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. 2025 Aug 15;25:395. doi: 10.1186/s12890-025-03872-x

The association between core number and complications in ultrasound-guided percutaneous lung core needle biopsy for subpleural primary lung cancer: a retrospective study

Mengjun Shen 1,2, Hongwei Chen 1, Jixin Shu 1, Yang Cong 1, Yi Zhang 1, Huiming Zhu 1, Yin Wang 1,
PMCID: PMC12355805  PMID: 40817041

Abstract

Background

With advances in lung cancer management, there is a growing need for larger tissue samples to enable tumor genomic analysis and characterization.This study aims to determine whether the core number obtained during Ultrasound-guided percutaneous lung core needle biopsy(US-PLCNB) is associated with post-procedural complications.

Methods

This retrospective study enrolled consecutive patients who underwent US-PLCNB for subpleural primary lung cancer at Shanghai Pulmonary Hospital between July 2019 and September 2021. Patient data were extracted from medical records, including demographics, lesion size, and core number. Post-procedural complications, including hemoptysis, pneumothorax, intolerable pain, pleural reaction, hemothorax, and delayed hemopneumothorax, were documented. Multivariate logistic regression models were used to evaluate whether the core number was an independent predictor of complications following US-PLCNB.

Results

A total of 1,151 patients (mean age, 64.47 ± 10.58 [SD] years; 278 [24.15%] females and 873 [75.85%] males) were included. The median lesion size was 58 mm (IQR, 41–77 mm). Among the 1,151 patients, 417 (36.23%) were diagnosed with lung adenocarcinoma, and 322 (27.98%) with lung squamous cell carcinoma. Post-procedural complications occurred in 41 patients (3.56%), including: hemoptysis (26 cases, 2.26%), pneumothorax (7 cases, 0.61%), intolerable pain (3 cases, 0.26%), vasovagal reaction (2 cases, 0.17%), hemothorax (2 cases, 0.17%), and delayed hemopneumothorax (1 case, 0.09%). The median number of biopsy cores obtained was 3 (range: 1–7). Multivariate analysis revealed no evidence of an association between the number of cores and complications: hemoptysis (OR = 0.820, P = 0.410), pneumothorax (OR = 1.220, P = 0.663), intolerable pain (OR = 0.520, P = 0.387), vasovagal reaction (OR = 1.087, P = 0.924), hemothorax (OR = 1.062, P = 0.944), delayed hemopneumothorax (OR = 1.118, P = 0.930).

Conclusion

In patients undergoing US-PLCNB for primary lung cancer, no evidence was found of an association between the core number biopsy samples obtained and post-procedural complications.

Keywords: Ultrasound-guided percutaneous lung core needle biopsy(US-PLCNB), Primary lung cancer, Core number, Complications

Background

While pathologists can diagnose pulmonary malignancies through morphological evaluation of minimal tissue samples [1], the rapid advancement of immunotherapy and precision therapies based on genomic profiling has precipitated a paradigm shift in tissue requirements. The exponential growth in biomarker targets requiring assessment—from programmed cell death ligand 1 (PD-L1) expression to driver mutations—has driven an unprecedented demand for larger biopsy volumes [2]. This paradigm evolution mandates the procurement of multiple core specimens to satisfy both diagnostic verification and comprehensive molecular profiling needs [3], thereby raising critical clinical questions regarding the safety implications of expanded sampling protocols.

Although CT-guided lung biopsy is widely used for peripheral pulmonary lesions, ultrasound-guided is gaining increasing popularity [4]. Ultrasound-guided percutaneous lung core needle biopsy(US-PLCNB) can be performed when the lesion is in contact with the pleura or when there is consolidation between the lesion and the pleura. Compared to CT-guided, US-PLCNB is a radiation-free, real-time, and cost-effective bedside procedure that allows operators to avoid blood vessels or necrotic areas during needle insertion using Doppler ultrasound or contrast-enhanced ultrasound [5, 6]. Although US-PLCNB is highly safe and minimally invasive, as an invasive diagnostic procedure, it still carries risks of needle-related complications during radiologist-performed punctures, such as hemoptysis, pneumothorax, and in severe cases, even fatal outcomes [79].

