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ORIGINAL ARTICLE
Year : 2021  |  Volume : 24  |  Issue : 12  |  Page : 1800-1807

Dynamic contrast-enhanced magnetic resonance imaging: A novel approach to assessing treatment in locally advanced esophageal cancer patients


1 Department of Radiology, The Affiliated Cancer Hospital of Nanjing Medical University and Jiangsu Cancer Hospital and Jiangsu Institute of Cancer Research, Baiziting Road, Nanjing, P. R. China
2 Department of Radiation Oncology, The Affiliated Cancer Hospital of Nanjing Medical University and Jiangsu Cancer Hospital and Jiangsu Institute of Cancer Research, Baiziting Road, Nanjing, P. R. China

Date of Submission15-Feb-2021
Date of Acceptance17-Jun-2021
Date of Web Publication09-Dec-2021

Correspondence Address:
Prof. W Shen
Department of Radiology, Jiangsu Cancer Hospital and Jiangsu Institute of Cancer Research and The Affiliated Cancer Hospital of Nanjing Medical University, 42 Baiziting Road, Nanjing, Jiangsu - 210000
P. R. China
Prof. Z Guo
Department of Radiology, Jiangsu Cancer Hospital and Jiangsu Institute of Cancer Research and The Affiliated Cancer Hospital of Nanjing Medical University, 42 Baiziting Road, Nanjing, Jiangsu - 210009
P. R. China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/njcp.njcp_78_21

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   Abstract 


Aims: This study aims to investigate the potential application of dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) to predict concurrent chemoradiation (CRT) in locally advanced esophageal carcinoma. Patients and Methods: This study involved 33 patients with locally advanced esophageal cancer and treated with CRT. The patients underwent DCE-MRI before CRT (pre) and 3 weeks after starting CRT (mid). The patients were categorized into two groups: complete response (CR) and non-complete response (non-CR) after 3 months of treatment. The quantitative parameters of DCE-MRI (Ktrans, Kep, and Ve), the changes and ratios of parameters (ΔKtrans, ΔKep, ΔVe, rΔKtrans, rΔKep, and rΔVe), and the relative ratio in the tumor area and a normal tube wall (rKtrans, rKep, and rVe) were calculated and compared between two timeframes in two groups, respectively. Moreover, the receiver operating characteristics (ROC) statistical analysis was used to assess the above parameters. Results: We divided 33 patients into two groups: 22 in the CR group and 11 in the non-CR group. During the mid-CRT phase in the CR group, both Ktrans and Kep rapidly decreased, while only Kep decreased in the non-CR group. The pre-Ktrans and pre-Kep in the CR group were substantially higher compared to the non-CR group. Moreover, the rKtrans was also apparently observed as higher at pre-CRT in the CR group compared to the non-CR group. The ROC analysis demonstrated that the pre-Ktrans could be the best parameter to evaluate the treatment performance (AUC = 0.74). Conclusion: Pre-Ktrans could be a promising parameter to forecast how patients with locally advanced esophageal cancer will respond to CRT.

Keywords: Concurrent chemoradiation, dynamic contrast-enhanced magnetic resonance imaging, esophageal cancer, parameters


How to cite this article:
Gu L, Xie X, Guo Z, Shen W, Qian P, Jiang N, Fan Y. Dynamic contrast-enhanced magnetic resonance imaging: A novel approach to assessing treatment in locally advanced esophageal cancer patients. Niger J Clin Pract 2021;24:1800-7

How to cite this URL:
Gu L, Xie X, Guo Z, Shen W, Qian P, Jiang N, Fan Y. Dynamic contrast-enhanced magnetic resonance imaging: A novel approach to assessing treatment in locally advanced esophageal cancer patients. Niger J Clin Pract [serial online] 2021 [cited 2022 Jan 25];24:1800-7. Available from: https://www.njcponline.com/text.asp?2021/24/12/1800/332090




