Outcomes of radial probe endobronchial ultrasound-guided transbronchial lung cryobiopsy using guide sheath and the target fixing technique

Introduction

Lung cancer is the second most common cancer and the leading cause of cancer-related mortality in 2020, accounting for approximately 11.4% of diagnosed cancers and 18.0% of deaths (1).

Low-dose computed tomography (CT)-based early cancer screening for high-risk individuals has been established as the primary strategy for reducing lung cancer mortality (2). Among patients with lung nodules suspected of malignancy, upfront video-assisted thoracoscopic surgery resulted in a final non-cancer diagnosis in 28 (34.1%) patients (3). Recent guidelines for non-small cell lung cancer have recommended perioperative treatment, including neoadjuvant combination chemotherapy and immunotherapy for selected patients (4). Small-cell lung cancer requires distinct treatment approaches (5). Therefore, pathological confirmation prior to treatment initiation has become essential to guide optimal management and avoid inappropriate interventions (3). Furthermore, the demand for tissue biopsies has increased with the growing use of molecular testing, including next-generation sequencing technology (6); therefore, the need to obtain high-quality samples from peripheral pulmonary lesions (PPLs) is expected to continue to rise.

Biopsy methods for diagnosing PPLs in early lung cancer include CT-guided percutaneous lung biopsy and bronchoscopic biopsy. The diagnostic yield of CT-guided percutaneous needle biopsy of intrathoracic lesion is 83.5%, which is higher than that of radial probe endobronchial ultrasound (RP-EBUS), especially for lesions measuring 1–2 cm (CT-guided percutaneous vs. RP-EBUS: 83% vs. 50%) (7). However, procedure-related complications, including pneumothorax and hemorrhage, have been observed in up to 61% and 5–16.9% of patients, respectively (8). Although the diagnostic yield remains a challenge, bronchoscopic methods for PPL biopsy, including RP-EBUS, guide sheath (GS), and electromagnetic navigation bronchoscopy (ENB), have been a recent advance (9). A previous meta-analysis reported that a positive and definite diagnosis was achieved in approximately 65% of patients, with an overall diagnostic accuracy of 74% and variable yields of 38.5–96.8% for SuperDimension™ and 33.0–90.2% for Veran™ (10-12). And ENB performed with cone-beam CT showed good diagnostic yields of 82.1–87.1% (13,14). Of the RP-EBUS GS-guided lung biopsies, the diagnostic yields of forceps biopsy and cryobiopsy were 65.3% and 71.5–84.4%, respectively (15,16). Diagnostic yield in forceps biopsies is influenced by target lesion morphology (solid vs. others) and RP-EBUS orientation (15). Although transbronchial lung cryobiopsy (TBLC) has demonstrated superior diagnostic performance compared with forceps biopsy (17), an unmet need for further improvement persists.

This study aimed to address certain technical limitations associated with this procedure. First, efforts are needed to address the semi-real-time nature of the procedure conducted through a guided system. Second, the lung moves during the biopsy due to repeated inhalation, exhalation, and coughing. Hence, this study proposes a target-fixing method and evaluates its impact on the diagnostic rate of tissue biopsy procedures. We present this article in accordance with the STARD reporting checklist (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-538/rc).

Methods

Study design and patient

This retrospective observational study analyzed the clinical data from 129 patients who underwent RP-EBUS-TBLC using GS without fluoroscopy at the Keimyung University School of Medicine, Dongsan Hospital (Daegu, South Korea) between January 2023 and April 2025. We included the cases to diagnosis of malignancy. The final analysis with 120 cases (Figure 1). PPLs were defined as lesions located within the lung parenchyma that were not directly visible on bronchoscopy but identifiable on CT.

Figure 1 Flow diagram illustrating the participant selection process. RP-EBUS-TBLC performed via a GS, not otherwise specified. GS, guide sheath; NOS, not otherwise specified; RP-EBUS-TBLC, radial probe endobronchial ultrasound-guided transbronchial lung cryobiopsy.

