An applied study of blood oxygenation level-dependent and arterial spin labeling in early transplant renal function based on renal magnetic resonance angiography examination

Introduction

Renal transplantation represents the optimal treatment for end-stage renal disease (1). Advances in surgical, pharmacological, and monitoring techniques have significantly improved transplant kidney survival rates and patient quality of life (2). However, postoperative complications can still compromise kidney function. Complications after kidney transplant can be divided into surgical and nonsurgical. Nonsurgical complications include delayed graft function (DGF), various types of infections, and cardiovascular disease. Surgical complications include vascular, urological problems, wound infections, and postoperative hernias (3,4). Consequently, early detection is essential. Clinical indicators have certain limitations, whereas renal puncture biopsy can provide information, but it is invasive and poorly reproducible (5). Renal functional magnetic resonance imaging (fMRI), a non-invasive technique, provides morphological and functional information regarding the transplanted kidney. It helps to elucidate renal function in the early postoperative period (6).

Blood oxygenation level-dependent (BOLD) imaging is presently the non-invasive tool utilized in clinical research to assess the distribution of blood oxygen levels (7). BOLD measures tissue oxygen utilization by using deoxyhemoglobin as an endogenous contrast agent. The apparent relaxation rate (R₂*) can potentially reflect the oxygen partial pressure (8). Arterial spin labeling (ASL) utilizes water protons in arterial blood as an endogenous tracer to evaluate tissue perfusion (9). Renal blood flow (RBF) is used as an indicator for quantitative assessment (10).

Although the application of multi-parametric fMRI in transplanted kidney assessment has been reported, existing studies have not excluded patients with significant vascular lesions such as transplanted renal artery stenosis (TRAS) (10,11). The functional alterations observed may be significantly confounded by abnormal blood flow. This limits in-depth analysis of the mechanisms underlying renal microcirculatory and metabolic dysfunction. Furthermore, previous studies have primarily focused on transplanted kidney fibrosis, long-term functional evolution, and the differential diagnosis of complications (12-14). This period is critical, as the transplanted kidney experiences ischemia-reperfusion injury (IRI), immune adaptation, and functional recovery. It is also a stage with a high incidence of complications. Therefore, this study employed non-contrast-enhanced (NCE)-MRA based on free-floating steady-state oscillation to exclude cases with significant vascular anastomotic abnormalities or stenosis. Subsequently, BOLD and ASL imaging techniques were utilized to evaluate their applicability in assessing early graft function status. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-180/rc).

Methods

Study population

This study prospectively consecutively recruited 68 recipients who underwent allogeneic kidney transplantation from May 2022 to August 2024. The donor sources for kidney transplantation in this study included two parts: one part comprised living relatives, and the other part comprised organ donation after death. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Institutional Ethics Committee of The First Affiliated Hospital of Soochow University (approval No. 2022-412), and informed consent was provided by all the patients. All recipients underwent ASL, BOLD, and NCE-MRA. The exclusion criteria were as follows: (I) the presence of magnetic resonance imaging (MRI) contraindications; (II) MRI examination shows the presence of hydronephrosis or renal artery stenosis in the transplanted kidney; (III) poor image quality; and (IV) failure to complete all MRI examinations. During the research process, 10 patients were excluded due to MRI contraindications, hydronephrosis, and renal artery stenosis.

All patients underwent serum creatinine (SCr) testing on the same day as the MRI scan. The estimated glomerular filtration rate (eGFR) was calculated using the Chronic Kidney Disease Epidemiology Collaboration (CKD-EPI) equation (15). Recipients were divided into three groups based on the eGFR: Group A, recipients with good renal allograft function (eGFR ≥60 mL/min/1.73 m²); Group B, recipients with mild-to-moderate impaired renal allograft function (30≤ eGFR <60 mL/min/1.73 m²); Group C, recipients with severe renal allograft function (eGFR <30 mL/min/1.73 m²) (Figure 1). This grouping method is employed to address clinical requirements in the early post-transplant phase concerning risk assessment, treatment guidance, complication early warning, and prognosis evaluation. It possesses a robust theoretical foundation (16-18).

Figure 1 Workflow of patient selection. eGFR, estimated glomerular filtration rate; MRI, magnetic resonance imaging.

