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 Table of Contents  
ORIGINAL RESEARCH
Year : 2022  |  Volume : 6  |  Issue : 1  |  Page : 13-20

A Pilot Project to Identify Simple Echocardiographic Tools as an Alternative to Cardiac Magnetic Resonance Imaging to Predict a Reduced Right Ventricular Ejection Fraction in Patients with Repaired Tetralogy of Fallot


Department of Pediatric Cardiology, Institute of Cardio Vascular Diseases, Madras Medical Mission, Chennai, Tamil Nadu, India

Date of Submission10-Jun-2021
Date of Acceptance11-Jul-2021
Date of Web Publication22-Oct-2021

Correspondence Address:
Dr. Kothandam Sivakumar
Department of Pediatric Cardiology, Institute of Cardio Vascular Diseases, Madras Medical Mission, 4-A Dr. JJ Nagar, Mogappair, Chennai - 600 037, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jiae.jiae_26_21

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  Abstract 


Background: Right ventricular (RV) dysfunction is an important predictor of adverse events after tetralogy of Fallot (TOF) repair. A study comparing echocardiography with cardiac magnetic resonance (CMR) might provide simple tools for their serial inexpensive assessment. Methods: Echocardiographic RV functional parameters including fractional area change (FAC), rate of pressure rise (dP/dt), free wall strain, myocardial performance index (MPI), tricuspid annular plane systolic excursion (TAPSE), and tissue Doppler S' velocity in patients with repaired TOF were correlated with CMR-derived ejection fraction (EF) using receiver operator characteristic (ROC) curves. Bland–Altman plots analyzed agreement between the RV end-diastolic volumes (EDVs), end-systolic volumes (ESVs), and EF derived from three-dimensional echocardiography (3DE) and CMR. Results: Eighteen patients were included. The echocardiographic parameters that showed a good positive correlation with CMR-derived EF were FAC (r = 0.851, P = 0.001), dP/dt (r = 0.730, P = 0.001), and free wall strain (r = −0.660, P = 0.003). ROC curve analysis provided a cutoff value for FAC (<36.6), dP/dt (<370 mmHg/s), free wall strain (<−18.5) and MPI (>0.565) to predict EF <45%. TAPSE and S' velocity had poor correlation. Correlation was strong between 3DE and CMR-derived EDV (r = 0.938, P <0.001), ESV (r = 0.936, P <0.001) and EF (r = 0.916, P <0.001). 3DE underestimated volumes compared to CMR with a mean bias of − 31.78 ± 18.8 ml for EDV and −17.28 ± 11.6 ml for ESV, but EF was not affected (mean bias − 1% ± 3.7%). Conclusions: RV free wall strain, FAC and dP/dt were simple tools with good accuracy to predict RV EF <45% in patients with repaired TOF. TAPSE and S' velocity assessed basal longitudinal function without considering the dysfunctional outflow tract and showed poor correlation. EF assessment by 3DE was a good alternative to CMR. Underestimation of volumes by 3DE might restrict its use in timing surgery.

Keywords: Bland–Altman plots, comparative study, cutoff discrimination, receiver operator characteristic curves, right ventricular systolic function, three-dimensional echocardiography


How to cite this article:
Mohakud AR, Sivakumar K, Singh AS, Sagar P. A Pilot Project to Identify Simple Echocardiographic Tools as an Alternative to Cardiac Magnetic Resonance Imaging to Predict a Reduced Right Ventricular Ejection Fraction in Patients with Repaired Tetralogy of Fallot. J Indian Acad Echocardiogr Cardiovasc Imaging 2022;6:13-20

How to cite this URL:
Mohakud AR, Sivakumar K, Singh AS, Sagar P. A Pilot Project to Identify Simple Echocardiographic Tools as an Alternative to Cardiac Magnetic Resonance Imaging to Predict a Reduced Right Ventricular Ejection Fraction in Patients with Repaired Tetralogy of Fallot. J Indian Acad Echocardiogr Cardiovasc Imaging [serial online] 2022 [cited 2022 Oct 5];6:13-20. Available from: https://jiaecho.org/text.asp?2022/6/1/13/329024




