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Diffusion-weighted MRI-Derived ADC and tumor volume as predictive imaging markers for neoadjuvant chemotherapy response in muscle-invasive bladder cancer

BMC Medical Imaging volume 25, Article number: 3 (2025) Cite this article

Abstract

Background

This prospective study tested the hypothesis that the apparent diffusion coefficient (ADC) value and tumor volume (TV) measured in diffusion-weighted magnetic resonance imaging (DW-MRI) before, during, and after the treatment are quantitative imaging markers to assess tumor response in muscle-invasive bladder cancer (MIBC) patients undergoing neoadjuvant chemotherapy (NAC).

Methods

Multi-parametric MRI was prospectively done for MIBC patients at 3 time points. Pre-treatment ADC value, pre-treatment TV, as well as, percent of changes (ΔADC%, and ΔTV%) in these parameters at mid- and post-treatment relative to baseline were calculated and compared between the patients with and without clinical complete response (CR). Also, further analysis was carried out based on the groups of patients with and without overall response (OR). Two different methods of ADC estimation including single-slice ADC measurement (ADCsingle-slice) and whole-lesion ADC measurement (ADCwhole-lesion) were used.

Results

A total of 50 eligible patients were included in the analysis. Of these, 20 patients (40%) showed clinical CR to treatment, while 30 (60%) did not. Our results showed that although there was no significant difference between the two groups of patients with and without CR in terms of mid-treatment ΔADC% and mid-treatment ΔTV%, significant differences were observed in terms of the pre-treatment ADC (p < 0.01), pre-treatment TV (p < 0.001), post-treatment ΔADC% (p < 0.05), and post-treatment ΔTV% (p < 0.05). The results of the OR-based analysis were in line with the CR-based results. There was also a strong and significant correlation between ADCsingle-slice and ADCwhole-lesion measurements (r > 0.9, P < 0.001).

Conclusion

Pre-treatment ADC, pre-treatment TV, post-treatment ΔADC%, and post-treatment ΔTV% could be considered as promising quantitative imaging markers of tumor response in MIBC patients undergoing NAC. Moreover, mid-treatment ΔADC% and mid-treatment ΔTV% should not be used as predictors of tumor response in these patients. Further larger studies are required to confirm these results.

Peer Review reports

Introduction

Muscle-invasive bladder cancer (MIBC) is one of the leading causes of mortality in patients with genitourinary cancer [1]. Neoadjuvant chemotherapy (NAC) is nowadays widely used for the treatment of MIBC, but only less than half of patients experience a substantial response to the NAC [2]. Thus, early assessment of the response to the NAC may allow to prevent the potential toxicity from ineffective therapy. Integrating non-invasive biomarkers into clinical practice could significantly enhance patient management in MIBC. Key advantages of these markers include avoiding unnecessary chemotherapy, making early treatment decisions, and using personalized therapy [3, 4]. This emphasizes the need for non-invasive markers for predicting and assessing tumor response.

Diffusion-weighted magnetic resonance imaging (DW-MRI) can provide functional information related to tumor characteristics and response to chemotherapy [5, 6]. There is an increasing body of evidence exploring the role of apparent diffusion coefficient (ADC) value measured in DW-MRI, as a promising imaging marker for predicting and monitoring response to chemotherapy in different tumor types [6,7,8,9,10,11,12], but research in bladder cancer patients treated with NAC is scarce. In a recent study by Hafeez et al. [11], the predictive role of post-treatment ADC has been shown in MIBC patients but, no mid-treatment MRI was done to evaluate the association of mid-treatment values with tumor response. In another study by Zhang et al. [12], MIBC patients who underwent MRI before and after the NAC were considered but, the mid-treatment MRI was overlooked. However, early identification of clinical response based on a mid-treatment imaging marker may help us in detecting the responders, and provide a chance to obtain alternative effective therapy for non-responders. To the best of our knowledge, there is no study on the simultaneous investigation of the pre- mid-, and post-treatment imaging markers, as potential indicators of tumor response in these patients.

