|Year : 2019 | Volume
| Issue : 1 | Page : 138-150
|Increased renal cortical stiffness in patients with advanced diabetic kidney disease
Ayse Selcan Koc1, Hilmi Erdem Sumbul2, Erdinç Gülümsek2
1 Department of Radiology, University of Health Sciences - Adana Health Practice and Research Center, Adana, Turkey
2 Department of Internal Medicine, University of Health Sciences - Adana Health Practice and Research Center, Adana, Turkey
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|Date of Submission||26-Jun-2018|
|Date of Decision||07-Aug-2018|
|Date of Acceptance||09-Aug-2018|
|Date of Web Publication||26-Feb-2019|
| Abstract|| |
We aimed to determine whether cortical stiffness (CS) values obtained by point shear wave elastography (pSWE) were increased in patients with diabetic kidney disease (DKD) according to increased disease stage and to determine the parameters associated with CS value in the same patient group. A total of 120 patients with Type-II diabetes mellitus who developed DKD and 22 healthy controls were included in the study. In addition to routine laboratory tests and renal ultrasonography (USG), CS levels were measured using pSWE. Carotid intima-media thickness (IMT) and aortic-IMT values were measured. Patients were grouped according to DKD stage (Stage I-II-III-IV-V), then the control group was added and, the six groups were compared within themselves. Renal CS values were found to be significantly higher in all stages of DKD than in the control group and were found to be increased in accordance with the increase in DKD stage (P <0.05). When receiver operating characteristic curve analysis was performed for determining patients with Stage IV-V DKD, it was found that AUC was >70% for parathyroid hormone (PTH), common and internal carotid-IMT, NT-proBNP, cortical thickness, and CS values. It was found that cortical thickness and PTH levels were independently associated with renal CS in DKD patients and independently determined the risk of increased CS (>9.0 kPa) in DKD patients (P <0.05). Renal CS is increased with increasing DKD stage and this is closely related to decreased cortical thickness and serum PTH levels. Renal CS measurement should be used during follow-up of a patient as part of the renal USG.
|How to cite this article:|
Koc AS, Sumbul HE, Gülümsek E. Increased renal cortical stiffness in patients with advanced diabetic kidney disease. Saudi J Kidney Dis Transpl 2019;30:138-50
|How to cite this URL:|
Koc AS, Sumbul HE, Gülümsek E. Increased renal cortical stiffness in patients with advanced diabetic kidney disease. Saudi J Kidney Dis Transpl [serial online] 2019 [cited 2021 Sep 22];30:138-50. Available from: https://www.sjkdt.org/text.asp?2019/30/1/138/252903
| Introduction|| |
The most important and frequent (30–40%) cause of chronic kidney disease (CKD) is diabetes mellitus (DM), and 20–30% of patients with DM develop diabetic kidney disease (DKD) in the long term., Renal damage due to Type-II DM is irreversible, and therefore, the diagnosis of patients before developing DKD has prognostic importance. Even though the disease is not completely cured by the early diagnosis of DKD, effective treatment can lead to a slow progression of DKD and may even prevent the development of end-stage renal disease. DKD is characterized by an increase in urinary albumin excretion in the first stage, a decrease in estimated glomerular filtration rate (eGFR) in the following period, and a decrease in renal size with increased fibrosis.
Renal ultrasonography (USG) is performed routinely in patients with Type-II DM without or with the development of nephropathy. Decrease in renal length, width, cortical thickness, and increased renal echogenicity occurs at different stages of nephropathy with progressive renal disease. Shear wave elastography (SWE), which has become popular in recent years, has begun to be used clinically in Type-II DM patients. SWE is a USG study that has been used to evaluate tissue elasticity and stiffness. It has been shown that cortical stiffness (CS) determined by SWE is not affected by systemic and demographic parameters, but is related to renal parenchymal disease and fibrosis.,,,,, One of the major advantages of SWE versus conventional renal USG is that by giving a quantitative value, it provides an objective data on renal elasticity and can be used for clinical follow-up. SWE is used for screening patients for many organ pathologies in addition to kidneys. These include patients with the liver, breast, prostate, pancreas, testicle, thyroid diseases, and renal transplant patients.,,, Although it is known that patients with Type-II DM and diabetic nephropathy have an increase in CS determined by SWE compared with healthy controls,,, there is also information that there is no increase or even decrease.,, As we investigated, we also found conflicting results regarding the CS value measured by SWE according to the increase in stages in patients with DKD.,,,, In some of these studies, there is information that there is an increase in CS with increasing DKD stage,, whereas in some cases, there is a decrease in CS with increasing DKD stage.,,
For this reason, we aimed to determine whether the CS values obtained by point SWE (pSWE) were increased according to the increased disease stage in patients with DKD as well as the parameters related to CS value in the same patient-group.