  Introduction Top


Progressive right ventricular (RV) dilatation and dysfunction due to pulmonary regurgitation is an important predictor of late adverse events after surgical repair of tetralogy of Fallot (TOF). While two-dimensional echocardiography (2DE) remains the conventional clinical tool in periodic serial assessment of such operated patients, complex geometry, and retrosternal location of the RV offer challenges in quantification of its function.[1] Cardiac magnetic resonance (CMR) overcomes these challenges and has emerged as the gold standard for evaluating RV function and volumes.[2] However, lack of its universal availability and high costs in restricted economies preclude a routine and frequent use of CMR in clinical practice. Validation of echocardiographic variables and fine-tuning of techniques for RV quantification is need of the hour, as it remains the first-line imaging modality.

Various echocardiographic indices are proposed to assess RV function, but none has been thoroughly validated in a dilated ventricle seen in repaired TOF.[3] While the complex geometry of RV precludes its volume measurements on 2DE, three-dimensional echocardiography (3DE) provides an opportunity to quantify RV volumes.[4] However, it is not routinely done in clinical practice. A recent study comparing CMR and 3DE found good correlation in the assessment of RV volumes; however, correlation of 2DE parameters with CMR-derived ejection fraction (EF) was suboptimal.[5]

We aimed to evaluate different 2DE variables of RV function as well as the measurements of RV volumes and EF on 3DE in patients with repaired TOF and significant pulmonary regurgitation. A correlation of these different echocardiographic indicators of RV function and CMR-derived RV EF was made to arrive at cut-off values for predicting RV systolic dysfunction. RV with EF below 45% might not recover its function despite successful surgical correction of pulmonary regurgitation.[3],[5],[6] A comparison was also made between RV volume measurements obtained from 3DE and CMR. This project would in addition assess the feasibility of acquiring various echocardiographic parameters in clinical set-up and study interobserver and intraobserver variability in these measurements.


  Methods Top


Study population

This prospective study from a single tertiary care institution included patients aged above 10 years who had previously undergone complete repair of TOF at least 5 years earlier. Patients with significant residual lesions like hemodynamically significant residual ventricular septal defect and residual RV outflow gradient more than 50 mmHg were excluded from the study. Patients were included only if they had a good echocardiographic window that permitted acquisition of different RV parameters as well as 3DE RV volume assessment. Patients were included if they were willing to undergo CMR study within 48 h of the echocardiographic assessment. Informed consent was taken from all patients. The institutional ethical committee and hospital review board gave approval for the study. A sample size of 16 patients was calculated based on a previous report comparing 3DE and CMR.[5] The confidence level was estimated at 95%; standard deviation was 20.1, Z-value for an alpha error of 5% was 1.96 and the confidence interval or margin of error was estimated at ±10.(1.96 × 20.1 divided by 10) 2.

Echocardiographic evaluation

All patients underwent complete 2DE using GE VIVID E95 echocardiography (GE Healthcare, Horten, Norway) using the M5Sc-D matrix array transducer. Image loops comprising of at least four cardiac cycles were acquired with electrocardiographic gating. The echocardiographic acquisition included RV-focused four-chamber view, M mode interrogation through the lateral tricuspid annulus, tissue Doppler images (TDIs) focusing on tricuspid annulus, and continuous wave Doppler trace of tricuspid regurgitation jet. Due care was taken to avoid loops with ventricular ectopics. RV-focused views were acquired with high frame rates with good quality images.

Two-dimensional echocardiography

The RV function was estimated on 2DE according to the recommendation of the American Society of Echocardiography.[3] Various parameters used for estimating RV function included tricuspid annular plane systolic excursion (TAPSE), rate of RV systolic pressure rise (dp/dt) from the continuous wave spectral Doppler trace of the tricuspid regurgitation jet, RV fractional area change (FAC), RV myocardial tissue systolic velocity (S' velocity) from the tricuspid annular TDI, RV myocardial performance index (MPI) calculated from the tricuspid annular TDI, and RV-free wall strain calculated by averaging the three segments of the RV-free wall by speckle tracking method.