In a meta-analysis of 12 studies [10] involving 3,830 patients who underwent ultrasound-guided percutaneous lung core needle biopsies, the most common complications were self-limited hemoptysis (2.3%) and asymptomatic pneumothorax (1.2%). Only 6 cases of pneumothorax requiring chest tube drainage and 1 case of severe hemorrhage were reported. Factors associated with an increased risk of post-biopsy hemoptysis, pneumothorax, or perilesional bleeding included smaller lesion size, shorter pleural contact length, bronchus sign, and perilesional vessels, whereas no correlation was observed with the number of biopsy cores [1114]. Similarly, Kim et al. [15], in a study of 827 patients undergoing CT-guided lung biopsies, similarly found no evidence of an association between the number of core biopsy samples obtained and post-procedural complications. However, Lovato et al. [16] found that the number of biopsies with the risk of pulmonary sepsis. Nevertheless, research evaluating the impact of the number of needle passes in US-PLCNB remains extremely limited. Therefore, this study aims to determine whether the core number obtained via US-PLCNB is associated with post-procedural complications.

Materials and methods

This was a single centre retrospective study of US-PLCNB in patients. Informed consent was obtained from each patient prior to undergoing US-PLCNB. The study was conducted in accordance with the Declaration of Helsinki. Institutional review board approval was obtained.

Patients and data collection

Consecutive patients aged over 18 years who underwent US-PLCNB for suspected primary lung cancer at Shanghai Pulmonary Hospital between July 2019 and September 2021 were included. A retrospective review was conducted on all US-PLCNB procedures, intraoperative ultrasound images, patient and procedural data recorded in the electronic medical records (eHis), and pathological reports of biopsy specimens. Data collection was performed by six trained researchers (MS, HC, JS, YC, YZ, HZ) and included: (1) gender, (2) age, (3) lesion size (longest diameter: ≤3 cm, > 3 cm), (4) core number. Post-procedural complications were recorded, including type (hemoptysis, pneumothorax, vasovagal reaction, intolerable pain, hemothorax, delayed hemopneumothorax). Patients with non-pulmonary metastatic malignancies, benign lesions, or incomplete medical records were excluded. All cases were pathologically confirmed (via biopsy or surgery).

Exclusion criteria for US-PLCNB were: Patients with severe psychiatric disorders unable to cooperate with the procedure; Patients or family members refusing the procedure; Patients with uncorrectable coagulopathy (INR > 1.5 or platelet count < 50 × 10⁹/L); Patients taking anticoagulants or antiplatelet agents within one week prior to biopsy; Patients with severe respiratory or circulatory failure. Patients presenting with any of the above contraindications were excluded from undergoing biopsy.

Procedure

Examiners utilized the LOGIQ E9 ultrasound system (GE Healthcare) equipped with a 1–6 MHz convex probe to independently conduct ultrasound examinations.

General considerations for needle entry included avoiding traversal of interlobar fissures, selecting the shortest path to the lesion, and circumventing blood vessels and bronchi along the needle trajectory, ideally positioning the lesion in a dependent or accessible location. After skin disinfection, 2% lidocaine was administered subcutaneously using a 22G needle. A biopsy device (Bard Mission; BD Biosciences) with a 12–22 mm throw and 18G or 16G core-cutting needle (adjusted based on lesion size) was deployed. Needle lengths ranged from 10 cm to 16 cm, tailored to the patient’s body habitus and lesion depth/location. In select cases, a Bard coaxial introducer needle was utilized as a guiding sheath, depending on the biopsy device configuration. Under real-time ultrasound guidance, the biopsy needle was advanced toward the target subpleural pulmonary lesions. Radiologists employed a freehand technique for needle manipulation. If gross inspection suggested inadequate or non-diagnostic samples, additional cores were obtained. Post-procedural protocol: Patients were instructed to maintain strict bed rest for 30 min with ice pack application to the puncture site for hemostasis. A 30-minute follow-up ultrasound was performed to evaluate for hemorrhage or pneumothorax. If no complications were identified: hospitalized patients returned to their wards; Outpatients were discharged after 2 h of observation, with instructions to seek emergency care immediately for acute pain or hemodynamic instability (e.g., hypotension, tachycardia). If patients exhibited symptoms and showed signs of respiratory distress due to postoperative pneumothorax or hemothorax, a chest tube was inserted. For hemothorax cases with hemodynamic instability, endovascular intervention was performed. The procedure was typically aborted in cases of hemoptysis, vasovagal reaction, or intolerable pain, based on cough severity and patient status.

