Additional 1.1-mm cryobiopsy trial guided by rapid on-site cytologic evaluation of touch imprint cytology result of small forceps biopsy in peripheral pulmonary lesions: a prospective single-center study

Introduction

Background

Ultrathin cryobiopsy (CB) using a 1.1-mm cryoprobe has enhanced the diagnostic yield of bronchoscopy for peripheral pulmonary lesions (PPLs) compared with small forceps biopsy (FB) (1). CB may not be actively adopted in some institutions due to concerns regarding bleeding and pneumothorax. Each facility must develop its own strategies for selective CB performance. To address these problems, the rapid on-site cytological evaluation of touch imprint cytology (ROSE-TIC) was proposed as a real-time tool for assessing specimen adequacy during transbronchial biopsy (TBB) using FB. The ROSE-TIC allows bronchoscopists to determine whether additional diagnostic procedures, such as CB, are warranted based on immediate cytologic feedback.

At our institution, to introduce a 1.1-mm CB for PPLs safely and efficiently, a selective approach was adopted: CB was performed only when ROSE-TIC results of a 1.5-mm FB were negative.

To validate this staged strategy, a prospective study was conducted using a 1.5-mm FB to evaluate the ROSE-TIC.

Objective

This study aimed to evaluate the safety and efficacy of an additional 1.1-mm CB in cases with ROSE-TIC-negative results following FB. Moreover, it investigated whether this selective approach improves diagnostic outcomes without compromising safety. We present this article in accordance with the STARD reporting checklist (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-797/rc).

Methods

Patients and study design

Patients with PPLs less than 30 mm in diameter requiring pathological diagnosis were enrolled at the NHO Okayama Medical Center. Patients with localized pulmonary lesions measuring less than 30 mm in maximum diameter on chest computed tomography (CT), for which a biopsy was required to determine the management plan, were included in the study. The key exclusion criterion was the presence of lesions unsuitable for CB, such as those located within the medial one-third of the distance from the hilum, those in contact with large vessels posing a high risk of bleeding, or those located less than 10 mm from the pleura. All enrolled patients underwent bronchoscopic biopsy using a 1.5-mm FB and ROSE-TIC. CB using a 1.1-mm cryoprobe was performed only if ROSE-TIC results from the FB samples were negative. Cases were defined as ROSE-TIC-positive when malignant cells were identified. In these cases, FB was performed five to ten times. If the ROSE-TIC results were negative, additional CB was performed using a 1.1-mm cryoprobe as ROSE-TIC-negatives (shown in the procedure flow chart in Figure 1).

Figure 1 The procedure flow of this prospective study is summarized. CB, cryobiopsy; FB, forceps biopsy; PPLs, peripheral pulmonary lesions; rEBUS, radial endobronchial ultrasound; ROSE-TIC, rapid on-site cytological evaluation of touch imprint cytology.

The study was registered with the UMIN Clinical Trials Registry (UMIN000052642). The 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 NHO Okayama Medical Center, Japan (No. RINKEN 2023-026), and informed consent was taken from all the patients.

Bronchoscopic procedures

All procedures were performed in accordance with institutional protocols. Bronchoscopies were conducted by physicians with 3–10 years of experience, under the supervision of board-certified respiratory endoscopy specialists. All procedures were performed in an X-ray fluoroscopy room with patients under intravenous sedation (fentanyl and midazolam) and topical anesthesia (2% lidocaine). Target bronchi were identified using radial endobronchial ultrasound (rEBUS) (UM-S20-17, Olympus, Tokyo, Japan), fluoroscopy, and virtual navigation (SYNAPSE VINCENT, Fujifilm, Tokyo, Japan). Either the BF-MP290F, or BF-P290 (Olympus) bronchoscope, equipped with endobronchial ultrasound with guide sheath (EBUS-GS) was used. Biopsies were performed using 1.5-mm single-use oval cup forceps. No conventional forceps or transbronchial needle aspiration was used in the procedure. FBs were performed a minimum of five times in all cases.

