The utility and feasibility of three-dimensional reconstruction in surgical planning for multiple pulmonary nodules: a prospective self-controlled study

Introduction

With the increasing popularity and quality of high-resolution computed tomography (CT), the detection of multiple lung nodules (MLNs) has become more common (1). As MLNs is a radiographic finding related to diseases ranging from benign to malignant, the preferable treatment varies depending on the different etiologies (2,3). Currently, there is no consensus on the standard diagnostic procedure and treatment of MLNs, but surgical resection still plays a dominant role in most medically appropriate cases. The American College of Chest Physicians (ACCP) guidelines recommend sublobar resection of all lesions suspected to be malignant in patients with suspected or confirmed multifocal lung cancer (4). Moreover, several randomized controlled trials (5-7) have reported that sublobar resection may not only enable the diagnosis but also curative treatment of lung nodules. According to the surgical procedure, sublobar resection can be divided into wedge resection and anatomical partial lobectomy (APL). APL is a general concept of anatomical sublobar resection, which includes segmentectomy, subsegmentectomy, combined segmentectomy and so on (8). For nodules located deep in the parenchyma, wedge resection is inappropriate, but APL is suggested. A smaller and more precise resection area means that APL requires a more detailed preoperative surgical plan and more precise localization of nodules compared to lobectomy (9). In addition, the complexity and frequent variations (10-12) of the bronchi and vessels of the lung segments make surgical planning solely relying on preoperative 2D chest CT difficult.

Three-dimensional (3D) reconstruction technology is widely used in the medical field. In thoracic surgery, 3D reconstruction can convert two-dimensional (2D) images of pulmonary bronchial and arteries on CT into 3D images of the vascular and bronchial tree, which can assist the surgeon to localize nodules more precisely and better understand the anatomy or variations of blood vessels and bronchi more clearly before surgery (13). In 2015, Chan et al. conducted a study to determine the feasibility of 3D reconstruction to segment the lung and compute accurate 3D margin (14). Subsequently, a series of retrospective studies demonstrated the benefits of 3D reconstruction including less intraoperative blood loss, shorter operative time, lower risk of hemoptysis, pulmonary air leakage, and fewer recurrences compared to the non-3D group (15-18). Previous studies have also suggested that APL using 3D reconstruction could achieve comparable long-term outcomes to lobectomy for small-sized non-small cell lung cancer (NSCLC) (19,20). However, there is a lack of prospective experience evaluating the benefits of preoperative 3D reconstruction in surgical decision-making and treatment planning.

The aim of this prospective self-controlled study was to evaluate the effect of 3D reconstruction in surgical planning and decision making compared with conventional clinical imaging (thin-slice CT) and to summarize the characteristics of patients and features of nodules that were of high priority for 3D reconstruction. We present this article in accordance with the STROBE reporting checklist (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-24-849/rc) (21).

Methods

This prospective self-controlled study was conducted between August 2020 and September 2023 at the National Cancer Center of China and was designed to evaluate the impact of 3D reconstruction on the surgical planning of MLNs. The study was approved by the Institutional Review Board of the National Cancer Center/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College (No. NCC2443) on June 30, 2020. Written informed consent was obtained from patients prior to their participation. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013).

Patients

Patients aged 18–79 years with synchronous MLNs confirmed by thin-section CT and with an Eastern Cooperative Oncology Group performance score (ECOG-PS) of 0 or 1 and intended to undergo APL were recruited for the study. At the time of enrollment, thin-section chest CT, contrast-enhanced chest CT, ultrasonography of neck and abdomen, bone scan, and cranial magnetic resonance imaging (MRI) were mandatory, and positron emission tomography (PET)-CT was performed if needed. The thin-slice CT had to fulfill two conditions: at least one side of the lung had multiple nodules, NSCLC was suspected, the maximum nodule diameter was less than 3 cm, and there was no evidence of lymph node metastasis. Clinical staging was limited to cT1bN0M0 according to the eighth edition of the tumor, node, and metastasis (TNM) classification of lung cancer (22) and T stage was based on highest T lesion (23). The exclusion criteria were: (I) history of thoracic surgery or other adjuvant treatments including radiotherapy and anticancer drugs; (II) lung nodules suspected as intrapulmonary metastases based on conventional imaging and clinical data; (III) pulmonary fibrosis and severe pulmonary emphysema; (IV) women during pregnancy and lactation; (V) uncontrollable diabetes, hypertension or heart disease; (VI) mentally retarded or incapacitated patients; and (VII) patients who did not eventually undergo APL. This study aimed to evaluated the impact of 3D reconstruction on surgical planning. Previous study on 3D reconstruction has primarily focused on the intraoperative and postoperative outcomes. Consequently, there is insufficient information to accurately calculate the sample size for this study. Due to the lack of reference, a panel of five thoracic experts discussed and reached a consensus that 50 patients would be sufficient for the present study.

