A modified cryobiopsy specimen retrieval method using a thin bronchoscope and small guide sheath for the diagnosis of peripheral pulmonary lesions

Introduction

Background

In the diagnosis of peripheral pulmonary lesions (PPLs), a large guide sheath (GS) allows cryobiopsy specimens to be retrieved while the therapeutic bronchoscope remains in the airway, and its usefulness has been reported as GS-UTCB (ultrathin cryobiopsy through a GS) (1). However, most therapeutic bronchoscopes can be advanced only to the segmental or subsegmental bronchi. Therefore, the use of a large GS is feasible only in selected patients (2). In contrast, a small GS (outer diameter, 1.91 mm, compatible only with a 2.0-mm working channel) is frequently required to diagnose smaller PPLs. However, because the inner diameter of a small GS is approximately 1.5 mm, cryobiopsy specimens usually cannot be retrieved through the GS.

Rationale and knowledge gap

The Delphi consensus statement recommends 1.1-mm ultrathin cryobiopsy using a pull-through technique in which the bronchoscope is maintained within the airway during cryobiopsy specimen retrieval (3). Recently, the utility and safety of pull-through retrieval techniques for ultrathin cryobiopsy specimens have been reported (4-6). Building on these technical advances, we adopted a modified biopsy method involving direct en bloc retrieval of the cryobiopsy specimen with a small GS through the channel of a thin bronchoscope (2.0-mm). Using this approach, cryobiopsy was selectively added for small PPLs when the transbronchial biopsy (TBB) with forceps specimen obtained under endobronchial ultrasound with guide sheath (EBUS-GS) guidance appeared macroscopically insufficient or when rapid on-site evaluation (ROSE) yielded negative results. Hence, we named this approach the CRYO-GRATHP (ultrathin Cryobiopsy specimen with Guide sheath en bloc RetrievAl Through a bronchoscoPe channel) method.

Objective

This pilot study retrospectively evaluated the efficacy, safety, and feasibility of the CRYO-GRATHP method at our institution for the diagnosis of PPLs. We present this article in accordance with the STROBE reporting checklist (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2026-0855/rc).

Methods

Patients and study design

We retrospectively analyzed patients with PPLs who underwent bronchoscopic cryobiopsy using the CRYO-GRATHP method with a thin bronchoscope (2.0-mm working channel) as a pilot feasibility study at the Department of Respiratory Medicine, Okayama Medical Center, between April 2023 and March 2026. The flow diagram is shown in Figure 1. Six patients investigated in our previous report (7) were also included in the present study. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was approved by the Institutional Review Board of the NHO Okayama Medical Center (Approval No. RINKEN 2026-018; approval date: May 7, 2026). The requirement for written informed consent was waived because of the retrospective nature of the study.

Figure 1 Flow diagram showing study enrollment. GRATHP, ultrathin CRYObiopsy specimen with Guide sheath en bloc RetrievAl THrough a bronchoscoPe channel.

Bronchoscopic procedures

Bronchoscopy was performed using a thin bronchoscope with a 2.0-mm working channel (Fujifilm, EB-710P or OLYMPUS, BF-P290, Tokyo, Japan). Under fluoroscopic guidance, physicians identified the target lesion using the small EBUS-GS method (sheath outer diameter 1.91-mm, OLYMPUS, Guide Sheath Kit 2 K401, Tokyo, Japan). Small forceps biopsy was performed first, and at least five specimens were obtained whenever possible. The bronchoscope was advanced as far as possible and wedged into the target bronchus to achieve hemostasis. Forceps samples were evaluated macroscopically and by rapid on-site evaluation with touch imprint cytology (ROSE-TIC). After the small forceps biopsy was completed, the 1.1-mm cryoprobe (Erbe, Tubingen, Germany) was inserted through the GS without exchanging the bronchoscopic devices. Cryobiopsy was performed at the same location as the forceps biopsy site with a 1.1-mm cryoprobe for a predetermined duration (2–4 s), after which the frozen specimen was rapidly retrieved through the working channel by assistants. The endoscopist maintained wedging of the bronchoscope in the target bronchus while the cryobiopsy specimen was retrieved, performing suction as needed while carefully preventing bleeding from spilling into the central airway (Figure 2). The required hemostasis time was 2 min.

Figure 2 Illustration of the CRYO-GRATHP method. This cryobiopsy method involves en bloc retrieval of the cryoprobe and guide sheath through the working channel of a thin bronchoscope while maintaining bronchoscopic wedging for hemostasis. CRYO-GRATHP, ultrathin CRYObiopsy specimen with Guide sheath en bloc RetrievAl THrough a bronchoscoPe channel.

