Abstract
Background:
While pulmonary hypertension (HTN) is more common in individuals with chronic renal disease, there is a dearth of information about the development of right ventricular failure. The purpose of this study was to evaluate RV systolic function using tissue Doppler and conventional echocardiography in individuals with chronic renal impairment.
Subjects and Methods:
One hundred participants of both sexes who were above the age of 18 years old were included in this study. They were divided into four equal groups: Groups 1 and 2 comprise individuals with chronic renal disease at Stages 4 and 5, respectively. Group 3 is end-stage renal disease on hemodialysis (HD). Group 4 is a control group consisting of healthy, age-matched, nonrenal subjects who are normotensive, nondiabetic, and do not have any other comorbid conditions.
Results:
Right ventricular basal diameter was significantly higher in groups chronic kidney disease (CKD) V and HD than control. Right ventricle tricuspid annular plane systolic excursion (RV TAPSE) and RV tissue Doppler imaging(S’) were significantly lower in CKD Group V than HD and control group. Pulmonary HTN is present in 22% of renal patients with significantly higher prevalence in HD group. There was a positive correlation between the estimated glomerular filtration rate (eGFR) and RV TAPSE and between eGFR and RV (S’) of CKD IV and CKD V groups. There was a negative correlation between RV TAPSE and pulmonary arterial systolic pressure by echocardiogram of the studied groups. There was a positive correlation between RV TAPSE and RV (S’) of the studied groups.
Conclusions:
HD patients showed better RV systolic indices than CKD Stage 5 patients. Pulmonary HTN, although present in all stages of CKD, showed higher prevalence in HD patients.
Keywords: Chronic renal disease, echocardiography, hemodialysis, right ventricular systolic function, tissue Doppler imaging
INTRODUCTION
In the 21st century, chronic kidney disease (CKD) has become one of the leading causes of mortality and suffering.[1,2]
Early diagnosis and proper monitoring of this major health problem are essential for slowing the progression and reducing the burden of the associated complications.[3] Patients with chronic renal disease show disturbance of the circulatory system, such as hyperdynamic circulation, causing functional and structural cardiac alterations.[4,5]
These changes induce myocardial remodeling in the right ventricle, resulting in systolic and diastolic dysfunctions and cardiomyopathy.[6,7] While individuals receiving regular dialysis have a higher incidence of pulmonary hypertension (HTN) during therapy, there is little information about the development of right ventricular dysfunction. Furthermore, in patients with pulmonary HTN, survival has been related to cardiac function rather than pulmonary pressure values.[8]
The assessment of right ventricle (RV) function by tissue Doppler imaging (TDI) has been established as a common approach to detect preclinical abnormalities and as a reliable predictor of prognosis.[9]
The aim of this work was to assess RV systolic function in patients with chronic renal disease by conventional and tissue Doppler echocardiography.
SUBJECTS AND METHODS
This current study was carried out on 100 subjects aged >18 years old from both sexes. Chronic renal disease was diagnosed by clinical view, laboratory, and imaging tests. The severity of chronic renal disease was evaluated using an estimated glomerular filtration rate (eGFR).[10] The study was done from April 2023 to October 2023 after approval from the ethical committee (approval code: 36264MS91/3/23). Informed written consent was obtained from the patients.
Exclusion criteria were patients with congenital heart disease, significant valvular pathology or arrhythmias, acute causes of kidney injury, or poor image quality of their echocardiographic examination. Subjects were divided into four equal groups: Group 1: chronic renal disease Stage 4 with estimated eGFR 15–30 ml/min, Group 2: Stage 5 with (eGFR <15 ml/min.), Group 3: end-stage renal disease (ESRD) on hemodialysis (HD) and Group 4: control group with healthy age-matched nonrenal subjects who are normotensive and nondiabetic with no other comorbid conditions
All subjects were evaluated by complete history taking, clinical examination, laboratory investigations (serum creatinine and eGFR), 12 lead electrocardiogram (ECG), and radiological investigations (abdominal ultrasound (US) and conventional and tissue Doppler echo).
