegaly, hepatomegaly, and lymphadenopathy.

Full cardiac examination was done to assess signs of heart failure like gallop rhythm, cardiomegaly, congested hepatomegaly, and arrhythmia by inspection, palpation, percussion, and auscultation.

Studied parameters include complete blood picture and serum ferritin within 2 h before echocardiography, ECG to detect arrhythmia or conduction disorders, and standard echocardiography with Doppler studies, using a GE vivid 9 machine (Horten, Norway); all participants were examined in the left lateral decubitus position according to the recommendations of the American Society of Echocardiography[4] and speckle tracking echocardiography.

Speckle tracking echocardiography has recently emerged as a quantitative ultrasound technique for accurately evaluating myocardial function by analyzing the motion of speckles identified on routine two-dimensional sonograms. It provides non-Doppler, angle-independent, and objective quantification of myocardial deformation and LV systolic and diastolic dynamics. By tracking the displacement of the speckles during the cardiac cycle, strain and the strain rate (SR) can be rapidly measured offline after adequate image acquisition. Speckle tracking echocardiography is a new noninvasive ultrasound imaging technique that allows for an objective and quantitative evaluation of global and regional myocardial function independently from the angle of insonation and from cardiac translational movements. Speckle tracking echocardiography is based on an analysis of the spatial dislocation (referred to as tracking) of speckles (defined as spots generated by the interaction between the ultrasound beam and myocardial fibers) on routine two-dimensional sonograms. Before the introduction of this sophisticated echocardiographic technique, only tagged MRI had enabled an accurate analysis of the several deformation components that characterize myocardial dynamics. Although tagged MRI may be considered the reference standard in this area of study, its routine use is limited by its high costs, poor availability, relative complexity of acquisitions, and time-consuming image analysis[5].

The average value of strain at each level (basal, middle, and apical) and global strain obtained from averaging the strain values of 18 LV segments was calculated.

The average value of peak systolic SR at each level (basal, middle, and apical) and global systolic SR obtained from averaging the peak systolic SR values of 18 LV segments was calculated.

The average value of peak early diastolic SR at each level (basal, middle, and apical) and global early diastolic SR obtained from averaging the peak early diastolic SR values of 18 LV segments was calculated.

The average value of peak late diastolic SR at each level (basal, middle, and apical) and global late diastolic SR obtained from averaging the peak late diastolic SR values of 18 LV segments was calculated.

Statistical analysis

The data collected were tabulated and analyzed by statistical package for the social sciences (SPSS, version 20; SPSS Inc., Chicago, Illinois, USA) software, on an IBM compatible computer.

The results were expressed as range, mean ± SD. The χ2 and Student t test were used for analysis. χ2 test was used to study association between two qualitative variables. Student t test is a test of significance used for comparison between two groups having quantitative variables.

Relation between different numerical variables was tested. P value less than or equal to 0.05 was considered significant and less than or equal to 0.001 was considered highly significant.

Pearson's correlation coefficient test is used to detect association between two quantitative variables.


  Results Top


For personal data, there was no significant difference in age and sex distribution among patient and control groups (P > 0.05).

As for the anthropometric measurements, there was no significant difference regarding weight, but there was statistically significant difference regarding height, being lower in the patient group than in the control group (P < 0.001).

Regarding serum ferritin level and hemoglobin, there were statistically highly significant differences between the group of thalassemic patients and the control. It was found that, the group of thalassemic patients was significantly higher than the control (P < 0.001) regarding serum ferritin level, but significantly lower than the control group regarding hemoglobin level [Table 1] and [Figure 1], [Figure 2].
Table 1: Comparison between the study groups regarding serum ferritin and hemoglobin levels

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Figure 1: Serum ferritin level among selected patients and controls.

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Figure 2: Hemoglobin level among selected patients and controls.

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As for the conventional echocardiographic parameters, there was a statistically nonsignificant difference between the group of thalassemic patients and the control regarding ejection fraction (EF), fractional shortening (FS), left ventricular end diastolic dimension (LVEDD), aorta, and tricuspid annular plane systolic excursion. However, it was found that the group of thalassemic patients was significantly higher than the control (P < 0.05) regarding left ventricular end systolic dimension (LVESD) and left atrium.

Moreover, there was a highly significant difference of interventricular septal thickness in diastole, LV posterior wall thickness in diastole, left atrium/aorta, LV mass, and left ventricular mass index (LVMI) (P < 0.001), as shown in [Table 2] and [Figure 3], [Figure 4], [Figure 5].
Table 2: Comparison between the study groups by conventional echocardiography

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Figure 3: Comparison between the study groups regarding IVSD, PWD, LVESD, and LVEDD. IVSD, interventricular septum in diastole; LVEDD, left ventricular end diastolic dimension; LVESD, left ventricular end systolic dimension; PWD, posterior wall thickness in diastole.