   Introduction Top


Esophageal cancer (EC) is currently ranked as the eighth most common cancer and is the sixth major reason for cancer-related mortality worldwide.[1] The overall 5-year survival ranges from 15 to 25%.[1] EC and cancers in the gastric, lung, liver, breast, and so on are among the most leading causes of cancer-related mortalities in China.[2] They tend to be diagnosed at advanced stages, and more than half of the patients are not potentially eligible for curative treatment.[3] Moreover, definitive concurrent chemoradiation (CRT) is an effective treatment therapy for patients with unresectable EC or those who cannot tolerate surgery in clinical trials.[4] However, complete pathologic response was achieved in around 29% of the patients treated with neoadjuvant CRT.[5] Thus, distinguishing complete response (CR) and non-complete response (non-CR) in the early stages is very important while receiving CRT to help clinicians make correct decisions in a locally advanced EC.

Functional imaging has been widely used recently to investigate the efficiency and forecast the prognosis of tumors. It includes 18F-fluorodeoxyglucose-positron emission tomography (FDG-PET) and diffusion-weighted magnetic resonance imaging (DWI-MRI), and so on. FDG-PET is more expensive than the other imaging tools and also causes high radiation and poor repeatability.

Meanwhile, some studies reported that FDG-PET should not assess early response in EC patients who take the neoadjuvant chemoradiotherapy.[6],[7] One study suggested that FDG-PET may not have much meaning for the survival in locally advanced EC.[8] Furthermore, DWI-MRI is a more functional imaging method based on the degree of water molecular  Brownian movement More Details and captures the contrast magnetic resonance (MR) images within the tissue voxel. However, studies in this area showed some conflicting results in predicting the response in EC patients receiving CRT.[9],[10] Inconsistent standard for setting the value of b (50, 800; 0, 600; and 0, 700) also exist.[10],[11]

This study chose the dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) as an inventive method to investigate the earlier response in EC patients who took CRT. The neovascularization wall of a malignant tumor is less mature than that of normal vessels. Therefore, the pharmacokinetic model can be analyzed to monitor the quantitative parameters (e.g. penetration of plasma contrast agent through the vessel wall and contrast agent in the extracellular space of the blood vessel). It shows great potential in response to treatment at the same time. The parameters obtained from the DCE-MRI pharmacokinetic model are the volume transfer constant (Ktrans, min−1), the rate constant (Kep, min−1), and the extravascular–extracellular volume fraction (Ve). Some previous studies found that DCE-MRI plays a promising role in predicting treatment response in the head, neck, breast, and rectal cancers, which was operated more on the 1.5-T MRI.[12],[13],[14] However, a few studies evaluated the efficiency of 3.0-T DCE-MRI in response to CRT in EC. Recent studies proved that EC invasion depth could be evaluated by the high-resolution MR images from 3.0-T MRI. Those images can provide a satisfying diagnostic accuracy in the preoperative stage.[15] Therefore, this research aims to evaluate the DCE-MRI parametric analysis potential combined with high-resolution scanning at 3.0-T MRI for the early prediction of the therapeutic effect of locally advanced EC with CRT. Consequently, pre- and mid-treatment were selected as the scanning time to explore the ability to evaluate CRT response potentially by collecting DCE-MRI parameters at two different timeframes.


   Materials and Methods Top


Study population

The hospital ethics committee approved this study (ZM201812). All participating patients provided written informed consent. This study recruited 37 patients diagnosed with advanced-stage EC from October 2018 to March 2020. Four patients with severe image artifacts at the second MRI scan were excluded from further analysis. According to the patient's clinical situation, the chemoradiation regimen consisted of 60–66 Gy (1.8–2.2 Gy/fraction, five fractions/week, and 30–33 fractions in total) radiation. The patients underwent concurrent chemo and radiation therapy with paclitaxel liposome (90 mg/m2) plus nedaplatin (40 mg/m2) for 4 weeks and no more than 6 weeks if necessary. The patients were categorized into CR and non-CR groups after 3 months of chemoradiation, combined with esophageal barium meal examination and chest enhancement Computed Tomography (CT), Response Evaluation Criteria in Solid Tumors (RECIST) Guideline version 1.1.

