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Vascular and Interventional Radiology |
1-cm) Pulmonary Lesions1
1 From the Departments of Diagnostic Radiology (M.J.W., S.G., K.A., F.A.M, M.E.H.), Pathology (S.K.), and Biostatistics (L.D.B.), University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Blvd, Box 325, Houston, TX 77030-4009. From the 2001 RSNA scientific assembly. Received September 4, 2001; revision requested October 26; final revision received April 5, 2002; accepted April 29. Address correspondence to M.J.W. (e-mail: mwallace@mdanderson.org).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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1.0-cm in diameter) pulmonary lesions. MATERIALS AND METHODS: Sixty-one patients (34 men and 27 women) 21–89 years old (mean age, 61.3 years) with lung nodules 1.0 cm or smaller underwent CT-guided transthoracic FNAB. Fifty-seven of the 61 patients had an underlying primary malignancy. Maximum nodule diameters were 0.5–0.7 cm in 10 patients and 0.8–1.0 cm in 51 patients. Cytopathologic evaluation of FNAB samples was immediate in all patients. Sensitivity and accuracy were calculated, and each case was reviewed for complications, including pneumothorax and thoracostomy tube insertion. Four patients were not included in our statistical analysis because of a lack of follow-up information.
RESULTS: FNAB samples were adequate for diagnosis in 47 (77%) of 61 patients. Diagnoses were malignancy (n = 29) or suspected malignancy (n = 3) in 52% (n = 32) and benign or atypical findings in 25% (n = 15). Findings were nondiagnostic in 23% (n = 14). Of the 29 patients without evidence of malignancy, 25 had follow-up findings available. Follow-up included chest CT in 16 patients and surgical resection in nine. Four patients were not included in statistical analysis because of a lack of follow-up information. Overall sensitivity was 82% (32 of 39); specificity, 100% (18 of 18); and diagnostic accuracy, 88% (50 of 57) on the basis of 57 patients being evaluable. Results for 47 0.8–1.0-cm lesions were considerably better (sensitivity, 88%; accuracy, 92%) than those for 10 0.5–0.7-cm lesions (sensitivity, 50%; accuracy, 70%). Sensitivity (75% vs 87%) and accuracy (87% vs 89%) also improved when comparing subpleural (1.0 cm from pleural surface, n = 30) with deeper (>1 cm from pleural surface, n = 27) pulmonary lesions, but the improvement did not indicate statistical significance. Core biopsy did not reveal malignancy in any of the nine patients in whom preliminary cytologic results were inconclusive and did not improve diagnostic yield. Thirty-eight (62%) patients had pneumothorax, with 19 (31%) requiring thoracostomy tube placement.
CONCLUSION: CT-guided FNAB of pulmonary lesions 1.0 cm or smaller can yield high diagnostic accuracy rates approaching those of larger lesions; FNAB of 0.8–1.0-cm lesions that are not subpleural offers the best opportunity for success.
© RSNA, 2002
Index terms: Computed tomography (CT), guidance, 60.12111, 60.12119 • Lung, biopsy, 60.1261 • Lung neoplasms, diagnosis, 60.1261, 60.30
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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As imaging techniques and technology advance our ability to detect smaller lesions, our definition of small pulmonary nodules continues to change. This results in increased demand for sampling lesions 1.0 cm or smaller. These lesions are usually difficult to detect with fluoroscopy and typically require computed tomography (CT) to guide any biopsy attempt. On rare occasions, pleural-based lesions can be identified and biopsy performed with ultrasonographic guidance. Investigators in several studies (6,8,10) have reported a decline in the accuracy of percutaneous biopsy to less than 75% for lesions 1.0 cm or smaller. Newer techniques with respiratory gating (7) and CT fluoroscopy (11,12) have been used to improve success rates.
Pneumothorax is the most frequently encountered complication during CT-guided lung biopsy, with an incidence of 22%–45% (8,10,12). Higher pneumothorax rates up to 64% for lesions 1.0 cm or smaller have been reported (13).