Dohyun’s method

All procedures were performed using Dohyun’s method, known as the “target-fixing technique”. As the GS-guided biopsy procedure is a semi-real-time procedure, the position of the biopsy probe within the lesion cannot be guaranteed once the RP-EBUS is removed. Although after identifying the target nodule using RP-EBUS, the lesion could be shift in position as the patient breathes.

Therefore, the bronchoscope was gently advanced as far as possible to secure its position (Figure 2). Subsequently, the RP-EBUS probe was slowly retracted and carefully positioned over the target. During repeated inhalation and exhalation, the target was continuously monitored on RP-EBUS images to ensure stability (Video S1, before Dohyun’s method; Video S2, after Dohyun’s method). Using this approach, tissue biopsy was performed with the target fixed at a point where it could be maintained as consistently as possible, even in challenging situations such as bronchus type II and III lesions (18) and during patient breathing or coughing.

Figure 2 Schematic diagram illustrating the Dohyun’s method (target-fixing method).

Procedure

An endobronchial approach was used for lung biopsy in patients with suspected malignant lesions identified on chest CT. When RP-EBUS was selected, all bronchoscopic procedures were performed by a pulmonologist (T.K.). The operator has 5 years of experience in the bronchoscopy, RP-EBUS, linear probe EBUS-transbronchial needle aspiration (TBNA), and TBLC.

The patients were administered intravenous midazolam (2–5 mg) and fentanyl (25–50 µg) for moderate-to-deep sedation at the start of the procedure. All procedures were performed under intubation using a 7.0-mm endotracheal tube along with oxygen supplementation at a flow rate of 2 to 6 L/min through the tube. Lidocaine hydrochloride solution (1%, 200 mg/20 mL) was administered to the vocal cords, carina, and right and left main bronchi via a bronchoscope (BF-P290 with a 2.0-mm working channel; Olympus, Tokyo, Japan) to induce local anesthesia. The PPL target was approached using a 1.4-mm RP-EBUS (UM-S20-17S; Olympus) and a 1.95-mm GS setup (K-201 or K-402; Olympus). When the target lesion was identified, it was considered successfully targeted. Following target fixation with Dohyun’s method, the RP-EBUS was removed, and a cryobiopsy probe [flexible cryoprobe, outside diameter (OD) 1.1 mm, length (L) 1.15 m; Erbe Elektromedizin GmbH, Germany] was introduced through the GS. The tissue was frozen for 4–8 s, and the probe was removed en bloc with the bronchoscope. Post-biopsy bleeding was immediately assessed using bronchoscopy through the endotracheal tube, with hemostasis achieved using epinephrine if necessary. If preoperative CT indicated the potential for significant bleeding (target lesion with cavitary lesion, severe bronchiectasis, or adjacent vascular shadowing), a hemostatic balloon catheter (B5-2C; Olympus) was pre-positioned in the segment targeted for biopsy, with balloon inflation performed immediately after the procedure. TBLC was repeated at the operator’s discretion. In cases of severe bleeding unresponsive to conservative measures, the hemostatic balloon catheter was used for treatment.

Data collection

Data obtained from the electronic medical records were retrospectively analyzed. The following variables were recorded and examined: (I) demographic characteristics including sex, age, height, weight, comorbidities, and smoking history; (II) lung function test results, including forced expiratory volume in 1 s (FEV1), forced vital capacity (FVC), and FEV1/FVC ratio; (III) radiologic characteristics on chest CT, including lesion size, lesion type (solid or sub-solid), pleural abutment, lobar location, and axial distribution; (IV) RP-EBUS findings, categorized as “within” vs. “adjacent to” and “dense sign” vs. “blizzard sign” (19); (V) procedural details, including procedure time, number of biopsies, use of epinephrine for hemostasis, and adverse events such as pneumothorax; and (VI) pathologic reports, including diagnosis and confirmation of the final diagnosis by follow-up CT or surgical biopsy. All cases that underwent TBLC were discussed multidisciplinary, including radiology and pathology, at the pulmonary pathology conference.