Therefore, this prospective study was performed to investigate whether the ADC value measured in DW-MRI, as well as tumor volume (TV) before, during, and after the treatment are potential imaging markers to determine tumor response in MIBC patients treated with NAC.

Methods

Study design

This prospective cohort study was conducted at two tertiary hospitals in Tehran, Iran, from July 2019 to July 2021. Consecutive male and female patients with histologically confirmed MIBC (clinical stage T2-T4a) who had undergone initial transurethral resection of bladder tumor (TURBT) were assessed for eligibility. All patients were candidates for platinum-based neoadjuvant chemotherapy and had a performance status of 0–2. The study included patients with adequate baseline bone marrow and hepatic function. This study was conducted in accordance with the Declaration of Helsinki, and the protocol was approved by the ethics committee of Shahid Beheshti University of Medical Sciences (IR.SBMU.UNRC.REC1398.14). The patients provided signed informed consent before inclusion in the study.

Treatment

The patients with creatinine clearance greater than 60 ml/min were given cisplatin on days 1 and 8 every 21 days at a dose of 35 mg/m2 for 60 min. They were also given gemcitabine intravenously at a dose of 1250 mg/m2 for 30 min on days 1 and 8, every 21 days for up to four cycles. Patients with creatinine clearance less than 60 ml/min were given carboplatin (AUC = 4, intravenously over 30 min) on day 1 every 21 days. In addition, they were given gemcitabine at a dose of 1000 mg/m2 for 30 min on days 1 and 8, every 21 days for up to four cycles. The carboplatin doses were adjusted for renal function using the Cockcroft-Gault formula as per label.

MRI examination

All MRI examinations were performed using a 1.5 Tesla MRI machine (Magnetum Avanto, Siemens, Erlangen, Germany) with a pelvic phased array coil. Pelvic MRI including DW imaging was performed before (pre-treatment), after two cycles (mid-treatment), and after completion of chemotherapy (post-treatment), based on the protocol proposed for multiparametric MRI (MP-MRI) for bladder cancer by Panebianco et al. [13]. Dynamic contrast-enhanced (DCE) study was only performed in the pre-treatment setting. The specifications of MP-MRI performed for the patients were as follows: axial, coronal and sagittal T2 weighted images (T2WI) (slice thickness: 4 mm; slice gap: 0.3 mm; number of excitation (NEX): 1; field of view (FOV): 23 cm; Matrix: 256*189–256; time of repetition (TR): 5000; time of echo (TE): 80), axial DWI (slice thickness: 4 mm; slice gap: 0.3 mm; NEX: 10–15; b values: 0-800-1000; FOV: 27 cm; Matrix: 128*109; TR: 4500; TE: 88), axial pre-contrast non-fat saturated T1WI (slice thickness: 5 mm; slice gap: 1 mm; NEX: 1; FOV: 30 cm; Matrix: 256*189–256; TR: 540; TE: 20), and axial DCE fat saturated T1WI (slice thickness: 2 mm; slice gap: 0.3 mm; NEX: 1; FOV: 30 cm; Matrix: 256*214; time of TR: 3.2; TE: 1.2).

Image analysis

All the performed images were evaluated by a radiologist with 10 years of experience in body MRI who was blinded to the pathology result of the patient. For TV evaluation, ROI was drawn in each axial T2WI image from the first image with tumor appearance until the last one in each pre-, mid-, and post-treatment MRI study. For ADC extraction, the ROIs were drawn in DWI images with the highest b-value and then transferred to ADC maps in each pre-, mid-, and post-treatment MRI (Fig. 1). To ensure the measurements’ accuracy and prevent the inclusion of the uninvolved bladder wall, the DWI/ADC maps and DCE (only in pre-treatment MRI) studies were reviewed in conjunction with the T2WI sequence. It is important to note that using a consistent slice thickness and slice gap for both the T2WI and DWI sequences facilitated the localization of the lesion in a similar position across all slices. Two different methods of ADC estimation including single-slice ADC measurement (ADCsingle−slice) and whole-lesion ADC measurement (ADCwhole−lesion) were used. The rationale for employing two distinct methods of ADC estimation was the intratumoral heterogeneity characteristic of bladder cancer and its potential impact on treatment outcomes [14]. We utilized a single-slice ADC map for the largest segment of the lesion to identify the most aggressive part of the tumor potentially. This approach also aimed to minimize the influence of artificially high ADC values from urine in the bladder periphery, thereby ensuring a more accurate assessment of the tumor itself. For extraction of ADCwhole−lesion, the ROI was drawn from the first image with tumor appearance until the last one, and for extraction of ADCsingle−slice, the ROI was drawn at the largest cross-sectional area of the tumor. Drawing the ROI for ADC evaluation in bladder cancer is challenging due to the potential interference of high ADC values from adjacent urine, particularly in small lesions where the peripheral region is proportionally larger. Despite these challenges, considering the relatively small size of our cohort, we decided to include these smaller lesions to maintain a comprehensive analysis. To mitigate the impact of urine on the ADC measurements, we employed the single-slice ADC method, aiming to reduce distortion and enhance accuracy. OsiriX DICOM viewer 13.0.1 (Pixmeo SARL, Bernex, Switzerland) was used to draw the ROIs.