Three-dimensional echocardiography

3DE images were acquired using 4V-D probe. The images were acquired at a frame rate of more than 12 frames/second as per the requirement of the offline workstation software. The images were transferred to a work station (EchoPAC Version 202, GE Healthcare) for calculation of RV end-diastolic volume (EDV), end-systolic volume (ESV), and EF [Figure 1] and [Figure 2]. In addition to these acquisitions, indirect indicators of elevated end-diastolic pressures were assessed by measuring pulmonary regurgitation pressure-half time and ratio of the duration of pulmonary regurgitation to total diastolic duration from the Doppler traces of RV outflow. Electrocardiographic measurement of QRS duration was measured as an indicator for conduction delay.
Figure 1: Multiplanar endocardial border delineation in estimation of the right ventricular volumes using three-dimensional echocardiography in a patient with moderately dilated right ventricle and preserved ejection fraction

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Figure 2: Right ventricular volumes on three-dimensional echocardiography in a patient with markedly dilated right ventricle and reduced ejection fraction

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Cardiac magnetic resonance assessment

CMR was performed on a 1.5 Tesla Symphony system (Siemens, Erlangen, Germany) with a phased-array radiofrequency receiver coil placed on the chest. All images were gated to the electrocardiogram. A double oblique long-axis and four-chamber scout was acquired to obtain a true short-axis and axial reference. Steady-state free-precession prospectively electrocardiogram-gated free breath images, encompassing the whole RV, were then acquired in the axial orientation, with no gaps between the slices (True FISP sequence: slice thickness, 5 mm; TE, 1.64 ms; TR, 88.29 ms [depending on the R-R interval]; matrix, 192 mm × 192 mm;). RV ESV, EDV and EF were measured on a postprocessing workstation, using commercially available software (Osirix MD), with appropriate plugins by a radiologist blinded to the results of the echocardiography. Pulmonary regurgitant fraction was measured from the velocity encoded phase contrast images taken in a plane perpendicular to the vessel. Three-dimensional contrast-enhanced magnetic resonance angiographic images were acquired by injecting gadolinium at a dose of 0.2-ml/kg with a maximum dose of 20 ml. Delayed enhancement images were also acquired for the identification of myocardial scar.

Statistical methods

The data were collected in the prescribed format, and analyzed using the SPSS statistical software 21.0 version (IBM Corporation, Armonk, NY). Descriptive statistics were calculated and used. Percentages and frequencies were used for categorical variables and mean and standard deviation were used for continuous variables. Intra-class correlation coefficient was used to determine the correlation between different observations. Student's t-test was used to determine the significance of association between a continuous variable and a categorical variable and analysis of variance test was used if the categorical variable had more than two categories. If the distribution of continuous variables was nonnormal, then nonparametric test was used. P <0.05 was considered statistically significant. Relation between echocardiographic variables of RV function and CMR-derived RV EF was evaluated using Pearson's correlation coefficient and linear regression statistics. Receiver operator characteristic (ROC) curve analysis was used to determine the cut off values of echocardiographic parameters for predicting low EF (<45%) on CMR. Bland–Altman plots were used to determine the bias between the RV volumes obtained by CMR and echocardiography.

Reproducibility analysis

Two independent observers analyzed all two-dimensional echocardiographic parameters. Each observer performed three measurements for each parameter and the average of these values was taken for statistical analysis. The intraobserver and interobserver variability was calculated for reproducibility.


  Results Top


Eighteen patients, including 12 males, aged 22.8 ± 11.6 years (14–58 years) formed the study group. The preoperative diagnosis was TOF in 16 patients and TOF with absent pulmonary valve syndrome in the other two. The two patients with absent pulmonary valve syndrome were operated at 1–2 years of age with a transannular patch rather than a conduit, as their anatomy and physiology were very similar to a conventional TOF without airway symptoms and pulmonary arterial enlargement was modest. Transannular patch reconstruction of the RV outflow was performed in 15 patients while 3 patients had pulmonary valvotomy. Sixteen patients were in New York Heart Association (NYHA) class II, while one each was in class I and III, respectively. The symptoms included palpitations in 7, nonanginal chest pain in one, and syncope in two patients.