Conventional echocardiography
In the left parasternal long axis view, the left atrium anteroposterior diameter was measured (Ref. range/male ≤40 mm – female ≤38 mm).[11] The left ventricular diameters (Ref. range/male ≤58 mm – female ≤52 mm)[11] and wall thickness (Ref. range/male ≤10 mm– female ≤9 mm) were measured at the mitral valve tips, ensuring the measurement was perpendicular to the left ventricle’s long axis. Two-dimensional (2D) guided M-mode echocardiography was used to calculate ejection fraction (EF) (Ref. range/male ≥52% – female ≥54%)[11] and fractional shortening (FS). In the apical four-chamber view, pulsed wave Doppler was employed to record transmitral flow at the mitral valve tips. The Doppler mitral flow’s early (E) and late atrial (A) diastolic filling peak velocities, as well as the E/A ratio, were determined. Right ventricular dimensions at the basal level were measured using RV-focused apical four-chamber view just before systole (Ref. rang ≤41 mm).[11] The M-mode US technique was used to measure tricuspid annular plane systolic excursion (TAPSE), which is the displacement of the tricuspid ring in the longitudinal direction of the RV (Ref. range ≥17 mm).[11] Continuous wave Doppler was used to record tricuspid regurge systolic jet velocity. High probability pulmonary HTN includes those with peak tricuspid regurgitation velocity (TRV) >3.4 m/s or TRV 2.9–3.4 m/s with additional echo PH signs.[12] In each view, all cardiac valves were assessed for: morphology and mobility in 2D and flow characteristics using pulsed, continuous, and color Doppler Figure 1.
Figure 1.
(a) Left parasternal long axis (PLAX) view m-mode tracing of the left atrium and aortic root (b) Left PLAX view with m-mode tracing of the left ventricle at the tips of the mitral valve (c) A4C view with pulsed wave Doppler tracing of the mitral flow (d) Right ventricle focused apical 4-chamber view with two-dimensional linear measurements of the right ventricle basal diameter (e) right ventricle focused apical 4-chamber view with m mode tracing of the tricuspid annular plane systolic excursion (f) continuous wave Doppler tracing of the tricuspid valve
Tissue Doppler imaging
A four-chamber view focused on the RV using a tissue Doppler mode with a pulsed-wave Doppler sample volume placed in the basal segment of the RV free wall to obtain (S’), which is defined as the peak longitudinal velocity of the basal RV free wall. Normal cutoff value ≥9.5 cm/s[11] Figure 2.
Figure 2.
Right ventricle focused apical 4-chamber view with pulsed wave tissue Doppler imaging tracing of the right ventricle free wall. IVCT = Isovolumic contraction time, IVRT = Isovolumic relaxation time
Statistical analysis
We used IBM Inc.’s SPSS v26 software (Chicago, IL, USA) for statistical analysis. The four groups were compared using the analysis of variance (F) test with post hoc Tukey testing, and quantitative data were provided as mean and standard deviation. Utilizing the Chi-square test, qualitative variables were analyzed and reported as frequency and percentage (%). Two quantitative variables were correlated to an estimated degree using Pearson correlation analysis. For statistical significance, a two-tailed P < 0.05 was used.
RESULTS
Age was insignificantly different between CKD groups but was significantly higher in CKD groups than control (P < 0.001). Sex was insignificantly different among all groups. Diabetes mellitus (DM) and HTN were significantly different between CKD groups (P < 0.05) Table 1.
Table 1.
Demographic data and comorbidities of the studied groups
| CKD IV (n=25) | CKD V (n=25) | HD (n=25) | Control (n=25) | P | |
|---|---|---|---|---|---|
| Age (years) | 49.8±12.81 | 53.8±14.54 | 48.2±10.47 | 33.3±9.51 | <0.001* |
| P1 | 0.656 | 0.963 | <0.001* | ||
| P2 | 0.362 | <0.001* | |||
| P3 | <0.001* | ||||
| Sex, n (%) | |||||
| Male | 11 (44.0) | 17 (68.0) | 16 (64.0) | 13 (52.0) | 0.294 |
| Female | 14 (56.0) | 8 (32.0) | 9 (36.0) | 12 (48.0) | |
| DM | 5 (20.0) | 5 (20.0) | 1 (4.0) | 0 | 0.037* |
| HTN | 11 (44.0) | 14 (56.0) | 16 (64.0) | 0 | <0.001* |
*Significant P<0.05. Data are presented as mean±SD or frequency (%). CKD=Chronic kidney disease, HD=Hemodialysis, DM=Diabetes mellitus, HTN=Hypertension, P1=P value compared to CKD IV, P2=P value compared to CKD V, P3=P value compared to HD, SD=Standard deviation
LVIDd, LA diameter, and left ventricle (LV) wall thickness were insignificantly different between CKD groups. However, they were significantly higher in CKD groups than control groups (P < 0.001). EF was insignificantly different among all groups most likely due to the exclusion of significant left ventricular impairment to minimize the role of the LV dysfunction on the RV function in CKD patients. Left ventricular diastolic dysfunction (LVDD) was significantly prevalent in CKD groups (50% of renal patients had LVDD of different severity grades) Table 2.
