Computed tomography-guided percutaneous biopsy for diagnosing pulmonary nodules: a prospective, multicenter observational study

Introduction

Currently, approximately 30% of chest computed tomography (CT) scans can detect lung nodules. Artificial intelligence (AI)-assisted CT screening has improved the sensitivity and accuracy in detecting lung nodules, revealing that at least 95% are benign (1,2). These nodules are classified into three categories: pure ground-glass nodules (pGGNs), part-solid nodules, and solid nodules (2). Although various risk prediction models for these nodules have been developed, they only estimate the probability of malignancy and have several limitations (3), including the need to consider multidimensional data and integrate multiple factors. Moreover, the examiner’s personal experience and comprehensive judgment also play very important roles in assessing the risk of lung nodules. Noninvasive examination methods, such as the blood DNA methylation-based lung nodule diagnosis model proposed by Liang et al. (4), are preferable but are yet to be suitably verified.

CT-guided percutaneous biopsy (CTPB) is an established method widely used for the histological and molecular investigation of lung nodules (5-7). Three meta-analyses reveal that CTPB achieves a diagnostic rate of 83.45% for solid lung nodules and 90% sensitivity for subsolid nodules but it carries a higher incidence of minor complications (8-10). Although the incidence of complications is acceptable, the incidence of minor complications is still greater than that after endoscopic biopsy, so CTPB is typically utilized as a second-line approach (6).

This study aimed to identify the application of CTPBs in real-world settings and understand the key factors affecting diagnostic accuracy by analyzing data from patients undergoing lung nodule biopsy at different medical institutions in China. The findings of this study may guide future clinical decisions and directions in clinical research. We present this article in accordance with the STARD reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1912/rc).

Methods

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was approved by the Ethics Committee of the First Affiliated Hospital of the Army Medical University (IRB No. KY2021084), and informed consent was obtained from all patients. All participating institutions were informed and agreed the study. The study was registered in the Chinese Clinical Trial Registry (ChiCTR, 2100044574). Most methods described in this manuscript were carried out in accordance with the relevant institutional guidelines and regulations of the Committee of the Chinese Society of Interventional Oncology, China Anti-Cancer Association (11). The study population in our researches belongs to the same category as that in the two previously published studies (12,13). However, this study focuses on analyzing the diagnostic accuracy of CTPB for pulmonary nodules, while the previously published studies mainly conducted multivariate analyses of pulmonary hemorrhage and pneumothorax to identify their protective factors.

Patient selection and data collection

In this study, researchers collected data on patients with pulmonary nodules from ten medical centers between April 2021 and April 2022. Exclusion criteria (Figure 1) included age >80 years, refusal to undergo CTPB, prior local treatments, blisters or bronchial dilation in the biopsy path, a bleeding tendency, severe chronic obstructive pulmonary disease (COPD) or asthma, a history of malignant tumors, unstable angina or myocardial infarction within 6 months, severe mental illness, pregnancy or lactation, suspected echinococcosis or vascular malformation, and cardiopulmonary insufficiency. Further exclusion criteria included the inability to cooperate with the biopsy, new health problems leading to treatment delays, lack of follow-up data, other operations conducted simultaneously, or withdrawal from the study. The primary characteristics of the included participants included age, sex, and follow-up time (the interval between the initial detection of lung nodules and CTBP. Smoking status was recorded as either “yes” or “no”. CT imaging device, biopsy device, biopsy process information, and complications from patients who underwent CTPB were also collected.

Figure 1 Flowchart showing the eligibility criteria for 591 patients who underwent CTPB. CTPB, computed tomography-guided percutaneous biopsy.

Nodule assessment

Lesion size was determined by measuring the maximal diameter of the target lesion on a standard lung window CT axial view (window level =−600 Hounsfield units, window width =1,500). Lung nodules were classified into two categories based on their lobular location: upper lobe (including the upper lobe and right middle lobe) and lower lobe. The nodules were further classified into three categories based on their location: peripheral nodules (<2 cm from the parietal pleura), hilar nodules (<2 cm from the hilum), and intermediate nodules (between peripheral and hilar nodules). The consolidation-to-tumor ratio (CTR) was classified as ≤50% or >50%.