The purpose of the current study was to report our experience with regard to the accuracy of percutaneous CT-guided FNAB for pulmonary lesions 1.0 cm or smaller.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Patients included 27 women and 34 men, with a mean age of 61.3 years (age range, 21–89 years). Fifty-seven of the 61 patients were known to have a primary malignancy, with three of the 57 having two concurrent malignancies. Subgroups based on lesion size (0.5–0.7 vs 0.8–1.0 cm), depth, and lobar location and on biopsy approach (tangential vs direct) were evaluated to determine potential differences in biopsy success rates (diagnostic result) and complications (pneumothorax). Nodules were 0.5–0.7 cm in 10 patients and 0.8–1.0 cm in 51 patients. Nodules were in the upper or middle lobes in 33 patients and in the lower lobes in 28. Lesions were also subdivided according to depth into either subpleural (n = 32) or deep (n = 29) sites. A subpleural nodule was defined as a lesion 1.0 cm or less from the pleural surface (not including pulmonary fissures). No patient had lesions 1.0 cm or less from a pulmonary fissure. Within this subgroup, the biopsy approach for FNAB was classified as either tangential or direct. Complications including pneumothorax, thoracostomy tube placement, and perilesional hemorrhage were evaluated, and the length of time thoracostomy tubes remained in place was recorded.
Procedure
A commercially available CT scanner (CTi Smart View; GE Medical Systems, Milwaukee, Wis) was used for biopsy. Patients underwent CT without contrast material enhancement in either the prone or supine position. In most situations, patient positioning was based on the shortest distance from the lesion to the visceral surface. Individual variables causing deviation from this practice included overlying skeletal structures and adjacent large pulmonary vessels in addition to potential fissures to be crossed. These deviations were most commonly used when subpleural lesions were encountered. Images were obtained through the region of interest by using a section thickness of 3–5 mm and were viewed by using lung window settings. One of six attending radiologists (M.J.W., S.G., K.A., F.A.M., or M.E.H.) or a fellow or resident with direct supervision performed all biopsies. No routine breathing instructions were given during preliminary imaging or FNAB.
The chosen entry site was prepared and draped in a sterile fashion, and 1% lidocaine hydrochloride (Xylocaine; AstraZeneca, Wilmington, Del), 10 mg/mL, was administered for local anesthesia. A coaxial biopsy technique was used in 47 patients by using an 18-gauge outer Chiba guide needle that was 5, 10, or 15 cm long and a 20–22-gauge inner Chiba aspiration needle that was 10, 15, or 20 cm long (Cook, Bloomington, Ind). Noncoaxial FNAB was performed in the remaining 14 patients by using 20–22-gauge Chiba needles (Cook, Bloomington, Ind). The depth from the skin to the lesion periphery was measured by using the CT images to choose the appropriate needle system length. After needle insertion, CT was used to confirm the adequacy of the needle tip position. Samples were then obtained by using either an aspiration or capillary (nonaspiration) technique and were submitted to an on-site cytotechnologist for sample preparation. This was followed by immediate evaluation by a cytopathologist. Twenty-gauge core samples obtained with a biopsy needle (Quick Core; Cook, Bloomington, Ind) were obtained from nine patients in whom preliminary cytologic results were inconclusive and core sampling was deemed feasible and safe.
Upright posteroanterior expiratory chest radiographs were obtained immediately after biopsy in all patients and evaluated by one of five faculty members (M.J.W., S.G., K.A., F.A.M., or M.E.H.). In the absence of pneumothorax, a 3-hour follow-up radiograph was obtained. If pneumothorax was apparent on the initial chest radiograph obtained after biopsy, a 1-hour follow-up radiograph was obtained. Thoracostomy tubes were inserted if the pneumothorax was moderate to large (
25%) on the basis of the distance from the lung apex to the cupola or on the basis of continued size increase on follow-up radiographs. Thoracostomy tubes were also inserted if patients experienced substantial pain, shortness of breath, or decrease in oxygen saturation in the presence of a small pneumothorax. All patients with thoracostomy tubes were treated as outpatients and returned the following working day for thoracostomy tube challenge (radiography before and 2 hours after thoracostomy tube clamping) and tube removal. Pneumothorax and thoracostomy tube insertion rates were recorded.