Fig. 1
figure 1

Representative images indicating ROIs in ADC maps of (a) pre-treatment, (b) mid-treatment, and (c) post-treatment MRIs. For ADC extraction, the ROIs were drawn in DWI images with the highest b-value and then transferred to ADC maps in each pre-, mid-, and post-treatment MRI

Full size image

Percentage changes of ADC (ΔADC%), and TV (ΔTV%) in mid-treatment and post-treatment values were calculated as the percent change of ADC and TV relative to the baseline value for each parameter. In cases with no lesion visualization in mid-/post-treatment DW-MRI, the higher ADC value measured in our study was considered the ADC of the disappeared lesions.

Outcomes and assessment

The primary outcome of the study was to evaluate the clinical complete response (CR) to chemotherapy [15, 16]. If there was no evidence of a primary tumor (T0) on cystoscopy with tumor site biopsy, urine cytology, and cross-sectional imaging, the patient was considered to have a clinical CR. Also, clinical overall response (OR) was considered as the secondary endpoint, and defined as downstaging to non-MIBC (< T2) [11, 17]. This assessment was conducted four weeks after the completion of treatment using a cystoscopy procedure and imaging. A timeline flowchart indicating the sequence of events is shown in Fig. 2. The cystoscopy was performed by an independent urologist who was blinded to the treatment. Only eligible patients who had pre-treatment MRI, and post-treatment cystoscopy were selected to be included in an available-case analysis.

Fig. 2
figure 2

Timeline flowchart indicating the sequence of events

Full size image

Statistical analyses

The association between categorical variables was assessed by Pearson’s chi-square and Fisher’s exact tests. Imaging parameters were compared between responders and non-responders using the Mann-Whitney U test. Within-group changes in pre-treatment values after treatment were assessed using paired t-test. Pearson’s correlation coefficient was used to evaluate the strength of the relationship between two ADC estimation methods, and also their relationship with TV and tumor characteristics. All statistical tests used in the study were two-sided, and any p-values that were less than or equal to 0.05 were considered to be statistically significant. The statistical analyses were conducted using IBM SPSS version 23 (IBM Corp., Armonk, NY, USA).

Results

Characteristics of patients

Between July 2019 and July 2021, 62 MIBC patients were prospectively assessed using multi-parametric MRI at 3 time points pre-, mid-, and post-NAC. From these, a total of 50 eligible patients who had pre-treatment ADC value and post-treatment cystoscopy were included in our available-case analysis. Of these, 20 patients (40%) showed clinical CR to the NAC, while 30 (60%) did not. There were also 29 (58%) patients with clinical OR and 21 (42%) without clinical OR. Patients’ characteristics are indicated in Supplementary Table 1. Also, the association between patients’ characteristics and clinical CR is shown in Table 1. As shown in this Table, age, sex, tumor stage, grade, and chemotherapy regimen were not associated with CR; however, the nodal status was significantly associated with CR. Among baseline variables, a significant association was found between age > 65 and Gem/Carbo regimen (P < 0.001).