Statistical analysis

Descriptive statistics were used. Quantitative data are presented as mean ± standard deviation (SD) or median and interquartile ranges (IQRs). Categorical data are expressed as counts and percentages.

A linear-by-linear association test was employed to evaluate correlations between the number of samples obtained and binary variables (gender, premature procedure termination, diagnostic biopsy, hemoptysis, pneumothorax, intolerable pain, vasovagal reaction, hemothorax, delayed hemopneumothorax). Kendall’s tau-b correlation coefficient was used to assess the relationship between the number of samples and continuous variables (age, lesion size).

Multivariate logistic regression models, adjusted for clinical and procedural characteristics, were applied to determine whether the number of cores was independently associated with the incidence of complications (hemoptysis, pneumothorax, vasovagal reaction, intolerable pain, hemothorax, delayed hemopneumothorax). A P value < 0.05 was considered statistically significant. All analyses were performed using IBM SPSS Statistics, Version 27.0.

Result

Patient characteristics and complication rates

The initial study cohort included 1,544 patients who underwent ultrasound-guided biopsies during the study period. 393 patients were excluded: 368 patients (23.83%) had pulmonary metastatic lesions, 14 patients (0.91%) had benign lesions, 11 patients (0.71%) had incomplete medical records. See Fig. 1 for details.

Fig. 1.

Fig. 1

Study cohort flow chart

The final analysis included 1,151/1,544 patients (74.55%) (mean age, 64.47 ± 10.58 years [SD]; 278 [24.15%] females; 873 [75.85%] males) with pulmonary lesions suspected of primary lung cancer who underwent US-PLCNB. Of these cases, 968(84.10%) utilized 18G core-cutting needles while 183(15.90%) employed 16G. Coaxial introducer needles were implemented in 581(50.48%) procedures. The overall diagnostic accuracy rate was 97.22% (1,119/1,151). Among the 1,151 diagnostic biopsies, 417 (36.23%) were pathologically confirmed as lung adenocarcinoma, and 322 (27.98%) as lung squamous cell carcinoma (Table 1). Overall complications occurred in 41/1,151 cases (3.56%), with hemoptysis in 26 of 1,151(2.26%), pneumothorax in 7 of 1,151 (0.61%), intolerable pain in 3 of 1,151 (0.26%), vasovagal reaction in 2 of 1,151 (0.17%), hemothorax in 2 of 1,151 (0.17%), delayed hemopneumothorax in 1 of 1,151 (0.09%) (Table 1). No air embolism or mortality occurred in the study. The median number of core biopsy passes was 3 (range: 1–7).

Table 1.

Patient characteristics, puncture characteristics, and Post-procedural complications

Characteristic Value
Mean age (y)* 64.47 ± 10.58(20–96)
Total no. of patients 1151
Sex
Female 278(24.15)
Male 873(75.85)
Lesion size (mm) 58(41 ~ 77)
Biopsy
Coaxial introducer needle 581(50.48)
18G core-cutting needle 968(84.10)
Diagnostic success 1119(97.22)
Histopathologic result
Adenocarcinoma 417(36.23)
Squamous cell carcinoma 322(27.98)
Non-small cell lung cancer 154(13.38)
Lung cancer (unclassified) 78(6.78)
Small cell carcinoma 72(6.26)
Lung cancer (poorly differentiated) 34(2.95)
Other§ 74(6.43)
Postprocedural complications 41(3.56)
Hemoptysis 26(2.26)
Pneumothorax 7(0.61)
Intolerable pain 3(0.26)
Vasovagal reaction 2(0.17)
Hemothorax 2(0.17)
Delayed hemopneumothorax 1(0.09)

Note.—Unless otherwise indicated, data are numbers of patients. Data in parentheses are percentages

* Value is mean ± SD; value in parentheses is the range

Data are medians; data in parentheses are IQRs

§Other included neuroendocrine carcinoma, sarcoma, sarcomatoid carcinoma, lymphoma, adenosquamous carcinoma, metastatic carcinoma, etc

In 4 patients, the procedure was terminated prematurely. These patients underwent 2 biopsy passes (range: 1–2 passes). Reasons for early termination included pneumothorax in 2 of 4 (50%), intolerable pain in 1 of 4 (25%), vasovagal reaction in 1 of 4 (25%).