Before MRI scanning, we recorded each patient’s systolic blood pressure (SBP), diastolic blood pressure (DBP), and mean arterial pressure (MAP). All patients’ blood pressure remained within a relatively normal range and remained stable throughout the scanning process without the use of vasoactive drugs.

MRI protocol

Before the examination, the recipients were required to fast and dehydrate for 4 hours, and undergo breathing training (breath-holding for more than 15 seconds). Fasting and dehydration were implemented to minimize interference from physiological variables, thereby ensuring the stability and comparability of measurement results. All patients were scanned using a Philips 1.5-T MRI (Ingenia Ambition, Philips Healthcare, Best, the Netherlands), which is equipped with a 28-channel phased array coil. The scanning range extended from below the costal arch to below the pubic symphysis. The scanning sequence included MRI routine scanning and ASL, BOLD, and renal magnetic resonance angiography (MRA). Conventional scanning acquired coronal T2-weighted images (T2WI) and axial T1-weighted images (T1WI) for morphological evaluation. Pseudo-continuous ASL (pCASL) examination was acquired using a three-dimensional (3D) gradient and spin echo (GRASE) sequence. The image parameters were as follows: repetition time (TR), 3,963 ms; echo time (TE), 15 ms; voxel size, 3.75×3.75×8 mm³; field of view (FOV), 240×240×88 mm³; turbo spin echo (TSE) factor, 20. The BOLD examination used gradient echo sequences. The image parameters were as follows: TR, 71 ms; TE, 4.60, 9.20, 14.00, 18.00, 23.00, 28.00, 32.00, 37.00, 41.00, 46.00, 51.00, 55.00, 60.00, 64.00, and 69.00 ms; voxel size, 1.79×2.55×5 mm³; FOV, 300×131×120 mm³; fast field echo (FFE) factor, 15. Renal MRA examination used NCE-MRA of the renal arteries based on free steady-state progression. The image parameters were as follows: TR, 9.4 ms; TE, 4.3 ms; voxel size, 1.56×1.53×2 mm³; FOV, 300×131×120 mm³; FFE factor, 65.

Image analysis

Images were post-processed on a Philips workstation (IntelliSpace Portal v10; Philips Healthcare). For ASL, the image at the level of the maximum renal transverse diameter was selected. The renal cortex was manually outlined on the axial T1WI. This was then replicated on the RBF map. For BOLD, six circular regions of interest (ROIs), each approximately 12 voxels in size, were placed at the upper, middle, and lower poles of the cortex and medulla of the coronal T2WI, avoiding areas of blood vessels, hematomas, and cysts, and replicated on the BOLD map (Figure 2). The corresponding R₂* value of each ROI on the R₂* map was recorded, and the mean value was calculated. An analysis was conducted by two physicians, with 8 and 3 years of experience in abdominal imaging diagnostics, respectively, using a blind method.

Figure 2 An example of RBF and R₂* ROI placement. Representative T1WI (A), RBF maps (B), T2WI (C), and T₂* maps (D) (R₂* = 1/T₂*). Red circles: renal medulla ROI. Blue circles: renal cortex ROI. R₂*, apparent relaxation rate; RBF, renal blood flow; ROI, region of interest; T1WI, T1-weighted image; T₂*, transverse relaxation time star; T2WI, T2-weighted image.

Renal allograft biopsy

Nine patients underwent percutaneous renal biopsy. According to the Banff diagnostic classification criteria (19), the histopathological classification of kidney transplant biopsies was divided into: (I) renal transplant biopsy, normal; (II) antibody-mediated rejection; (III) critical changes, also known as suspected acute T-cell-mediated rejection; (IV) T-cell-mediated rejection; (V) interstitial fibrosis and tubular atrophy; (VI) other acute or chronic lesions; and (VII) other non-rejection lesions.