ROSE-TIC and cytological procedures

Tissue samples obtained by FB were gently imprinted onto glass slides, air-dried, and stained using Cytoquick (Muto Pure Chemicals Co., Tokyo, Japan). One slide was evaluated immediately on-site, while the other was fixed in 95% ethanol and later stained with the Papanicolaou method. ROSE-TIC results were classified as either positive (confirming malignant cells) or negative by a cytotechnologist and at least two attending respiratory physicians. Neither bronchial lavage nor brushing cytology was performed; the cytological evaluation in this study was limited to ethanol-fixed touch imprint cytology and fluid rinse with 0.9% sodium chloride solution from the biopsy forceps.

CB procedures

A 1.1-mm cryoprobe (Erbe, Tubingen, Germany) was introduced into the same bronchus approached for FB under fluoroscopy. For cryoprobe guidance, a thin bronchoscope with the EBUS-GS technique or an ultrathin bronchoscope was used to approach the target lesion under radial EBUS guidance. Hemostatic strategies included the two-scope method, tube wedging (2), and the non-intubated CB method (3). The initial freezing time was set at 3 seconds, with adjustments permitted between 2 and 5 seconds, as needed. The presence of pneumothorax was checked post-procedure using chest X-ray. CB was discontinued if complications occurred or the target lesion became inaccessible. The aim was to perform three CB passes per patient. However, in real-world clinical practice, the additional CB was discontinued if the patient had inadequate sedation, bleeding occurred, or the lesion could no longer be reached.

Study outcomes

The primary endpoint of this study was the incidence of bleeding complications in the ROSE-TIC-positive and ROSE-TIC-negative groups. Secondary endpoints included diagnostic yield (specific histological or cytological diagnosis), specimen size, and the diagnostic accuracy (sensitivity, specificity, positive/negative predictive values) of ROSE-TIC. Specimen areas were measured for the largest FB sample and for all CB samples obtained.

Statistical analysis

As this prospective study was a feasibility study with no prior data, the number of patients was not determined by sample size analysis. Instead, the number of participants who could be clinically enrolled over approximately one and half year was estimated, and the target sample size was set at a minimum of 50 patients overall, including 20 for the ROSE-TIC negative group. Descriptive statistics were presented as numbers and frequency percentages, and numerical data were presented as medians (ranges). Differences were compared using Fisher’s exact test, Mann-Whitney U test, and McNemar’s test. A P value <0.05 was considered statistically significant. McNemar’s test was used to evaluate differences in diagnostic yield between FB alone and the combination of forceps and CB performed on the same lesions. All statistical analyses were conducted using EZR (version 1.61; Saitama Medical Center, Jichi Medical University, Saitama, Japan).

Results

Patient characteristics and lesion findings

From November 2023 to March 2025, 51 patients were enrolled in the study, and 50 patients underwent bronchoscopic examination according to the protocol (Figure 1). One patient was excluded from the analysis because of having a lesion with a diameter of ≥30 mm. Table 1 summarizes the patient characteristics and their target lesions. The median age was 73 years, and 26 patients were male. The median lesion diameter on CT was 14.5 mm (range, 8–29 mm). Thirty-eight cases had target lesions measuring ≤20 mm, and 12 cases had lesions measuring >20 mm and up to 30 mm. Half of the patients had solid nodules, 17 had partial solid nodules, and eight had ground-glass nodules (GGNs). Most target lesions were located bilaterally in the upper lobes and predominantly in the right lung. All lesions had radiological air bronchus signs with target lesions on prebronchoscopy CT.

Procedure data

The procedural data is also included in Table 1. rEBUS findings were categorized into within, adjacent to, blizzard, and invisible, and most patients showed ‘within’ or ‘adjacent to’. The median number of specimens obtained per patient was 10 (range, 5–10) for FB and 3 (range, 1–3) for additional CB. The median procedure time was 34.5 minutes (range, 14–90 minutes). ROSE-TIC of FB revealed 24 positive and 26 negative results. CB was subsequently administered to 26 cases. The median freezing time was 3 s (range, 2–5 s). Histopathological findings (n=50) are listed in Table 2.

Evaluation of safety

Bleeding grade was defined according to the criteria described by Folch et al. (4). Grade 1 or 2 bleeding was observed in five (20.8%) patients with ROSE-TIC-positives and nine (34.6%) with ROSE-TIC-negatives (Table 3). However, no significant difference existed between the two groups (P=0.35). All bleeding was well controlled by bronchoscopic suction, and no Grade ≥3 events occurred.