Statistical Analysis
Cytologic results were evaluated and divided into diagnostic categories that included malignant, suspicious for malignancy, benign, atypical, and nondiagnostic. A designation of malignancy or suspicious for malignancy was considered a positive result. A positive FNAB result was considered a true-positive result if there was surgical confirmation or if histologic findings in the sampled lesion were compatible with the patient’s known primary malignancy in the presence of unequivocal cytomorphologic findings. Positive FNAB results were considered false-positive results if there was no evidence of malignancy at surgical resection (in the absence of preoperative chemotherapy) or if there was nodule regression at follow-up CT in the absence of therapy. Negative results were considered true-negative results if there was no lesion growth or regression at subsequent CT or if no tumor was identified at surgical specimen examination. A benign diagnosis at culture or identification of organisms also was considered a true-negative finding. Nodule growth or surgical confirmation of malignancy was considered a false-negative finding. Diagnostic accuracy was calculated by comparing the cytologic diagnosis with findings of postsurgical pathologic examination or follow-up imaging 2–18 months after biopsy. Patients without follow-up (n = 4) were not included in statistical analysis for sensitivity and accuracy; thus, 57 of 61 patients were included. The sensitivity, specificity, and accuracy of FNAB, in addition to pneumothorax and thoracostomy tube placement rates, were calculated. Sensitivity and diagnostic accuracy were compared for the two levels of each factor (lesion size, location, and lobe and biopsy approach) by using the 
2 test and were reported as P values (Tables 1–4). In a similar way, pneumothorax and thoracostomy tube placement rates were compared for the two levels of each factor (Tables 5–8). In addition, univariate and multivariate logistic regression analyses were performed by using lesion size, location, and lobe as independent variables; the dependent variable was coded as 0 or 1 for false-negative or true-positive lesions, respectively.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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In the 29 patients without evidence of malignancy (benign, atypical, or nondiagnostic findings), follow-up findings were available in 25. Nine patients underwent surgical resection, and 16 underwent subsequent chest radiography or CT. Nondiagnostic samples were obtained from six of the nine lesions resected. Of the 16 lesions monitored, three had enlarged and three had decreased in size at follow-up imaging, with one lesion demonstrating calcification (not previously identified) consistent with a granuloma. In the remaining nine patients, there was no change in lesion size and a mean follow-up of 13.7 months (range, 3–24 months). Two of these nine patients had fewer than 12 months of follow-up at our institution secondary to further treatment and imaging by their local physician. Lesions in these two patients remained stable in size, despite progression (n = 2) or regression (n = 1) of disease elsewhere in the body. The remaining seven patients had a mean CT follow-up time of 16.5 months.
Malignancy was finally diagnosed in 39 patients, with 32 true-positive and seven false-negative findings and an overall sensitivity rate of 82% (32 of 39) (Table 1). A benign lesion was finally diagnosed in 18 patients. This represents 18 true-negative and no false-positive results, generating a specificity rate of 100% (Table 1). The overall accuracy was 88% (50 of 57), with a positive predictive value of 100% and a negative predictive value of 72%.