MRI acquisition

All MRI examinations with the neck and a phased-array body coil were performed on Philips Medical Systems Ingenia 3.0T Tesla MRI scanner. The MRI sequences included T1-weighted and sagittal T2-weighted imaging for anatomical location, a small-field high-resolution T2-weighted imaging, DWI imaging, and DCE imaging. The parameters of a small-field high-resolution T2-weighted turbo spin-echo sequence scanning includes repetition time (TR, 2,000 ms), echo time (TE, 90 ms), acceleration factor (NSA2), slice thickness (4 mm), matrix (232 × 232), and field of view (FOV; 140 mm × 140 mm). Moreover, the process uses a navigator for respiratory triggering. Cross-section DWI scans are based on echo-planar imaging and have the parameters: TR, 250 ms; TE, 64 ms; NSA 3; matrix, 64 × 64; b = 0 and 800 s/mm2; and thickness, 4 mm. Moreover, the apparent diffusion coefficient (ADC) diagram was reconstructed. Based on Tofts standard pharmacokinetic model, the DCE series consisted of two parts: the T1 mapping with two flipped angles (5° and 15°) for the precontrast scan (TR, 10 ms; TE, 2 ms) and the DCE images were acquired with an axial dynamic T1-weighted 3D fast field echo (TR, 4 ms; TE, 2 ms; the field of view, 240 mm × 240 mm; matrix, 172 × 172; and NSA, 1). The dynamic contrast-enhanced sequence was operated with 80 dynamic phases. One dynamic period time was 3.7 s. A bolus of MRI contrast (Magnevist, Bayer) was injected at 0.1 mmol/kg of total body weight using an automatic syringe pump at 3 mL/s followed by saline injection when the scanning in the fourth phase was finished. Consequently, all patients were asked to breathe gently and smoothly during the collection of data.

Image analysis

MRI images were obtained at two selected times: before treatment (pre) and 3 weeks after the first therapy (after 15 fractions of radiotherapy, mid). The pre/mid-MR images were consistently analyzed by two radiation oncologists (with 5 and 9 years experienced experts in esophageal MR images) blinded to this clinical trial and data. DCE-MRI images were exported to a quantitative DCE-MRI analyzing software package (Philips IntelliSpace Portal).

The radiologists selected three regions of interest (ROIs) in the mass from the images of dynamic scanning, including the largest and distinct regions on the tumor sites as well as the upper and lower part of these sections, and averaged the measured ROIs. ROI was drawn along the edge of the tumor, directed by corresponding oblique axial high-resolution T2WI. Consequently, they ignored the area of calcification, hemorrhage, blood vessels, and necrotic tissue. Simultaneously, the radiologists determined that the normal EC wall's DCE-MRI parameters were 3–4 cm away from the mass and calculated the relative ratio.

The parameters Ktrans (min−1), Kep (min−1), and Ve; the changes in the values and ratios of KtransKtrans and rΔKtrans), Kep (ΔKep and rΔKep), and Ve (ΔVe and rΔVe) were obtained. The relative ratio in the tumor area and normal tube wall (rKtrans, rkep, and rVe) were also obtained.

Statistical analysis

The Statistical Package for the Social Sciences software (v. 23.0, Microsoft Windows x64, SPSS, Chicago, IL, USA) was used for data analysis. The Shapiro–Wilk's test was used to determine whether the quantitative parameters are subjected to normal distribution. The presentation of continuous variables was mean ± standard deviation. Categorical data (including location, gender, and clinical T- and N-stages) were presented as frequencies and percentages; they were compared by the Chi-square test. Moreover, Fisher's exact test was used when the Chi-square conditions were not met.

The point-biserial correlation was used for evaluating the correlation between DCE-MRI parameters and response evaluation related to CRT and treat time point. Paired Student's t-test identified the significant differences of the parameters pre-CRT and 3 weeks after CRT in two groups (CR and non-CR groups). The Wilcoxon Rank-Sum test compared the abnormally distributed data. An independent Sample t-test compared all kinds of parameters derived from DCE-MRI between the two groups. The Mann–Whitney U test compared whether the data were presented in a nonparametric distribution. Subsequently, the major parameters' ability to predict CR or non-CR was assessed by the receiver operating characteristic (ROC) curve analysis. Moreover, the area under the ROC curves (AUC) was measured. A P value < 0.05 was statistically significant.