In the univariate analysis, there was no significant correlation between the number of samples obtained and the incidence of hemoptysis (P = 0.429), pneumothorax (P = 0.804), intolerable pain (P = 0.444), vasovagal reaction (P = 1.000), hemothorax (P = 1.000), or delayed hemopneumothorax (P = 1.000), nor with the combined use of coaxial introducer needles (P = 0.857) or core-cutting needle gauge specifications (P = 0.872). Notably, a higher number of samples was obtained with larger lesion size (P < 0.001); the proportion of male patients increased with the number of samples obtained (P = 0.028); Notably, the incidence of premature procedure termination was significantly higher in patients receiving 1–2 core needle biopsies (3.70% and 1.36%, respectively) compared with no occurrences in other patients (P = 0.001). See Table 2 for details.

Table 2.

Patient characteristics and postoperative complications by the core number of US-PLCNB

Variable No. of Samples
One
(n = 27)
Two
(n = 221)
Three
(n = 583)
Four or More
(n = 320)
P Value
Age* 63(58 ~ 71) 63(60 ~ 71) 66(60 ~ 71) 65(58 ~ 72) 0.522
Lesion size(mm)* 43(31 ~ 57) 50(37 ~ 74) 58(42 ~ 75) 64(46 ~ 86) <0.001
Male sex 16(59.26) 161(72.85) 445(76.33) 251(78.44) 0.028
Procedure terminated early 1(3.70) 3(1.36) 0 0 0.001
Coaxial introducer needle 13(48.15) 113(51.13) 291(49.91) 164(51.25) 0.857
18G core-cutting needle 23(85.19) 186(84.16) 491(84.22) 268(83.75) 0.872
Diagnostic success 25(92.59) 215(97.29) 570(97.77) 309(96.56) 1.000
Hemoptysis 0 7(3.17) 14(2.40) 5(1.56) 0.429
Pneumothorax 0 2(0.90) 2(0.34) 3(0.94) 0.804
Intolerable pain 1(3.70) 0 1(0.17) 1(0.31) 0.444
Vasovagal reaction 0 1(0.45) 0 1(0.31) 1.000
Hemothorax 0 0 2(0.34) 0 1.000
Delayed hemopneumothorax 0 0 1(0.17) 0 1.000

Note.—Data are numbers of patients; data in parentheses are percentages. US-PLCNB, Ultrasound-guided percutaneous lung core needle biopsy

*Data are medians; data in parentheses are IQRs

Multivariate analysis of the association between core number and complications

Multivariate analysis revealed no evidence of an independent association between the number of cores obtained and the incidence of post-procedural complications: hemoptysis (OR = 0.820, P = 0.410), pneumothorax (OR = 1.220, P = 0.663), unbearable pain (OR = 0.520, P = 0.387), vasovagal reaction (OR = 1.087, P = 0.924), hemothorax (OR = 1.062, P = 0.944), delayed hemopneumothorax (OR = 1.118, P = 0.930) (Table 3). Age and diagnostic failure was significantly associated with intolerable pain (OR = 0.904, P = 0.040; OR = 15.039, P = 0.041) (Table 3).

Table 3.