Table 1 The association between patients’ characteristics and clinical complete response
Full size table

Pre-treatment imaging parameters

A significant and strong correlation was found between pre-treatment ADCsingle-slice and ADCwhole-lesion (r = 0.926, P < 0.001). Also, weak and negative correlations were found between pre-treatment ADC measurements with pre-treatment TV values (rwhole-lesion= -0.360, P = 0.015; rsingle-slice= -0.312, P = 0.037). Significant but weak correlations of T stage with pre-treatment TV, ADCsingle-slice, and ADCwhole-lesion were found (r = 0.353, P = 0.016; r= -0.321, P = 0.026; r= -0.308, P = 0.032, respectively). Also, significant weak correlations of nodal status with pre-treatment TV, and ADCsingle-slice were observed (r = 0.390, P = 0.007; r= -0.357, P = 0.013, respectively).

The pre-treatment imaging parameters were compared regarding the response status (Table 2). As shown in Table 2, significant differences were observed in terms of pre-treatment ADCsingle-slice, ADCwhole-lesion, and TV between patients with and without clinical CR to the NAC. Compared with non-responders, the mean ADC of responders was higher, and their mean TV was lower at the pre-treatment time point. Almost similar results were observed when patients were divided into clinical OR and non-OR groups. Thus, significant differences were observed regarding pre-treatment ADCwhole-lesion, and TV between patients with and without clinical OR (Table 2), although for ADCsingle-slice, a trend towards significance was reported (P = 0.055).

Table 2 Comparison of pre-treatment imaging parameters between patients with and without clinical complete response to chemotherapy
Full size table

Mid-treatment imaging parameters

As noted for pre-treatment ADC values, a significant strong correlation was also found between mid-treatment ADCsingle-slice and ADCwhole-lesion (r = 0.962, P < 0.001).

As shown in Fig. 3, the pre-treatment ADC values significantly increased in both groups of patients with and without CR at the mid- and post-treatment MRIs (within-group changes, P < 0.01). Also, a significant decrease relative to the pre-treatment TV was observed at the mid- and post-treatment images in the two groups of patients (within-group changes, P < 0.05).

Fig. 3
figure 3

Comparison of mean ADCsingle-slice between patients with and without CR at each time point. The pre-treatment ADC values significantly increased in both groups of patients with and without CR at the mid- and post-treatment MRIs (within-group changes, P < 0.01)

Full size image

As indicated in Table 3, there was no significant difference between patients with and without CR in terms of mid-treatment ΔADC% and ΔTV%. Similar results were observed when patients were divided into clinical OR and non-OR groups.

Table 3 Comparison of percent changes in mid-treatment parameters between patients with and without clinical complete response to chemotherapy
Full size table

Post-treatment imaging parameters

The post-treatment ADCsingle-slice and ADCwhole-lesion were found to be strongly correlated (r = 0.977, P < 0.001).

Significant differences were observed in terms of the post-treatment ΔADC%single-slice, ΔADC%whole-lesion, and ΔTV% between patients with and without CR to the NAC (Table 4). In the clinical CR group, our results showed an average increase of 54.84%, and 44.94% for ΔADC%single-slice, and ΔADC%whole-lesion, respectively, but in the non-CR group, data only showed an average increase of 23.54%, and 18.16% for ΔADC%single-slice, and ΔADC%whole-lesion, respectively. Also, an average decrease of 77.49% and 62.69% was observed for ΔTV% in responders, and non-responders, respectively. Similar results were observed when patients were divided into clinical OR and non-OR groups (Table 4).

Table 4 Comparison of percent changes in post-treatment parameters between patients with and without clinical complete response to chemotherapy
Full size table

Discussion

In recent years, ADC measured in DW-MRI has gained interest as a potential imaging marker for chemotherapy response. During cancer therapy, a decrease in cellular density due to treatment-induced cell death and apoptosis can lead to an increase in ADC values [6]. This increase in ADC is associated with favorable treatment response, and changes in tumor size. Some previous studies have shown that changes in TV and ADC after the start of NAC can be indicative of the final response to treatment [5, 7, 18,19,20].