Statistical analysis

Statistical analyses were performed using SPSS 26.0 statistical software (IBM Corp., Armonk, NY, USA). Measures with a normal distribution were presented as mean ± standard deviation (SD). Measures that did not fit the normal distribution were expressed as median [quartile (Q)1, Q3]. The differences in each index between the cortex and medulla in each group were compared using a paired t-test. The comparisons of general clinical data and MRI indicators among the three groups were performed with one-way analysis of variance (ANOVA) or the Kruskal-Wallis H test, as appropriate. The repeatability of MRI measurements among observers was assessed using the intraclass correlation coefficient (ICC). Categorical variables were compared using the Chi-squared test or Fisher’s exact probability method. To assess potential validation bias arising from insufficient biopsy rates, we conducted corresponding sensitivity analyses. Pearson’s correlation coefficient was used to analyze the correlation between MRI parameters and eGFR. Receiver operating characteristic (ROC) curves were used to assess the differential diagnostic efficacy of MRI parameters for different functional transplanted kidneys. Post-hoc pairwise comparisons were conducted using the DeLong test. A difference was considered statistically significant with a two-sided P value <0.05.

Results

Patient characteristics

This study included 58 patients who had undergone kidney transplantation. Table 1 provides a summary of the study characteristics.

Inter-observer and intra-observer reproducibility for MRI measurements

All the MRI parameters showed excellent agreement. Following the first measurement, the inter-observer ICCs were 0.966 [95% confidence interval (CI): 0.914–0.986], 0.782 (95% CI: 0.423–0.915), and 0.849 (95% CI: 0.617–0.940) for cortical RBF, cortical R₂*, and medullary R₂*, respectively. Following the second measurement, the inter-observer ICCs were 0.957 (95% CI: 0.861–0.984), 0.755 (95% CI: 0.388–0.903), and 0.787 (95% CI: 0.465–0.916). The ICCs within two observers were 0.972 (95% CI: 0.931–0.989), 0.845 (95% CI: 0.611–0.938), and 0.865 95% CI: (0.665–0.946) and 0.943 (95% CI: 0.852–0.978), 0.840 (95% CI: 0.603–0.937), and 0.857 (95% CI: 0.630–0.944), respectively.

Differences in cortical and medullary MRI parameters of transplanted kidneys between groups

Each group of kidney transplant patients had significantly higher mean R₂* values in the renal medulla compared to the renal cortex. Comparisons between the three groups of cortical RBF, cortical R₂*, and medullary R₂* revealed statistically significant differences (P<0.001). Cortical RBF in Group A (259.74±47.52 mL/100 g/min) was higher than that in Group B (166.50±19.79 mL/100 g/min, P<0.001) and Group C (112.76±32.08 mL/100 g/min, P<0.001). Similarly, the cortical R₂* in Group A (10.933±0.996 sec⁻¹) exceeded those in Group B (10.503±1.136 sec⁻¹, P=0.174) and Group C (9.471±0.997 sec⁻¹, P<0.001), as did medullary R₂* of Group A (12.689±1.348 sec⁻¹) compared to Group B (11.609±1.665 sec⁻¹, P=0.014) and Group C (10.785±1.114 sec⁻¹, P<0.001) (Table 1, Figures 3,4).

Figure 3 mpMRI in a 44-year-old man (Patient A, 13 days after surgery) from Group A (eGFR, 95.5 mL/min/1.73 m²), a 44-year-old man (Patient B, 13 days after surgery) from Group B (eGFR, 48.7 mL/min/1.73 m²), and a 46-year-old woman (Patient C, 12 days after surgery) from Group C (eGFR, 21.2 mL/min/1.73 m²). Patient B was confirmed to have acute T-cell-mediated rejection by pathologic biopsy. Patient C had antibody-mediated rejection confirmed by pathologic biopsy. Representative T2WI (A,F,K), T₂* maps (B,G,L) (R₂* = 1/T₂*), T1WI (C,H,M), RBF maps (D,I,N), and renal-MRA maps (E,J,O). Group A, recipients with good renal allograft function (eGFR ≥60 mL/min/1.73 m²); Group B, recipients with mild to moderate impaired renal allograft function (30≤ eGFR <60 mL/min/1.73 m²); Group C, recipients with severe renal allograft function (eGFR <30 mL/min/1.73 m²). eGFR, estimated glomerular filtration rate; mpMRI, multi-parametric magnetic resonance imaging; MRA, magnetic resonance angiography; R₂*, apparent relaxation rate; RBF, renal blood flow; T1WI, T1-weighted image; T₂*, transverse relaxation time star; T2WI, T2-weighted image.