Study design

Three sequential phases were performed to evaluate the value of 3D-reconstruction in assisting surgical planning of MLNs (Figure 1).

• At phase I, thin-slice (0.625–1.25 mm) chest CT were performed for all patients. Each surgeon conducted surgical plans only based on preoperative CT images respectively and give a standard output (initial surgical plan). For example: in one case, the “output” might be: wedge resection of the apex of the left upper lobe and combined segmentectomy of the S⁸a + S⁹a.
• At phase II, 3D-reconstruction was performed for all patients by a designated experienced group. Each surgeons got 3D reconstruction and crafts another plan. It might be the same plan, but it might differ based on the new knowledge and details provided by the 3D reconstruction.
• At phase III, final surgical approach was decided after intraoperative inspection. Surgeons C and D as the primary operating surgeon, each performed the surgery on half of the patients. The surgeries that actually took place with negative resection margins and without intraoperative accident and without major postoperative complications were held as the “gold standard”. If the hypothetical plans (including initial plans and revised plans) were identical to the actual surgery performed, then they were coded as successful plans.

Figure 1 Study protocol design. 2D, two-dimensional; CT, computed tomography; 3D, three-dimensional.

At each phase, the surgical plans/approaches and reasons for changing surgical plans/approaches were recorded via questionnaires. Both initial and revised surgical plans were conduct independently by surgeons based on their personal knowledge, without any assistance from other surgeons or a radiologist.

Surgeons and principals of surgical planning

Four thoracic surgeons were selected on the basis of their experience with sublobar resections and divided into two groups: novice and experienced surgeons. Two novice surgeons (A and B) were in their fourth to sixth grade postgraduate and could not perform APL independently. Two experienced surgeons (C and D) could perform more than 300 thoracic operations per year. To reduce potential bias due to different surgical practices among the surgeons, surgeons were required to adhere to the following guidelines when planning the surgical approach. For nodules located in the outer 1/3 of parenchyma, wedge resection was suggested; For nodules deeply located in parenchyma, APL was suggested. For nodules less than 2 cm in diameter, the shortest distance from the resection margin to the edge of the nodule should be greater than the maximal nodule size. For nodules larger than 2 cm in diameter, the margin distance should be at least 2 cm. Lobectomy was performed as an alternative measure to ensure the safety of the surgical margin. Under the premise of ensuring a sufficient surgical margin, another requirement for surgeons was to preserve as much normal lung tissue as possible. If the lesions are confirmed malignant pathology in the fast-track procedure, nodal sampling (systemic or N1) or systemic nodal dissection was performed.

CT imaging and 3D reconstruction

Preoperative CT scans were performed with 64-detector-row CT scanners (Lightspeed Ultra, GE Healthcare, Waukesha, WI, USA; Toshiba, Japan) for all patients enrolled in the study. The digital imaging and communications in medicine (DICOM) data of preoperative thin-slice CT images (0.625–1.25 mm) were retrieved for 3D reconstruction. A designated experienced group performed all 3D reconstructions by using Mimics 21.0 (Materialise, Leuven, Belgium). Arterial tree, venous vessel tree, and bronchi were constructed. The segments were subdivided according to the distribution of blood vessels. Lung nodules were extracted manually or by threshold. Finally, an appropriate spherical margin was superimposed surrounded nodules according to the features of the nodules. Figure 2 shows an example 3D reconstruction model.