Technical factors of nodule biopsy

Technical factors included the use of coaxial (using a cannula to ensure that repeated punctures are not required during multiple sampling) or noncoaxial techniques, semiautomatic (tru-cut) (manually control the direction of the cutting slot) or automatic (end-cut) (automatically pop out the cutting slot) needles, and breathing exercises (yes or no). Patients initiated breathing exercises the day before the procedure to maintain regular breathing frequency and depth, which is beneficial for improving the accuracy of puncture and avoiding deviation caused by large variations in breathing amplitude (14). The exercises involved taking rhythmic breaths at 16–20 breaths per minute and holding their breath for 3–5 seconds at the end of inhalation. The number of times the tissue was cut during the procedure was recorded, and the operation time was defined as the time elapsed from scanning the first image to scanning the last image. Three-dimensional reconstruction (yes or no) employs the three-dimensional reconstruction modality of CT to evaluate the puncture or cutting process. Depending on the location of the nodule, patients were positioned in supine, prone, or lateral positions (right or left) to ensure the safest and shortest path to the lesion and was not always the straightest path to the lesion. The needle diameters ranged from 19G to 16G and were divided into two groups: 16G–17G and 18G–19G. To clearly present the courses of the intercostal arteries or nodule edges and internal blood vessels and to avoid bleeding caused by injury to these vessels, the operators performed immediate contrast-enhanced CT (ICECT) during surgical positioning and preoperative contrast-enhanced CT (PCECT).

Diagnostic criteria

The following definitions for malignant lesions (15) were applied: malignant nodules were diagnosed through histological confirmation of malignant disease in surgical specimen tissue; a clear diagnosis of malignancy in biopsy tissue specimens (excluding glandular precursor lesions); the presence of gene mutations [epidermal growth factor receptor (EGFR), anaplastic lymphoma kinase (ALK), c-ros proto-oncogene 1 (ROS1), mesenchymal-epithelial transition factor (MET), etc.] through standard tumor gene testing; biopsy pathological diagnosis consistent with the patient’s subsequent malignant disease diagnosis, or the patient’s clinical process consistent with malignancy; biopsy diagnosis of malignancy, and the lesion nodule increases within a 2-year follow-up period or shrinks or disappears after chemotherapy, immunotherapy, or targeted therapy based on the biopsy pathological results. A benign nodule was diagnosed using the following criteria: histological examination after surgery confirmed that the nodule was benign or a glandular precursor lesion; for patients with lesions dominated by ground-glass opacity (GGO), biopsy confirmed that the lesion was a glandular precursor lesion and who received ablation therapy. This study regarded these lesions as benign nodules. In the case of GGO lesions, biopsy findings of glandular precursor lesions, chronic tissue inflammation, hyperplasia, at the 2-year follow-up, if the GGO did not change, these lesions were classified as benign. In addition, spontaneous shrinking or the disappearance of nodules or nodules that remained unchanged for at least 2 years were defined as benign.

Diagnostic metrics

True-positive (TP) lesions were determined based on a malignant biopsy result and the patient meeting the criteria defined for a malignant nodule. False-positive (FP) lesions were indicated by a malignant biopsy without the patient meeting the definition of a malignant nodule. True-negative (TN) lesions were indicated when the biopsy result was benign, and the patient met the definition of a benign nodule. False-negative (FN) lesions were indicated when the biopsy result was benign, but the patient met the definition of a malignant nodule. Accuracy = (TP + TN)/(TP + TN + FP + FN).