Table 2.
Echocardiographic data of the left heart
| CKD IV (n=25) | CKD V (n=25) | HD (n=25) | Control (n=25) | P | |
|---|---|---|---|---|---|
| LVIDD (mm) | 53.9±5.08 | 50.6±5.57 | 54.3±6.52 | 48±3.35 | <0.001* |
| P1 | 0.122 | 0.993 | 0.001* | ||
| P2 | 0.066 | 0.291 | |||
| P3 | <0.001* | ||||
| LA diameter (mm) | 42.8±5.89 | 43.1±5.44 | 44.2±6.26 | 35.6±2.84 | <0.001* |
| P1 | 0.998 | 0.813 | 0.001* | ||
| P2 | 0.898 | 0.001* | |||
| P3 | <0.001* | ||||
| LV wall thickness (mm) | 11.1±1.88 | 11.2±1.39 | 11±1.41 | 8.9±1.27 | <0.001* |
| P1 | 0.992 | 0.992 | 0.001* | ||
| P2 | 0.943 | 0.001* | |||
| P3 | 0.001* | ||||
| EF (%) | 63.9±6.25 | 64.2±5.87 | 64.2±8.23 | 67.2±3.41 | 0.213 |
| LVDD, n (%) | 13 (52.0) | 12 (48.0) | 13 (52.0) | 0 | 0.001* |
*Significant P<0.05. Data are presented as mean±SD or frequency (%). P1=P value compared to CKD IV group, P2=P value compared to CKD V group, P3=P value compared to HD group, LVDD=Left ventricular internal end-diastolic diameter, LA=Left atrium, LV=Left ventricle, EF=Ejection fraction, LVDD=Left ventricle diastolic dysfunction, CKD=Chronic kidney disease, HD=Hemodialysis, SD=Standard deviation
RV basal diameter was significantly higher in groups CKD V and HD than control (P < 0.001). RV TAPSE and RV (S’) were significantly lower in CKD Group V than in HD and control group (P < 0.001). High probability pulmonary HTN is present in 22% of renal patients distributed as follows (12%, 20%, and 36% in CKD IV, CKD V, and HD, respectively) Table 3.
Table 3.
Echocardiographic parameters of the right heart
| CKD IV (n=25) | CKD V (n=25) | HD (n=25) | Control (n=25) | P | |
|---|---|---|---|---|---|
| RV basal diameter (mm) | 36.4±4.87 | 37.3±3.93 | 39±3.29 | 34.2±2.5 | <0.001* |
| P1 | 0.802 | 0.068 | 0.182 | ||
| P2 | 0.393 | 0.021* | |||
| P3 | 0.001* | ||||
| RA diameter (mm) | 38.3±5.76 | 40.9±6.11 | 43.3±4.67 | 34.8±2.76 | <0.001* |
| P1 | 0.261 | 0.003* | 0.068 | ||
| P2 | 0.316 | 0.001* | |||
| P3 | 0.001* | ||||
| RV TAPSE (mm) | 19.4±3.19 | 16.5±4.25 | 19.8±4.87 | 21.7±3.51 | <0.001* |
| P1 | 0.065 | 0.985 | 0.166 | ||
| P2 | 0.026* | <0.001* | |||
| P3 | 0.314 | ||||
| RV (S`) (cm/s) | 11.6±2.14 | 9.4±2.38 | 10.5±2.93 | 12.6±2.14 | <0.001* |
| P1 | 0.007* | 0.363 | 0.537 | ||
| P2 | 0.019* | <0.001* | |||
| P3 | 0.332 | ||||
| High probability pulmonary HTN | 24.8±6.49 | 28.3±8.18 | 34.8±15.1 | 23.5±2.77 | <0.001* |
| P1 | 0.549 | 0.001* | 0.958 | ||
| P2 | 0.072 | 0.267 | |||
| P3 | <0.001* | ||||
| 3 (12.0%) | 5 (20.0%) | 9 (36.0%) | 0 |
*Significant P<0.05. Data are presented as mean±SD or frequency (%). P1=P value compared to CKD G IV, P2=P value compared to CKD G V, P3=P value compared to HD, RV=Right ventricle, RA=Right atrium, RV TAPSE=Right ventricle tricuspid annular plane systolic excursion, RV (S`)=Right ventricle systolic excursion velocity by tissue Doppler, HD=Hemodialysis, CKD=Chronic kidney disease, HTN=Hypertension, SD=Standard deviation
There was a positive correlation between eGFR and RV TAPSE and between eGFR and RV (S’) of CKD IV and CKD V groups (P = 0.021). There was a negative correlation between RV TAPSE and PASP of the studied groups (P < 0.001). There was a positive correlation between RV TAPSE and RV (S’) of the studied groups (P < 0.001). There was no correlation between the duration of dialysis and (RV TAPSE, RV (S’), and PASP) of HD patients Table 4.