Figure 2 An example of 3D reconstruction. (A) 3D rendering of the bronchial airways (shown in green) and nodules (shown in yellow) on the left lung. (B) 3D rendering of the arteries (shown in blue). (C) 3D rendering of the veins (shown in pink). (D) Superimposition of a reasonable spherical safety margin (translucent light red area) based on the imaging features of the nodules determined suitable for APL. Other translucent color areas represent the anatomical segments of left lung. 3D, three-dimensional; APL, anatomical partial lobectomy.

Statistical analysis

Categorical variables were presented as frequency (percentage). Continuous variables following a normal distribution were presented as mean ± standard deviation, whereas those not conforming to a normal distribution were delineated by median and range. We handled missing data as missing without data imputation. Normality was tested using the Shapiro-Wilk test. Kappa (κ) coefficient was calculated to quantify the agreement between initial and revised surgical plans and the agreement between surgical plans and final surgery approach. Kappa value was interpreted according to the criteria proposed by Landis and Koch (24): a κ value below 0 indicates poor agreement; κ between 0 and 0.2 indicates slight agreement; κ between 0.2 and 0.4 indicates fair agreement; κ between 0.4 and 0.6 indicates moderate agreement; κ between 0.6 and 0.8 indicates substantial agreement; and κ between 0.8 and 1 indicates almost perfect agreement. Concordance rate was calculated as cases with identical initial and revised surgical plan in percent of total cases. Surgical planning success rate was calculated as cases with identical surgical plan and final surgery approach in percent of total cases. The McNemar test was used to compare paired proportions. Other categorized variables between groups were compared using the Chi-squared test and Fisher exact test. Because the parallel and before-after comparisons of surgical planning success rates were based on four pairwise comparisons, to prevent α error accumulation, Bonferroni correction was applied. Values of P<0.0125 were considered statistically significant in parallel and before-after comparisons of surgical planning success rates. Other P values were calculated using two-sided tests and those less than 0.05 were considered statistically significant. We compared the surgeons’ surgical planning success rates both at phase I and phase II between final surgeries performed by Surgeon C and Surgeon D as sensitive analysis. All tests were performed using SPSS 27.0 software (IBM Corp., Armonk, NY, USA).

Data collection and follow up

Patient demographics, clinical characteristics, imaging data and tumor clinicopathological feature were systematically collected using a pre-designed form. Intraoperative conditions including blood loss, operation time and conversion to open thoracotomy were documented. Postoperative complications and postoperative clinical outcomes were recorded. Follow-up methods included outpatient visits, online consultations, and telephone interviews.

Results

Overall, 50 patients with MLNs were recruited, of which 49 patients with 165 resected nodules were included in the final analysis and one patient was excluded because he had received lobectomy. Of these participants, 13 (26.5%) finally underwent APL only and 36 (73.5%) underwent APL plus wedge resection. All participants had at least one nodule that underwent APL. Of these 165 nodules, 101 (61.2%) underwent APL and 64 (38.8%) underwent wedge resection. Most nodules were of size less than 1 cm (112/165, 67.9%) and most were pure ground glass nodules (127/165, 77.0%). Most nodules were invasive adenocarcinomas (45/165, 27.3%), microinvasive adenocarcinomas (27/165, 16.4%), and adenocarcinomas in situ (73/165, 44.2%). The baseline characteristics of the study population and features of the resected nodules are shown in Tables 1,2. Figure 3 shows the details of surgical management decisions and changes during the study. All 49 patients underwent surgery with negative resection margins and without major complications. The median follow-up time for overall survival was 171.8 weeks and one patient was lost to follow-up after discharge. No death was observed within 30 days after surgery. One patient died of viral pneumonia without recurrence and one patient developed a recurrence (Table S1).

Figure 3 Surgical management decision. (A) Surgical management decision of Surgeon A. (B) Surgical management decision of Surgeon B. (C) Surgical management decision of Surgeon C. (D) Surgical management decision of Surgeon D. Arrows: change in surgical plan. Numbers in each cell: number of nodules planned/underwent for this surgery approach. Numbers on the arrows: red numbers represent number of nodules that have been expanded resection range in surgical plan; blue numbers represent number of nodules that have been reduced resection range in surgical plan. Combined APL included combined segmentectomy, combined subsegmentectomy and combined segment and sub-segment resection. 2D, two-dimensional; CT, computed tomography; 3D, three-dimensional; APL, anatomical partial lobectomy.