Study outcomes

The primary endpoint was diagnostic yield, which was defined using the standardized Delphi consensus definition for guided bronchoscopy studies (8). The secondary endpoints included safety, procedure duration, specimen size, sampling success according to freezing time, and biomarker test results. Bleeding complications were defined according to the Delphi consensus statements (9). Specimen size was measured using Olympus cellSens Standard software (Olympus, Tokyo, Japan).

Statistical analysis

Statistical significance was defined as P<0.05. The Mann-Whitney U test was used for statistical comparison of specimen sizes, and the McNemar test was used to evaluate differences in diagnostic yields. All statistical analyses were conducted using EZR (version 1.61; Saitama Medical Center, Jichi Medical University, Saitama, Japan).

Results

Patient characteristics and lesion findings

A total of 28 patients who underwent the CRYO-GRATHP method for PPLs were included (Table 1). The median patient age was 76 years (range, 56–84 years). Fifteen patients (54%) were male, and 13 (46%) were female. The median lesion size was 17 mm (range, 9–50 mm). Twenty lesions (71%) were smaller than 20 mm, whereas eight lesions (29%) were larger than 20 mm. Most lesions were in the upper lobes (79%), followed by the lower lobes and the middle lobe or lingular segments. On computed tomography, 43% of lesions were solid, and 57% were part-solid. All patients underwent additional cryobiopsy because rapid on-site cytological evaluation of small forceps biopsy specimens was negative.

Procedure data

Detailed procedural data are shown in Table 2. R-EBUS findings were classified as within the lesion in 61%, adjacent to the lesion in 18%, and blizzard in 21%. The median number of samples retrieved per patient was 5 (range, 5–15) for forceps biopsy and 3 (range, 1–5) for cryobiopsy, respectively. The median freezing time for cryobiopsy was 3 s (range, 2–4 s), and the median procedure time was 42 min (range, 24–76 min). Nineteen patients (68%) underwent the procedure without endotracheal intubation. The nine intubated patients were included in the early implementation phase of the CRYO-GRATHP method. In principle, both forceps biopsy and cryobiopsy were performed because these two sampling methods were considered complementary for diagnostic purposes.

Diagnostic yield of bronchoscopic biopsy

Detailed information on diagnostic yield is presented in Figure 3. The overall diagnostic yield was 75.0% [95% confidence interval (CI): 56.6–87.3%]. Forceps biopsy alone established a diagnosis in three patients, cryobiopsy alone in 14 patients, and both methods in four patients. The diagnostic yield was 25.0% (95% CI: 12.7–43.4%) for forceps biopsy and 64.3% (95% CI: 42.4–76.4%) for cryobiopsy (P=0.02). Of the 14 patients diagnosed exclusively by cryobiopsy, 10 (71.4%) had upper-lobe lesions.

Figure 3 The Venn diagram illustrates the complementary diagnostic yield of forceps biopsy and cryobiopsy. Four diagnoses were established by both biopsy methods, three by forceps biopsy alone, and 14 by cryobiopsy alone. Among the 14 lesions diagnosed exclusively by cryobiopsy, 10 (71.4%) were located in the upper lobe. Cryobiopsy showed a higher diagnostic yield than forceps biopsy (P=0.02).

Malignancy was diagnosed in 17 patients (60.7%), all of whom had non-small cell lung cancer (NSCLC), including one patient with invasive mucinous lung adenocarcinoma. Benign disease was diagnosed in four patients (14.3%), including cryptococcosis (n=1), granuloma (n=1), an IgG4-related nodule (n=1), and organizing pneumonia (n =1). These diagnoses were confirmed by disappearance or regression of PPLs in follow-up CT scans. Nonspecific pathological findings were observed in seven patients (25.0%). Of these seven patients, five were subsequently diagnosed with lung cancer following surgical resection.

Diagnostic yield according to visual parameters

Detailed data are presented in Table 3. The diagnostic yield was 70.0% (95% CI: 45.7–88.1%) for lesions ≤20 mm and 87.5% (95% CI: 47.3–99.7%) (7 of 8) for lesions >20 mm. According to CT appearance, the diagnostic yield was 91.6% (95% CI: 64.6–98.5%) for solid nodules and 62.5% (95% CI: 38.6–81.5%) for part-solid nodules.

Based on lesion location, a specific diagnosis was achieved in 77.3% (17 of 22) of upper-lobe lesions and in both lesions located in the middle lobe or left lingular segment, whereas the diagnostic yield for lower-lobe lesions was 50.0% (95% CI: 6.8–93.2%). The overall diagnostic yield was 88.2% (95% CI: 63.6–98.5%) for lesions with a within sign, 60.0% (95% CI: 14.7–94.7%) for those with an adjacent-to sign, and 50.0% (95% CI: 11.8–88.2%) for lesions showing a blizzard sign. Both lower-lobe cases that failed to yield a diagnosis exhibited a blizzard sign on radial EBUS.