The complications, except for bleeding, included pneumothorax and pneumonia (Table 3). The former occurred in 4.1% of the ROSE-TIC-positives (n=1, 1/24), and the latter occurred in 3.8% of the ROSE-TIC-negatives group (n=1, 1/26). One patient in the FB group had an asymptomatic pneumothorax that spontaneously improved with conservative treatment, and one patient in the FB + CB group developed pneumonia around the sampling area, requiring hospitalization. No serious adverse events related to bronchoscopic examinations were observed in the present study.

Diagnostic yield by ROSE-TIC results

The specific diagnostic yield of the ROSE-TIC-positive group was 87.5% [95% confidence interval (CI): 67.6–97.3%] with histology (Table 4), and notably, 95.8% (95% CI: 78.9–99.9%) of cases made a specific diagnosis combined with cytological findings. The only case in which a specific diagnosis could not be made showed atypical cells in histopathology and cytology but was finally diagnosed with lung cancer through surgical resection. In the ROSE-TIC-negative group, the result of solely FB made a specific diagnosis in 34.6% (95% CI: 17.2–55.7%) and was enhanced with additional CB [73.1% (95 % CI: 44.3–82.8%)].

Comparison of diagnostic yield according to visual parameters and sample sizes

As shown in Figure 2, the total diagnostic yield was 80% (40/50) (95% CI: 66.3–90%), and FB-only diagnostic yield was 60% (30/50) (95% CI: 45.2–73.6%). Diagnostic yield was significantly higher in the combined group (McNemar’s test, P<0.01) than in the FB group (including FB-only results from both ROSE-TIC-positive and -negative cases).

Figure 2 Diagnostic yield according to ROSE-TIC results and the impact of additional cryobiopsy. The diagnostic yield of FB alone was 60% (30/50). ROSE-TIC-positive cases (n=24) achieved a specific diagnosis in 87.5% (21/24), while ROSE-TIC-negative cases (n=26) showed a lower diagnostic rate of 34.6% (9/26) with FB alone. An additional 1.1-mm CB in ROSE-TIC-negative cases improved the overall diagnostic yield to 80% (40/50). CB, cryobiopsy; FB, forceps biopsy; ROSE-TIC, rapid on-site cytological evaluation of touch imprint cytology.

Small nodules of ≤20 mm particularly benefited from the addition of CB [73.6% (95% CI: 56.9–86.6%) vs. 53.0% (95% CI: 35.8–69%), P=0.01] (Table 5). According to rEBUS findings, the diagnostic yield was 100% (23/23) (95% CI: 85.2–100%) when the rEBUS probe was within the lesion, 77.8% (14/18) (95% CI: 52.4–93.6%) when adjacent to the lesion, and 33.3% (3/9) (95% CI: 7.5–70.1%) for blizzard signs. CB contributed additional diagnostic value in 4 cases showing the “within”, 4 cases in the “adjacent”, and 2 cases in the “blizzard”. Partially solid nodules on CT were more beneficial for pathological confirmation with additional CB. Figure 3 shows the case with the smallest nodule (8 mm) included in this study, and the diagnosis was made using solely CB alone.

Figure 3 Effective case of additional cryobiopsy for ROSE-TIC negative lesion. (A) A case of an 8-mm right upper lobe pulmonary nodule. (B) EBUS-GS revealed the lesion adjacent to the bronchus. (C) Histopathological findings of forceps biopsy have no specific findings (hematoxylin and eosin staining). (D) Histopathological findings of cryobiopsy showed adenocarcinoma (hematoxylin and eosin staining). EBUS-GS, endobronchial ultrasound with guide sheath; ROSE-TIC, rapid on-site cytological evaluation of touch imprint cytology.

CB yielded significantly larger specimens than maximum specimens of FB [median: 2.70 mm² (range, 0.54–8.17 mm²) vs. 1.35 mm² (range, 0.46–3.92 mm²); Mann-Whitney U test, P<0.001] (shown in Figure 4).

