American Journal of Respiratory and Critical Care Medicine Vol 166. pp. 377-381, (2002)
© 2002 American Thoracic Society
Transbronchial Needle Aspiration in Diagnosing and Staging Lung Cancer
How Many Aspirates Are Needed?
Robert Chin, Jr.,
Trent W. McCain,
Michael A. Lucia,
James O. Cappellari,
Norman E. Adair,
James F. Lovato,
Donnie P. Dunagan,
Michael A. Brooks,
Hollins P. Clark and
Edward F. Haponik
Section of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Department of Pathology, Department of Radiology, and Department of Public Health Sciences, Wake Forest University School of Medicine, Winston-Salem, North Carolina; Section of Pulmonary and Critical Care Medicine, Department of Internal Medicine, University of Reno, Reno, Nevada; and Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Johns Hopkins University, Baltimore, Maryland
Correspondence and requests for reprints should be addressed to Robert Chin, Jr., M.D., Wake Forest University Baptist Medical Center, Section of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Medical Center Boulevard, Winston-Salem, NC 27157-1054. E-mail: Rchin{at}wfubmc.edu
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ABSTRACT
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Transbronchial needle aspiration has emerged as a key technique for sampling mediastinal adenopathy but variable yields are reported. To determine the number of aspirates needed to optimize yield, we prospectively studied transbronchial needle aspiration and the sequential effect of each successive specimen on diagnostic yield in 79 patients with known or suspected lung carcinoma and mediastinal adenopathy. A total of 451 aspirates were performed in 79 patients (mean, 5.7 aspirates per patient; range, 2–13) with 45 cases (57%) positive for malignancy. A cytologically positive transbronchial needle aspiration occurred with the first aspirate in 42% of patients in whom this procedure established mediastinal nodal involvement. All positive results were achieved with seven or fewer aspirates. Similar yields were obtained for small cell and non-small cell lung cancer after seven aspirates. Rapid on-site specimen cytologic evaluation was used in 55 of 79 cases (70%), with a positive diagnosis obtained in 39 of 55 cases (71%) with on-site evaluation compared with six of 24 cases (25%) performed without on-site evaluation. The data suggest there is a plateau in yield after seven transbronchial needle aspirates, which may be sufficient to obtain an optimal yield in assessing patients with lung cancer and mediastinal adenopathy.
Key Words: biopsy, needle • bronchoscopy • cytodiagnosis • lung neoplasms • neoplasm staging
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INTRODUCTION
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Transbronchial needle aspiration (TBNA) is a well-validated (1–8), but underutilized bronchoscopic method (9, 10) of mediastinal staging in patients with lung cancer. TBNA has been shown to increase the yield of lung cancer diagnosis when combined with bronchoscopic washing, brushing, and forceps biopsy (2, 3, 5, 7, 11). Several investigations have assessed factors influencing TBNA yield, including the use of endoscopic ultrasound guidance (12), rapid on-site cytopathologic examination (ROSE) (13, 14), the use of larger gauge needles providing histologic specimens (15–17), site of the lymph node sampled (2, 12, 13), and real-time computed tomography (CT)–fluoroscopic guidance (18). These studies have involved either a variable number of aspirates performed per procedure or not specified the number of specimens obtained at each nodal site. Bronchoscopists with extensive experience have provided recommendations regarding the number of separate needle insertions that should be obtained (3), but there have been few prospective investigations of this procedural detail, and the optimum number of aspirates has not been established.
We prospectively examined the number of aspirates performed during flexible bronchoscopy in patients with known or suspected lung cancer and enlarged mediastinal lymph nodes to determine the average number of aspirates needed to be successful in obtaining a positive cytologic diagnosis and the cumulative effect of successive samples on yield in each patient. In addition, we appraised the relationships of TBNA yield to lymph node site according to American Thoracic Society (ATS) location and to the neoplastic cell type.
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METHODS
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All patients undergoing bronchoscopy with TBNA between April 1, 1997, and December 31, 1998, at Wake Forest University School of Medicine (Winston-Salem, NC) were eligible to be included in data collection. The Institutional Review Board of Wake Forest University granted permission for data collection and reporting. Data from 88 patients were prospectively gathered for analysis. Most procedures were performed by a pulmonary fellow who was directly supervised and assisted by the faculty member in attendance at the bronchoscopy. Patients were premedicated with anticholinergic, benzodiazepine, and narcotic agents based on bronchoscopist preference. After topical lidocaine anesthesia, bronchoscopy was performed via the transnasal route, using Olympus (Melville, NY) series bronchoscopes. Supplemental oxygen was routinely administered and intravenous sedation with midazolam was given if needed.
