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(Chest. 2005;128:869-875.)
© 2005 American College of Chest Physicians

Impact of Rapid On-Site Cytologic Evaluation During Transbronchial Needle Aspiration*

Daniel Baram, MD; Ruel B. Garcia, MD and Paul S. Richman, MD

* From the Division of Pulmonary/Critical Care, Stony Brook University, Stony Brook, NY.

Correspondence to: Daniel Baram, MD, Assistant Professor of Medicine, Stony Brook University, Division of Pulmonary/Critical Care, T-17, 040 HSC, Stony Brook NY 11794-8172; e-mail: dbaram{at}notes.cc.sunysb.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 References
 
Study objective: To determine the extent to which rapid on-site cytologic evaluation (ROSE) of transbronchial needle aspiration (TBNA) samples can safely and cost-effectively reduce the need for additional biopsy during bronchoscopy.

Setting: University Hospital in Long Island, NY.

Patient and methods: Forty-four bronchoscopies with TBNA, most of which utilized ROSE, were evaluated prospectively. The number and types of biopsies performed during each procedure were compared to a preprocedural algorithm to determine the impact of knowing ROSE results during the procedure. Bronchoscopies performed with and without ROSE were compared, as were bronchoscopies with diagnostic and nondiagnostic ROSE results. A cost analysis was performed comparing the Medicare reimbursement for ROSE to the savings of deferring multiple biopsies.

Results: Thirty-two bronchoscopies were performed with ROSE; 12 were performed without ROSE. Fewer biopsies were performed during bronchoscopies utilizing ROSE. Diagnostic yield, TBNA sensitivity and accuracy, and procedural time were similar between these two groups.

Conclusions: ROSE during TBNA allows for deferring additional biopsy without loss in diagnostic yield, likely lowers procedural risk, and is cost-effective.

Key Words: bronchoscopy • cancer diagnosis • transbronchial needle aspiration


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusions
 References
 
Transbronchial needle aspiration (TBNA) is a valuable technique for sampling mediastinal and pulmonary lesions. The diagnostic yield of TBNA varies widely in reported series, ranging from 20 to 90%.123456 Rapid on-site cytologic evaluation (ROSE) is commonly used during thyroid, breast, and transthoracic needle aspirations, and the use of ROSE improves the diagnostic yield of endoscopic ultrasound-guided fine-needle aspiration.7 Several authors89101112 have suggested that ROSE may improve the yield of TBNA. However, its utility remains unproven, and its potential advantages may not outweigh the cost and inconvenience.13

During bronchoscopy, there are often multiple biopsy targets and multiple sampling modalities available. Several studies141516 have shown that obtaining multiple samples increases the diagnostic yield of bronchoscopy. However, performing multiple biopsies adds to the cost, length, and risk of bronchoscopy.17

ROSE is used frequently in our hospital, though the cytotechnologists are occasionally not available. If ROSE is used and the results are positive, we often defer further biopsy. ROSE is not being utilized to improve yield but rather to minimize the risk and duration of a procedure. Determining whether deferring further biopsy based on ROSE is safe and cost-effective has not been previously studied. Bronchoscopies utilizing TBNA were studied prospectively to assess the impact of ROSE.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusions
 References
 
Patients scheduled to undergo TBNA at Stony Brook University Hospital were approached for study consent. The utilization of ROSE was decided by the pulmonary attending independent of the patient’s decision to participate in this study and was generally determined by scheduling concerns.

Prior to the procedure, the attending physician delineated a biopsy algorithm that listed which biopsies would be performed if ROSE were not available, which biopsies would be performed if ROSE were available and diagnostic, and which biopsies would be performed if ROSE were available and nondiagnostic (Fig 1 ).



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  		Figure 1.. Preprocedure algorithm.

 
TBNA were performed using the Wang nodal mapping system based on preprocedure CT scans.18 Endobronchial ultrasound was available and was utilized for lesions in atypical locations. Histologic needles (model 319; Mill-Rose Laboratories, Inc; Mentor, OH) were preferentially used during most procedures. Cytologic needles (model 222; Mill-Rose Laboratories) were used for some peripheral lesions.