Figure 4 Comparison of the sample size between CB and FB. Statistical analysis was made by the Mann-Whitney U test. CB samples were significantly larger than FB samples (median: 2.70 vs. 1.35 mm²; P<0.001). CB, cryobiopsy; FB, forceps biopsy.

ROSE-TIC accuracy

ROSE-TIC demonstrated a sensitivity of 79.3% (95% CI: 60.3–92%), a specificity of 95.2% (95% CI: 76.2–99.9%), a positive predictive value of 95.8% (95% CI: 78.9–99.9%), and a negative predictive value of 76.9% (95% CI: 56.4–91%).

Discussion

This prospective study evaluated a selective approach of adding a 1.1-mm CB to a 1.5-mm small FB for diagnosing small PPLs, guided by the results from ROSE-TIC of FB. These findings demonstrate that this strategy significantly improves the diagnostic yield without increasing the risk of severe complications. Notably, additional CB contributed diagnostic value, particularly in small lesions of ≤20 mm.

Additional ultrathin CB using a 1.1-mm cryoprobe has been shown to improve the diagnostic accuracy of bronchoscopy for PPLs compared with conventional FB (1,3,5). Furthermore, CB has shown particular efficacy for adjacent lesions (4,6) and blizzard patterns on rEBUS (7). However, by integrating the ROSE-TIC into the decision-making process, unnecessary use of CB can be avoided, optimizing both safety and resource utilization. Thus, this bronchoscopic intervention approach may serve as a practical model for the safe introduction of CB into real-world clinical practice.

No Grade ≥3 bleeding complication was observed in either the ROSE-TIC-positive or -negative groups. This favorable safety profile is likely due to the use of a short freezing time with smaller sample sizes compared to those obtained with 1.7- or 1.9-mm cryoprobes. Additionally, the use of non-intubated CB techniques, which have been reported to reduce the risk of bleeding (3), may have contributed to the reduced complication rate. Therefore, shorter freezing times and the use of non-intubated CB are thought to ensure procedural safety. In contrast, it may be beneficial to attempt longer freezing times using methods such as the two-scope technique for cases with GGNs or where tumor exposure in the bronchi is not anticipated. Other complications, except bleeding, were tolerable in this study, suggesting that the overall risk profile of the procedure was comparable to that of conventional bronchoscopy.

In the present study, when ROSE-TIC of the FB yielded a positive result, a definitive diagnosis of malignancy, including a cytological diagnosis, was achieved in 23 of 24 cases. In other words, a positive ROSE-TIC result strongly suggests that the diagnostic process can be completed using FB alone. Conversely, when the ROSE-TIC of the FB was negative, additional CB contributed to enhanced diagnostic yield in 10 cases. Our institution’s approach to determining the need for extra CB in real-time, based on on-site cytology, appears to be effective in improving the diagnostic yield.

The overall specific diagnostic yield was significantly higher for the combined results than for the FB-only results. Sumi et al. (6) reported a diagnostic yield of 81.8% for all lesions using a combination of 1.1-mm CB and FB via an ultrathin bronchoscope, whereas the yield using FB alone was 62.1%. The results of this study are comparable to those of a previous study. However, two key differences existed: the freezing time used in this study was shorter (5–7 s in the previous report), and the cryoprobe was not used in all cases. These findings suggest that even with the application of the ROSE-TIC and limited freezing time, a comparable diagnostic yield could be achieved.

The diagnostic yield in the subgroup of lesions measuring 21–30 mm was 100% (12/12) when FB and CB were combined. In two of these cases, additive CB provided an incremental diagnostic benefit. For lesions measuring 20 mm or less, the diagnostic yield was 73.6% (28/38), with CB contributing to enhanced yield in eight cases. This implies that small nodules (<20 mm) benefit particularly from the addition of CB. Previous articles’ review (8) has shown a diagnostic yield for EBUS-UT of 61% for lesions <20 mm. In another Japanese review of EBUS-GS (9) reported by Minami et al. the diagnostic yield of EBUS-GS was 61.3% for lesions ≤20 mm. Compared with these reviews, the diagnostic yield for lesions of ≤20 mm was likely higher in this study (74% in lesions < 20 mm, n=38).