TBNA were performed with a 13-mm, 22-gauge Millrose needle (Millrose, Mentor, OH), using a flexible bronchoscope. Consistent technique for TBNA had been developed through a comprehensive education program (9) applying methods reported previously (19). TBNA was performed before endobronchial inspection or other sampling to limit contamination of the working channel. Lymph node targets were selected on the basis of chest CT scans. Neither real-time CT nor endobronchial ultrasound was used. In general, N2–N3 sites were sampled first, followed by sampling of N1 sites. When bulky multistation lymphadenopathy was present (with equivalent staging implications), the bronchoscopist selected the most accessible TBNA target. Typically, mediastinal lymph nodes approached by TBNA exceeded 1 cm in their short axis diameter, but nodal dimensions were not recorded prospectively. However, subsequently, the chest CT scans were retrospectively reviewed independently by two chest radiologists (M. A. B. and H. P. C.) to size the lymph nodes aspirated. Short axis size data were available for 85% of the patients included in the analysis. These data were then correlated with the cytologic results.
Aspirates were numbered sequentially in order of sampling and processed by a dry-smear technique (20). Factors determining whether ROSE was used were not recorded nor did we set a priori parameters for its use, but the two major factors were the timing of bronchoscopy and whether the bronchoscopist specifically requested this resource. Adequacy was assessed on a slide-by-slide basis at the time of ROSE by a cytotechnologist, pathology resident or fellow, or by an attending cytopathologist. Each slide was labeled with the sequence number and the nodal location according to ATS station (21). All slides were then independently reviewed in a blinded fashion by a pathologist (J. O. C.) to identify which slide number and location were positive or negative for cancer.
Only patients who had a least one positive aspirate for cancer were included in our determination of the mean number of aspirates needed to obtain a diagnosis of malignancy. Means ± standard deviations are reported. The Wilcoxon rank-sum test was used when comparing the number of aspirates needed to establish a diagnosis and when comparing the number of aspirates performed. The Pearson  2 test was used to compare the number of positive diagnostic cases when ROSE was present versus when ROSE was absent. S-PLUS 2000 for Windows (MathSoft, Cambridge, MA) was used for all analyses and plots. Statistical significance of observed differences was accepted for p < 0.05.
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RESULTS
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Data were collected for 88 patients. Fifty-six patients were male. Ages ranged from 28 to 81 years, with a mean age of 62 years. Nine patients, four of whom had positive aspirates for cancer, were excluded from the analysis because the reported number of aspirates did not match the number of pathology slides submitted. For the remaining 79 patients, a total of 451 aspirates was performed, with an average of 5.7 aspirates per patient (range, 2–13); 27% of the 451 aspirates had cytologic evidence of cancer. Altogether, a total of 45 patients had cancer diagnosed by TBNA. The distribution of their diagnoses by lung cancer type is shown in Table 1
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The locations of diagnostic and nondiagnostic aspirates are shown Table 2
. The most common sites for TBNA were subcarinal lymph nodes (ATS 7, 47.6% of total TBNAs) and right paratracheal lymph nodes (ATS 4R, 21% of total TBNAs). Sixty-four percent and 38% of all patients who had a subcarinal or right paratracheal TBNA performed, respectively, had a diagnosis of malignancy established. The relationship of the ATS nodal station location to the number of aspirates needed to obtain the first positive specimen is outlined in Table 3
. Figure 1
shows the percent positive aspirates for lung cancer per total number of aspirates done at each of the ATS lymph node sites. For the two most common target sites (ATS 4R and 7), the proportion of positives was similar.
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Figure 1. Proportion of positive aspirates performed at each ATS lymph node site in all included patients (n = 79). n = 449 aspirates (one aspirate performed at an unknown ATS site was excluded, and one attempted aspirate at ATS 2R did not provide any material and was excluded) (y-values X's 100).