| Methods|| |
In this cross-sectional study, 152 patients with DKD were screened. One hundred and twenty patients (65 males, 55 females and mean age 59.9 ± 9.1) and 22 healthy controls (13 males, 9 females, mean age 56.2 ± 6.4 years) were included in the study. Twenty-three patients screened for the study but with a renal cortical thickness <10 mm [a radius of 10 × 5 mm is fixed for region of interest (ROI)], and nine patients with a ROI depth of >8 cm for CS measurement were excluded from the study. The KDIGO staging was used in patients' staging for DKD: stage I: eGFR ≥90 mL/min/1.73 m2, stage II: eGFR 60–89 mL/min/1.73 m2, stage III: eGFR 30–59 mL/ min/1.73 m2, stage IV: eGFR 15–29 mL/min/ 1.73 m2, stage V: eGFR <15 mL/min/1.73 m2. For Stages I and II, the presence of markers of kidney damage (urinary albumin/creatinine ratio 30 mg/g) is necessary to diagnose DKD. Patients with hydronephrosis, kidney stones, renal tumor, polycystic renal disease, Type I DM, serious valvular heart disease, decompen-sated heart failure, alcohol addiction, abdominal aortic aneurysm and dissection, inflammatory diseases, hematological diseases, active thyroid disease, chronic liver disease and/or pregnancy were not included in the study.
The study was conducted according to the recommendations of the Declaration of Helsinki about biomedical research involving human subjects and the protocol was approved by the Institutional Ethics Committee. All forms of voluntary consent for all patients were explained in detail and patients were included in the study after receiving written approval.
Detailed history was obtained from all patients and detailed physical examination was performed. Subsequently, baseline characteristics from all groups were recorded, including age, gender, pulse rate, systolic blood pressure (SBP), and diastolic blood pressure (DBP). Body mass index (BMI) was calculated by measuring weight and height. Glucose and HbA1c, renal function tests, lipid panel, NT-proBNP, uric acid, parathyroid hormone (PTH), calcium, phosphorus, and 25-hydroxy Vitamin D levels were evaluated in all patients. eGFR was calculated using the modification of diet in renal disease (MDRD) formula. The eGFR was calculated initially by the Cockcroft-Gault formula and was confirmed to be 30 mL/min/1.73 m2 or higher according to the MDRD Study Group formula as follows: eGFR (mL/min/1.73 m2) = 186 × (serum creatinine) – 1.154 × (age) – 0.203 (0.742 for female patients). Subsequently, renal USG (B mode and SWE) and carotid and abdominal aortic USG (B mode) examinations were performed in addition to routine laboratory examination of all patients.
The abdominal aorta and left and right common carotid and internal carotid (CC and IC) arteries were examined with a high-resolution ultrasound system [(Philips EPIQ 7) equipped with a 1–5 MHz convex and 12 MHz linear transducer (Philips Health Care, Bothell, WA, USA)]. All arteries were examined both longitudinally and transversely. All arteries were scanned longitudinally to visualize the intimamedia thickness (IMT) on the posterior or distal wall of the artery. All measurements were made on frozen images. Two images of best quality were selected for analysis on each study. IMT was defined as the distance from the anterior margin of the first echogenic line to the anterior margin of the second line. The first line represents the intima-lumen interface and the second line represents the collagen-containing top layer of adventitia. Vascular IMT was measured using ultrasonic calipers in the presence of two independent and blind observers. All IMT values were calculated as the average of six measurements. The patients were examined in the supine position with their heads rotated by 45° from where they were scanned for the examination of the carotid arteries. CC-IMT and IC-IMT were measured about 10–20 mm proximal before bifurcation (for the main carotid artery) and at the distal segment of the right and left main carotid artery in the distal segment after bifurcation (for the internal carotid artery), respectively. Abdominal A-IMT was investigated at the level ranging from renal artery bifurcation to iliac artery bifurcation. IMT measured from the posterior wall of the abdominal artery was accepted as A-IMT.
