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(Chest. 2006;129:725-733.)
© 2006 American College of Chest Physicians

Angled Forceps Used for Transbronchial Biopsy in Which Standard Forceps Are Difficult To Manipulate*

A Comparative Study

Shinji Sasada, MD; Yoshitaka Ogata, MD; Masashi Kobayashi, MD; Tomonori Hirashima, MD; Kunimitsu Kawahara, MD, PhD; Kaoru Matsui, MD and Ichiro Kawase, MD

* From the Departments of Thoracic Malignancy (Drs. Sasada, Kobayashi, Hirashima, and Matsui) and Pathology (Dr. Kawahara), Osaka Prefectural Medical Center for Respiratory and Allergic Diseases, Osaka, Japan; and the Department of Respiratory Medicine, Allergy and Rheumatic Diseases (Drs. Ogata and Kawase), Osaka University Graduate School of Medicine, Osaka, Japan.

Correspondence to: Shinji Sasada, Department of Thoracic Malignancy, Osaka Prefectural Medical Center for Respiratory and Allergic Disease, 3-7-1 Habikino, Habikino-Shi, Osaka 583-8588, Japan; e-mail: s-sasada{at}hbk.pref.osaka.jp

Abstract

Objectives: To evaluate the usefulness of the Sasada transbronchial angled forceps (STAF) in patients with peripheral pulmonary lesions (PPLs), which are difficult to manipulate with standard forceps.

Methods: We have invented the STAF, a forceps with an angled tip. One hundred ten patients with PPLs that were difficult to reach with standard forceps were retrospectively evaluated. The patients first underwent bronchoscopy with a standard forceps and then with the STAF. The specimens obtained with standard forceps and those obtained with STAF were separately fixed and analyzed histologically. We compared the histologic diagnosis of the specimens obtained by STAF with that obtained by the specimens obtained with standard forceps. Statistical significance was calculated with the McNemar {chi}2 statistic.

Results: The diagnostic yield of all lesions from the specimens obtained with STAF (86 of 110 lesions; 78.2%) was significantly higher than that of lesions from the specimens obtained with standard forceps (43 of 110 lesions; 39.1%; p < 0.001). Among malignant lesions, the yield obtained with STAF (60 of 72 lesions; 83.3%) was significantly higher than that obtained with standard forceps (32 of 72 lesions; 44.4%; p < 0.001). Among benign lesions, the yield obtained with STAF (26 of 38 lesions; 68.4%) was also significantly higher than that obtained with standard forceps (11 of 38 lesions; 28.9%; p < 0.001). Among the different lesion areas, the right upper lobe plus the left upper division gave the greatest difference in yield (STAF, 46 of 60 lesions; 76.7%; standard forceps, 22 of 60 lesions; 36.7%; p < 0.001). Among the different size ranges, the diagnostic yields obtained with STAF were significantly higher than that obtained with standard forceps except for the size range of ≤ 10 mm. There were two complications, pneumothorax and bronchial bleeding, both of which were controlled easily.

Conclusions: The STAF was shown to be useful for obtaining specimens that were sufficient for histologic diagnosis from PPLs that were difficult to manipulate with standard forceps.

Key Words: angled forceps • peripheral pulmonary lesions • transbronchial biopsy

Since the 1970s, transbronchial biopsy (TBB) of the lung performed through a flexible bronchoscope has gained wide acceptance and has become the most common method of performing lung tissue biopsy.1234 The numbers of patients with peripheral pulmonary lesions (PPLs) have increased along with the incidence of lung adenocarcinoma.56 Patients in whom a diagnosis cannot be made by flexible fiberoptic bronchoscopy need to undergo CT scan-guided needle biopsy (CTGNB) or video-assisted thoracic surgery (VATS).78 However, CTGNB is associated with critical complications, including air embolism and pleural dissemination.910 On the other hand, in patients with poor performance status or in elderly patients, VATS is not always performed. Therefore, TBB with a flexible bronchoscope is still the recognized first-choice procedure used to diagnose PPLs. Nevertheless, we have experienced diagnostic failure with PPLs, even though PPLs can be visualized by radiographic fluoroscopy. With such lesions, conventional straight forceps are difficult to reach, and we cannot obtain a sufficient amount of material for histologic diagnosis. To solve this problem, we invented the Sasada transbronchial angled forceps (STAF). Our experience with 110 patients is reported in the present study.