Specimen size of bronchoscopic biopsy

The median size of the largest forceps biopsy specimen (n=28) retrieved per patient was 1.00 mm² (range, 0.59–2.79 mm²). In contrast, the overall median specimen size of cryobiopsy specimens (n=81) was 3.73 mm² (range, 0.70–10.8 mm²). Cryobiopsy specimens were significantly larger than forceps specimens (P<0.001) (Figure 4). Cryobiopsy specimen size according to freezing time was as follows: 2.71 mm² (range, 1.60–2.96 mm²) with 2 s (n=5), 3.91 mm² (range, 0.70–10.8 mm²) with 3 s (n=69), and 4.30 mm² (range, 2.42–9.56 mm²) with 4 s (n=7).

Figure 4 Comparison of specimen size between cryobiopsy and small forceps biopsy. Statistical analysis was performed using the Mann-Whitney U test. Cryobiopsy specimens were significantly larger than forceps samples (median 3.73 vs. 1.00 mm2; P<0.001).

Biomarker test

Among the 17 patients diagnosed with NSCLC, 13 had stage I disease. Among the four patients with advanced NSCLC who underwent molecular testing, two specimens were analyzed using the Oncomine Dx Target Test, and two were analyzed using the AmoyDx. An EGFR exon 19 deletion was identified in one patient by the Oncomine Dx Target Test. No other treatable driver alterations were detected. Programmed death-ligand 1 (PD-L1) testing was successfully performed in all advanced NSCLC cases.

Evaluation of safety

The safety profile is shown in Table 4. Regarding bleeding severity, grade 0 bleeding occurred in 75.0% (95% CI: 55.1–89.3%), grade 1 in 10.7% (95% CI: 2.3–28.2%), and grade 2 in 14.3% (95% CI: 4.0–32.7%). No severe bleeding events (grade ≥3) were observed with this method.

Non-bleeding complications included pneumonia, fever, and pseudogout, which were manageable with antibiotics or nonsteroidal anti-inflammatory drugs. Pneumothorax was not observed during the study.

No bronchoscope damage, GS damage, or airway injury attributable to the retrieval technique was observed during the bronchoscopic procedures.

Discussion

Key findings

This retrospective pilot study evaluated the feasibility of the CRYO-GRATHP method for diagnosing PPLs at our institution. The CRYO-GRATHP method may be particularly useful in four clinical settings: (I) patients undergoing bronchoscopic biopsy without endotracheal intubation; (II) upper-lobe lesions, where bronchoscopic advancement is technically challenging; (III) cases in which cryobiopsy is expected to improve diagnostic yield or biomarker testing success beyond that achievable with forceps biopsy alone, particularly when forceps samples are insufficient (e.g., small macroscopic size or inadequate samples based on ROSE-TIC findings); and (IV) cases in which cryobiopsy is required but conventional hemostatic techniques are considered unreliable.

Comparison with similar research

Nakai et al. reported the diagnostic utility and safety of ultrathin cryobiopsy specimen retrieval through a 2.0-mm working channel (without a small GS), a technique referred to as “non-intubated cryobiopsy” (5). Because this technique yields relatively small cryobiopsy specimens, it is considered safe and can be performed without endotracheal intubation. In the CRYO-GRATHP method, although a GS is used, the cryobiopsy sample passes through a 2.0-mm working channel; therefore, specimen size is theoretically expected to be comparable to that reported in the previous study. In fact, the median specimen size in this study was comparable to that of non-intubated cryobiopsy (5), and 68% of the procedures were performed without intubation; together with the low incidence of bleeding complications, this finding suggests that endotracheal intubation is unnecessary for the CRYO-GRATHP method.

Bronchoscopic advancement into the peripheral bronchi of the upper lobes is generally considered technically challenging. Oki et al. reported that the diagnostic yield was significantly higher in the GS group than in the non-GS group for right upper lobe lesions (10). In the present study, 79% of the lesions were located in the upper lobes, and an overall specific diagnosis was obtained in 77.3% of patients. These findings support the feasibility of the CRYO-GRATHP method for upper-lobe lesions.

Previous studies have demonstrated that adding ultrathin cryobiopsy to small forceps biopsy could improve the diagnostic yield for PPLs (11-13). Moreover, performing ultrathin cryobiopsy when ROSE-TIC of small forceps samples yields negative results can further increase the overall diagnostic yield (7).

Implications and actions needed

In this pilot feasibility study, ROSE-TIC of the forceps biopsy samples was negative in all cases. Cryobiopsy via the CRYO-GRATHP method may be particularly advantageous for small PPLs when forceps biopsy yields insufficient tissue. We also included one patient in whom invasive mucinous adenocarcinoma was diagnosed solely by cryobiopsy. Thus, cryobiopsy may represent a useful diagnostic strategy in selected cases in which this method is expected to provide additional diagnostic value (14).