Table 4.
Correlation between (right ventricle tricuspid annular plane systolic excursion and estimated glomerular filtration rate, pulmonary arterial systolic pressure, and right ventricle systolic) and between duration of dialysis and right ventricle tricuspid annular plane systolic excursion, right ventricle and pulmonary arterial systolic pressure
| R | P | |
|---|---|---|
| RV TAPSE | ||
| EGFR | 0.323 | 0.021* |
| PASP | −0.348 | <0.001* |
| RV (S`) | 0.765 | <0.001* |
| Duration of dialysis | ||
| RV TAPSE | 0.036 | 0.863 |
| RV (S`) | 0.08 | 0.702 |
| PASP | −0.194 | 0.351 |
*Significant P<0.05. R: Correlation coefficient. HD=Hemodialysis, eGFR=Estimated glomerular filtration rate, RV TAPSE=Right ventricle tricuspid annular plane systolic excursion, PASP=Pulmonary arterial systolic pressure by echocardiogram, RV (S`)=Right ventricle systolic excursion velocity by tissue Doppler
Case 1
Male patient, 61 years old, hypertensive, diagnosed with CKD 6 months ago, presented to the internal medicine clinic for his regular follow-up. The impairment in the patient renal function was discovered accidentally during routine lab work as a preparation for elective surgery. By examination: He was afebrile, blood pressure (BP) of 130/80 mmHg, respiratory rate of 16 breaths per minute, and heart rate (HR) of 90 beats per minute. His physical exam was nonimpressive, apart from mild pallor. Investigation: RFTs: Serum creatinine was 3.7, and eGFR was 21 ml/min/1.73 m2. ECG: Normal sinus rhythm with signs of left ventricular hypertrophy (LVH). Echo: RV showed impaired RV systolic function with TAPSE 16 mm, TDI S’ 9 cm/s, PASP 25 mmHg with normal RV basal diameter. He diagnosed was subclinical RV dysfunction, and more regular follow-up was recommended Figure 3.
Figure 3.
Case 1 (a) Measurement of peak longitudinal velocity of the basal RV free wall by pulsed wave tissue Doppler and (b) right ventricle tricuspid annular plane systolic excursion by m-mode
Case 2
Male patient, 56 years old, diabetic and hypertensive, diagnosed with CKD for 2 years, presented to the internal medicine clinic with dyspnea with increased effort. By examination: He was afebrile, BP 160/90 mmgh, respiration 25 breaths per minute, and HR 100 beats per minute. His physical examination showed dyspnea, orthopnea, and bilateral lower limb edema Grade II despite being maintained on high-dose diuretic. RFTs: Serum creatinine was 6, and eGFR was 12 mL/min/m2. His last RFTs were 1 month prior and had similar results despite strict BP, blood sugar control, and renal support medication. ECG: Normal sinus rhythm with HR 100 BPM. Echo showed impaired RV systolic function with TAPSE 14 mm and TDI S’ 8 cm/s. PASP was 29 mmgh with normal RV basal diameter. The patient was referred for a permanent AV shunt to start regular HD Figure 4.
Figure 4.