The confirmation of findings of CT images was reviewed jointly by one radiologist (Jung Hee Hong) from the same medical center specializing in lung imaging, and cross-comparison was not possible because our center only has one radiologist specializing in lung imaging. CT-bronchus sign (CT-BS) was classified as either present (airway sites adjacent to or directly aligned with the target) or absent. The bronchus type 1 that directly reached within the target lesion, of those classified as bronchus type 2, the bronchus was compressed or invisible (20-24). The axial distribution was categorized into inner, middle, and outer third. Vertical distribution was classified into upper lungs (right and left upper lobes, right middle lobe) and lower lungs (right lower lobes, and left lower lobes). Lesion size on CT was measured as the longest diameter. Lesion type was classified as solid, sub-solid, or ground-glass opacity; however, no ground-glass opacities were identified among the participants. The number of biopsies was defined as the total number of samples obtained.

Statistical analysis

Data were expressed as frequencies (%) for categorical variables and as means ± standard deviations (SDs) for continuous variables. The diagnostic yield was calculated as the proportion of patients with true positive (TP) and true negative (TN) results out of the total number of patients (25). Among patients with unconfirmed diagnoses, TNs were defined as those whose lung lesions improved after at least 3 months of follow-up, with confirmed tuberculosis and achieved resolution following anti-tuberculosis treatment, or with surgically proven granuloma. Patients with initially negative results but insufficient information owing to loss to follow-up or refusal to undergo further evaluation were classified as having an indeterminate diagnosis. These patients were included in the sensitivity analysis, assuming that all were TNs or false negatives (FNs). Low and high estimates of diagnostic yield, sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) were calculated.

To evaluate the association between two nominal variables, a Chi-squared test was performed. Logistic regression analysis was used to evaluate the factors associated with pathologic confirmation. Variables with a P value of <0.2 in the univariate analysis were included in the multivariable analysis, which was performed using the backward log-likelihood ratio method. A P value of <0.05 was considered significant. All statistical analyses were performed using SPSS Statistics version 25 (IBM Corp., Armonk, NY, USA) and R version 4.1.1.

Ethical statement

This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Institutional Review Board of the Keimyung University School of Medicine (approval No. 2024-04-049). The requirement for informed consent was waived due to the retrospective nature of this study by the Institutional Review Board of the Keimyung University School of Medicine.

Results

Participant and baseline characteristics

As shown in Figure 1, the results of 120 patients who underwent RP-EBUS-TBLC using GS were evaluated. Table 1 presents a summary of the participant characteristics. The average age was 68.1±9.8 years, with 66 (55.0%) patients classified as ever-smokers and 72 (60.0%) being men. The most common location of the target lesion was the left upper lung (31.7%), followed by the right upper lung (26.7%). The mean lesion size on CT was 2.50±1.20 cm, and 27 (22.5%) lesions were classified as sub-solid nodules. With regard to axial distribution, lesions were located in the inner third (3 lesions, 2.5%), middle third (57 lesions, 47.5%), and outer third (60 lesions, 50.0%). CT-BS was in 108 (90.0%) patients (Table 1). The within for RP-EBUS findings were observed in 72 (60.0%) patients, and a dense sign was observed in 84 (70.0%) patients. The mean number of TBLC was 3.93±1.22, and the procedure time from the administration of sedatives to the administration of antidote was 31.9±11.3 minutes. A correlation was found between PPL characteristics on CT (solid vs. part-solid) and RP-EBUS findings (dense vs. blizzard sign) (Pearson’s Chi-squared =50.523, P<0.001) (Table S1).