Immediately following the bronchoscopy, data were collected regarding the duration of the procedure, whether ROSE was utilized, the number and results of each pass, and whether the procedure followed the designated algorithm. Also tracked were the utilization of fluoroscopy, the need for a postprocedure radiograph, and the number of pathologic and microbiological samples sent to the laboratory. In our hospital, transbronchial biopsy and TBNA of lesions past the segmental bronchus are performed under fluoroscopy. Chest radiographs are routinely ordered after bronchoscopies requiring fluoroscopy.

A TBNA was classified as diagnostic if it yielded a final pathologic diagnosis. "Suspicious," "atypical," or "negative" results were classified as nondiagnostic. If more than one TBNA was performed, each site was evaluated separately. A diagnostic TBNA specimen was considered to be a true positive (TP) if it yielded a cytologic or histologic diagnosis of malignancy. A false-positive result was defined as a biopsy result that was diagnostic for malignancy but was later proven to be in error. A diagnostic TBNA specimen was considered to yield a true-negative (TN) result if it yielded a pathologic diagnosis of benign disease. A nondiagnostic TBNA specimen was further evaluated in view of later pathologic specimens; a nondiagnostic TBNA specimen was reclassified as a TN result if benign disease was demonstrated at surgical resection, and as false-negative (FN) result if a later pathologic specimen showed a malignancy. A nondiagnostic TBNA specimen that was not definitively diagnosed or was resected after neoadjuvant chemotherapy was classified as unknown.

Each bronchoscopy procedure was then analyzed to determine the impact of ROSE. The accuracy of ROSE was determined by comparing the ROSE result to the final TBNA cytology and histology report. The number of biopsies and cultures deferred by a positive ROSE result was determined from the preprocedural algorithm. Bronchoscopies performed without ROSE were compared to the preprocedural algorithm to evaluate whether the algorithms predicted physician behavior.

Cost analysis was performed. Charges for each biopsy and culture deferred were calculated based on published 2003 Medicare rates including bronchoscopist reimbursement and technical and professional laboratory fees. If ROSE obviated the need for parenchymal biopsy, fluoroscopy and chest radiograph fees were also included. As Medicare reimburses the endoscopy suite based on time, not for the individual biopsy performed or equipment costs, endoscopy suite costs were not included in our analysis. Medicare reimbursement to the hospital for ROSE costs was determined.

A statistical comparison was performed utilizing the {chi}2 test for categoric data and nonpaired t test for continuous data. The data are reported as the mean ± SD unless otherwise noted. This study was approved by the institutional review board, and all patients signed informed consent forms prior to enrollment.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusions
 References
 
Overall TBNA Results
In all, 44 bronchoscopies were performed on 42 patients (Table 1 ). Sixty-eight TBNAs were performed, of which 32 were of mediastinal lesions, 14 were of hilar lesions, and 22 were of parenchymal lesions. Ultrasound guidance was utilized for only one lesion; a lesion abutting the left mainstem lesion was aspirated and found to be a loculated pericardial effusion. No complication occurred during these bronchoscopies.


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  		Table 1.. Bronchoscopy and TBNA Results

 
Based on the final pathology report and the clinical information available, 41 TBNAs had TP results, 0 had false-positive results, 17 had TN results, 1 had an FN result, and 9 results remained unknown. Of the nine TBNA results that remained unknown, six were performed in patients who had not undergone resection secondary to medical inoperability or distant metastases, and three were pathologically negative after patients received neoadjuvant chemotherapy. Accuracy (TP + TN/all) using best-case and worst-case analysis (ie, best-case analysis assumes that all unknowns are TN; worst-case assumes that all unknowns are FN) was 85 to 99%, sensitivity (TP/TP + FN) was 79 to 98%, and the overall diagnostic yield was 72%.