Cardiac magnetic resonance findings

The mean RV EDV and ESV were 167.1 ± 42.4 ml/m2 and 85.7 ± 25.5 ml/m2 respectively. The mean EF was 48.9% ±9.2%. The patients were divided into two groups: 14 patients with normal EF >45% and 4 patients with low EF <45%. The pulmonary regurgitant fraction was 49.9% ±11.8%. It was not different (P = 0.435) between the patients with normal EF (51.1 ± 10.7) and those with low EF (45.8 ± 15.9). Gadolinium-enhanced images showed late enhancement in 10/18 patients. Four patients had left ventricular dysfunction.

Chest X-ray and electrocardiogram

Electrocardiogram in all patients showed sinus rhythm with complete right bundle branch block with a mean QRS duration 147 ± 32.3 ms. The mean QRS duration was significantly different (P = 0.018) in patients with normal EF (138.6 ± 25.4 ms) and patients with low EF (180 ± 36.5 ms). The mean cardiothoracic ratio on chest X-ray was 56.9% ± 4.9% and was not significantly different between the two groups.

Reproducibility

The intraobserver and interobserver variability were low for all 2DE parameters with high co-efficient of correlation except for the RV end-systolic area and the observations were statistically significant for all these parameters in both intraclass and interclass measurements [Table 1].
Table 1: Intra-observer and inter-observer variability

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Two-dimensional echocardiography variables of RV systolic function

Among the six variables studied on 2DE, the mean values of FAC, free wall strain and dP/dt were significantly different between patients with normal and low EF derived from CMR [Figure 3]. The differences in the other three variables namely MPI, TAPSE, and S' velocity did not reach statistical significance [Table 2]. While the FAC (r = 0.851, P = 0.001) and dP/dt (r = 0.730, P = 0.001) had a good positive correlation with EF, free wall strain (r = −0.660, P = 0.003) and MPI (r = −0.446, P = 0.049) had moderate correlation [Figure 4]. There was poor correlation with TAPSE and S' velocity. A cutoff value of 36.7% for FAC (area under the curve [AUC] =0.938) predicted low EF with a sensitivity of 100% and specificity of 83.3% [Figure 5]. Similarly, a dP/dt showed a cutoff of 370 mmHg/s (AUC = 0.938) to predict low EF with a sensitivity of 100% and specificity of 91.7% [Table 2].
Figure 3: Multiple echocardiographic variables (i) Fractional area change, (ii) Free wall strain, (iii) Myocardial performance index and (iv) Rate of pressure rise (dP/dt) correlated with ejection fraction

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Table 2: Pearson's correlation coefficient and receiver operator characteristic curve analysis between echocardiographic variables and ejection fraction from magnetic resonance imaging

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Figure 4: Pearson's correlation coefficient between cardiac magnetic resonance imaging derived ejection fraction and echocardiographic parameters. (i) Fractional area change (FAC), (ii) Rate of pressure rise (dp/dt), (iii) Right ventricular (RV) free wall strain and (iv) Myocardial performance index (MPI)

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Figure 5: Receiver operating characteristic curve analysis for echocardiographic parameters to determine discriminating cutoff values for identifying low right ventricular ejection fraction <45%. (i) Fractional area change, (ii) rate of pressure rise, (iii) Myocardial performance index and (iv) free wall strain
AUC: Area under the curve, dp/dt: Rate of right ventricular systolic pressure rise, EF: Ejection fraction, FAC: Fractional area change, MPI: Myocardial performance index, ROC: Receiver operating characteristics, RV: Right ventricular


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Three-dimensional echocardiography-derived volumes