Materials and Methods

Patient Eligibility
We enrolled patients with PPLs that had been visualized by radiographic fluoroscopy and were difficult to manipulate by using standard forceps. Difficult-to-manipulate lesions presented in some situations as follows: the forceps could not really reach them, could hardly reach them, or could barely reach them. Such lesions were defined as difficult PPLs, and they mainly included solitary pulmonary lesions and mediastinum-involved tumors. Patients with diffuse pulmonary lesions or invasive shadows were excluded from the study. We judged the eligibility of the patient during bronchoscopy.

Study Design
The study was designed to retrospectively evaluate the usefulness of TBB with STAF in patients with difficult PPLs. Patients with difficult PPLs first underwent bronchoscopy with a standard forceps and then with STAF. The specimens obtained with standard forceps and those obtained with STAF were separately fixed and analyzed histologically. When either forceps absolutely could not reach a lesion that had been visualized by radiographic fluoroscopy, we did not perform a biopsy for safety reasons. Both specimens were diagnosed by two pathologists. We compared the histologic diagnosis obtained from the specimens by STAF with that from the specimens obtained by standard forceps. Cytologic and bacterial examinations were excluded in this study, because technical contamination was possible and could have caused misdiagnosis. Informed consent was obtained from all patients prior to undergoing the procedure.

Equipment
We have invented a new forceps, called STAF (HBF-2010SH; Machida; Tokyo, Japan), that has an angled tip for obtaining adequate amounts of tissue from PPLs for histologic diagnosis. The structure of STAF is basically the same as that of standard forceps. STAF has a 12° angle 10 mm from the tip, so that the tip is perpendicular to the direction of the opening and shutting of the cup (Fig 1 ). STAF is a reusable product that can be fitted to any standard bronchoscope with channels having a diameter of ≥ 2.2 mm (eg, BF 1T-30, 40, or 1T-200, 240; Olympus; Tokyo, Japan). The cost is almost the same as that of standard forceps.


Figure 1
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  		Figure 1.. STAF. Left, A: Open position; the STAF has an angled tip. Right, B: the general shape of the STAF is almost the same as that of a standard forceps except for the angled tip.

 
A New Biopsy Technique
To obtain adequate amounts of tissue for diagnosis, we invented a new biopsy technique called curve-shaped (CS) TBB. The CS-TBB method consists of five steps (Fig 2 ), which are clearly different from those of the conventional TBB method. First, we use standard forceps to identify the bronchus nearest to the lesion. Second, we switch to STAF and open the cup in front of the lesion. We search for a part of the lesion while letting the STAF turn and slide. Next, we make a CS motion by operating the bronchoscope, enabling a more perpendicular approach to the lesion. Finally, we push the forceps forward and perform the biopsy.


Figure 2
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  		Figure 2.. Method of performing CS-TBB. Step 1: search for the bronchus nearest to the lesion by using a standard forceps. Step 2: switch to STAF. Step 3: open the cup in front of the lesion. Step 4: turn and slide the STAF at the same time, and push forward. Step 5: make a CS motion by operating the bronchoscope, and obtain some tissue.

 
Statistical Analysis
The proportion of positive samples using STAF was compared with the proportion of positive samples using standard forceps. The patients who underwent bronchoscopy using STAF were exactly the same as those who underwent bronchoscopy using standard forceps. The statistical significance was calculated with the McNemar {chi}2 statistic. A difference with a p value of < 0.05 was considered to be significant. The statistical analysis software was used for the analysis.

Representative Cases

Case 1
A 25-year-old woman had a 23-mm lesion in the right upper lobe (Fig 3 , top, A). Bronchoscopy was performed to confirm the diagnosis of the lesion. TBB with standard forceps failed to obtain specimens through the right B1a because the forceps could not reach the mass (Fig 3, bottom left, B). However, TBB with STAF succeeded in obtaining a sufficient amount of tissue for the specimens (Fig 3, bottom right, C), and the diagnosis of tuberculosis was histologically confirmed. The culture from the specimen was negative for tuberculosis.


Figure 3
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  		Figure 3.. Case 1. A tuberculoma. Top, A: a chest CT scan reveals a coin lesion in the right upper lobe. Bottom left, B: a bronchoscopic image shows a standard forceps approaching a tumor through the right B1a. Bottom right, C: bronchoscopic image shows the STAF approaching the tumor. It forms a CS (ie, J-shape).