Two patients underwent repeat biopsy at the request of the treating oncology service, despite obtaining tissue that was diagnostic at the time of first biopsy. One patient had a large right lower lobe mass and an enlarged subcarinal node; both lung biopsy specimens revealed mixed small cell and non-small cell carcinoma, and the subcarinal TBNA specimens revealed lymphocytes without cancer. After neoadjuvant chemotherapy, the lung mass and subcarinal node were pathologically tumor-free at resection, and therefore both subcarinal TBNA results were classified as unknown. Another patient underwent TBNA of a 2-cm right upper lobe mass while receiving prolonged mechanical ventilation. Cytology revealed a neuroendocrine neoplasm. As she was medically inoperable, she was referred to an oncologist who requested rebiopsy. Histologic TBNA sampling of the right upper lobe mass confirmed the mass to be a carcinoid tumor.

TBNA With ROSE
ROSE was utilized in 32 bronchoscopies during which 46 TBNAs were performed. ROSE was performed on each TBNA pass, except that ROSE was not performed on the last of three locations during one bronchoscopy. Forty-five ROSE results were available for analysis. In one instance, ROSE was read as being preliminarily positive, but the final pathologic result was nondiagnostic. In three instances, the ROSE was nondiagnostic, but the TBNA was diagnostic at the time of the final pathology report. The overall accuracy was 91%, with a sensitivity of 88% and a specificity of 94% (Table 2 ).


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  		Table 2.. Accuracy of ROSE in Predicting Final TBNA Diagnosis of Malignancy

 
ROSE results were positive in 24 sites in 23 bronchoscopies. In most bronchoscopies (17 of 23), the preprocedure algorithm correctly predicted that no further sampling would be performed. In three bronchoscopies, the algorithm correctly predicted that additional biopsies would be obtained, as the cases were complex with broad differential diagnosis and concern existed for multiple disease processes. In three bronchoscopies, endobronchial biopsies specimens were obtained despite the algorithm predicting that no further biopsy specimens would be taken. The algorithm correctly predicted that in the nine bronchoscopies with nondiagnostic ROSE, five patients underwent multiple other biopsies including transbronchial biopsy, and four underwent no further biopsy.

Comparing bronchoscopies performed with and without ROSE, the accuracy (86 to 98% vs 86 to 100%, respectively) and sensitivity (77 to 96% vs 82 to 100%, respectively) of TBNA was similar. When ROSE was used, fewer samples were sent for microbiology tests (16% vs 62% of cases, respectively; p < 0.001 [{chi}2 test]) and pathology tests (3.6 ± 1.8 vs 5.7 ± 1.9, respectively; p < 0.01), fewer chest radiographs were ordered (9% vs 56%, respectively; p < 0.001 [{chi}2 test], but the procedural length was similar (39 ± 20 vs 39 ± 19 min, respectively; p = 0.9). Note that TBNA usually yielded two pathology specimens, as histology was obtained in most biopsies. The reduction in sampling was accounted for by the bronchoscopies in which ROSE was diagnostic. Procedures conducted with diagnostic ROSE were of shorter duration than nondiagnostic ones (34 ± 21 vs 52 ± 13 min, respectively; p < 0.03). Nondiagnostic ROSE procedures were of longer duration than cases not utilizing ROSE (52 ± 13 vs 39 ± 14 min, respectively; p < 0.05); diagnostic ROSE procedures were not significantly shorter than those not utilizing ROSE (34 ± 21 vs 39 ± 14 min, respectively) [Tables 3, 4 ].


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  		Table 3.. Comparison of Bronchoscopies With and Without ROSE*

 

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  		Table 4.. Bronchoscopies With at Least One TBNA Site With a Diagnostic ROSE vs Bronchoscopies With all TBNA Sites With Nondiagnostic ROSE

 
A subgroup analysis of TBNAs of hilar and mediastinal lesions was performed. The results were similar comparing hilar and mediastinal lesions to all TBNA sites in regard to the impact of ROSE on the sensitivity, accuracy, length of procedure, number of aspirates obtained, and deferral of further biopsy (data not shown).