Although the success rate of biomarker testing using specimens obtained by small EBUS-GS-TBB is reportedly poor than other techniques (15,16), additional ultrathin cryobiopsy may improve the success rate (17). In the present study, biomarker testing and PD-L1 evaluation were successfully completed in all four patients with advanced NSCLC, although 13 of the 17 patients with NSCLC had stage I disease and did not require biomarker testing in clinical practice. Thus, further evaluation is needed in larger cohorts.

Regarding complications of the CRYO-GRATHP method, bleeding was manageable, and no grade 3 or higher bleeding was observed. The balloon-blocking method for cryobiopsy can sometimes be technically challenging in the bilateral upper-lobe bronchi (18); therefore, this method may be particularly well suited to upper-lobe lesions, where the EBUS-GS approach is frequently advantageous. Although the two-scope technique can serve as an alternative for bleeding control, the CRYO-GRATHP method has potential advantages in that endotracheal intubation may not be required, and the use of two bronchoscopes is unnecessary.

Although repeated specimen retrieval while maintaining bronchoscope wedging at the bronchus could theoretically increase the risk of mechanical injury to the thin bronchoscope, GS, or distal airway, no such complications were observed in this pilot study. One possible explanation is that the relatively short freezing time (typically 3 s) produced smaller cryobiopsy specimens than those typically obtained with conventional cryobiopsy, thereby reducing retrieval resistance through the working channel. Nevertheless, given the limited sample size, further prospective studies are required to confirm the safety and reproducibility of this technique in a broader clinical setting.

As novel or modified cryobiopsy techniques using a 1.1-mm cryoprobe continue to evolve beyond conventional cryobiopsy, accumulating clinical evidence will be essential to establish the optimal technique for individual lesion characteristics and institutional practice (19,20).

Strengths and limitations

The principal strength of this pilot study is that it provides initial clinical evidence supporting the feasibility of the CRYO-GRATHP method in patients with PPLs. Compared with the previously reported radial probe endobronchial ultrasound-guided transbronchial lung cryobiopsy (RP-EBUS-TBLC) technique (21) using a 1.1-mm cryoprobe and thin bronchoscope with a small GS, the CRYO-GRATHP method demonstrates a similar bronchoscope configuration but differs in several procedural aspects. RP-EBUS-TBLC generally requires endotracheal intubation and retrieves the bronchoscope, GS, and cryoprobe en bloc with a longer freezing time (4–8 s), whereas CRYO-GRATHP employs a shorter freezing time (2–4 s) and retrieves the frozen specimen directly through the 2.0-mm working channel while maintaining the bronchoscope in a wedged position, thereby allowing immediate bronchus visualization and suction if needed. A comparison of the technical characteristics of RP-EBUS-TBLC and CRYO-GRATHP is summarized in Table 5. Because each technique has distinct technical advantages and limitations, they should be considered complementary, and the choice of technique should be based on the clinical scenario, lesion characteristics, and procedural objectives.

Furthermore, the CRYO-GRATHP concept is not limited to thin bronchoscopes and may be adaptable to bronchoscopes with larger working channels when larger tissue samples are required for specific clinical indications. Prospective studies are warranted to evaluate the feasibility, safety, and diagnostic performance of this expanded application.

This study has some limitations. First, it was a single-center pilot feasibility study conducted during the early implementation phase of this method and included a relatively small sample size. Therefore, prospective multicenter studies are needed to confirm the true clinical utility of this approach. Second, pure ground-glass nodules (GGNs) were not included in the present cohort, which may have introduced selection bias. The diagnostic utility of cryobiopsy with a limited freezing time for pure GGNs remains uncertain. At present, conventional cryobiopsy using the pull en bloc technique may be preferable for the diagnosis of pure GGNs (22). Finally, the use of a 1.1-mm cryoprobe with a small GS may increase procedural costs, which should be considered when adopting this method.

Conclusions

In this pilot feasibility study, the CRYO-GRATHP method appeared to be a feasible and safe cryobiopsy technique for PPLs, especially in upper-lobe lesions.

Acknowledgments

We express our sincere gratitude to the cyto-screeners (Fujita K, Muramoto S, Oishi K) 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 STROBE reporting checklist. Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2026-0855/rc

Data Sharing Statement: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2026-0855/dss

Peer Review File: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2026-0855/prf

Funding: This work was supported by a Grant-in-Aid for Clinical Research from the National Hospital Organization (Young Principal Investigator Development Research Grant).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2026-0855/coif). Y.T. received speaker fees from AMCO Inc. Ken Sato received speaker fees from Olympus Marketing, Inc., Kaneka Medix Co., and AMCO Inc. 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 Institutional Review Board of the NHO Okayama Medical Center (Approval No. RINKEN 2026-018; approval date: May 7^th, 2026). The requirement for written informed consent was waived because of the retrospective nature of 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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