Surgical plan changes after 3D reconstruction evaluation

In the 101 nodules that received APL, 65.3% (Surgeon A) and 70.3% (Surgeon B) of surgical plans were identical after 3D reconstruction evaluation. In the experienced group, most surgical plans remained unchanged (Surgeon C: 91.1% of surgical plans; Surgeon D: 88.1% of surgical plans). The Kappa coefficient (κ) was calculated to quantify the degree of agreement between the initial surgical plans only based on 2D CT images and the revised plans aided by 3D reconstruction. The surgical plans of the novice group had moderate agreement before and after 3D reconstruction, whereas the experienced group showed substantial to almost perfect agreement of surgical plans: Surgeon A (κ=0.425), Surgeon B (κ=0.511), Surgeon C (κ=0.858), and Surgeon D (κ=0.796). Further analysis indicated that 3D reconstruction may lead to a higher proportion of changes to CT-guided surgical plans at the patient level. Approximately a half of the surgical plans in the novice group (57.1% of Surgeon A and 46.9% of Surgeon B) were modified after 3D reconstruction reconsideration. In the novice group, only fair to moderate agreement between initial and revised surgical plans was observed: Surgeon A (κ=0.289) and Surgeon B (κ=0.432). In the experienced group, 16.3% (Surgeon C) and 22.4% (Surgeon D) of surgical plans were modified after the reexamination of the 3D reconstruction. The Kappa coefficient summarized the difference between the surgical plans before and after 3D reconstruction, Surgeon C (κ=0.799) and Surgeon D (κ=0.698) (Table 3).

Final surgical approach changes after intraoperative inspection

A total of 50 operations were performed, of which only one case was excluded from the final analysis because a lobectomy was performed due to serious adhesion. All patients were operated without intraoperative accident and without major postoperative complications (Table S1). In most cases, the information obtained from intraoperative inspection did not lead to changes in surgical plan. After re-evaluating the 3D reconstruction of nodules that underwent APL, the surgical plans of each surgeon achieved a success rate of over 90%: Surgeon A (92.1%), Surgeon B (94.1%), Surgeon C (100%) and Surgeon D (98.0%). The Kappa coefficient showed almost perfect agreement between final surgical approaches and revised surgical plans aided by 3D evaluation both at patient level and nodule level (Table 3).

Difference in surgical planning success rates

The before-after comparison evaluated the difference in surgical planning success rates between initial surgical plans (based on 2D CT) and revised surgical plans (aided by 3D reconstruction) (Figure 4). At the patient level, 3D reconstruction significantly increased the surgical planning success rates: Surgeon A, from 40.8% to 87.8% (P<0.001); Surgeon B, from 49.0% to 89.8% (P<0.001); Surgeon C, from 83.7% to 100% (P=0.008); Surgeon D, from 75.5% to 95.9% (P=0.002) (Table 4). For nodules treated with APL, 3D reconstruction also significantly increased the surgical planning success rates: Surgeon A, from 64.4% to 92.1% (P<0.001); Surgeon B, from 68.3% to 94.1% (P<0.001); Surgeon C, from 91.1% to 100% (P=0.004); Surgeon D, from 87.1% to 98.0% (P<0.001) (Table 4).

Figure 4 Before-after comparisons of surgical planning success rates between surgical plans based on 2D CT images and 3D reconstruction. (A) Before-after comparisons of surgical planning success rates at the patient level. (B) Before-after comparisons of surgical planning success rates at the nodule level. *, P<0.0125 deemed significant. 2D, two-dimensional; CT, computed tomography; 3D, three-dimensional.

The parallel comparison evaluated the surgical planning success rates of different surgeons in the same study phase (Figure 5). Before 3D reconstruction, novice surgeons had lower surgical planning success rates compared with experienced surgeons. With the assistance of 3D reconstruction, the surgical planning success rates of novice surgeons showed no significant difference from those of the experienced Surgeon at the patient levels (Table 5). At patient level, 3D reconstruction closed the gap in surgical planning success rates between the novice surgeons and experienced surgeons. At nodule level, three comparisons (Surgeon A versus Surgeon D, P=0.07; Surgeon B versus Surgeon C, P=0.03; Surgeon B versus Surgeon D, P=0.22) demonstrated no significant difference in surgical planning success rate, while one comparison (Surgeon A versus Surgeon C, 92.1% versus 100%, P=0.008) still demonstrated significant difference (Table 5).