The use of ROSE in these 32 patients obviated the need for 12 microbiological cultures, 15 BAL cytology samples, 15 brushings, 1 endobronchial biopsy, and 11 transbronchial biopsies. Fluoroscopy and postprocedure chest radiographs were saved in nine of these patients, as two patients whose transbronchial biopsy results were saved had TBNA performed under fluoroscopy. The resulting savings at 2003 Medicare reimbursement rates was $8,466 or $265 per case. The cost of the ROSE is largely salary of the technologist, after the upfront institutional cost for equipment. Approximately 1 h of time for cytotechnologist was required per bronchoscopy when travel time was added to the procedural time. Assuming a median US salary of $53,000 and a 40-h work week, cytotechnologists earn $25 per hour. If a cytopathologist is present, Medicare pays $40 per case in supplemental reimbursement; Medicare pays nothing additional if only cytotechnologists are present, as was the case in our institution.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusions
 References
 
In our study, a diagnostic ROSE result frequently spared the need for additional sampling without a reduction in diagnostic yield. Avoiding transbronchial biopsy likely reduced procedural risk. Reducing the number of samples sent to the laboratory lowered the overall cost of the procedure, and therefore ROSE was cost-effective. Utilizing ROSE did not shorten procedure time as time saved when ROSE was diagnostic was balanced by the additional time spent waiting for nondiagnostic ROSE results (Tables 3, 4).

Bronchoscopies utilizing ROSE resulted in a lower utilization of laboratory and radiographic resources. This reduced utilization was accounted for by the bronchoscopies performed with diagnostic ROSE. Bronchoscopies with nondiagnostic ROSE had similar sampling and fluoroscopy use as bronchoscopies not utilizing ROSE. This suggests that bronchoscopies performed with and without ROSE were of similar complexity, which was important considering that the use of ROSE was neither randomized nor blinded in this study.

TBNA increases the diagnostic yield of bronchoscopy and reduces the need for staging mediastinoscopy, but TBNA remains underutilized.19 Yield varies widely in published studies and depends on lesion characteristics, disease prevalence, and operator experience. Yields are typically highest for mediastinal lesions and lowest for peripheral parenchymal lesions.2 Intermediate results are seen for hilar and central lesions. Ultrasound-guidance,202122 CT fluoroscopy,2324 and ROSE89 have all been studied as means to improve yield. Few randomized data are available to compare among these modalities. In this study, ROSE did not increase TBNA accuracy or yield, as a high accuracy was seen in TBNA without ROSE.

Bronchoscopy without biopsy can cause hypoxemia, arrhythmia, infection, and fever, but major complications and fatality are rare, and are most commonly related to anesthesia. Transbronchial biopsy raises the risk of major complication 10-fold to 22-fold.2526 Pneumothorax rates vary from 1 to 4% and depend on the use of fluoroscopy, the need for mechanical ventilation, and immunocompromised status.2728 Significant hemorrhage occurs in approximately 1% of patients undergoing transbronchial biopsy.272829 TBNA is safe,30 with only case-reportable complications, including pneumomediastinum, pneumothorax, purulent pericarditis, and hemomediastinum. There were no complications seen in this study, but it was not powered to prove the occurrence of reduced complications. However, deferring transbronchial biopsy likely reduces the risk of major complication during bronchoscopy.

Our data suggest that preprocedure planning can predict the cases in which ROSE would be most useful. In centers with limited availability, the bronchoscopist is able to predict the possible impact of ROSE and to prioritize scheduling appropriately. The largest impact is in cases with multiple targets available for biopsy, especially when a positive result would spare the patient a transbronchial biopsy. If the bronchoscopist plans to sample all lesions regardless of ROSE results, the potential impact is smaller. In cases with only a single target, ROSE is unlikely to have a major impact. Though not seen in this study, we have had occasional prior cases in which ROSE was instrumental in making an otherwise unexpected diagnosis, such as suggesting the need for flow cytometry to diagnose lymphoma. A larger study would be needed to quantify this advantage of ROSE, as these cases are uncommon.