   Results Top


Finally, the study included 33 patients; 32 patients with squamous cell carcinoma, confirmed through pathological biopsy, and 1 patient with adenocarcinoma, confirmed by histopathologic tumor-type comprising. Moreover, 22 and 11 patients were in the CR and non-CR groups, respectively. Furthermore, eight males (mean age, 66 ± 5.7 years) and three females (mean age, 67.3 ± 2.8 years) were in the non-CR group and 10 males (mean age, 63.9 ± 10.3 years) and 12 females (mean age, 68.8 ± 4.2 years) were in the CR group. No apparent statistical differences were recognized in gender, age, EC location, and clinical T and N-stages [all P > 0.05; [Table 1]]. At mid-CRT, the Ktrans and the Kep values of the CR group showed a significant drop compared with the pre-CRT phase [P < 0.05; [Figure 1]]. The rKtrans and rKep significantly decreased from pre- to mid-CRT in the CR group [P < 0.01; [Figure 1]]. However, the Ktrans increased slightly from pre- to mid-CRT in the non-CR group [Figure 2]. The rKtrans was approximately lying at pre- and mid-CRT. Moreover, Kep and rKep were higher before CRT than mid-CRT [Figure 2]. However, only the Kep values showed a significant drop compared with pre-CRT in the non-CR group [P < 0.05; Figure 2]. Furthermore, Ve and rVe values did not show a significant difference between before CRT and per-CRT in both the groups [Table 2]. There were two representative cases shown in [Figure 1] and [Figure 2] of the CR and non-CR groups. Warm colors prompt the information of higher values, while cool colors prompt the information of lower values of the parameter.
Table 1: Summary of demographic data of 33 patients

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Figure 1: Axial MR images acquired in a 66-year-old man with complete response. The arrow marked tumor region (a and b) Axial high-resolution T2-weighted and T1-weighted enhanced image showed an obvious enhancement mass in the cervical esophagus at pre-CRT (c) The color-coded DCE-MRI map showed the mixed color in the corresponding tumor (d and e) Axial high-resolution T2-weighted and T1-weighted enhanced image showed residual wall thickening in the cervical esophagus at mid-CRT (f) The color-coded DCE-MRI map showed dominant green in the corresponding tumor bed

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Figure 2: Axial MR images acquired in a 64-year-old woman with an incomplete response. The arrow marked the tumor region (a and b) Axial high-resolution T2-weighted and T1-weighted enhanced image showed an inhomogeneous enhancement mass in the upper thoracic esophagus at pre-CRT (c) The color-coded DCE-MRI map showed the mixed color in the corresponding tumor (d and e) Axial high-resolution T2-weighted and T1-weighted enhanced image showed residual wall thickening with high signal intensity in the corresponding tumor at mid-CRT (f) The color-coded DCE-MRI map showed dominant red in the corresponding tumor bed

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Table 2: Comparison of DCE-MRI parameters before and after the start of 3 weeks of CRT in the two groups

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The Ktrans and Kep demonstrated a significantly higher value in the CR group than the non-CR group before CRT (P < 0.05). However, the Ktrans and the Kep at week 3 of CRT showed no statistical significance between the two groups. Consequently, the mid-Ve values were higher than the pre-Ve in both groups but not reaching statistical significance. The changes in value and ratios of KtransKtrans and rΔKtrans), Kep (ΔKep and rΔKep), and Ve (ΔVe, rΔVe) showed no significant difference between the two groups from the pre-CRT to week 3 of CRT [Table 3].
Table 3: Comparison of DCE-MRI parameters between the CR and non-CR groups

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The rKtrans (pre-rKtrans) in the CR group was significantly higher than the non-CR group before CRT (P < 0.01). On the contrary, the rKtrans (mid-rKtrans), as well as the rKep (pre-rKep and mid-rKep) and rVe (pre-rVe and mid-rVe) values were not significantly different between the two groups at week 3 of CRT [Table 3].