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Figure 4: Comparison between both groups regarding LA, AO, and LA/AO. AO, aorta; LA, left atrium.

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Figure 5: Comparison between both groups regarding LVM and LVMI. LVM, left ventricular mass; LVMI, left ventricular mass index.

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As for tissue Doppler data, it was found that thalassemic group was significantly higher than control group regarding peak A velocity and E/A ratio (P < 0.001). Moreover, by comparing both groups, it was found that thalassemic group was significantly higher than control group regarding E/e' lateral and E/e' septal, as shown in [Table 3] and [Figure 6], [Figure 7].
Table 3: Comparison between the study groups regarding mitral Doppler inflow and mitral annular TDI parameters

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Figure 6: Comparison between both groups regarding E, A, and E/A ratio.

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Figure 7: Comparison between both groups regarding E/e' lateral and septal.

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By speckle tracking analysis, it was found that there was a statistically highly significant difference between the thalassemic group and the control with impairment of the global LV longitudinal systolic strain in the thalassemic group in comparison with the control [Table 4] and [Figure 8], [Figure 9], [Figure 10].
Table 4: Comparison between the study groups regarding left ventricular peak systolic longitudinal strain of all analyzed myocardial segments

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Figure 8: Speckle tracking echocardiographic measurements of longitudinal strain in the apical four-chamber view in a thalassemic patient.

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Figure 9: Speckle tracking echocardiographic measurements of longitudinal strain in the apical two-chamber view in a thalassemic patient.

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Figure 10: Speckle tracking echocardiographic measurements of longitudinal strain in the apical three.chamber view in a thalassemic patient.

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Moreover, global LV longitudinal systolic SR and early diastolic SR were reduced in the thalassemic group in comparison with the control (P < 0.05), as shown in [Table 5], [Table 6], [Table 7].
Table 5: Comparison between both groups regarding left ventricular strain rate at peak systole (s-1) of all analyzed myocardial segments

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Table 6: Comparison between both groups regarding left ventricular early diastolic strain rate (s-1) of all analyzed myocardial segments

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Table 7: Comparison between both groups regarding left ventricular late diastolic strain rate (s-1) of all analyzed myocardial segments

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Moreover, in our study, there was a highly significant negative correlation between serum ferritin level and global LV late diastolic SR in thalassemic group (P < 0.001) [Figure 11]. A highly significant positive correlation was present between serum ferritin level and LVMI in thalassemic group [Figure 12]. Moreover, there was a significant negative correlation between serum ferritin level and LVESD, LVEDD, and global LV systolic strain [Table 8] and [Figure 13], [Figure 14], [Figure 15].
Table 8: The correlation between serum ferritin level and left ventricular end systolic dimension, left ventricular end diastolic dimension, ejection fraction, left atrium/aorta, left ventricular mass index, E/A, E/e' lateral, E/e' septal, global left ventricular peak systolic strain, global left ventricular systolic strain rate, global left ventricular early diastolic strain rate and global left ventricular late diastolic strain rate

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Figure 11: The correlation between serum ferritin level and LV SRa s-1 in thalassemic group. LV, left ventricular; SR, strain rate.

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Figure 12: The correlation between serum ferritin level and LVMI in thalassemic group. LVMI, left ventricular mass index.

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Figure 13: The correlation between serum ferritin level and LVESD in thalassemic group. LVESD, left ventricular end systolic dimension.

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Figure 14: The correlation between serum ferritin level and LVEDD in thalassemic group. LVEDD, left ventricular end diastolic dimension.

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Figure 15: The correlation between serum ferritin level and LV Esys% in thalassemic group.

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  Discussion Top


Iron-mediated cardiomyopathy is the main cause of death in patients with β-TM. Anemia causes enlargement of the ventricular chambers, increased cardiac output, and reduced total vascular resistance. Cardiac iron overload owing to long-term transfusion causes further chamber dilation, decreased contractility, and arrhythmia. Many patients with thalassemia remain asymptomatic until decompensation occurs. However, once overt heart failure is present, only 50% of patients survive. Therefore, early recognition of patients with thalassemia at risk of heart failure is needed. The conventional echocardiographic parameters such as LVEF or LVFS are not sensitive enough to detect subclinical cardiac dysfunction. Global ventricular function and exercise capacity may remain normal until late in the disease process[6].