Results for 0.8–1.0-cm lesions (n = 47; 51 originally minus four without follow-up) were considerably better (sensitivity, 88%; accuracy, 92%) than those for 0.5–0.7-cm lesions (n = 10) (sensitivity, 50%; accuracy, 70%). The improvement in sensitivity was statistically significant (P = .026), but the improvement in accuracy was not (P = .06). Nondiagnostic samples were obtained in three of the 10 patients in the 0.5–0.7-cm group and in 11 of the 47 patients in the 0.8–1.0-cm group. Sensitivity (75% vs 87%, respectively) and accuracy (87% vs 89%, respectively) also improved but were not statistically significant (P = .339 and P = .799, respectively) when comparing subpleural lesions (1.0 cm from the pleural surface) with deeper pulmonary nodules (Table 2). Nondiagnostic samples were obtained in 11 of 30 subpleural lesions and in three deep lesions. There was no significant difference in sensitivity (P = .966) or accuracy (P = .799) when comparing lesions in the upper or middle lobes (n = 30; 82% or 87%, respectively) with lesions in the lower lobes (n = 27; 82% or 89%, respectively) (Table 3). For subpleural lesions (30 of 33 patients available for follow-up), the tangential approach (n = 19) demonstrated significantly better results than did the direct approach (n = 11), with sensitivity rates of 100% and 50%, respectively (P = .021), and accuracy rates of 100% and 64%, respectively (P = .005) (Table 4). Nondiagnostic samples were obtained in seven of 19 tangential and four of 11 direct approaches taken for subpleural lesions.
Logistic regression was used to investigate the effect of various predictive factors on sensitivity. Univariate and multivariate logistic regression analysis was performed, with lesion size and location and lobar location used as independent variables and with a dependent variable coded as 0 for false-negative lesions and as 1 for true-positive lesions. The adjusted effect of lesion size was to increase the odds of a true-positive finding by 7.36 as one went from a small to a large lesion. The Hosmer-Lemeshow goodness-of-fit test was performed for the logistic model and resulted in a P value of .679, indicating adequate fit. A high P value indicates an adequate fit of the data with the model. The classification table for this analysis resulted in 29% for predicting a false-negative finding and in 97% for predicting a true-positive finding (Table 9).
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Thoracostomy tubes remained in place for a mean of 1.2 days (range, 1–5 days) and were all managed on an outpatient basis. Hemorrhage around the biopsy site was present in 34 patients without major clinical sequelae. Hemorrhage was considered substantial in three patients who underwent FNAB at which the lesion was obscured and thus precluded additional sampling. None of these three patients demonstrated malignancy at FNAB, but interval enlargement was noted at subsequent imaging in one patient.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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1.0 cm). In an attempt to increase diagnostic accuracy, Tomiyama et al (7) used respiratory gating during biopsy in 23 patients with lesions 0.7–1.5 cm. They reported a diagnostic accuracy rate of 96% but failed to subdivide their patient population to adequately evaluate the utility of FNAB for subcentimeter lesions. Their results compare favorably with those obtained by Westcott et al (14), in which no respiratory gating was used. It is uncertain whether their results reflect a disproportionate number of lesions larger than 1.0 cm or relate to the effect of respiratory gating. The experience of the physician performing the procedure must also be included when success rates are compared. The overall sensitivity of 82% and diagnostic accuracy of 88% in our series compare favorably with those in similar series discussed in the literature. When we subdivide the current patient population by size, our sensitivity (88%) and accuracy (92%) for 0.8–1.0-cm lesions approach those for larger lesions in other published series (1–5). Diagnostic accuracy decreased substantially for lesions smaller than 0.8 cm. This decline may have been due in part to the insufficient number of lesions sampled in this subgroup (n = 10).
Subpleural pulmonary nodules are often more challenging than deeper lesions. The ribs or scapula can be an obstacle when the nodule lies behind them (13). Tanaka et al (15) compared the "oblique path" (tangential approach) with the right-angle path (direct approach) to define the optimal needle route for sampling subpleural lesions. In their series of 61 subpleural lesions, there was a significant difference between success rates in the oblique path (81.2%) when compared with those in the right-angle path (43.3%) (15). Similarly, we demonstrated a significant difference in accuracy between tangential (100%) and direct (64%) approaches. Differences in the success rates of these two approaches may relate to the length of the parenchymal tract and the amount of subcutaneous tissue overlying the access route. In the direct route, the parenchymal tract is, by definition, 1.0 cm or less in length. Aside from the obvious obstacle of overlying ribs, the short distance does not allow for correction or redirection of the needle without pulling it back across the pleural surface. This problem is compounded when subcutaneous tissues are sparse and inadequate for needle stabilization during initial positioning. If a pneumothorax occurs at any point during the procedure, the lung may retract from the needle and hinder further sampling.