Diagnostic outcomes and complications

The final diagnostic results, including those not confirmed by RP-EBUS-TBLC using GS, are presented in Figure 3. Malignancy was confirmed by RP-EBUS-TBLC using GS in 89 of 120 (74.2%) patients. Among those with confirmed malignancies, non-small cell lung cancer was the most common diagnosis (83 patients), with adenocarcinoma being the predominant subtype (62 patients). Of the patients without confirmed malignancy via RP-EBUS-TBLC using GS, six were diagnosed with malignancy through CT-guided percutaneous lung biopsy or surgical lung biopsy. Twenty patients demonstrated TN results; four were confirmed to have inflammation, which eventually resolved within 3 months as shown on follow-up CT; four were diagnosed with tuberculosis, which improved following anti-tuberculosis treatment; and three confirmed granulomas unrelated to tuberculosis, as confirmed by surgical lung biopsy. One patient was diagnosed with a carcinoid tumor through TBLC and after lobectomy, and this diagnosis was consistently confirmed. Five patients were not initially diagnosed with malignancy and not further evaluated owing to loss of follow-up or refusal to undergo further invasive workup.

Figure 3 Diagnostic outcomes of the study participants. RP-EBUS-TBLC performed via a GS, not otherwise specified. GS, guide sheath; NOS, not otherwise specified; RP-EBUS-TBLC, radial probe endobronchial ultrasound-guided transbronchial lung cryobiopsy.

The final diagnostic yield of RP-EBUS-TBLC using GS with Dohyun’s method was 94.8%, calculated by dividing the sum of TPs and TNs by the total number of patients, excluding those with an indeterminate diagnosis (Table 2). When an indeterminate diagnosis was considered as either a FN or a TN result, the diagnostic yield ranged from 90.8% to 95.0%. The sensitivity and specificity were 93.7% and 100.0%, respectively (Table 2).

Pneumothorax developed as a complication in 5.0% (6/120) of the patients, with three requiring chest tube placements. Two patients experienced grade 3 or higher bleeding, and five patients underwent preemptive placement of a Fogarty balloon catheter at the operator’s discretion (Table 1).

Factors associated with higher diagnostic yield

Univariate and multivariate analyses of the factors associated with diagnosis are shown in Table 3. In the univariate analysis, a larger lesion size on CT, the presence of CT-BS, and upper lung distribution were associated with a higher diagnostic yield. In the multivariate analysis, CT-BS [odds ratio (OR): 14.901, P=0.001] was identified as a significant factor for diagnosis (Table 3). However, lesion size, eccentricity, and lung distribution were not significant factors for diagnosis. The within showed more diagnosis but there was not statistically significant (within vs. eccentric: 94.4% vs. 85.4%, P=0.09) (Table S2). Diagnostic yields by size were 76.5%, 85.0%, and 98.4% for ≤10, >10–20, and >20 mm, respectively (Table S3).

Discussion

This study retrospectively evaluated the diagnostic yield of RP-EBUS-TBLC using GS with Dohyun’s method. The diagnostic yield of RP-EBUS-TBLC using GS was 94.8%, indicating that RP-EBUS-TBLC using GS is a reliable diagnostic method for diagnosing lung lesions. Although a previous study showed bronchus type I and within finding is significant factor for higher diagnostic yields in RP-EBUS biopsy (20,26), when biopsies were performed using Dohyun’s method in PPL with “non-within”, we could diagnose 85.4%. The complication rate was acceptable, with pneumothorax observed in 5.0% of patients. On average, 3.93 cryobiopsies were performed per procedure, with a mean procedure time of 31.9 minutes, all conducted without general anesthesia. Among the 89 patients with a confirmed malignancy, 20 were examined using next-generation sequencing, including a driver mutation test. The tissue samples obtained via TBLC were sufficient for next-generation sequencing, allowing the analysis of all samples from 20 patients. Same as the previous study, TBLC could be a useful and safe tool for NGS analysis (27).