Patients with thalassemia have early regional systolic and/or diastolic dysfunction even if they do not have overt heart failure, thus the necessity of precocious diagnosis of cardiac involvement[7].

Recent tissue Doppler imaging modalities including tissue velocity imaging and strain imaging (SI) have proven to be very sensitive for the assessment of myocardial dysfunction[6].

Assessment of the LV systolic and diastolic function in the two studied groups has been based on parameters obtained from transthoracic echocardiography.

In the present study, there was no significant difference between both groups regarding age, sex, and weight, but there was a significant difference regarding the mean value of height between both groups. This came in agreement with the study of Merchant et al.[8].

By comparing the two groups regarding serum ferritin level, there was a statistically significant difference between the group of thalassemic patients and the control. It was found that the group of thalassemic patients was significantly higher than the control regarding serum ferritin level, and this came in agreement with the study of Garadah et al.[9].

Regarding the hemoglobin level, there was a statistically significant difference between the group of thalassemic patients and the control. It was found that the group of thalassemic patients was significantly lower than the control regarding hemoglobin level, and this came in agreement with the study of Amoozgar et al.[10].

On assessment of LV systolic function by conventional echocardiography, it was found that there was no significant difference between thalassemic group and control group regarding LVEF. These findings are compatible with the study of Bilge et al.[6] who studied 32 patients with β-TM and 25 healthy controls of similar age and found that EF and FS were similar between both groups.

This came in agreement with Ragab et al.[11] who found no significant difference between asymptomatic 25 patients with β-TM and 20 age-matched control individuals regarding LVEF.

Similar results to these findings were recorded by Garadah et al.[9] who studied 38 patients with transfusion-dependent β-TM and 38 patients with no thalassemia and found no significant differences in FS at the base and at mid-cavity sector or in LVEF % between the two groups.

The LVESD was significantly larger in β-TM compared with control group. This finding is compatible with Garadah et al.[9] and Kostopoulou et al.[12].

Moreover, there was a highly significant difference between thalassemia group and control group regarding interventricular septal thickness in diastole and LV posterior wall thickness in diastole, which were more in thalassemia group. This came in agreement with Garadah et al.[9].

Moreover, regarding left atrial diameter, our study demonstrated a highly significant difference between thalassemic patients and control group, being higher in thalassemic group. This came in agreement with Bilge et al.[6] who studied 32 patients with β-TM and 25 healthy controls of similar age and sex.

The mean values of LVM and LVMI were significantly higher in thalassemic group than control group as increased LVM and LVMI is a parameter of cardiac involvement in patients with thalassemia. This was in agreement with the previous studies of Cheung et al.[13], Ibrahim et al.[14], and Bilge et al.[6].

However, Monte et al.[15], who studied 27 asymptomatic patients with TM and 27 healthy controls, demonstrated no significant difference between both groups regarding LVM and LVMI.

Compared with controls, the diastolic indices of LV in patients with β-TM showed higher early diastolic filling of LV and high E/A ratio suggesting restrictive diastolic pattern and thus stiff myocardial wall. These findings are concomitant with another study by Garadah et al.[9] who demonstrated that patients with β-TM (n = 63) had significantly higher E wave, E/A ratio, and lower A wave velocity, suggesting restrictive pattern in 54% in the study population. Similar observations were reported by Spirito et al.[16], who demonstrated that transmitral diastolic filling measured by Doppler in patients with β-TM (n = 32, none of them had heart failure) was described of restrictive pattern.

This was also in agreement with a previous report by Kremastinos et al.[17] that high E/A ratio is the most common finding in patients with β-TM. On the contrary, no significant difference regarding E/A ratio was reported by other reports, such as Bilge et al.[6], Oztarhan et al.[18], and Ibrahim et al.[14].

In our study, it was found that E/e' was significantly higher in thalassemic group than control group, which agrees with the previous studies of Garadah et al.[9] and Ibrahim et al.[14].

Moreover, our study demonstrated a significant difference between thalassemic and control group regarding mitral annular plane systolic excursion, being higher in thalassemic group.

In the present study, there was a significant negative correlation between serum ferritin level of thalassemic patients and LVESD, LVEDD, global LV systolic strain, and global LV late diastolic SR.

Moreover, there was a highly significant positive correlation between serum ferritin levels of thalassemic patients and LVMI.

By speckle tracking analysis, it was found that there was a statistically highly significant difference between the thalassemic group and the control group, with impairment of the global LV longitudinal systolic strain in the thalassemic group in comparison with the control.