Figure 5 Parallel comparisons of surgical planning success rates among surgeons. (A) Parallel comparisons of surgical planning success rates at the patient level. (B) Parallel comparisons of surgical planning success rates at the nodule level. *, P<0.0125 deemed significant.

Characteristics of patients and features of nodules that lead novice surgeons prone to surgical plan failure based on only 2D CT images

Table 6 shows the characteristics of patients and the features of nodules which lead the novice surgeons prone to surgical plan failure based on 2D CT images. At the patient level, more than two nodules that required resection and a surgical range involving more than one lobe were identified as risk factors for failure of surgical plan. Of nodules that received an APL, those located on the right lung or with diameter larger than 1 cm had a higher probability of surgical plan failure. Nodules that required a subsegmentectomy or combined APL were associated with an increased probability of surgical plan failure.

Additional analysis

In 49 patients finally included in the analysis, as the primary surgeon, Surgeon C performed 24 surgeries and Surgeon D performed 25 surgeries. We compared the surgeons’ surgical planning success rates both at phase I and phase II between final surgeries performed by Surgeon C and Surgeon D (Figure S1), no significant difference was observed. At the patient level, Surgeon C showed similar surgical planning rates in his own cases and cases performed by Surgeon D (initial surgical plan success rates: 83.3% versus 84.0%; revised surgical plan success rates: 100% versus 100%). Surgeon D also showed similar surgical planning rates in his own cases and cases performed by Surgeon C (initial surgical plan success rates: 72.0% versus 79.2%; revised surgical plan success rates: 96.0% versus 95.8%) (Tables S2,S3).

Discussion

In recent years, several studies have shown the benefit of preoperative 3D reconstruction in terms of intraoperative safety and short-term surgical outcomes after thoracoscopic surgery (15-17). To our knowledge, there is little literature evaluating preoperative 3D reconstruction as an adjunct to surgical strategies in APL. Methodologically, a randomized controlled trial would be the optimal approach to evaluate the effect of 3D reconstruction as an aid in the surgical planning of APL. However, randomization could raise ethical issues regarding the allocation of patients to a clinical pathway which may potentially be disadvantaged by the lack of 3D reconstruction evaluation (25). Retrospective studies are limited by the potential risk of selection bias, and the high heterogeneity of MLNs makes it challenging to match baseline characteristics of the experimental and control groups. In this study, these limitations were overcome by a self-controlled design. Patients in this study served as their own controls. In phase I, surgeons made surgical plan only based on 2D CT images. Subsequently, surgeons re-evaluated the surgical plans with the information provided by 3D reconstruction. This design ensured that all operations were performed with the help of 3D reconstruction and the impact of 3D reconstruction in surgical planning was evaluated. However, the lack of blinding could exaggerate the surgical planning success rates of 3D reconstruction. We did the additional analysis to compare the surgical planning success rates for cases operated by Surgeon C and Surgeon D. No significant difference in success rate was observed, which suggests a limited influence of this potential bias on this study. Furthermore, given the heterogeneity of surgical practices among different surgeons, this study standardized the principles of surgical planning in advance.