 
Case 2
A 44-year-old man had a 30-mm lesion in the left lower lobe (Fig 4 , left, A). Bronchoscopy was performed, and TBB performed with standard forceps failed to obtain specimens through the left B10e. However, TBB with performed STAF succeeded in obtaining a sufficient amount of tissue from the specimens to confirm a diagnosis of hamartoma (Fig 4, right, B).


Figure 4
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  		Figure 4.. Case 2. A hamartoma. Left, A: a chest CT scan reveals a lesion in the left lower lobe. Right, B: a bronchoscopic image shows the STAF approaching a tumor through the left B10e. It forms a CS (ie, S-shape).

 
Case 3
A 54-year-old man had a mediastinum-involved tumor in the left lung (Fig 5 , left, A). Only STAF was able to reach the lesion (Fig 5, right, B), and a sufficient amount of tissue was obtained for the specimens to confirm a diagnosis of non-small cell lung cancer (NSCLC).


Figure 5
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  		Figure 5.. Case 3: NSCLC. Left, A: a chest CT scan reveals a mediastinum-involved tumor shadow on the left side. Right, B: a bronchoscopic image shows the STAF approaching the tumor through the left B3c.

 
Case 4
A 74-year-old man had a 15-mm nodule in the right upper lobe (Fig 6 , top, A). Specimens were obtained with standard forceps and STAF through the right B3a. The specimens obtained with standard forceps revealed only a normal bronchial wall (Fig 6, bottom left, B); in contrast, the specimens obtained with STAF revealed adenocarcinoma (Fig 6, bottom right, C).


Figure 6
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  		Figure 6.. Case 4: a lung adenocarcinoma. Top, A: a chest CT scan reveals a coin lesion in the right upper lobe. Bottom left, B: the biopsy specimen obtained with standard forceps through the right B3a reveals only normal bronchial wall (hematoxylin-eosin, original x40). Bottom right, C: STAF biopsy specimen reveals adenocarcinoma (hematoxylin-eosin, original x40).

 
Case 5
A 34-year-old man had a 14-mm nodule in the right lower lobe (Fig 7 , top, A). Specimens were obtained with standard forceps and STAF through the right B6b. The specimens obtained with standard forceps were insufficient for pathological diagnosis, revealing only normal bronchial wall (Fig 7, bottom left, B). However, the specimens obtained with STAF revealed necrotizing epithelioid granuloma (Fig 7, bottom right, C), which suggested pulmonary tuberculosis. TBB with STAF succeeded in obtaining a specimen large enough for histologic examination.


Figure 7
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  		Figure 7.. Case 5: a tuberculoma. Top, A: a chest CT scan reveals a coin lesion in the right lower lobe. Bottom left, B: the biopsy specimen obtained with standard forceps through the right B6b reveals a normal bronchial wall (hematoxylin-eosin, original x40). Bottom right, C: STAF biopsy specimen reveals necrotizing epithelioid granuloma (hematoxylin-eosin, original x40).

 
Results

One hundred ten consecutive patients with difficult PPLs who underwent bronchoscopy between August 2001 and July 2004 at the Osaka Prefectural Medical Center for Respiratory and Allergic Diseases were enrolled into the study. Of the 110 patients, 64 were men and 46 were women. The median age of the group was 67 (range, 25 to 86). The median size of the longest diameter of a lesion in the group was 20 mm (range, 6 to 60 mm). The longest diameters of all lesions revealed by chest CT scan were recorded.

Table 1 shows the diagnostic yields, and Table 2 shows the pathologic diagnoses in the 110 patients. The diagnostic yield of all lesions from the specimens obtained with STAF (86 of 110 lesions; 78.2%) was significantly higher than the that of lesions from the specimens obtained with standard forceps (43 of 110 lesions; 39.1%; p < 0.001). In malignant lesions, the yield obtained with STAF (60 of 72 lesions; 83.3%) was significantly higher than that obtained with standard forceps (32 of 72 lesions, 44.4%; p < 0.001). The pathologic diagnoses and the yields obtained with STAF included the following: adenocarcinoma, 86% (43 of 50 lesions); squamous cell carcinoma, 90% (9 of 10 lesions); small cell carcinoma, 100% (2 of 2 lesions); undifferentiated carcinoma, 80% (4 of 5 lesions); metastasis, 50% (2 of 4 lesions); and carcinoid tumor, 0% (0 of 1 lesion). In benign lesions, the yield obtained with STAF (26 of 38 lesions; 68.4%) was significantly higher than that obtained with standard forceps (11 of 38 lesions; 28.9%; p < 0.001). The diagnoses and yields obtained with STAF included the following: nonspecific inflammation, 57.1% (8 of 14 lesions); mycobacteriosis, 77.8% (7 of 9 lesions); hamartoma, 50% (4 of 8 lesions); organizing pneumonia, 100% (4 of 4 lesions); cryptococcosis, 100% (2 of 2 lesions); and lung abscess, 100% (1 of 1 lesion). Three patients underwent a second bronchoscopy when the first procedure failed to yield a specific diagnosis. Two of the specimens obtained in the second bronchoscopy resulted in a diagnosis.