Moreover, global LV longitudinal systolic SR and early diastolic SR were reduced in the thalassemic group in comparison with the control.

The result of the present study has demonstrated the presence of subclinical myocardial systolic and diastolic dysfunction in thalassemic patients, with no cardiac manifestations, and was asymptomatic.

Despite a normal LVEF with two-dimensional echocardiography, the thalassemic patients showed impairment of LV longitudinal strain, SR, and early diastolic SR.

This came in agreement with the study of Monte et al.[15] who studied 27 asymptomatic patients with TM and 27 healthy controls and found that longitudinal deformation analysis revealed subtle alterations of cardiac mechanics along the longitudinal axis of the heart, with reduced longitudinal displacement. Their study provided evidence of impaired LV rotational deformation, with alterations of normal patterns.

Similarly, Cheung et al.[13] showed that patients with β-TM have reduced longitudinal systolic SR, longitudinal early diastolic SR, and circumferential early diastolic SR.

Longitudinal studies to determine the usefulness of myocardial diastolic deformation rates in the early detection of iron overload are warranted.

Moreover, Garceau et al.[19] revealed that echocardiographic measurements of myocardial mechanics accurately detect the degree of myocardial iron deposition assessed by CMR T2 values. This technique can be used when CMR is not available or cannot be used.

Moreover, Karamanou et al.[20] showed that patients with β-thalassemic major with preserved LV systolic function had impaired left atrial function at the longitudinal axis and LV function at the radial axis. The new echo markers have better prognostic value than the traditional echo indexes in detecting latent diastolic dysfunction in β-TM, earlier than E/e' ratio.


  Conclusion Top


Patients with thalassemia have early regional systolic dysfunction in the LV walls even if they do not have overt heart failure. SI is helpful in early detection and quantitative assessment of LV longitudinal systolic functions in patients with thalassemia and may provide additional data for management of patients with thalassemia suspected of iron-mediated cardiomyopathy. Elevated ferritin levels in thalassemic patients have been associated with both the presence and severity of ventricular dysfunction.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Amoozgar H, Farhani N, Karimi M. Early echocardiographic findings in β-thalassemia intermedia patients using standard and tissue Doppler methods. Pediatr Cardiol 2011; 32:154–159.  Back to cited text no. 10
    
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Ragab SM, Fathy WM, El-Aziz WF, Helal RT. The diagnostic value of pulsed wave tissue doppler imaging in asymptomatic beta-thalassemia major children and young adults; relation to chemical biomarkers of left ventricular function and iron overload. Mediterr J Hematol Infect Dis 2015; 7:2015051.  Back to cited text no. 11
    
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Ibrahim MH, Azab AA, Kamal NM, Salama MA, Ebrahim SA, Shahin AM, et al. Early detection of myocardial dysfunction in poorly treated pediatric thalassemia children and adolescents: two Saudi centers experience. Ann Med Surg 2016; 9:6–11.  Back to cited text no. 14
    
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Spirito P, Lupi G, Melevendi C, Vecchio C. Restrictive diastolic abnormalities identified by Doppler echocardiography in patients with thalassemia major. Circulation 1990; 82:88–94.  Back to cited text no. 16
    
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Kremastinos DT, Tsiapras DP, Tsetsos GA, Rentoukas EI, Vretou HP, Toutouzas PK. Left ventricular diastolic Doppler characteristics in β-thalassemia major. Circulation 1993; 88:1127–1135.  Back to cited text no. 17
    
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Oztarhan K, Delibas Y, Salcioglu Z, Kaya G, Bakari S, Bornaun H, et al. Assessment of cardiac parameters in evaluation of cardiac functions in patients with thalassemia major. Pediatr Hematol Oncol 2012; 29:220–234.  Back to cited text no. 18
    
19.
Garceau P, Nguyen ET, Carasso S, Ross H, Pendergrast J, Moravsky G, et al. Quantification of myocardial iron deposition by two-dimensional speckle tracking in patients with β-thalassaemia major and Blackfan–Diamond anaemia. Heart 2011; 97:388–393.  Back to cited text no. 19
    
20.
Karamanou AG, Hamodraka ES, Vrakas SC, Paraskevaidis I, Lekakis I, Kremastinos DT. Assessment of left ventricular and atrial diastolic function using two-dimensional (2D) strain imaging in patients with β-thalassemia major. Eur J Haematol 2014; 92:59–65.  Back to cited text no. 20
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10], [Figure 11], [Figure 12], [Figure 13], [Figure 14], [Figure 15]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8]



 

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