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The cumulative effects of the number of aspirates on yield are summarized in Figures 2 and 3
. The initial specimen was diagnostic in 42% of patients with a positive TBNA and rose incrementally with successive aspirates. No diagnosis of cancer was obtained after the seventh TBNA. The incremental yield for patients with small cell lung cancer is compared with that for patients with non-small cell lung cancer in Figure 3. Patients with small cell lung cancer and patients with non-small cell tumors required 2.2 ± 2.0 and 2.9 ± 1.9 aspirates, respectively, to establish the diagnosis (p = 0.13). Among patients with small cell lung cancer, the initial aspirate was diagnostic in 59%. Yields were similar in both groups after the seventh TBNA.
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Figure 2. Percentage of positive aspirates for malignancy in a single nodal station by aspirate number out of the total number of aspirates done in those nodal sites with diagnosis of cancer established by TBNA. n = 58 nodal sites (y-values X's 100).
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Figure 3. Percentage of positive aspirates for malignancy in a single nodal station by aspirate number out of the total number of aspirates done in those nodal sites with a diagnosis of small cell lung cancer (solid line, n = 17) versus non-small cell lung cancer (dotted line, n = 28). After aspirate number 7, the lines are superimposed (y-values X's 100).
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The relationship of nodal size to the percent positive TBNA specimens in the patients in whom nodal diameter (short axis) was measured is shown in Table 4
. A higher proportion of positive aspirates was obtained from larger size nodes. A diagnosis of malignancy could be established by two aspirates in 92% of the cases where the short axis was greater than or equal to 2 cm (see Table 5)
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ROSE was used in 70% of cases. When ROSE was used, 6.2 ± 2.5 (range, 2–13) aspirates per patient were performed compared with 4.5 ± 1.7 (range, 2–7) aspirates per patient when ROSE was not available (p = 0.005). A diagnosis of cancer was obtained in 71% of the cases when ROSE was present, whereas only 25% were positive without ROSE (p < 0.001). When the TBNA was diagnostic for malignancy, the mean number of aspirates until the first positive TBNA was 2.5 ± 2.0 with ROSE versus 3.7 ± 1.6 without ROSE.
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DISCUSSION
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TBNA is a minimally invasive outpatient technique for diagnosing and staging patients with mediastinal cancer, yet this procedure remains underutilized (22, 23). Accordingly, improved understanding of procedural details that might enhance TBNA performance has important and pragmatic implications for chest clinicians. Needle placement is not visually exact, and although attempts are made to have the needle perpendicular to the bronchial wall in proper location, shortening the path to the target node and to avoid bronchial epithelial cell aspiration, positioning on each pass can be difficult. Much of the literature regarding TBNA describes varying numbers of aspirations performed per patient. Most reports do not provide details regarding the number of aspirates in relationship to yield and have predominantly retrospective, rather than prospective, designs. Patients in Davenport's investigation underwent two to four TBNAs (13), whereas in the study by Diette and coworkers the mean number of TBNAs was 5.2 for patients when ROSE was present (14). Shure recommended that at least three TBNAs be performed for each target lymph node site (3), consistent with the Wang and coworker approach in the original report of TBNA during flexible bronchoscopy (19). However, no prospective investigation to date has specifically evaluated the number of TBNAs that should be attempted to optimize the yield for diagnosis of malignancy.
In this series of 79 patients, all diagnoses of cancer were obtained within the first seven TBNA attempts (Figure 2). Similarly, Shannon and colleagues found that a diagnosis of malignancy was obtained by the eighth sample in their group of 40 patients who underwent both ultrasound-guided TBNA and blind TBNA (12). Our study demonstrates the new findings of a high plateau in TBNA yield by the seventh aspirate at a lymph node site. Importantly, 77% of our diagnostic aspirates for malignancy were obtained in the first four overall attempts, and 93% of the diagnostic aspirates were obtained in the first four attempts at a single nodal location. We did observe further increment in yield (7%) going to the seventh specimen. Perhaps the lower yield and enthusiasm reported by many pulmonologists may be due to performing only a small number of aspirates per procedure, whereas we often will perform six to eight aspirates.
The overall yield for malignancy (57%) in our study was slightly higher than those reported in several other series. Shannon and colleagues reported a 48% yield in patients undergoing ultrasound-guided TBNA and a 45% yield without ultrasound (12), which is similar to the 46% yield seen in the study by Diette and coworkers (14). Our yield likely reflects patient selection (all had radiologically demonstrated mediastinal adenopathy prompting evaluation by TBNA), and a vigorous approach to and long-term experience with TBNA, as it has become central in institutional algorithms for lung cancer diagnosis and staging. That most positive TBNA specimens are achieved with a relatively low number of needle passes is important to bronchoscopy time management. Generally, TBNA is one component of a procedure that may require multiple complementary sampling procedures. A plateau as identified in this study in the yield from TBNA may help optimize the time spent in this part of the process. Unfortunately, the negative predictive value of TBNA cannot be determined by our analysis. Consequently, we cannot recommend a number of adequate negative aspirates with lymphoid material that would confidently exclude nodal metastasis to a given nodal site.