Renal USG examinations were performed after a minimum 8 h of fasting, and after a minimum 20 min of rest. B-mode USG evaluation was first performed on the gray scale and then quantitative Doppler parameters were obtained. Kidney sizes, cortical thickness, and parenchymal echogenicity were assessed on gray scale. Kidney length was measured in the coronal plane from the upper pole to the lower pole of the kidney. Renal width was measured from middle pole, and it was recorded as the distance between renal hilum and renal capsule. Cortical thickness was recorded as the distance from the medial section of the renal medullary pyramid base to the renal capsule.
pSWE evaluation was performed using 1–5 MHz convex abdominal probe and ElastPQ technique. All measurements were performed as described previously. Patients were examined in the left and right lateral decubitus position for renal USG. The measurement was calculated by placing the ROI on the target [Figure 1]a, [Figure 1]b, [Figure 1]c, [Figure 1]d, [Figure 1]e, [Figure 1]f on the conventional USG image, after the target region was determined. The ROI was placed perpendicularly to a vascular-free or cyst-free zone in the renal cortex. The main axis of the ROI was adjusted parallel to the axis of the kidney pyramid (perpendicular to the surface of the kidney). In our study, the ROI target distance was maximum 8 cm and the ROI fixed box size was 1 cm – 0.5 cm. The compression applied was minimized as much as possible during imaging to avoid mechanical pressure to the kidney. Then, the same examination procedure was repeated for the contralateral kidney. In each case, three valid measurements were obtained for each kidney and six total measurements were obtained, and the mean value was calculated. The result is expressed in kPa value.
|Figure 1. Cortical stiffness measurement by point shear wave elastography in patients with stages I–V diabetic kidney disease. (a) In control subjects; normal cortical stiffness measurement of 7.05 ± 1.62 kPa; (b) In stage I diabetic kidney disease: normal or mild increased renal CS measurement of 8.07 ± 4.43 kPa (c) In stage II diabetic kidney disease: mildly increased renal cortical stiffness measurement of 8.27 ± 3.09 kPa (d) In stage III diabetic kidney disease: moderately increased renal CS measurement of 8.27 ± 3.09 kPa (e) In stage IV diabetic kidney disease: severely increased renal CS measurement of 16.51 ± 17.84 kPa (f) In stage V DKD: more severe increased renal CS measurement of 25.27 ± 8.67 kPa|
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| Statistical Analysis|| |
All analyses were performed with Statistical Package for the Social Sciences (SPSS) software version 20.0 (Chicago, IL, USA) statistical software package. The variables were divided into two groups as categorical and continuous variables. The normal distribution of continuous variables was assessed using the Kolmogorov–Smirnov test. The continuous variables in the group were expressed as mean ± standard deviation. Categorical variables are given in numbers and percentages. Continuous variables that showed normal distribution were compared using the Student's t-test and ANOVA, whereas the Mann–Whitney U test and Kruskal–Wallis test were used for non-normally distributed samples. The statistical details between the groups are indicated in the tables. Chi-square (χ2) test was used to compare categorical variables. In the DKD group, univariate correlation analysis of the parameters associated with renal CS was performed using Pearson's and Spearman's correlation method. Statistically significant parameters were included in the linear regression analysis and the parameters most closely related to renal CS were determined. Multivariate logistic regression analysis was performed by including multivariate models with P <0.01 in univariate analyses and statistically significant parameters for independent determination of patients with increased CS (CS ≥9 kPa) in the DKD patient group. Receiver operating characteristic (ROC) curve analysis was performed to determine the advanced stage DKD (Stage IV–V) of the parameters that differed among the study groups. Parameters with area under the curve (AUROC) >0.70 were determined. From these parameters, limit value determination was made to determine the best sensitivity and specificity in the determination of advanced stage DKD. Statistical significance level was accepted as P <0.05.