Definition of complications

Pneumothorax was identified during the procedure and postprocedural CT scans, wherein the presence of air densities in the pleural cavity indicated pneumothorax (12). Pulmonary hemorrhage was defined as new consolidative or GGOs in the perilesional, peri-needle path, or other lung lobes on post biopsy images. It was categorized as low-grade (with a range ≤2 cm) or high-grade (with a range >2 cm) (13). Hemothorax was determined after biopsy via a CT review showing liquid density, a chest X-ray review the following day showing a blunted costophrenic angle, or a follow-up CT scan indicating a liquid density shadow. Other complications, such as pleural reaction and air embolism, were recorded according to the patient’s condition during the operation.

Follow-up

Patients with persistent nodules after biopsy needed to undergo a minimum of 2 years of follow-up. However, if patients received clinical intervention following biopsy and met the diagnostic criteria established by this study, the requirement for follow-up was terminated.

Statistical analysis

Univariate analyses were conducted using t-tests for continuous variables and Pearson’s χ² test for categorical variables. Multivariate logistic forward stepwise (likelihood ratio) regression were employed to identify factors that significantly impacted diagnostic accuracy. The data were expressed as the mean ± standard deviation for continuous variables and as numerical values (percentages) for categorical variables. For nonnormally distributed data, the median (interquartile range) was used. All reported P values are two-sided and were not adjusted for multiple testing. A P value <0.05 was considered to indicate statistical significance. SPSS Statistics (version 26, IBM) was used for the statistical analysis.

Results

Diagnostic accuracy of CTPB

To determine the diagnostic efficacy of CTPB for pulmonary nodules, we compared its diagnostic results with clinical diagnoses for the first time in real-world settings, thereby clarifying its actual performance. A total of 593 patients were enrolled in this study, with two patients lost to follow-up after biopsy. One patient with a subsolid nodule (CTR ≤50%) diagnosed with atypical adenomatous hyperplasia (AAH) was unable to be contacted, and one patient with a solid nodule diagnosed with lung tissue refused CT re-examination during the 2-year follow-up. Ultimately, 591 patients were included in the analysis. The accuracy rate of malignant and benign pulmonary nodule diagnosis was 95.10%, with a specificity of 100% and a sensitivity of 92.79%. The positive predictive value was 100%, and the negative predictive value was 86.76% (Figure 2). The diagnostic performances of different types of nodules are presented in (Table 1).

Figure 2 Diagnostic biopsy results for patients with pulmonary nodules. CT, computed tomography; CTR, consolidation-to-tumor ratio; F/U, follow-up; FN, false negative; TN, true negative; TP, true positive.

Univariate analysis of accuracy

Our analysis of factors affecting the accuracy of the diagnosis revealed that inaccurately diagnosed lesions were smaller (in the inaccurate group, 1.60±0.68 cm vs. the accurate group, 1.86±0.69 cm; P=0.04), but lesion sizes were not different between the two groups (P=0.22). Biopsy of lung nodules predominantly showing GGO had a lower diagnostic accuracy than those predominantly showing consolidation [118 of 136 patients (86.8%) in the accurate group vs. 444 of 455 patients (97.6%) in the inaccurate group; P<0.001] (Table 2). In terms of technical aspects, an increased number of cuts (P<0.001) and the use of a coaxial needle (P=0.02) technique were associated with increased diagnostic accuracy (Table 3).

Multivariate logistic regression analysis of accuracy

Multivariate logistic regression analysis (Figure 3) revealed that the diagnostic accuracy for solid nodules was 11.159 times greater than that for pGGNs (P<0.001), and the diagnostic accuracy for subsolid nodules with a CTR >50% was 17.974 times greater than that for pGGNs (P=0.001); however, there was no significant difference in diagnostic accuracy between subsolid nodules with a CTR ≤50% and pGGNs (P=0.15). The diagnostic accuracy of automatic biopsy needles was 0.345 times lower than that of semiautomatic biopsy needles (P=0.02). Biopsy of peripheral and intermediate lung nodules showed superior diagnostic accuracy compared to biopsy of lesions located in the hilar region (P=0.02, P=0.006). In addition, an increased number of cuts was positive factors for predicting the diagnostic accuracy of biopsy (P=0.01). These factors have certain value in predicting the diagnostic accuracy of lung nodule biopsy (area under the receiver operating characteristic curve, 0.812) (Figure 4).