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  		Table 1.. Diagnostic Yields From PPLs Biopsied With STAF and Standard Forceps

 

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  		Table 2.. Clinical Diagnosis of PPLsin 110 Patients Who Underwent Bronchoscopy With STAF

 
Table 3 shows the diagnostic yield for each lesion area. Among the different lesion areas, the right upper lobe plus the left upper division gave the greatest difference in yield (STAF, 46 of 60 lesions [76.7%]; standard forceps, 22 of 60 lesions [36.7%]; p < 0.001). Table 4 shows the diagnostic yield for each size range. Among the different size ranges, the diagnostic yields obtained with STAF were significantly higher than that obtained with standard forceps except for those with a size of ≤ 10 mm.


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  		Table 3.. Effect of Lesion Area on Diagnostic Yield of PPLs Obtained With STAF and Standard Forceps*

 

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  		Table 4.. Effect of Lesion Size on Diagnostic Yield of PPLs Obtained With STAF and Standard Forceps*

 
Of 24 patients in whom a diagnosis could not be established, 11 were operated on. Diagnosis was made by transbronchial needle aspiration in two further patients. In 1 patient diagnosis was made by transcutaneous needle biopsy, and in 10 further patients it was made by serial observations. There were two complications (pneumothorax and bronchial bleeding), both of which were controlled easily.

Discussion

Flexible fiberoptic bronchoscopy is routinely used for the diagnosis of PPLs. Flexible fiberoptic bronchoscopy in conjunction with TBB, bronchial brushing, or bronchial washing cytology has given physicians an additional procedure to aid in diagnosis. In patients with peripheral lung cancer, transbronchial needle aspiration has been developed.1112 However, benign pulmonary lesions are not usually diagnosed by cytologic examination, and thus lung resections are ultimately needed. Active tissue biopsy is required for the improvement of the diagnostic efficiency of PPLs, including benign lesions.

We had a patient in whom a critical air embolism developed during CTGNB, and we were thus confronted with the necessity of developing a new diagnostic procedure. We considered that the following three conditions are required in a new method. The first is that it must be safe for the patient and the staff. The second is that it should be inexpensive and easily introduced into many institutions. The final condition is that it is able to obtain specimens that can be used to histologically diagnose even benign lesions. Therefore, to satisfy these requirements, we should approach a lesion more perpendicularly by a standard bronchoscope to improve tissue collection.

We invented STAF as a new device for diagnosis to be used with a standard bronchoscope (Fig 1). STAF has a 12° angle 10 mm from the tip, and this structure was the most controllable in our experience. If the tip angle is ≤ 10°, the forceps cannot grasp the edge of the lesion. On the other hand, if the tip angle is > 15°, the forceps flexes too much during the approach. We also invented a new biopsy technique to control STAF more effectively (Fig 2). The CS-TBB method enables a perpendicular approach. The slight angle of the tip, the flexural direction perpendicular to the opening, and the shutting of the cup are necessary conditions to make a CS motion successfully. The CS-TBB method has two typical approach patterns, called the J-shape (Figs 3, bottom right, C, and 5, right, B) and the S-shape (Fig 4, right, B) in bronchoscopic images. These approach patterns are thought to be very effective for obtaining specimens from PPLs, because we can apply force directly to the lesion.

In this study, the diagnostic yield from the malignant lesions obtained with STAF was 83.3%. This result is thought to be almost the same as or greater than that obtained in patients with PPLs, counting what a standard forceps can easily reach.1314 Previous studies1516 have reported that the diagnostic yields in peripheral pulmonary benign lesions were 50 to 65.8%. In the present study, the diagnostic yield obtained with STAF was 84.6%. This result is significantly higher than that obtained in previous studies. In the diagnostic analysis of lesions in each area of the lung (Table 3), the STAF was often used to obtain a specimen from a lesion in the right upper lobe and the left upper division. This reflects the fact that the upper lobe is difficult to reach anatomically. STAF was found to be effective for obtaining specimens form these lesions. In the diagnostic analysis of each size range (Table 4), efficacy was poor for lesions < 10 mm, which cannot be clearly visualized by radiographic fluoroscopy. STAF is thought to be effective for use with all lesions that can be visualized by radiographic fluoroscopy. Using the STAF, the lesion can be visualized by radiographic fluoroscopy; it seems that using STAF has a benefit even if it is any difficult area.