| Results|| |
Patients were grouped according to DKD stage (Stages I-II-III-IV-V), then the control group was added and the six groups were compared within themselves [Table 1]. There were 28, 20, 26, 24, 22, and 22 people in the study with DKD stages I-II-III-IV-V and control group, respectively.
|Table 1: Demographic, clinical, laboratory, and ultrasound findings of the controls and patients according to stage of diabetic kidney disease.|
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Demographic, clinical, laboratory, and ultrasonographic findings of all the study groups
When the clinical and demographic findings were compared between the study groups, it was found that the SBP and DBP values were significantly higher in DKD patients than in the control group, and this elevation was increased from DKD stages I to stage V [Table 1]. Duration of DM was significantly different between groups and this difference increased from DKD Stage I to Stage V [Table 1]. In laboratory data, glucose, blood urea nitrogen, creatinine, eGFR, low-density lipoprotein cholesterol, high-density lipoprotein cholesterol, triglyceride, HbA1c, NT-proBNP, uric acid, PTH, calcium, and phosphorus levels were found to be significantly different between the groups [Table 1]. Serum levels of blood urea nitrogen and creatinine were significantly increased from the control group to the stage V DKD, whereas the eGFR level decreased in the same way. When comparing vascular USG data, CC-IMT, IC-IMT, and A-IMT values were found to be increased from control group to Stage V DKD. B-mode renal USG data showed that kidney length and width, cortical thickness, and echogenicity were different between the groups. Renal echogenicity was found to be increased, whereas renal thickness, kidney width, and cortical thickness were decreased from DKD Stage I to Stage V. The CS value determined by pSWE was found to be significantly higher in all DKD stages than in the control group, and increased from DKD Stage I to Stage V [Table 1] and [Figure 2].
|Figure 2: Renal cortical stiffness was significantly higher in diabetic kidney disease groups than the control group and this was increased according to advanced stage of diabetic kidney disease.|
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Receiver operating characteristic analysis for determining advanced stage diabetic kidney disease
Clinical, demographic, laboratory, and USG data, which differed between control and DKD patient groups, were evaluated by ROC analysis for the determination of advanced stage DKD (eGFR <30 mL/kg/1.73 m2 or Stage IV–V). Limit values were determined for parameters with AUC > 70% in ROC analysis and these data are shared in [Table 2]. According to this analysis, the advanced stage DKD was determined by the order of the parameters found significant; PTH, IC-IMT, NT-proBNP, CC-IMT, cortical thickness, and CS [Table 2].
|Table 2: ROC curve analysis for predicting advanced diabetic kidney disease (stage IV-V).|
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Parameters associated with cortical stiffness in univariate and multivariate analyses in the diabetic kidney disease patients
Correlation analysis between renal CS and other demographic, clinical, laboratory, and USG parameters was performed in patients with DKD and the significant data are summarized in [Table 3]. Linear regression analysis was performed with parameters significantly related to renal CS [Table 3]. Renal cortical thickness and PTH levels were found to be independently associated with renal CS [Table 3]. The relationship between renal CS and cortical thickness and PTH levels are shown in [Figure 3] and [Figure 4].
|Table 3: The parameters associated with renal cortical stiffness and linear regression analysis for parameters significantly correlated with renal cortical stiffness.|
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|Figure 3: Significant correlation seen between renal cortical thickness and cortical stiffness in patients with diabetic kidney disease.|
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|Figure 4: Significant correlation seen between serum parathyroid hormone and cortical stiffness in patients with diabetic kidney disease.|
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Demographic, clinical, laboratory, and ultrasonography findings which were significantly different in patients with increased cortical stiffness in the diabetic kidney disease patients
Median (minimum and maximum) and mean CS value of the studied DKD patients were 9.08 (4.6–18.1) kPa and 9.69 ± 2.73 kPa, respectively. For the increased CS value, the limit value was taken as 9.0 kPa and patients were divided into two groups as CS ≥9.0 kPa and CS <9.0 kPa. Demographic, clinical, laboratory, and USG parameters of patients with CS ≥9.0 kPa and CS <9.0 kPa were compared [Table 4]. In patients with elevated CS, the duration of DM, female sex, total cholesterol and PTH levels, nephropathy and renal echogenicity stages, and CC-IMT values were significantly higher and renal width and cortical thickness values were significantly lower and these parameters are shown in [Table 4].