Figure 3 Multivariate analysis (forward stepwise: LR) showing that solid nodules, subsolid nodules (CTR >50%), semiautomatic (tru-cut) needles, and nonhilar nodules significant impacts the diagnostic accuracy of lung nodule biopsy. CI, confidence interval; CTR, consolidation-to-tumor ratio; LR, likelihood ratio; OR, odds ratio; pGGN, pure ground-glass nodule.

Figure 4 The accuracy probability for each patient was calculated, and the ROC curve was plotted based on this probability (AUC =0.812, 95% CI: 0.724–0.900). AUC, area under the curve; CI, confidence interval; ROC, receiver operating characteristic.

Complications associated with CTPB

The incidence of immediate and delayed pneumothorax was 13% (77/591); 12 patients with immediate pneumothorax underwent direct drainage, and 8 patients with delayed pneumothorax underwent catheter drainage. The presence of pneumothorax did not affect the accuracy of biopsy diagnosis [pneumothorax group, 90.9% (70/77) in 70 patients vs. nonpneumothorax group, 95.7% (492/514) in 514 patients; P=0.07]. The incidence of high-grade hemorrhage was 27.1% (160/591), and high-grade hemorrhage did not affect the accuracy of biopsy diagnosis [high-grade hemorrhage group, 93.1% (149/160) in 160 patients vs. low-grade hemorrhage group, 95.8% (413/431) in 431 patients; P=0.18]. The incidences of pneumothorax were 8.3%, 9.2%, 15.0%, and 14.0% for ground-glass nodules (GGNs), subsolid nodules (CTR ≤50%), subsolid nodules (CTR >50%), and solid nodules, respectively (χ²=2.856, P=0.41). The incidences of high-grade hemorrhage were 33.3%, 28.9%, 31.0%, and 24.3% for GGNs, subsolid nodules (CTR ≤50%), subsolid nodules (CTR >50%), and solid nodules, respectively (χ²=3.559, P=0.31). In addition, the incidences of hemothorax, pleural reaction, chest wall hematoma, and air embolism were 3.6% (21/591), 0.7% (4/591), 0.2% (1/591), and 0.2% (1/591), respectively, without biopsy-related deaths.

Discussion

In this prospective, multicenter, real-world study, our rationale was to accurately assess the diagnostic performance of CTPB for lung nodules in real-world clinical settings. The aim was to determine its accuracy, associated complication rates, and identify factors influencing the biopsy diagnoses. We found that CTPB had a diagnostic accuracy of 95.1% for lung nodules, with a pneumothorax rate of 13% and a high-grade pulmonary hemorrhage rate of 27.1%. It is crucial to recognize that real-world factors such as automatic needles, ground-glass-predominant nodules, and hilar nodules can impact the accuracy of lung biopsy diagnoses. These results may be beneficial for the technical application and clinical assessment of CTPB.

Multiple randomized controlled studies have shown through meta-analysis that CTPB has greater diagnostic accuracy for peripheral lung nodules than radial endobronchial ultrasound-transbronchial biopsy (rEBUS-TBB), especially when the nodule size is between 1 and 2 cm (10). In this study, there was no statistically significant difference in diagnostic accuracy between hilar and peripheral lung nodules, but hilar nodules were identified as one of the factors for inaccurate lung nodule diagnoses. At the same time, we also agree that CTPB has advantages in the diagnosis of nodules less than 2 cm in size, as there was no significant difference in diagnostic accuracy between ≤2 cm (1.38±0.39 cm) nodules and 2–3 cm nodules in this study (χ²=2.743, P=0.10). Nonetheless, the study results suggest that CTPB and cryo-radial biopsy yield similar diagnostic rates for lung nodules, with cryo-radial biopsy being associated with lower complication rates (16). However, confirmation of these findings with even larger sample sizes is necessary. In summary, among the study population, nodule size did not influence diagnostic accuracy; however, nodules located in the hilar region remained a significant factor contributing to diagnostic inaccuracy.