There are three principal reasons why the diagnostic yield from TBB specimens obtained with STAF was superior to that from specimens obtained with standard forceps. First, STAF was able to approach the lesion after being advanced into the bronchus of choice by flexure of the tip. Second, STAF was able to grasp the lesion well by a more perpendicular application of the conventional biopsy method. Third, STAF was able to obtain enough tissue for histologic examination. STAF also has some original applications. In patients with a mediastinum-involved tumor that a standard forceps cannot really reach, STAF easily reaches the lesion and can obtain sufficient material for histological examination. STAF is also useful for benign tumors or metastatic lesions, which communicate poorly with the bronchi. In these lesions, we expect that STAF can break a surrounding bronchial wall and grasp a lesion. We think that these types of lesions are most effectively approached using the STAF. To obtain further effects, several variations of a product are essential, such as shaft flexibility, flexure angle of the tip, and shape of the cup.

The complications from TBB performed with STAF, such as bronchial bleeding and pneumothorax, were mostly mild. These were similar to those from conventional TBB. We think that this is because our new method is basically conventional bronchoscopy performed with a new device and a new technique. But a carelessly performed operation could cause critical complications; for example, the rupture of great vessels due to approaching adjacent mediastinal lesions. In addition, if the channel of the bronchoscope is ≤ 2 mm in diameter, a careless operation may cause fiber damage. The use of bronchoscopes with a channel diameter of > 2.2 mm is preferable.

CTGNB and VATS have been performed worldwide.78 But CTGNB is considered to be more invasive than TBB because of the possibility of critical complications, including air embolism and pleural dissemination,910 while VATS is not always performed in patients with poor performance status or in the elderly. Other transbronchial diagnostic procedures include bronchoscopy with an ultrathin bronchoscope coupled with virtual navigation,17 and endobronchial ultrasonography-guided TBB.18 But these procedures involve complicated methods and are not yet widely used. Widely used diagnostic procedures should be safe and easy to use. When we compare our new diagnostic procedure with other diagnostic procedures, we find that its safety characteristics are superior to those of CTGNB and VATS, while its ease of operation is superior to that of the ultrathin bronchoscope with virtual navigation and endobronchial ultrasonography-guided TBB. Furthermore, we do not require a new investment because the cost is almost the same as that of standard forceps. Consequently, from the point of view of safety, ease of operation, and cost-effectiveness, STAF can be used in any patients at any institution. However, physicians must learn and understand this biopsy technique well, and training is necessary.

In some studies,1920 a subgroup of patients with NSCLC have had specific mutations in the epidermal growth factor receptor gene that correlated with clinical responsiveness to the tyrosine kinase inhibitor gefitinib. But the accuracy of histologic diagnosis of peripheral lung cancer with TBB specimens is not always sufficient. We achieved a superior accuracy of histologic diagnosis in peripheral lung cancer (89.5%) between April 2002 and March 2003, and it was thought to be an additive effect of the innovation of STAF. Successful TBB with a low risk of severe complications is also important for predicting the efficacy of target therapies, because such information requires repeated biopsies. The adequate TBB specimens that were obtained with STAF are expected to contribute to the performance of gene analysis in patients with NSCLC in the future.

Conclusions

STAF was shown to be useful for obtaining sufficient specimens for histologic diagnosis from PPLs, which are difficult to manipulate with standard forceps, and the use of STAF resulted in a significant improvement in the diagnostic efficiency of TBB. CS-TBB performed with STAF can provide a high accuracy with safety and ease, so that this new device and technique may become widespread.

Acknowledgements

We thank the Machida Corporation (K. Miyagi) for technical support.

Footnotes

Abbreviations: CS = curve-shaped; CTGNB = CT scan-guided needle biopsy; NSCLC = non-small cell lung cancer; PPL = peripheral pulmonary lesion; STAF = Sasada transbronchial angled forceps; TBB = transbronchial biopsy; VATS = video-assisted thoracic surgery

Received for publication March 31, 2005. Accepted for publication September 23, 2005.

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