Multivariate logistic regression analysis of complications of US-PLCNB

Characteristic B SE Wals df P Value OR 95% CI for OR
95% CI for OR
Lower Upper
Hemoptysis
Male sex 0.215 0.487 0.195 1 0.659 1.240 0.477 3.220
Age −0.010 0.019 0.296 1 0.587 0.990 0.953 1.028
Lesion size −0.010 0.008 1.494 1 0.222 0.990 0.974 1.006
No. of samples −0.199 0.241 0.680 1 0.410 0.820 0.511 1.315
Diagnostic failure 1.115 0.765 2.128 1 0.145 3.050 0.682 13.649
Constant −2.124 1.493 2.026 1 0.155 0.120
Pneumothorax
Male sex −0.358 0.853 0.176 1 0.674 0.699 0.131 3.718
Age 0.041 0.042 0.961 1 0.327 1.042 0.959 1.132
Lesion size −0.018 0.018 1.073 1 0.300 0.982 0.948 1.017
No. of samples 0.199 0.456 0.190 1 0.663 1.220 0.499 2.985
Diagnostic failure −15.979 6928.295 0 1 0.998 0 0 -
Constant −7.158 3.307 4.685 1 0.030 0.001
Intolerable pain
Male sex −0.747 1.356 0.303 1 0.582 0.474 0.033 6.764
Age −0.101 0.049 4.206 1 0.040 0.904 0.820 0.996
Lesion size −0.030 0.030 1.039 1 0.308 0.970 0.916 1.028
No. of samples −0.654 0.756 0.748 1 0.387 0.520 0.118 2.289
Diagnostic failure 2.711 1.323 4.196 1 0.041 15.039 1.124 201.198
Constant 3.338 3.913 0.728 1 0.394 28.160
Vasovagal reaction
Male sex −1.434 1.433 1.002 1 0.317 0.238 0.014 3.952
Age 0.142 0.089 2.515 1 0.113 1.152 0.967 1.372
Lesion size −0.021 0.036 0.331 1 0.565 0.980 0.913 1.051
No. of samples 0.083 0.879 0.009 1 0.924 1.087 0.194 6.092
Diagnostic failure −14.588 6080.269 0 1 0.998 0 0 -
Constant −14.478 7.284 3.951 1 0.047 0
Hemothorax
Male sex 15.190 2085.833 0 1 0.994 3951117.410 0 -
Age −0.013 0.073 0.033 1 0.855 0.987 0.856 1.138
Lesion size −0.084 0.050 2.788 1 0.095 0.920 0.833 1.015
No. of samples 0.060 0.860 0.005 1 0.944 1.062 0.197 5.732
Diagnostic failure −14.099 5908.758 0 1 0.998 0 0 -
Constant −16.979 2085.840 0 1 0.994 0
Delayed hemopneumothorax
Male sex 14.093 2181.816 0 1 0.995 1319765.188 0 -
Age 0.087 0.126 0.471 1 0.492 1.090 0.852 1.396
Lesion size −0.049 0.062 0.627 1 0.429 0.952 0.844 1.075
No. of samples 0.111 1.262 0.008 1 0.930 1.118 0.094 13.273
Diagnostic failure −13.250 6226.227 0 1 0.998 0 0 -
Constant −24.779 2181.837 0 1 0.991 0

Note.—The logistic regression models included all relevant patient and biopsy characteristics

US-PLCNB, Ultrasound-guided percutaneous lung core needle biopsy; B, coefficient; CI, confidence interval; df, degree of freedom; OR, odds ratio; SE, standard error; Wald, χ2 value

Discussion

Advances in lung cancer treatment now require more tissue samples than before, which may expose patients to additional complications during US-PLCNB. In our retrospective study of 1151 patients undergoing US-guided lung core biopsy for suspected primary lung cancer, no evidence was found of an independent correlation between the number of samples obtained and any postoperative complications.

Optimizing lung biopsy sample acquisition holds significant clinical value for guiding precision medicine practices, particularly in the era of targeted therapies where adequate tumor tissue volume is essential for high-quality genomic analysis [17, 18]. Existing evidence demonstrates that increasing biopsy sample quantity not only enhances the accuracy of tumor heterogeneity assessment—such as providing more comprehensive characterization of PD-L1 spatial heterogeneity [19]—but also directly impacts molecular testing efficacy. Clinical data reveal that three core-needle biopsies optimize diagnostic sensitivity for malignancy detection [20], while four or more biopsy cores simultaneously improve both sensitivity and specificity for successful next-generation sequencing [3]. The novel contribution of this study lies in demonstrating that even when exceeding four biopsy passes, there is no statistically significant increase in complication rates. Consequently, we propose adopting 4–5 core-needle biopsies as a standardized protocol for patients requiring genomic profiling. This approach ensures sufficient tissue yield for molecular diagnostics while maintaining procedural safety.

Our findings demonstrate that hemoptysis and pneumothorax were the most common complications of US-guided lung biopsy in our study. The hemoptysis rate in our cohort was 2.26%, and the pneumothorax rate was 0.61%. These values fall within or are slightly lower than the ranges described in the literature (2.3–5.1% for hemoptysis and 1–6% for pneumothorax) [10, 13, 21, 22]. The lower incidence of hemoptysis at our institution may be attributed to our protocol of performing bleeding risk assessments prior to the procedure, prophylactic administration of hemostatic agents for high-risk patients, and routine pre-biopsy utilization of color Doppler flow imaging and contrast-enhanced ultrasound to avoid vascular-rich areas during needle insertion. Similarly, the reduced pneumothorax rate likely stems from our practice of meticulously avoiding lesions exhibiting the “bronchus sign” during puncture, thereby minimizing the risk of pleural injury.