|Table 4: Demographic, clinical, laboratory, and ultrasonography findings in patients with increased cortical stiffness in the diabetic kidney disease patient group showing significant difference.|
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Identification of patients with increased cortical stiffness in the diabetic kidney disease patients
When the parameters found to be significant on univariate analysis for determining patients with elevated CS (≥9 kPa) were evaluated by logistic regression analysis, PTH levels and cortical thickness were found to independently predict the risk of having increased CS (OR: 1.147 95% CI: 1.063–1.237 and P = 0.016, and 0R:0.766 95% CI: 0.652–0.899 and P = 0.001, respectively). According to this analysis, it was determined that every 20 pg/mL increase in serum PTH level and 1 mm decrease in cortical thickness increased the risk of elevated CS by 14.7% and 18.7%, respectively.
| Discussion|| |
The most important finding of our study was the increase in the CS value with the increase in the DKD stage, and also finding a higher renal CS in patients with DKD compared to healthy controls. Our study is the first study in which all stages of DKD are discussed and the increase in the CS value with the increase in the DKD stage is shown. The SWE study is a USG study used to evaluate tissue elasticity and, CS obtained from renal cortical SWE has become a more popular study to determine renal parenchymal disease.,,,,, Fibrosis occurring in renal parenchyma is the most important sign of renal disease and makes changes in renal mechanical properties and these changes can be measured objectively by SWE. Renal SWE studies have been shown to be useful in identifying renal fibrosis, identifying renal allograft rejection, diabetic nephropathy, and CKD.,,,,, However, renal SWE data are not indicated in the USG reports and are only measured in specific diseases or in academic studies, because CS limit values are not determined clearly in patients with nephropathy, and in the case of healthy individuals, and because it is still not possible to perform a renal SWE study in some clinics. The CS change obtained by SWE has begun to be used in DKD recently, there are conflicting results with increase and decrease in stages and there are no clear data on the limit value. Recently, a study by Bob et al reported a decrease in the CS value with an increase in the DKD stage. In the same study and in previous studies of the same authors, CS values were reported to be significantly lower in patients with DKD when compared to CS values between the control group and DKD patients., The CS values measured by SWE in Stages I, II, III, IV, and V CKD patients were 2.34, 2.44, 2.12, 2.06, and 2.08 m/s, respectively, and the CS value in the control group was reported as 2.58 m/s. The study by Goya et al reported differently from the previous study. They found that patients with DKD had higher CS values than healthy controls, but had decreasing CS values with increasing stages of DKD. In this study, the CS values of Stages I, II, III, IV, and V CKD patients were found to be 2.87, 3.14, 2.95, 2.68, and 2.55 m/s, respectively, and the CS value of the control group was reported to be 2.35 m/s. The relationship between increased DKD stage and fibrosis is clearly known, increased DKD stage and reduced CS in these two studies are debatable. However, Bob et al found that the most important limitation in the study was that the ROI distance used for CS measurement of patients with DKD was much deeper (>8 cm) than the control group. This may be the most important reason for decreased CS in patients with DKD compared to controls and the absence of CS increase in progressing DKD stages. Because the inverse relationship between increased ROI depth and CS is clearly demonstrated, ROI >8 cm was an exclusion criterion in our study and in all other SWE studies., Another reason may be that the number of patients with Stage IV–V DKD in both studies is very small, 30 and 29, respectively., The average ROI distance in our study was similar in the controls and patients with different DKD stages, also the number of patients with Stage IV–V DKD included in the study was 42. In addition, 22 patients, with a majority being in Stage IV-V, were excluded from our study because the cortical thickness was <10 mm.