Our study supports findings from a recent study in MIBC patients treated with NAC, indicating a greater increase of post-treatment ADC in responders versus non-responders. In a study of 48 MIBC patients, Hafeez et al. [11] showed that NAC response (< T2) was associated with a significant increase in post-treatment ΔADC% compared to poor response (21.70% versus 8.23%, respectively; p = 0.013). Also, similar results were indicated by the authors in 34 MIBC patients treated with chemoradiation [17]. However, no mid-treatment MRI was done in these studies to assess the association of mid-treatment values with the outcome. As an important result in our study, we observed that mid-treatment ΔADC% was not related to tumor response, probably in order to slow changes of ADC during the treatment course of these patients. Thus, the mid-treatment ΔADC could not be considered a reliable tool to assess early treatment response in MIBC patients.

It should be noted that the timing of ADC increase is substantially variable depending on the type of tumor and treatment. Some studies in breast, head and neck, cervical, and rectal cancers have indicated an increase in ADC within the initial two weeks of chemotherapy or radiotherapy [5, 19, 20]. Nevertheless, several other studies in other patients including breast, and prostate cancer patients reported an ADC increase at later time points (e.g. at 3 months or beyond) [8, 21]. In patients with locally advanced breast cancer undergoing neoadjuvant chemotherapy, Sharma et al. [19] reported that the highest sensitivity in distinguishing between responders and non-responders was observed after the third cycle of treatment, although an increase in ADC could be observed after the first cycle. In a prospective multicenter study of 272 breast cancer patients enrolled at 10 institutions, Partridge et al. [8] indicated that ΔADC was not predictive of CR at early treatment (3 weeks), but after 12 weeks, the mean ΔADC was higher in CR patients than in non-CR patients (50% and 36%, respectively). These results are highly consistent with our study, in which a significant difference in ADC value was observed after 12 weeks of treatment initiation.

In our study, the mean pre-treatment ADC of the CR group was significantly higher than that of the non-CR group. The relationship between pre-treatment ADC values and tumor response has been studied in various contexts, but conflicting results have been reported. Although some previous studies, consistent with ours, have indicated that a higher pre-treatment ADC value may be related to better tumor response [22], several other studies showed paradoxical results [23, 24]. Moreover, in some studies conducted in breast cancer patients undergoing NAC, no statistical differences were reported in pre-treatment ADC between responders and non-responders [7, 8, 25].

In our study, no association was found between NAC response and the main characteristics of patients, including age, sex, tumor stage, grade, and chemotherapy regimen, except for nodal status. Our results are consistent with previous studies, where no association was found between age, sex, tumor stage, and chemotherapy regimen with NAC response [26,27,28].

Previous studies indicated the overall agreement between DWI findings and histopathological results was significantly better than that of conventional imaging methods, with a Kappa value indicating strong agreement (Kappa = 0.756). This suggests that DWI can be a reliable method for accurately staging bladder cancer [29]. High diagnostic performance of mp-MRI, including the DWI sequence, was found for detecting muscle invasion in different subtypes of urothelial carcinoma [30]. Also, previous studies stated that the shape of the tumor signal on DWI could potentially serve as an imaging biomarker to predict the clinical aggressiveness of bladder cancer [31].

Some previous studies consistent with our results indicate that lower ADC values correlate with higher tumor stages across different types of cancers [29, 32,33,34]. This relationship suggests that ADC derived from DWI can be an effective imaging biomarker for evaluating tumor characteristics and staging. Gupta et al. [34] in a study on patients with bladder cancer concluded that MRI is an effective tool for determining T stage. Another research showed that ADC values are negatively correlated with pathological T stages in bladder cancer [29]. As the T stage increases, ADC values tend to decrease, highlighting the potential of ADC as a biomarker for assessing tumor invasiveness. Further research with a larger number of patients is warranted to solidify these findings and explore their clinical applications in oncology.