Case 2 (a) Measurement of peak longitudinal velocity of the basal right ventricle free wall by pulsed wave tissue Doppler, (b) right ventricle tricuspid annular plane systolic excursion by m-mode, (c) continuous wave Doppler of tricuspid valve regurge and (d) color Doppler of tricuspid valve regurge
Case 3
A female patient, 47 years old, nondiabetic and nonhypertensive, presented to the nephrology department for her regular tri-weekly HD session. The patient has been on regular dialysis for 13 years. By examination: She was afebrile with HR 95 BPM and BP 110/70 mmHg. She has pallor, mild bilateral lower limb edema, and palpable thrill over the A-V dialysis fistula in the left arm. By auscultation, a pansystolic murmur is heard parasternal. RFTs: Serum creatinine was 4, and eGFR was 13 mL/min/1.73 m2. ECG Normal sinus rhythm with LVH. Echo showed dilated RV with impaired RV systolic function (TAPSE 11 mm and TDI S’ 6 cm/s), moderate TR, and dilated collapsible IVC. PASP was 47 mmHg. The patient was diagnosed with right-side heart failure, and regular follow-up was recommended Figure 5.
Figure 5.
Case 3 (a) Measurement of peak longitudinal velocity of the basal right ventricle free wall by pulsed wave tissue Doppler, (b) right ventricle tricuspid annular plane systolic excursion by m-mode, (c) continuous wave Doppler of tricuspid valve regurge and (d) color Doppler of tricuspid valve regurge
DISCUSSION
A significant worldwide public health issue, CKD is characterized by pathological abnormalities of renal structure or function with preserved GFR or a decline in eGFR below 60 ml/min/1.73 m2 for more than 3 months.[13] Cardiovascular complications such as heart failure, coronary artery disease, atherosclerosis, and HTN are the primary causes of mortality in CKD.[14]To clarify the relationship between the severity of renal disease and right ventricle systolic function, this study sought to evaluate right ventricular systolic function in patients with chronic renal disease using conventional (TAPSE) and tissue Doppler echocardiography.
This study was carried out on 100 participants equally divided into four equal groups: CKD IV group, CKD V group, hemodialysis group, and control group.
In the current study, age was insignificantly different between CKD groups and was significantly higher in CKD groups compared to the control group. In “CKD, prevalence model” developed by Grant Aitken[15] states that there is a clear association between increasing age and higher CKD prevalence. Out of the 100 participants, 57 were males and 43 were females. Gender distribution was shown to be insignificantly different among all groups. Walied et al.[16] reported that there was no significance among groups regarding gender.
According to our results, DM and HTN were present in 14% and 54% of renal patients, respectively, with significant prevalence among CKD groups. Elhusseiny[17] showed that DM and HTN were significantly different among groups being higher in CKD patients.
CKD patients frequently have abnormalities in the structure and function of their left ventricles. LV dilatation affects around 35.8% of patients who begin dialysis. The primary cause of this is elevated preload, which is brought on by several conditions such as anemia, hypervolemia, and (in HD patients) high blood flow arteriovenous fistula (AVF). Volume overload causes a succession of new myocardial sarcomeres to accumulate, which causes LV dilatation (eccentric LVH).[18]
Based on our findings, 17% of renal patients had enlarged left ventricular end-diastolic diameter over the upper limit of normal gender specific, suggesting that chronic renal disease is a major risk factor for LV dilatation. Schneider et al.[19] stated that left ventricle dilatation without LVH was found in 4% of cases. Foley et al.[20] determined that after starting dialysis therapy, especially in the 1st year, left ventricular dilatation, among other changes in heart shape and function, accelerates quickly as renal function falls. These changes occur throughout the pre-ESRD era.
According to our results, LV hypertrophy is the most common structural defect observed in this study and was found in 57% of patients. Similar findings were reported by Jameel et al.[21] LVH was reported in 55% of patients.
In the current study, LVDD was significantly prevalent in CKD groups, with almost equal distribution among them, suggesting an early and persistent association with renal impairment. It is the most common functional defect observed in our study and was found in 50% of patients. Similar findings were reported by Jameel et al.[21] LVDD was reported in 47% of patients.
RV basal diameter was significantly higher in groups CKD V and HD than in the control. This could be explained by the loading conditions of both volume (fluid overload) and pressure (PH) in these groups. Supporting our results, Yahia et al.[22] and Karavelioğlu et al.[23] reported that patients receiving HD had significantly larger right ventricular basal diameters than the control group.