There are two studies similar to our study conducted in patients with diabetic nephropathy. In one of these studies, the study group was divided into four groups, namely, normal, microalbuminuria and macroalbuminuria groups according to the urinary albumin excretion in the DKD patients and healthy control group and it was reported that increase of albuminuria increases CS. In the same study, patients with Stage III DKD had higher CS than those with stage II DKD, with 2.98 m/s versus 2.53 m/s, respectively. Stage I-II-III DKD patients were included in this study, but Stage IV–V patients were not. Another study showing increased CS with increasing DKD stage was conducted by Hassan et al. In this study, patients with Stage IV DKD were reported to have higher CS values than those with stage III DKD. Unlike these two studies, all stages were evaluated in our study, and it was determined that there was a more significant CS difference between Stage I and Stage V DKD, especially in the sub-group analysis.
One of the most important aims of current treatment of DM is to prevent the development of DM-induced nephropathy or to stop the progression of DKD by diagnosing it at an early stage. For this purpose, blood glucose levels and blood pressure levels are the targets to be controlled. However, despite these treatment options, development of nephropathy cannot be fully controlled. DKD is diagnosed with micro- or macro-albuminuria, changes in renal size and morphologic pattern of decrease in cortical thickness, and changes in fibrosis formation in advanced stages. The main characteristic finding in Type II DM is interstitial fibrosis in the renal parenchyma, which is the main characteristic finding for renal dysfunction. Histological examination with renal biopsy shows the ongoing fibrosis clearly but cannot be used because it is an invasive procedure. Detection of microalbuminuria in the urine is important for the earliest diagnosis of DKD and microalbuminuria is a strong predictor of DM-associated nephropathy., However, in addition to DM, microalbuminuria is affected by HT, exercise and blood glucose levels and may vary by 40–50% during the day. Another study is the morphological evaluation of renal USG. With conventional USG, renal size, cortical or parenchymal thickness, renal echogenicity, and renal resistive index are evaluated. However, the morphological changes are clear only when renal function deteriorates in advanced stages of DKD. For this reason, a more objective and stable parameter is needed for the early diagnosis of patients with DKD. SWE is a promising and non-invasive study that shows the renal elasticity or tissue stiffness objecttively and can be used for this purpose. The most important problem for renal SWE is deeper placement and harder measurement than other organs. It is known that experimental studies on rats and rabbits and biopsies in renal transplant patients have an increase in renal CS when fibrosis is objectively indicated.,,, Despite the absence of a histological examination in our study, it has been shown that CS values are increased with increasing stage of DKD, which is interpreted as related to DKD pathophysiology.
To the best of our knowledge, our study is the first in the literature including patients with all stages of DKD and showing that increase in DKD stage also increases CS. We also found that when the CS limit was taken as 8.5 kPa, we determined the presence of Stage IV-V DKD (eGFR <30 mL/kg/m2) with acceptable sensitivity and specificity.
Our study has some important limitations. First, the study was conducted in a single center and the number of patients included in the study is relatively small. There is a need for a multi-centered study with more patients. In our study, there was no histopathological evaluation determined by renal biopsy, which is the gold standard for the development of nephropathy, which could make our findings more meaningful when evaluated together. In addition, some patients were excluded from the study (surface-kidney distance >8 cm and renal cortical parenchyma thickness <1 cm) because our ROI target distance was maximum 8 cm and ROI constant box size was 1–0.5 cm; therefore, our data cannot be used for patients with advanced atrophic (<10 mm) and deep-located (>8 cm) kidneys.
| Conclusion|| |
According to our results, renal CS is increased with increasing DKD stage and this is closely related to decreased cortical thickness and serum PTH levels. According to our study, in addition to the conventional renal USG examination used for morphological evaluation for DKD, CS measurement should also be used as a routine follow-up. Patients who have an increase in renal CS during follow-up or patients who have CS ≥8.5 kPa should be closely monitored and treated. When the results of previous data and our study are evaluated together, CS value determined by SWE is simple, practical, objective, reproducible, reliable, and cost-effective to be used objectively in the diagnosis of early stage DKD. However, there is a need for a multicenter study which includes a larger number of patients receiving standardized measurement techniques and methods.
Conflict of interest:
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Ayse Selcan Koc
Department of Radiology, University of Health Sciences - Adana Health Practice and Research Center, Adana
[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2], [Table 3], [Table 4]
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