The performance of these parameters in predicting the therapeutic effect was assessed by the ROC curve analysis [Figure 3]. Furthermore, pre-Ktrans was the best-evaluated parameter and showed an AUC of 0.74 with a cutoff value of 0.296. Moreover, sensitivity and specificity were achieved at 90.9 and 54.5%, respectively.
Figure 3: The receiver operating characteristic (ROC) curve analysis for pre-Ktrans of predicting CR and non-CR groups AUC for pre-Ktrans was 0.74. Moreover, sensitivity and specificity were achieved at 90.9 and 54.5%, respectively

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   Discussion Top


This retrospective study evaluated DCE-MRI parameters involved in EC before and during treatment. The correlation of needed DCE-MRI parameters with therapeutic effect, the changes during CRT, ratios of parameters, and the relative ratio in tumor area and normal tube wall were recorded. Finally, we determined the optimal parameters distinguishing the CR from the non-CR group.

The esophagus is particularly challenging for functional MRI imaging because of its anatomical location in the thoracic cavity, and cardiac respiration affects imaging. Thus, finding the optimized sequence to minimize the esophagus movement's impact is crucial to provide a dependable quantitative assessment of treatment-predicted response. Moreover, this study chose the 3D fast field-echo sequence for DCE-MRI. Consequently, one dynamic period was 3.7 s, and the total time of DCE-MRI was <5 min. Thus, a competent sampling of the rapid wash-in of contrast into the tumor was enabled. During the DCE image acquisition phase, the administration of anisodamine is important for eliminating esophageal movement and guaranteeing the signal intensity for each pixel over the accurate 80 timepoints. Moreover, patients were free-breathing in the DCE-MRI scan. At the same time, ROI guided by the corresponding small-field high-resolution T2-weighted images was acquired, which ensured the accuracy of the ROI sketch.

This study presented no significant difference in gender, age, location in EC, and clinical T and N-stages. The esophagus is subdivided into cervical, upper thoracic, middle thoracic, and lower thoracic in the AJCC Cancer Staging Manual. We did a more detailed division of tumor location because tumors often involve multiple segments in clinical practice. Shi et al.[16] indicated that tumor location is an indepenedent prognostic factor for the long-term survival of T2-3N0M0 esophageal squamous cell carcinoma in the literature. Our study found that tumor location did not influence short-term survival in EC. Moreover, most of them were squamous cell carcinomas.

This study chose 3 weeks after the first therapy as the second MRI scan time because it is the CRT halfway point and was convenient for evaluating treatment response. No uniform standards exist for setting the second MRI scan time. Moreover, van Heijl et al.[6] reported completing FDG-PET scanning before neoadjuvant CRT and two weeks after the start of the treatment therapy. A previous study found that the first 2 weeks of neoadjuvant CRT were DWI-MRI scanning's optimal timing to predict EC patients' pathological complete response.[9] Furthermore, Xie et al.[17] reported that DCE-MRI parameters were collected before CRT and after the fifth radiotherapy between the CR and partial response (PR) groups.

According to the statistical data, the patients on CR had significantly higher Ktrans and Kep values than those of the non-CR group before CRT. Higher Ktrans means a higher combination of tumor blood, microvascular permeability, and capillary surface area. Similarly, a higher Kep in the CR group implies that the interstitial tumor space has an increased return flow to neovessel, showing a more permeable neovasculature that allows a better exchange between the vessels and interstitial space. Moreover, Gaustad et al.[18] reported that Ktrans correlates strongly with hypoxia for tumor models and found no correlations between Ve and hypoxia. This study means that Ktrans reflects hypoxia that occurred by low blood perfusion. This view also supports the findings of the current study. Moreover, the present study results showed that the Ktrans value in the CR group at mid-CRT showed a significant drop compared with the pre-CRT phase. Conversely, the Ve value did not show significant differences between before and per-CRT in both the groups. However, the Ktrans was slightly increased from pre- to mid-CRT in the non-CR group. Gaustad et al.[18] also indicated that the Ktrans reveals radiation response with hypoxia's radiation resistance caused by hypoxia. Moreover, Ktrans can forecast prognosis in cervical cancer patients, and high Ktrans manifest higher overall survival rates than low Ktrans following the current study. Thus, pre-Ktrans was a good parameter for predicting CRT response in the locally advanced EC patients. The AUC was 0.74 when the ROC data indicated that the cutoff value of pre-Ktrans was 0.296. Consequently, sensitivity and specificity reached 90.9 and 54.5%, respectively. This observation was consistent with the previous studies.[17],[19] Furthermore, Sun et al.[19] reported that pre-Ktrans values indicated a good diagnostic performance and showed an AUC of 0.678. Also, Xie et al.[17] reported that the efficacy of radiotherapy in EC treatment was best evaluated when Ktrans before CRT with an AUC of 0.790. Previous studies showed the correlation between pretreatment Ktrans values and treatment response for breast, rectal, and cervical cancers.[20],[21],[22] However, Kep and Ve may not serve as prognostic biomarkers in this study to assess CRT response in EC patients. This result is in line with the previous studies.[19]