Chin et al10 reported on 451 TBNA aspirates in 79 patients, of whom 45 had cancer. In that study, 42% of diagnoses were made on the first pass and 93% were made by the fourth pass. Xie et al31 reported that the diagnosis of cancer was made on the first pass in 58% of TBNAs, the second pass in 12%, the third pass in 10%, the fourth pass in 6%, the fifth pass in 8%, and additional 2% in the sixth, ninth, and 11th passes. In the 68 sites in our study, there was an mean of 2.7 ± 0.9 aspirates per site with a range of one to five samples per site; there were a mean of 2.8 ± 1.0 aspirates per site when ROSE was present and 2.7 ± 0.8 when ROSE was not present. Sixty-four aspirates were obtained from the 24 TBNA sites with diagnostic ROSE, and 53 of these aspirates (83%) had diagnostic cells seen during ROSE. Seventeen aspirates (71%) were positive on the first pass, 5 more (92%) were positive by the second pass, 1 more (96%) was positive by third pass, and 1 required a fourth pass prior to obtaining diagnostic tissue. The first sample was usually obtained by the attending physician, and further needle passes were then taken by the fellow while awaiting the ROSE results from the first pass. If the ROSE result was nondiagnostic, the attending would either take additional aspirates from that site or move on to the next step of the algorithm. As second and third passes were performed prior to the first ROSE result being evaluated, many TBNA sites had multiple positive samples.

Three sites had nondiagnostic ROSE results but were diagnostic for cancer at the time of the final report. One site was positive on final cytologic interpretation, and two sites had negative cytology results but diagnostic histologic biopsy results. The number of aspirates needed to obtain diagnostic tissue in these three patients was not available.

Histologic core biopsy specimens were obtained from 61 of the 68 sites; 16 of 22 parenchymal lesions had histologic sampling. In all, 30 histologic samples were diagnostic for cancer, 3 were diagnostic for sarcoidosis, and 1 revealed a hematoma. Of the 41 TP TBNA results, 26 had positive cytology and positive histology, 6 had positive histology and negative cytology, 5 had positive cytology and negative histology, and 4 had positive cytology without histologic sampling. This confirms prior reports of an additive yield of histologic sampling during TBNA.3233

TBNA has been shown to be useful in the diagnosis of sarcoidosis,343536 as it was in three of the four patients with sarcoidosis in this series. Nine sites were sampled by TBNA; 3 sites had granuloma on histology and 3 had "aggregates of epithelioid histiocytes consistent with granulomatous inflammation." Only one patient required mediastinoscopy for diagnosis.

We have a high level of familiarity with ROSE and have confidence in the results. This is in large part due to a close working relationship with the cytotechnologists. To duplicate our results in another hospital would require the bronchoscopist to develop a similar relationship with their cytologists and cytotechnologists. The major risk of ROSE is prematurely ending a procedure before diagnostic tissue is obtained. Our data suggest that, with proper planning and experience, this risk is low.

ROSE is cost-effective. Most of the cost savings is from reducing the number of samples sent to the pathology laboratory. Additional cost savings were derived from reduced physician reimbursement and from a reduced need for radiographs and fluoroscopy. Poor reimbursement likely contributes to the reduced availability of ROSE.37 In this study, ROSE was used in 73% of the bronchoscopies, which is similar to the rate in a prior study at our institution.6 In our hospital, many practitioners utilize ROSE, and therefore ROSE is often not available unless scheduled several days in advance.


   Conclusions
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
References
 
ROSE is accurate during TBNA and allows the deferral of additional biopsy without compromising yield. This is cost-effective and likely reduces procedural risk. ROSE did not affect diagnostic yield or procedure length. Careful preprocedure planning can predict the possible impact of ROSE, allowing optimized scheduling in institutions with limited ROSE availability. TBNA is highly accurate, and in most cases diagnostic tissue can be obtained with the first two passes. Histologic biopsy adds a larger incremental gain than taking additional cytologic aspirates.


   Acknowledgements
 
We thank the cytotechnologists and endoscopy staff who provided invaluable assistance to us in the care of our patients.


   Footnotes
 
Abbreviations: FN = false negative; ROSE = rapid on-site cytologic evaluation; TBNA = transbronchial needle aspiration; TN = true negative; TP = true positive

Received for publication December 13, 2004. Accepted for publication February 14, 2005.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 References
 

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