Figure 4 Comparison of RBF (A), cortical R₂* (B), and medullary R₂* (C) among Group A, Group B, and Group C. *, P<0.05; **, P<0.01; ***, P<0.001; ns, no statistical significance. Group A, recipients with good renal allograft function (eGFR ≥60 mL/min/1.73 m²); Group B, recipients with mild to moderate impaired renal allograft function (30≤ eGFR <60 mL/min/1.73 m²); Group C, recipients with severe renal allograft function (eGFR <30 mL/min/1.73 m²). eGFR, estimated glomerular filtration rate; R₂*, apparent relaxation rate; RBF, renal blood flow.

Renal allograft biopsy

Nine patients underwent percutaneous renal biopsy. Four patients had acute T-cell-mediated rejection and five had active antibody-mediated rejection.

Sensitivity analysis

All nine patients who underwent biopsy were excluded from the primary analysis cohort. Differences in parameters were compared between Groups A, B, and C. Following exclusion of these cases with definitive histological diagnosis, we observed that parameter differences between groups A, B, and C remained broadly consistent with the preliminary analysis results (Table 1). This indicates that our grouping based on eGFR remains robust within a broader cohort of patients not validated by biopsy.

Relationships between cortical and medullary MRI parameters of transplanted kidneys and eGFR

Cortical RBF values positively correlated with eGFR (r=0.877, P<0.001). Additionally, cortical R₂* values were positively correlated with eGFR (r=0.536, P<0.001), and medullary R₂* values were positively correlated with eGFR (r=0.359, P<0.05) (Figure 5).

Figure 5 Correlation of RBF (A), cortical R2* (B), and medullary R2* (C) with eGFR. eGFR, estimated glomerular filtration rate; R₂*, apparent relaxation rate; RBF, renal blood flow.

Diagnostic performances of BOLD and ASL

In this study, MRI parameters demonstrated differential discriminatory capabilities for transplanted kidneys across distinct functional groups. RBF exhibited superior performance in distinguishing kidney function across all groups, with higher area under the curve (AUC) values. Regarding tissue oxygenation parameters, cortical R₂* values demonstrated discriminatory capability between Groups B and C (AUC =0.763). Meanwhile, the medullary R₂* value could differentiate between Group A and Group B (AUC =0.724). Further analysis revealed that the diagnostic efficacy of the combined multi-parameter MRI model was significantly superior to that of BOLD. Multi-parametric MRI demonstrated significantly superior diagnostic efficacy to BOLD in distinguishing Group A from Group B (P=0.002) and Group A from Group C (P=0.021, 0.023). Furthermore, ASL parameters yielded significantly higher AUC values than BOLD parameters (P<0.05), highlighting the value of perfusion parameters in transplanted kidney function assessment (Table 2, Figure 6).

Figure 6 MRI parameters and multiple parameters (ASL combined with BOLD) distinguished allografts with different kidney functions. (A) Group A vs. Group B; (B) Group B vs. Group C (RBF overlaps with mpMRI), and (C) Group A vs. Group C. Group A, recipients with good renal allograft function (eGFR ≥60 mL/min/1.73 m²); Group B, recipients with mild to moderate impaired renal allograft function (30≤ eGFR <60 mL/min/1.73 m²); Group C, recipients with severe renal allograft function (eGFR <30 mL/min/1.73 m²). ASL, arterial spin labeling; BOLD, blood oxygenation level-dependent; eGFR, estimated glomerular filtration rate; mpMRI, multi-parametric magnetic resonance imaging; MRI, magnetic resonance imaging; R₂*, apparent relaxation rate; RBF, renal blood flow.

Discussion

Kidney transplantation has significantly increased survival and improved quality of life for patients with end-stage renal disease. However, the incidence of postoperative renal impairment remains high, with its etiology being complex and multifactorial (20,21). ASL and BOLD were initially applied to cerebral function research (22-25). Recently, they have been preliminarily explored for transplanted kidney function assessment (10,26). This study employed NCE-MRA technology based on free-steady-state oscillation to exclude cases of TRAS. Vascular structural factors interfering with functional assessment were controlled. Additionally, the observation window was focused on the period between 1 and 4 weeks post-transplantation. During this period, the transplanted kidney undergoes critical processes including repair from IRI, immune adaptation, and functional establishment. Regarding diagnostic efficacy, RBF measured by ASL was found to be superior to BOLD in predicting the recovery trajectory of graft function. Within the established combined diagnostic model, RBF exhibited dominant predictive contribution. This study provides a novel technical pathway for the early identification of transplanted kidney dysfunction, holding significant clinical translational value.