RV TAPSE and RV (S’) were found to be significantly lower in the CKD Group V compared to the HD and control groups in the current study. This shows that the right ventricular systolic function indices have deteriorated in this late stage of CKD and that these indices may improve once dialysis is started. Tanasa et al. (2021)[24] carried out a prospective cohort study enrolling 79 consecutive patients with ESRD starting HD and assessed in four steps – at baseline before HD and at 3, 6, and 12 months. It showed a significant increase in right ventricular free wall longitudinal strain, fractional area change (FAC), and TAPSE values at 3/6/12 months from baseline. HD can improve myocardial perfusion with a steady reduction amid the interdialytic hiatus. In time, this reduction could lower the cardiac chamber size or the pulmonary circulation loading, ultimately improving all the RV systolic indices, as confirmed by our outcomes. The strength of this study (Tanasa et al. 2021) is that it assesses long-term RV function after HD initiation as compared to other studies – including the current study – that were short-term studies evaluating TAPSE or FAC within hours or days but not months after HD initiation.
Pulmonary HTN is present in 22% of renal patients, with its prevalence in groups as follows (12%, 20%, and 36% in CKD IV, CKD V, and HD, respectively), which indicates the presence of risk factors and different mechanisms precipitating pulmonary HTN in all CKD stages. It’s significantly more prevalence in the hemodialysis group further implicates proximal arterio-venous fistula as a main precipitator of pulmonary HTN in this group. Confirming our results, Momtaz et al.[25] reported that patients on HD had statistically significant higher systolic pulmonary pressure compared with those in the control group. Mavrakanas et al.[26] reported that pulmonary artery pressure was significantly different among eGFR different levels groups, being higher in the eGFR 30–59 group. Furthermore, Floccari et al.[27] found that PASP exceeded 30 mmHg in 28.7% of patients, overcoming 40 mmHg in 5% of them. This higher prevalence of pulmonary HTN in dialysis patients cannot be solely explained by high-flow AVF as only half of the hemodialysis patients develop PH, plus its prevalence in different dialysis modalities and different CKD stages.
There was a positive correlation between RV TAPSE and RV (S’) of the studied groups. These results were confirmed by López-Candales et al.[28] A strong correlation was noted between TAPSE and TDI (S’) for this study population.
There was a negative correlation between RV TAPSE and PASP of the studied groups. TAPSE and pulmonary artery pressure measurements exhibited a significant negative correlation, as demonstrated by Floccari et al.[27] It should be noted that individuals in the early stages of CKD who were not receiving dialysis were included in the research by Floccari et al.[27] The discovery of a patient subgroup at risk of getting PH was this study’s strongest point. The authors state that these patients should not be eligible for proximal or high AVF dialysis in the event of abrupt CKD development; instead, they should be considered for distal AVF or peritoneal dialysis. However, in contrast to our study, Floccari et al.[27] showed that there was no correlation observed between eGFR and TAPSE. The different sample sizes and disease severity (Stage III) may explain this difference from our results. However, Dini et al.[29] documented that TAPSE was a significant predictor of eGFR.
The limitations in our study included that it was a single-center study with the sample size was relatively small and it was a cross-sectional study which didn’t allow for the follow-up and observation of the different changes that occur overtime in the same patient. For early diagnosis and management of cardiac problems, we advise more regular cardiac workups for patients with chronic renal disease at various stages, at least at first evaluation and with any change in clinical condition or deterioration of renal function. Echocardiography should also be considered when determining the best course of treatment for ESRD patients, especially those being considered for HD and proximal AVF, as they have a higher risk of developing pulmonary HTN. Either RV TAPSE and TDI S’ or both can be used to evaluate RV systolic function according to the availability of machine and skilled operator. Renal replacement therapy should not be delayed in case of hopeless regain of renal function if at least to preserve RV function. To gain a deeper comprehension of the many alterations that transpire as renal disease advances, further research is required, ideally with a bigger sample size and longer follow-up periods.
Ethical statement
The research was carried out in the Department of Cardiovascular Medicine, Faculty of Medicine, University of Tanta, Egypt, from April 2023 to October 2023 (Approval code: 36264MS91/3/23).
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms. In the form, the patients have given their consent for their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
Conflicts of interest
There are no conflicts of interest.
Funding Statement
Nil.
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