Unfortunately, there were no significant differences in the changes of DCE-MRI parameters (ΔKtrans, ΔKep, and ΔVe) and percentage change of Ktrans (rΔKtrans), Kep (rΔKep), and Ve (rΔVe) between the CR and non-CR groups, indicating that the early perfusion variation in tumors may have little benefit in predicting the outcomes for CRT in EC patients. The aforementioned have never been reported in the two groups for EC patients between pre- and mid-CRT (3 weeks after starting CRT). Thus, it may be a rather more meaningful time to supervise the therapeutic effect at the pretherapy phase compared to the halfway point of the therapy. A previous study showed that a relative change in Ktrans between pre- and post-CRT was predictive for the pathological response for rectal cancer.[22] Thus, this study inferred that the reason might be the different time of the second MRI scan in the two studies.

This seems to be the first study to investigate the value of rKtrans, rKep, and rVe for response prediction in locally advanced EC patients. Moreover, this was another innovative point of this study. Furthermore, the quantitative value of rKtrans, rKep, and rVe was essentially a ratio, and the ratio was >1 of prior treatment in the CR group in this study. Thus, tumors in the CR group with the abnormal microvascular network were inclined to indicate a larger increase in DCE-MRI signal intensity than the normal esophageal wall. According to statistical data, the pre-rKtrans value before CRT had statistical significance in the CR group compared with the non-CR group before CRT. This result further verified that pre-Ktrans could availably distinguish between the two groups. Moreover, other parameters (mid-rKtrans, pre-rKep, mid-rKep, pre-rVe, and mid-rVe) showed no distinct difference between the CR and non-CR groups. Further studies are required to explore the relationship between the rKtrans, rKep, and rVe value and treatment effect at multiple timepoints.

The rΔKtrans and rKtrans discussed in this study were the absolute change of Ktrans and the relative ratio and were more representative and stable. Although these data showed no statistical difference between the pre- and mid-CRT, it explores these data in EC patients receiving CRT.

The project was limited in several ways. First, this exploratory research sample size was not large enough and may have led to bias. Therefore, gathering more cases will be continued to provide more dependent observations. Second, the optimal time of taking DCE-MRI during the treatment has not been determined consistently in clinical practice, though it could be explored in the future. Third, only the DCE-MRI data were obtained, while multiparametric image analysis has become growingly relevant in cancer therapy response prediction because it can offer a more complete physiological tumor evaluation.[23] Thus, further study of correlation analysis of multiparametric functional MRI research combined with PET-CT would be necessary for predicting treatment response for EC. Fourth, the results of this study showed a short follow-up time. Moreover, the overall survival and progression-free survival rates were not recorded. Further studies are required to assess the predictive effectiveness by collecting DCE-MRI parameters at pre-, mid-, and post-treatment.

In conclusion, this study's results demonstrated that the pre-Ktrans was a meaningful predictor of the short-term therapeutic effect of EC treated with CRT.

Ethics approval and consent to participate

No animal was included in the current study. The hospital ethics committee approved this study (ZM201812)

Consent for publication

All patients agreed to participate in the study and a written consent was obtained.

Financial support and sponsorship

This research was supported by Jiangsu Cancer Hospital Program (No. ZM201812).

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
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