ASL can identify changes in renal perfusion, which typically accompany allogeneic kidney transplant damage (27). The RBF values of the different transplanted kidney function groups varied significantly in this study (P<0.05). As a circulatory organ (28), early functional abnormalities in transplanted kidneys typically manifest as capillary damage. This impairs renal perfusion, ultimately leading to reduced cortical blood flow. Chhabra et al. (29) studied several papers on ASL assessment of IRI in transplanted kidneys. They found that renal ASL perfusion values were significantly lower in patients with imbalanced transplanted kidneys than in healthy kidney transplant recipients. It was recommended that ASL should be performed within the first 6 months for early detection of renal damage in transplanted kidneys. In addition, Jiang et al. (30) used ASL to assess renal function in patients with long-term survival after renal transplantation, finding that ASL had high diagnostic power and the relevant parameter values had moderate correlation with Banff histological score. All these results indicate that ASL can assess the blood perfusion level of early transplanted kidneys and evaluate the long-term status of transplanted kidney function. It provides valuable information for the diagnosis of different functional states of transplanted kidneys.

The present study shows a significant correlation between transplanted renal cortical RBF values and eGFR, which is consistent with the findings of previous studies. Radovic et al. (10) and Lanzman et al. (31) correlated renal cortical RBF values with eGFR values in 18 and 20 transplanted kidneys, respectively. Their findings revealed a positive correlation. This suggests that when the transplanted kidney function is reduced, the transplanted renal capillaries are damaged, the glomerular filtration rate decreases, and the perfusion distribution changes, resulting in reduced renal cortical blood flow. These factors demonstrate the potential application value of ASL in assessing early functional changes in transplanted kidneys.

The oxygen partial pressure gradient between the renal cortex and medulla is substantial in normal kidneys. Physiologically, the renal medulla has a higher R₂* value than the cortex, and the results support this (32). The results of this study indicate that there was no significant difference in cortical R₂* values between Group A and Group B (P=0.174). However, the cortical R₂* values in Group C were significantly lower than those in Group A (P<0.001). Early renal dysfunction primarily manifests as glomerular and tubular injury resulting from vascular anastomosis and reperfusion damage, with warm ischemia representing a significant contributing factor. Warm ischemia induces energy metabolism disorders in renal tubular epithelial cells, precipitating cellular edema, necrosis, or apoptosis. Concurrently, it activates inflammatory responses, exacerbating tissue damage and microcirculatory impairment (33,34). As the renal cortex belongs to a high blood flow and high oxygen content area, it is insensitive to blood flow perfusion as well as to slight changes in blood oxygen level. As renal impairment progresses, the diminished function of damaged tubular epithelial cells leads to a marked reduction in sodium reabsorption. This alteration results in decreased oxygen utilization within the renal cortex, causing oxygen to be carried away with the bloodstream before being fully utilized. Consequently, deoxyhemoglobin levels decrease, leading to a reduction in R₂*. Moreover, due to the sharp decline in oxygen consumption, the delivered oxygen exceeds the actual capacity required following tissue damage. These processes eventually lead to oxygen accumulation.

Comparisons of renal medullary R₂* values between groups revealed that the medullary R₂* values in Group A were significantly higher than those in Groups B and C (P<0.05). In the early stage of renal dysfunction, local inflammatory reactions, cytokine release, and decreased oxygen consumption cause blood flow to be shunted from the cortex to the medulla, resulting in a relative increase in blood flow in the medulla of the transplanted kidney. Concurrently, the medulla of a transplanted kidney has a special counter-current multiplication system and low efficiency of oxygen extraction. Therefore, it is in a physiological hypoxic state and is particularly sensitive to ischemic hypoxia damage. Early renal tubule injury directly inhibits the active sodium reabsorption process. Under these two influences, on the one hand, medullary blood supply is relatively increased, and on the other hand, the actual consumption of oxygen is greatly reduced. This leads to an “oxygen accumulation” phenomenon in the medulla. This results in a reduction in deoxyhemoglobin content, a decrease in the concentration of paramagnetic substances, and a reduction in R₂*. This is consistent with previous studies (35).