Recent advancements in bronchoscopy for PPL biopsy, particularly with RP-EBUS or navigation systems, have led to improvements; however, the diagnostic yields remained limited. A recent study reported a diagnostic yield of 74.9% for navigation systems, with a median lesion size of 20.9 mm (28). When combining navigation systems with RP-EBUS, no significant additional benefit in the overall diagnostic yield was observed (navigation/combination/RP-EBUS: 63.8%/64.2%/62.6%, P=0.94). However, the combination approach did show superior diagnostic yield for nodules with bronchus type II or III and a solid component of <20 mm (OR: 1.96, P=0.02) (18). Thus, RP-EBUS can provide more detailed and precise information about the target PPL in patients with bronchus type II or III. However, despite accurate access to the exact segment, the diagnostic yield remained limited. A review article reported that RP-EBUS-TBLB using forceps achieved a diagnostic yield of 70% (29). PPL biopsy with TBNA with guidance with RP-EBUS, diagnostic yields showed 53% and TBNA showed a higher accuracy when directly compared to TBB (60% vs. 45%) (30). Most recently, robotic-assisted bronchoscopy was introduced, TBLC showed higher diagnostic yield compare to TBNA (31). Recently, the TBLC technique was introduced and recommended for diagnosing interstitial lung disease in patients who are not eligible for surgical biopsy (32). Similarly, for suspected lung cancer targets, diagnostic yields ranging from 71.5% to 84.4% have been reported (15,16).

A target-fixing method was used in this study. We believe that lung biopsy remains challenging and offers limited diagnostic yield, particularly for small lesions and non-bronchus types I, as the target moves continuously during the biopsy procedure. The application of the GS technique can reduce misalignment between RP-EBUS removal and biopsy device insertion. But when performing a bronchoscopy, it is difficult to obtain accurate target tissue due to the gap between the removal of the RP-EBUS and the introduction of the biopsy probe by various factors such as respiration gaiting and coughing. It does not ensure on-target confirmation at the time of biopsy, as the procedure remains semi-real-time. The Dohyun’s method might help to reduce the error.

In this study, Dohyun’s method was used to minimize errors that occur in semi-real-time procedure during biopsy process. The RP-EBUS-TBLC using GS is also reported as a practical option for guiding cryobiopsy in this study. Although a double-arm comparison was not conducted, Dohyun’s method may theoretically offer an advantage in improving the diagnostic yield. Given the favorable diagnostic rate, this technique may be considered a viable option for lung biopsy.

Our study has some limitations. First, this was a retrospective study conducted at a single center. Therefore, the results require further validation in a larger study. Second, the diagnostic yield may have been overestimated, as the procedure was performed in patients selected based on CT findings that suggested suitability for bronchoscopy, and there were five indeterminate cases from the primary denominator for calculating the diagnostic yield. Third, the learning curve associated with TBLC and the effects of fluoroscopy have not been fully elucidated; therefore, evidence remains limited to support the initial routine application of this procedure or discuss its clinical utility. Fourth, Dohyun’s method proposed in this study is based on the operator’s continuous visualization of the target on the RP-EBUS screen despite the patient’s respiratory changes. This is a subjective judgment depending on the procedure environment and operator and is considered a limitation of this study.

Despite these limitations, this study aimed to evaluate the diagnostic value and safety of RP-EBUS-TBLC using GS without fluoroscopy. Furthermore, Dohyun’s method for target fixation was introduced. Accordingly, this study provides a meaningful contribution to the evidence supporting the use of TBLC in cancer diagnosis.

Conclusions

RP-EBUS-TBLC using GS with Dohyun’s method for diagnosing lung lesions suspected of malignancy demonstrated favorable diagnostic yield and safety outcomes. To address challenges associated with non-within or non-bronchus type I PPLs and respiratory gaiting, Dohyun’s method may aid in consistently maintaining alignment during semi-real-time biopsy procedures.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STARD reporting checklist. Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-538/rc

Data Sharing Statement: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-538/dss

Peer Review File: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-538/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-538/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. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Institutional Review Board of the Keimyung University School of Medicine (approval No. 2024-04-049). The requirement for informed consent was waived due to the retrospective nature of this study by the Institutional Review Board of the Keimyung University School of Medicine.

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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