In addition to focusing on the size and location of the lesion, it is important to understand the influence of ground-glass components in the nodule on the results of CTPB. A study utilizing propensity score matching that examined GGO and solid nodule tendencies suggested that CTPB has similar diagnostic accuracy and complication rates (17). However, in real-world scenarios, this may vary significantly. Compared to solid nodules (CTR >50%), GGNs (CTR ≤50%) had a significantly greater FN rate of biopsy confirmation after surgical resection [GGN group, 16/62 (25.8%) vs. solid nodule group 5/92 (5.4%); P<0.001]. Although interstitial invasion in CTPB samples is underestimated compared to that in surgical pathology, especially in pure GGO lesions, its role cannot be ignored, as CTPB is a good way to determine the pathological nature of GGNs (18). In this study, the FN rate of biopsy for lesions with a predominantly ground-glass component was 12.5% (17/136); of these patients, 10 had biopsy pathological types of AAH or adenocarcinoma in situ (AIS) and were identified as having invasive adenocarcinomas postoperatively. Additionally, 15 patients (including 2 patients with glandular precursor lesions) with primary GGOs did not undergo surgery after biopsy but continued to be followed up. However, the sensitivity and specificity of biopsy in diagnosing subsolid nodules (CTR ≤50%) are consistent with the results of a previous meta-analysis (8). Therefore, when patients with primary GGOs have a negative or glandular precursor lesion diagnosis from biopsy, the pathological results should be treated with caution.

In this study, we focused not only on the accuracy of diagnosis but also on the common complications of CTPB. The rate of high-grade pulmonary hemorrhage associated with CTPB in this study was 27.1%, which was not significantly different from the incidence of high-grade pulmonary hemorrhage in lung nodules reported by Tai (P=0.10) (19). Due to its higher rate of common complications relative to transbronchial lung biopsy, CTPB cannot currently be considered as a first-line treatment option (5,6,10). Therefore, reducing the occurrence of common complications is essential for the further application and development of this technology, even if these complications do not affect the diagnostic accuracy of lung nodules. Numerous studies have reported technical suggestions for preventing common complications such as pneumothorax and pulmonary hemorrhage to minimize the occurrence of these complications as much as possible (12,13). In addition, it is still necessary to monitor the occurrence of rare complications, especially the fatal complication of venous air embolism. Therefore, standardized operation procedures, appropriate instrument use, and surgical techniques may all contribute to reducing the incidence of these common and rare complications.

From the perspective of device use, there was no significant difference in diagnostic accuracy between the two types of biopsy needle cutting methods for lung nodules of different sizes. However, multivariate analysis revealed that the use of automatic (end-cut) needles is an influencing factor for diagnostic accuracy. In terms of complications, the use of semiautomatic (tru-cut) needles is a protective factor against pulmonary hemorrhage (13) but not pneumothorax (12). Compared to an automatic cut (end-cut), a semiautomatic cut (tru-cut) is more directional when pushing the cutting slot needle and can clearly distinguish the relationship between the cutting surface and blood vessels, helping to avoid damaging adjacent blood vessels during cutting and thus reducing the risk of bleeding in the lesion area (Figure 5). These findings differ from that of a single-center, prospective study that revealed that using automatic tru-cuts and end-cuts achieves similar complications and diagnostic effects and that an end-cut needle has advantages in diagnosing smaller nodules (20). Additionally, in this study, we found that coaxial technology did not show diagnostic benefits; however, previous researches have shown that it was a protective factor for bleeding but not for pneumothorax (12,13).