Our experimental results revealed a positive correlation between both medullary R₂* and cortical R₂* and eGFR. Following kidney transplantation, impaired glomerular and tubular function in the transplanted kidney leads to a decrease in glomerular filtration rate. At the same time, reduced oxygen consumption in the renal cortex and medulla results in elevated levels of oxygenated hemoglobin within the transplanted kidney. This indicates early damage may manifest as oxygen accumulation within the transplanted kidney. In addition, studies by Song et al. (36) and Seif et al. (37) demonstrated that BOLD imaging can noninvasively monitor early functional changes in donor-recipient kidneys after renal transplantation.

DGF is a common and severe complication in the early post-operative period following kidney transplantation (38,39). It serves as an important clinical marker reflecting early graft injury. In this study, nine patients were diagnosed with DGF. Only RBF was found to exhibit a statistically significant difference between the DGF and non-DGF groups (P<0.001). The pathological alterations associated with DGF relate to IRI. This compromises the renal microcirculatory system, leading to increased intrarenal vascular resistance and reduced effective blood perfusion (6). This manifests as a significant reduction in RBF values, which aligns closely with the observations in this study. The BOLD R₂* parameter failed to demonstrate discriminatory efficacy. This may be attributed, on the one hand, to the small sample size, which compromised the power of statistical testing. On the other hand, it may relate to the complex pathophysiological mechanisms underlying DGF. Future research should further investigate the potential value of BOLD technology in DGF assessment within larger cohort studies.

ASL has very high diagnostic efficiency in identifying early graft renal function (AUC =0.967, 0.914, and 0.991, respectively), similar to previous findings (13,18). The AUC of both cortical and medullary R₂* values for the differential diagnosis of the functional status of transplanted kidneys reached the level of significance, with high differential diagnostic efficacy. Previous studies (40,41) have shown the efficiency of medullary R₂^* values in diagnosing acute rejection. The combined application of ASL and BOLD significantly enhanced diagnostic efficacy compared to BOLD alone (P<0.05). This technical combination enables simultaneous assessment of RBF perfusion and tissue oxygenation levels in transplanted kidneys. Consequently, it provides a more comprehensive and sensitive identification of early functional abnormalities. Of particular note, ASL parameters demonstrated superior predictive value compared to BOLD in forecasting graft functional recovery. Specifically, elevated perfusion levels correlated strongly with favorable clinical outcomes, whereas persistent hypoperfusion signaled a markedly increased risk of complications.

There are some limitations to this study. Firstly, as a single-center study, the limited sample size and relatively short follow-up period may have reduced the statistical power of the tests. This introduces uncertainty regarding the assessment of long-term prognosis. Constrained by this sample size limitation, we were unable to conduct internal validation. This shortcoming may affect the accurate evaluation of the model’s generalizability. We plan to expand the sample size or initiate multicenter collaborations in subsequent studies, alongside rigorous validation. Secondly, only partial histopathological results were obtained. This reliance on early eGFR grouping carries a risk of validation bias, but sensitivity analyses indicate that its impact is minimal. Furthermore, the study design excluded cases with hydronephrosis or renal artery stenosis. Although this helped to maintain cohort homogeneity, it also introduced selection bias, limiting the generalizability of findings to the entire transplant recipient population. Future studies should incorporate more heterogeneous cases within large-scale, multicenter prospective cohorts. Standardized data collection protocols, long-term systematic follow-up, and rigorous validation of pathological biomarkers are essential to thoroughly validate and refine the findings of this study.

Conclusions

Both BOLD and ASL have the potential to predict renal impairment in allografts. ASL demonstrates better diagnostic efficacy than BOLD. Early kidney transplant patients’ renal function can be accurately and noninvasively evaluated by combining the use of BOLD and ASL. This provides clinicians with more reliable and detailed information in the management of early transplanted kidneys and helps to better monitor and maintain the health of transplanted kidneys.

Acknowledgments

The authors would like to thank Peng Wu, an engineer at Philips, for providing technical support for this article.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-180/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-180/dss

Funding: This work was supported by the Science and Technology Development Program of Suzhou City (No. SYW2025008), the Basic Research Pilot Program of Suzhou City (No. SSD2024049), and the Major Project of the National Medical Device Innovation Center (No. NMED2025KF-05-047).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-180/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Institutional Ethics Committee of The First Affiliated Hospital of Soochow University (approval No. 2022-412), and informed consent was obtained from all the patients.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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