The current experience also reaffirms that performing TBNA without the real-time guidance of direct imaging can be successful and without the added costs. The mean number of TBNAs required to establish a diagnosis of cancer was two with ultrasound guidance in Shannon's study and three without ultrasound guidance (12), whereas the mean number of TBNAs performed to make a malignant diagnosis was 2.7 in our study. The node size in its short axis diameter, however, did influence diagnostic yield as noted by Harrow and colleagues, with larger nodes having a higher percentage of positive aspirates for malignancy (24). It is also noteworthy that in most instances, supervised pulmonary fellows were the primary bronchoscopists who obtained positive aspirates, successfully applying basic principles of TBNA performance to achieve satisfactory yields.
When comparing the success rate for TBNA by ATS lymph node station, our rates of 64% for subcarinal and 38% for right paratracheal lymph nodes are similar to those in other studies (24, 25). Schenk and coworkers reported overall rates of 54% for positive TBNA of subcarinal lymph nodes and 57% for paratracheal lymph nodes, but only 39% for parabronchial nodes (2). We also compared the number of positive aspirates with the total number of aspirates for each lymph node station, with results of 24 and 28% for subcarinal and paratracheal lymph nodes, respectively. The finding that most (65%) of our positive aspirates were obtained from either the right paratracheal or subcarinal nodes is consistent with previous reports and reinforces the clinical impression that bronchoscopists should attain particular proficiency in approaching these common sites of mediastinal metastasis (24). We did not evaluate differences in the number of samples needed to establish a diagnosis in patients who had right lung primary tumors, carinal widening, signs of extrinsic airway compression, or submucosal involvement by tumor, characteristics that are associated with higher TBNA yield (9).
Previous experience at our institution has found TBNA to be especially valuable in diagnosing small cell lung cancer and, not surprisingly, small cell lung cancer was the most frequently obtained histologic type of lung cancer in our series (26). The mean number of aspirates performed to make a diagnosis of small cell lung cancer was lower than that needed to make a diagnosis of non-small cell lung cancer. Interestingly, the discrepancy between small cell lung cancer and non-small cell lung cancer appears to be largely due to the much higher yield (59%) for small cell lung cancer on the first aspirate. The difference in yield disappeared by the fifth aspirate (Figure 3). Thus, although small cell lung cancer may be especially amenable to diagnosis by TBNA, similar yield with non-small cell lung cancer may be achieved if enough aspirates are performed.
As in previous experiences, the presence of ROSE was associated with a higher yield for obtaining a malignant diagnosis by TBNA in our series of patients (71 versus 25% if ROSE was absent). This yield is similar to that seen by Diette and coworkers (81%) (14) and Davenport (56%) (13) when they evaluated the influence of ROSE on obtaining a positive TBNA. Because the initial needle passes are often diagnostic, the presence of ROSE often allows a more abbreviated procedure, with a positive TBNA obviating the need for further diagnostic sampling. Our investigation was not designed to appraise specific effects of ROSE, and selection biases may have influenced these observations
In conclusion, TBNA is an effective method for diagnosis and staging of lung cancer. Our data indicate that a high yield occurs with the "first stick," an increment in yield occurs with successive aspirates, and a plateau in the yield from TBNA occurs after seven aspirates. We recommend that at least four TBNAs in a single node station be attempted to obtain adequate material, but seven passes will maximize yield in the staging of mediastinal disease in patients with lung cancer and mediastinal adenopathy. This approach to TBNA is modified further as the bronchoscopists actively appraise the patient's tolerance of the procedure and balances TBNA plans with other goals of the bronchoscopy.
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FOOTNOTES
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This abstract was presented at the 1999 ATS meeting in San Diego, California, on April 24–29, 1999.
Received in original form June 29, 2001;
accepted in final form April 8, 2002
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Copyright © 2002 American Thoracic Society
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ABSTRACT
INTRODUCTION