Compared to CMR, 3DE significantly underestimated RV volumes in all patients in our study. The mean EDV derived from 3DE was lower than CMR-derived EDV (135.33 ± 28.07 ml/m2 vs. 167.11 ± 42.39 ml/m2). Similar differences were seen in the ESV also, derived from the two modalities (68.44 ± 19.47 ml/m2 vs. 85.72 ± 27.54 ml/m2). However, there was no significant difference in the estimation of EF between these two imaging modalities. The Bland-Altman analysis reflected these findings. Although the mean bias was −31.8 ± 18.8 ml for EDV and −17.3 ± 11.6 ml for ESV between 3DE and CMR measurements, a good agreement was seen between EF predicted by 3DE and CMR with a mean bias of − 1% ±3.7% [Table 3]. Despite these systematic differences, the RV volumes and EF estimated by 3DE had a very good correlation with CMR-derived volumes and EF [Figure 6].
Table 3: Bland-Altman analysis for comparing ventricular volumes and function derived from three dimensional echocardiography and cardiac magnetic resonance

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Figure 6: Regression plots showing correlation between indexed end-diastolic and end-systolic volumes and ejection fraction derived using three-dimensional echocardiography and magnetic resonance imaging; Bland–Altman analysis of agreement between the tests with the mean bias is shown in the lower row 3D: Three-dimensional echocardiography, EDV: End-diastolic volume, EDVI: End-diastolic volume index, ESV: End-systolic volume, ESVI: End-systolic volume index, EF: Ejection fraction, MRI: Magnetic resonance imaging, RV: Right ventricular

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Doppler interrogation of pulmonary regurgitation

Spectral Doppler evaluation of RV outflow showed short pressure half time (93.9 ± 13.1 ms) of the pulmonary regurgitation jet indicating a possibility of elevated end-diastolic pressures. The ratio between the duration of pulmonary regurgitation to total diastolic duration was 0.73 ± 0.15, another indicator of high end-diastolic pressures. The mean pulmonary regurgitation velocity-time integral was 50.42 ± 5.52 cm [Figure 7]. This showed a positive correlation with the pulmonary regurgitation fraction on CMR, with a r = 0.728 and P = 0.001. However, our study sample calculated to assess the RV systolic function parameters was not powered to study these Doppler variables of diastolic regurgitation. Even though we observed a large dimensions of the RV outflow on 2DE measurements in patients (proximal RV outflow in parasternal long axis - 3.2 ± 0.4 cm; in short axis – 3.2 ± 0.5 cm; distal RV outflow in parasternal short axis – 2.8 ± 0.5 cm), we did not correlate these values with QRS duration as the study was not powered to observe these differences [Figure 7].
Figure 7: Elevated right ventricular end-diastolic pressures were indirectly predicted on Doppler trace of pulmonary regurgitation (PR) by the assessment of velocity time integral (VTI), duration of PR (PRD) to total diastolic duration (TDD) ratio, pressure half-time (PHT) and end-diastolic forward flow (DFF) evaluation. The bottom panel indicates measurement of the right ventricular outflow to indicate the anatomical-electrical relation to QRS delay
PSLAX: Parasternal long-axis, PSSAX: Parasternal short-axis


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  Discussion Top


RV dilatation and dysfunction due to pulmonary regurgitation are predictive of morbidity and mortality after surgical repair of TOF. Outcomes such as death, the occurrence of sustained ventricular arrhythmia, and NYHA functional class were correlated with EDV and EF.[7] EDV is an important predictor for RV remodeling after pulmonary valve replacement.[8],[9] Reliable and accurate echocardiographic methods to assess RV volumes and EF are clinically important in follow-up of this patient cohort. Unlike a symmetric left ventricle, the complex geometry of RV offers challenges for echocardiography.[8] It is known that echocardiography underestimates volumes and hence, direct and indirect measures of RV systolic function are crucial indicators during clinical follow-up of these patients.[10]