Figure 5 Comparison of semi-automatic and automatic needle biopsy of lung nodules and related hemorrhage conditions. (A) A solid nodule in the dorsal segment of the lower lobe of the right lung, encircled by surrounding blood vessels (arrows); (B) the semiautomatic (tru-cut) needle clearly illustrates the relationship between the cutting needle slot and adjacent blood vessels; (C) post-biopsy, a low-grade pulmonary hemorrhage manifests in the lesion area; (D) a solid nodule in the lateral segment of the middle lobe of the right lung, with discernible blood vessels at the edge of the lesion (arrow); (E) the automatic (end-cut) needle sheath reaches the edge of the lesion, situated on a layer superior to the blood vessels at the edge of the lesion; (F) automated cutting results in damage to this blood vessel, leading to high-grade pulmonary hemorrhage.

There are several limitations to our study. First, this was a prospective real-world study that lacked patient randomization, which may have affected the comparability of the results. Second, our follow-up time may have been insufficient, as there were 15 patients with GGOs for whom only biopsy pathology results were available at the end of follow-up, which may have affected the overall diagnostic accuracy. Third, these observed patients were treated only by physicians at each center, even though all of these physicians completed percutaneous biopsies according to relatively uniform standards (11); as a result, the data from this study do not reflect the overall population suitable for lung nodule biopsy. In addition, there may be some differences in pathological diagnosis among pathologists in different centers, which potentially reduces the diagnostic accuracy of lung nodule biopsy.

Conclusions

In summary, CTPB is a minimally invasive procedure that can provide highly accurate technique with an acceptable complication rate. Solid nodules, subsolid nodules (CTR >50%), number of cuts, semiautomated (tru-cut) needles, and nonhilar nodules are favorable factors for achieving an accurate diagnosis with CTPB. These results from real-world data can facilitate the development of prospective randomized controlled trials. Additionally, some methods from this study can be appropriately adopted to improve the diagnostic accuracy of CTPB and control complications within the scope of this study until higher-level evidence emerges.

Acknowledgments

We would like to thank the following ten medical centers for providing patients’ data: (I) Department of Nuclear Medicine (Treatment Center of Minimally Invasive Intervention and Radioactive Particles), First Affiliated Hospital of the Army Medical University, Chongqing, China; (II) Department of Minimally Invasive Interventional Medicine, Yunnan Cancer Hospital, Kunming, Yunnan, China; (III) Department of Radiology, Affiliated Hospital of Qingdao University, Qingdao, Shandong, China; (IV) Department of Computer tomograph, Baoshan People’s Hospital, Baoshan, Yunnan, China; (V) Treatment Center of Imaging Minimally Invasive, Beijing Jingxi Cancer Hospital, Beijing, China; (VI) Department of Thoracic Surgery, Shanghai Cancer Center of Fudan University, Shanghai, China; (VII) Department of Interventional, Affiliated Zhongshan Hospital of Dalian University, Dalian, Liaoning, China; (VIII) Department of Oncology, The Second Hospital of Tianjin Medical University, Tianjin, China; (IX) Department of Radiology, Second Affiliated Hospital of Fujian Medical University, Quanzhou, Fujian, China; (X) Department of Oncology, Dazhou Integrated Traditional Chinese Medicine and Western Medicine Hospital, Dazhou, Sichuan, China.

Footnote

Reporting Checklist: The authors have completed the STARD reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1912/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1912/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1912/prf

Funding: This study was supported by the National Natural Science Foundation of China (Grant No. 52275015 to C.H.) as well as the Medical Research Projects of Chongqing Science and Technology Bureau and Health Committee (Grant No. 2021MSXM342 to C.H.).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1912/coif). C.H. reports that this study was supported by the National Natural Science Foundation of China (Grant No. 52275015 to C.H.) as well as the Medical Research Projects of Chongqing Science and Technology Bureau and Health Committee (Grant No. 2021MSXM342 to C.H.). The other 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. This study was approved by the Ethics Committee of the First Affiliated Hospital of the Army Medical University (IRB No. KY2021084), and informed consent was obtained from all patients. All participating institutions were informed and agreed the study.

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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