According to the rEBUS findings in this study, the diagnostic yields of combined FB and CB were better than those of FB alone. CB contributed approximately 20% of the additional diagnostic value in each finding of within, adjacent to, and blizzard. Oki et al. previously reported that using a small forceps with an ultrathin bronchoscope yielded diagnostic rates of 82% for “within” lesions and 42% for “adjacent” lesions (10). The diagnostic performance of FB alone in this study was comparable, and the additional utility of CB was demonstrated.

The CB yielded significantly larger samples than the largest FB specimens in each case. However, due to the intentionally short freezing seconds, extremely large specimens (median sample size of CB was 7.0 mm², median freezing time 8 s, range, 4–12 seconds) were not obtained, as previously reported (1). Previous studies have suggested that extending the freezing time (6 s) may improve the diagnostic yield (11). Nonetheless, in this prospective study conducted during the introduction phase of a 1.1-mm CB, limited freezing times proved to be a practical and safe strategy for minimizing bleeding risk.

ROSE-TIC during TBB has been reported to provide immediate diagnostic feedback and may contribute to improved success rates in molecular analysis of lung cancer (12). ROSE-TIC not only enhances diagnostic yield but also shortens the overall procedure time (13). Previous studies suggest that when ROSE-TIC is negative during TBB with a 1.5-mm FB and EBUS-GS, an additional 1.9-mm FB after a 1.5-mm FB guided by the ROSE-TIC may improve diagnostic yield (14). Similarly, these findings indicate that adding a 1.1-mm CB guided by ROSE-TIC-negative cases of small FB further enhances diagnostic performance. Given the limitations of cost and manpower, the ROSE-TIC enables selective application of CB only when required to enhance diagnosis and optimize resource utilization.

As a limitation, the study included a relatively small sample size (n=50) and was conducted at a single center. Larger multicenter studies are required to establish the generalizability and validity of this method. Additionally, this study focused on diagnostic yield but did not evaluate the adequacy of specimens for next-generation sequencing (NGS) analysis. When NGS or other molecular testing is anticipated, the routine addition of CB may be preferable to obtain larger and higher-quality tissue samples (15).

Adding CB after FB, rather than proceeding directly to CB, may sometimes increase anesthesia time, bronchoscopy suite time, and overall cost (including pathology cost) due to the additional procedure. However, for small lesions or cases with a ground-glass component, direct CB without relying on ROSE-TIC may be a reasonable option. These results may only apply to lesions with a positive radiological air bronchus sign and to patients who do not meet the study exclusion criteria.

Conclusions

The selective addition of a 1.1-mm CB based on ROSE-TIC results of the FB is a feasible and effective strategy for improving the diagnostic yield. This approach may be particularly beneficial for small PPLs (≤20 mm) and part solid nodules, offering a minimally invasive method to guide biopsy decisions.

Acknowledgments

We express our sincere gratitude to the patients who consented to participate in the study. We also thank the cyto-screeners (Kenta Fujita, Yukari Harada, Shota Muramoto, Kyohei Oishi) in the Department of Pathology at NHO Okayama Medical Center for their dedicated support. We would also like to thank Editage (www.editage.com) for their English language editing services.

Footnote

Reporting Checklist: The authors have completed the STARD reporting checklist. Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-797/rc

Data Sharing Statement: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-797/dss

Peer Review File: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-797/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-2025-797/coif). Y.T. received lecture fees from AstraZeneca, AMCO, Chugai Pharmaceutical, and MSD. Ken Sato received lecture fees from OLYMPUS, AstraZeneca, and Harada Sangyo. H.W. has received honoraria from AstraZeneca, Chugai Pharmaceutical, and Eli Lilly. K.K. has received honoraria from MSD, Daiichi Sankyo, AstraZeneca, Kyowa Kirin, Chugai Pharmaceutical, Taiho Pharmaceutical, and Bristol Myers Squibb. K.F. received honoraria from AstraZeneca, Chugai Pharmaceutical, Ono Pharmaceutical Co. 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. The study was approved by the Institutional Review Board of the NHO Okayama Medical Center, Japan (No. RINKEN 2023-026) and informed consent was taken from all the patients.

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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