The patient cohort in this study comprised individuals with MLNs, with each nodule having a maximum diameter of less than 3 cm. Up to now, there has been no standard approach to surgical treatment for MLNs, but sublobar resection was preferred. Solely relying on 2D CT images, localizing nodules to a specific segment and estimating the resection range using a “mental model” was difficult. Moreover, planning sublobar resections for MLNs was more complex compared to single lung nodules. Despite this, we acknowledged that not all experienced surgeons considered that 3D reconstruction was necessary for performing sublobar resections, even in cases of patients with MLNs. However, our study found that only 20 (40.8%) cases of Surgeon A and 24 (49.0%) cases of Surgeon B did not change the surgical plan after 3D reconstruction and intraoperative inspection. Even in the group of experienced surgeons, a certain proportion of cases ultimately do not adopt the surgical plans which designed only based on 2D CT images. This means that using CT images alone for planning sublobar resection for patients with MLNs is challenging, especially for less-experienced surgeons. In this study, 3D reconstruction significantly increased the surgical planning success rates compared to preoperative evaluation only based on 2D CT images. At the patient level, surgical plan success rates reached 87.8% (Surgeon A), 89.8% (Surgeon B), 100% (Surgeon C), and 95.9% (Surgeon D), highlighting the effect of 3D reconstruction in surgical planning. The absence of major complications or tumor-positive resection margins also indicated a good geometrical match between individual specific anatomy and 3D reconstruction model.

Conducting surgical planning for APL is associated with a high technical difficulty and a long learning curve, making it challenging for novice thoracic surgeons. Our results indicated that 3D reconstruction might close the gap in surgical planning ability between novice surgeons and experienced surgeons at patient level. In accordance with the present results, previous study (26) has demonstrated that surgeons had more accurate surgical planning of chest wall resection using immersive 3D CT compared with CT, and this was particularly true in the resident surgeon group. This raises the possibility that 3D reconstruction could even shorten the learning curve of novice surgeons in planning APL. However, we noted the significant difference in surgical planning success rates between Surgeon A and Surgeon C at nodule level. In addition to the limited number of surgeons, these findings should be interpreted with caution.

The time and financial costs associated with 3D reconstruction should be overlooked; in a small hospital, it is impractical to perform 3D reconstruction for all patients with MLNs. To our knowledge, there is no consensus or recommendation on the selection MLNs for 3D reconstruction. According to the results of this study, 3D reconstruction was recommended for patients with more than two nodules requiring resection or surgery involving multiple lobes. At the nodule level, nodules located on the right lung or with diameter larger than 1 cm were more likely to require 3D reconstruction. In addition, nodules in complex segments (8,15) {segments in left lung [7–10], segments in right lung [1–5] and segments in right lung [7–10]} may be associated with a higher probability of an inappropriate surgical plan compared with those in simple segments, although the difference was not entirely significant. Lower surgical planning success rates were also observed in nodules that eventually underwent subsegmentectomy and combined APL, and 3D reconstruction is suggested. Overall, surgical planning success of novice surgeons are mainly affected by location of nodules and surgical procedure.

Limitations

First, this study was conducted in a single institution and included a limited number of surgeons, which might limit the inferential reproducibility of the findings. Taking ethical concerns into account, all operations were performed after experimental/control crossover and with the help of 3D reconstruction. Therefore, the effects of 3D reconstruction on surgical outcomes could not be assessed. Comparing the same surgeon for each case on both sides of the crossover may have potentially eliminated the surgery practice bias. However, since the surgeons needed to reconsider the surgical plan based on 3D reconstruction, it was difficult to blind the surgeons and other participants. The lack of blinding may have exaggerated the effects of 3D reconstruction. Finally, another limitation is the large heterogeneity and variability of MLNs. Considering the above limitations of this exploratory study, conclusions should be cautiously interpreted.

Conclusions

This prospective self-controlled study objectively investigated the effect of 3D reconstruction on surgical plan modification in 49 patients with MLNs. This study indicates 3D reconstruction significantly improves the surgical planning success rates. Whilst this study did not comprehensively confirm the effect of 3D reconstruction on narrowing experience gap among difference surgeons, it did partially substantiate 3D reconstruction could close the surgical planning gap between novice and experienced surgeons at patient level. Studies included a larger number of surgeons are needed to further explore this.

Acknowledgments

Funding: This study was supported by the Major Program of Scientific and Technical Innovation 2030 (No. 2020AAA0109504), the Science and Technology Planning Project of Beijing City (No. Z191100006619116), and the Beijing Hope Run Special Fund of Cancer Foundation of China (No. LC2020A05).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-24-849/rc

Data Sharing Statement: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-24-849/dss

Peer Review File: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-24-849/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-24-849/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 approved by the Institutional Review Board of the National Cancer Center/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College (No. NCC2443) on June 30, 2020. Written informed consent was obtained from patients prior to their participation. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013).

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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