In our study, we observed a higher incidence of early procedure termination when fewer samples (1–2 cores) were collected (P = 0.001). This finding supports the concept that complications may occur early in the procedure and are not necessarily dependent on the number of samples obtained [23]. Our findings are consistent with prior research by Kim et al. [15], despite their use of CT guidance rather than ultrasound.

Furthermore, this study revealed a positive correlation between lesion size and the number of specimens obtained (P < 0.001). We identified two potential explanations for this phenomenon: First, larger lesions may be associated with lower complication rates, which could enhance operator confidence and encourage a tendency to obtain additional samples. Second, larger lesions are more prone to necrosis, necessitating multiple passes by operators to ensure adequate sample collection.

In our multivariate analysis examining the relationship between core sample quantity and complications, we identified a significant association between age and intolerable pain (P = 0.040), with older patients demonstrating better pain tolerance. This phenomenon may be potentially attributable to age-related neurodegenerative changes and slowed nociceptive transmission in elderly populations [24]. Furthermore, we found that intolerable pain was an independent predictor of diagnostic failure in US-PLCNB. Since pain primarily occurs during needle insertion through the skin rather than upon reaching the lesion, episodes of intolerable pain often result in failure to obtain any tissue sample whatsoever. Therefore, pain predominantly causes diagnostic failure by interfering with the procedural workflow.

Our study has several limitations that should be acknowledged. First, as a single-center retrospective investigation, the study design may have facilitated the inclusion of confounding factors. Moreover, in this single-center study, all personnel performing and guiding the biopsy procedures possessed extensive expertise. As such, we cannot be certain whether these findings are generalizable to other centers. Second, inclusion was restricted to patients with primary lung cancer, resulting in a limited sample size. Third, the bias arising from insufficient sample size due to biopsy complications cannot be completely eliminated. Fourthly, for outpatient cases, only 24-hour telephone follow-ups were conducted, meaning delayed complications beyond this timeframe were not fully captured. Fourth, patients’ pre-existing comorbidities were not incorporated into the risk analysis. Finally, during the procedures, the assessment of specimen adequacy relied solely on the operator’s experience and visual inspection, lacking standardized criteria.

Conclusion

This study found no link between core sample quantity and complication risks in ultrasound-guided lung biopsies for cancer patients. These results are crucial for precision medicine: (1) Adequate tissue sampling is vital for NGS-driven molecular profiling and personalized treatment; (2) Multiple biopsies can be safely performed, overcoming traditional sampling limitations. Future multicenter studies should validate these findings and assess lesion-specific sampling impacts.

Acknowledgements

Not applicable.

Abbreviations

US-PLCNB

Ultrasound-Guided Percutaneous Lung Core Needle Biopsy

SD

Standard Deviation

IQRs

Interquartile Ranges

PD-L1

Programmed Cell Death Ligand 1

Author contributions

M.S. and Y.W. designed the study; H.C. provided the data; J.S., Y.C. Y.Z.and H.Z. collected and analyzed the data; M.S. wrote the manuscript; Y.W. supervised the study. All authors have reviewed the manuscript.

Funding

This work was supported by the Shanghai Health Commission 2023 Shanghai Health Industry Clinical Research Special Project (Grant No. 202340246), National Natural Science Foundation of China (Grant No.82272007) and Shanghai Pulmonary Hospital National Natural Science Foundation Cultivation Project (Grant No. fkzr2466).

Data availability

The datasets used and analyzed in the current study are available from the corresponding author upon reasonable request.

Declarations

Ethics approval and consent to participate

This study was conducted in accordance with the Declaration of Helsinki and approved by the Institutional Review Board of Shanghai Pulmonary Hospital, China (approval number K18-197Y). Written informed consent was obtained from all patients.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Clinical trial number

Not applicable.

Footnotes

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The datasets used and analyzed in the current study are available from the corresponding author upon reasonable request.


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