This study has some limitations. As the main limitation, the patient population is relatively small, and further larger studies are required to confirm the findings. Also, some P-values in our study are close to the threshold of significance, and thus, these results should be interpreted with caution. As a technical limitation, it was difficult to delineate a region of interest on an ADC map in cases of small bladder cancer. This challenge arises particularly due to the very high ADC values in the adjacent urine within the bladder and very low ADC values in the normal bladder muscularis layer, potentially reducing the reliability of ADC values in these small bladder lesions. Moreover, due to technical factors, findings from a single study are not widely generalizable. The lack of standardization for ADC measurement technique should be considered as an inherent limitation of such studies, and thus a certain cut-off for ADC value could not be universally applied. However, previous studies showed that ADC measurements appear to be highly reproducible in different settings [5]. As a positive point, the coefficient of variance of ADC measurements in different studies was found to be about 7% [35, 36]. Moreover, the strong correlation between single-slice and whole-lesion ADC measurements in our study suggests that both methods can provide complementary information regarding tumor characteristics, and may also refer to the reliability and reproducibility of the two measurement methods. Further testing for technical validation of our results is warranted.

Finally, our primary results showed that pre-, and post-treatment DW-MRI offer insights into tumor response in MIBC patients treated with NAC. After validation in larger studies, our significant findings could improve patient management. The clinical benefits of pre-treatment markers may include preventing unnecessary chemotherapy and facilitating prompt treatment decisions. Also, post-treatment markers may predict long-term outcomes and enable personalized therapy approaches.

Conclusion

We reported a prospective study in MIBC patients undergoing NAC, indicating the promising role of pre-, mid-, and post-treatment DW-MRI in the assessment of tumor response. We concluded that pre-treatment ADC, pre-treatment TV, post-treatment ΔADC%, and post-treatment ΔTV% could be considered noninvasive imaging markers of tumor response in MIBC patients undergoing NAC. Moreover, considering slow changes of ADC and TV over the treatment course, mid-treatment changes should not be considered predictors of tumor response in these patients. The potential utility of pre-treatment markers may include preventing unnecessary chemotherapy and facilitating prompt treatment decisions. Also, post-treatment markers may predict long-term outcomes and enable personalized therapy approaches. Further larger studies are required to confirm these results.

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

The authors would like to acknowledge Dr. Zahra Mahboubi for their helpful comments.

Funding

Not applicable.

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Author notes

  1. Abolfazl Razzaghdoust and Anya Jafari contributed equally to this work.

Authors and Affiliations

  1. Urology and Nephrology Research Center, Research Institute for Urology and Nephrology, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Abolfazl Razzaghdoust

  2. Department of Radiation Oncology, Shohada-e Tajrish Medical Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Anya Jafari & Bahram Mofid

  3. Department of Radiology, University of Washington School of Medicine, Seattle, WA, USA

    Arash Mahdavi

  4. Urology and Nephrology Research Center, Research Institute for Urology and Nephrology, Shahid Labbafinejad Hospital, Shahid Beheshti University of Medical Sciences, No.103, Shahid Jafari St., Pasdaran Ave., Tehran, 1666677951, Iran

    Abbas Basiri

Authors
  1. Abolfazl Razzaghdoust
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  2. Anya Jafari
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  3. Arash Mahdavi
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  4. Bahram Mofid
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Contributions

Conception and design: AR, BM, and AB. Acquisition of data: AR, AJ, and AM. Analysis and interpretation of data: AR, AJ, AM, AB, and BM. Writing, review, and/or revision of the manuscript: AR, AJ, AM, AB, and BM.

Corresponding authors

Correspondence to Bahram Mofid or Abbas Basiri.

Ethics declarations

Human ethics and consent to participate

This study was conducted in accordance with the Declaration of Helsinki, and the protocol was approved by the ethics committee of Shahid Beheshti University of Medical Sciences (IR.SBMU.UNRC.REC1398.14). Written informed consent was obtained from all participants.

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Not applicable.

Competing interests

The authors declare no competing interests.

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Razzaghdoust, A., Jafari, A., Mahdavi, A. et al. Diffusion-weighted MRI-Derived ADC and tumor volume as predictive imaging markers for neoadjuvant chemotherapy response in muscle-invasive bladder cancer. BMC Med Imaging 25, 3 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12880-024-01547-3

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  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12880-024-01547-3

Keywords

BMC Medical Imaging

ISSN: 1471-2342

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