Different two-dimensional echocardiography variables

The variables on 2DE that correlated well with CMR-derived EF were FAC, dP/dt and free wall strain in our study. MPI had a moderate inverse correlation; TAPSE and S' velocity had poor correlation. Two previous studies demonstrated a good correlation of free wall strain with EF.[1],[11] Free wall strain <−18.5 predicted EF <45% in our study. FAC also showed a good correlation in other studies and we identified FAC <36.6 to predict EF <45%.[11] Similarly, dP/dt was identified as the third predictor for EF with a predictive cutoff of 370 mmHg/s to identify low EF.[12] However, MPI did not demonstrate a strong correlation with EF in our study and others.[13] MPI >0.565 predicted low EF in our study. TAPSE and S' velocity showed poor correlation in our and other reports too.[11] Altered regional contraction with preserved basal contractility and dyskinetic outflow tracts result in normal TAPSE and S' velocity despite a low EF.[14],[15]

Cutoff values for different two-dimensional echocardiography variables

ROC analysis identified cutoff values for different 2DE variables in previous reports.[11] A comparative study of RV with 2DE parameters and CMR in different diseases other than operated TOF showed a FAC cutoff value of 41.4% (AUC = 0.77) and free wall strain cutoff value of −17% (AUC = 0.92) with sensitivity and specificity of 96% and 93% respectively for predicting RV EF <45%.[11] The cutoff value for RV free wall strain was higher and that of FAC was lower in our study. The diagnostic accuracy of dp/dt was the highest in our study with an AUC similar to FAC but with a higher specificity than FAC. MPI and dP/dt also demonstrated reasonable diagnostic accuracy in our study. A previous study too demonstrated a cutoff value of 0.5 for MPI to predict poor EF, but this study was not conducted on patients with repaired TOF.[16]

Correlation between three-dimensional echocardiography and cardiac magnetic resonance

Various researchers who compared 3DE and CMR for quantifying RV volumes uniformly found good correlation, though the 3DE underestimated volumes with a significant bias.[5],[17] However it was reassuring that there was no statistically significant bias in the assessment of EF in those groups as shown in our study too. The differences between the volumes measured by these two different modalities (mean bias) varied in different studies.[10],[17] The good correlation between the two modalities noted in our study was similar to that seen in few other studies.[18],[19] A meta-analysis of 23 similar reports found reasons for the underestimation of volumes by 3DE compared to CMR.[20] Older age and larger volumes were more related to underestimation of volumes and EF. The increased distance from the transducer in dilated RV blurred the endocardial borders resulting in wider band of hues inside the edge of the RV walls. This blurred wall was often traced inside on manual tracking leading to underestimation of volumes.[20]

Limitations

Small patient numbers and lack of follow-up imaging in this cross-sectional study are the major limitations. Investigator's learning curve in image acquisition and offline analysis was another limitation. As patients undergoing CMR was an inclusion criterion, it introduced a bias by including patients with significantly dilated RV. 3DE-derived volumes required more accuracy in image acquisition and correct endocardial border delineation and this depended on adequate image quality and proper inclusion of the outflow tract. Even though indirect indicators of elevated RV end-diastolic pressure by assessing the pulmonary regurgitation Doppler traces were obtained, our sample size did not permit a detailed analysis. For similar reasons, a correlation between the anatomical RV dilatation and the electrical delay was also not feasible.


  Conclusions Top


Free wall strain, FAC and dP/dt were simple echocardiographic tools with good predictive accuracy to predict CMR-derived EF <45% in patients with repaired TOF. TAPSE and S' velocity showed poor correlation as they assessed basal longitudinal function without considering the dysfunctional outflow tract. EF assessment by 3DE was a good alternative to CMR. Underestimation of volumes by 3DE compared to CMR might restrict its use in deciding the time of pulmonary valve replacement. A detailed echocardiographic multi-parameter imaging is more suited for serial follow-up of patients with repaired TOF as it reduces the burden of cost on health care by reducing the use of CMR imaging. This pilot project can serve as a template for planning a multicenter evaluation of these simple echocardiographic tools in a larger patient population after TOF repair.

Financial support and sponsorship

Nil.

Conflicts of interest

K Sivakumar is an editorial board member of the Journal of The Indian Academy of Echocardiography & Cardiovascular Imaging. The article was subject to the journal's standard procedures, with peer review handled independently of this editor and their research groups.

There are no other conflicts of interest.



 
  References Top

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    Figures

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

  [Table 1], [Table 2], [Table 3]



 

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