The tangential route offers more access options than can the direct route by allowing either a posterior or anterior approach to avoid overlying bone structures. The longer transparenchymal and subcutaneous tracks provide greater needle stability and allow easier needle correction without additional violation of the pleura. When comparing subpleural and deep pulmonary lesions, there were higher rates of sensitivity (75% vs 87%) and accuracy (87% vs 89%) for deep lesions, but the improvement was not considered statistically significant. This difference may be artificial because of the use of the direct approach in 11 of 30 subpleural lesions.
Respiratory variability, in spite of consistent breathing instructions, potentially raises the degree of difficulty encountered with small lesions in the lower lobes (bases) when compared with those in the middle and upper lobes. We were unable to demonstrate any significant difference in sensitivity or accuracy after dividing the lesions into lower and upper middle lobe categories.
Despite our rates of diagnostic accuracy, we encountered high rates of pneumothorax (62%) and thoracostomy tube insertion (31%). In the literature, factors discussed in relation to increased risk of pneumothorax include smaller lesion size (16–18), increasing lesion depth (16,18,19), number of passes, pleural surfaces crossed, and underlying lung disease (16,18,20,21). Kazerooni et al (18) described a higher incidence of pneumothorax in smaller and deeper lesions on which biopsy was performed in 121 procedures, with a mean lesion diameter of 1.7 cm. Their pneumothorax rate is at the high end of the wide range (16.0%–44.6%) reported in the literature (2,4,6–9,17). Cox et al (17) also reported a higher pneumothorax rate with smaller lesion size. While their overall rate was 40.4% of 356 biopsies, their pneumothorax rate for lesions 1.0 cm or smaller (n = 23) was 65%. Their analysis also failed to demonstrate any correlation between lesion depth and pneumothorax rate when aerated lung was traversed. Our pneumothorax rates are comparable with those in similar patients in this latter series. Like Cox et al (17), we did not demonstrate any difference in pneumothorax rates between peripheral (1-cm) and deep (>1-cm) pulmonary nodules, contrary to the findings of authors of other reports in the literature (16,18,19).
Owing to the retrospective nature of our report, there was a lack of standardization among operators and of meticulous documentation of variables (number of passes, number of times the pleural surface was crossed, and presence of underlying lung disease). While these variables may have been useful in addressing issues of complications, we believe that they would not have changed the focus of this study to determine the diagnostic accuracy of FNAB for pulmonary nodules smaller than 1.0 cm. An additional limitation was the available follow-up in nine lesions sampled. Two patients with fewer than 12 months of observation were no longer followed up at our institution. In both cases, nodule size remained stable, with evidence of progression of disease elsewhere. The remaining seven patients had a mean 16.5-month follow-up, with no lesion growth. The 24 months of follow-up accepted as the time to confirm lesion stability as an indication of benignity may not have been necessary in our unique patient population. Unlike those in most reported series, 93% of the patients in the current series had an underlying primary malignancy, and all of the nine patients requiring imaging follow-up had preexisting neoplasms.
The high frequency of patients with preexisting malignancies is unique to our cancer center. Our patient population differed from the general population, with over 90% (57 of 61) of patients having a known primary malignancy. Such patients undergo CT at a higher rate than do those in the general population. As a result, small pulmonary lesions are detected with a higher frequency. Our goal in a majority of patients is to identify metastases rather than diagnose primary neoplasms. Thus, our pretest probability was higher for a diagnosis of malignancy. Confirmation is often required before including patients in experimental protocols.
CT-guided FNAB of pulmonary lesions 1.0 cm or smaller can yield high diagnostic accuracy rates approaching those of larger lesions; FNAB of lesions 0.8–1.0 cm that are not subpleural offers the highest opportunity for success.
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, M.J.W.; study concepts and design, M.J.W.; literature research, M.J.W.; clinical studies, M.J.W., S.G., K.A., F.A.M., M.E.H.; data acquisition and analysis/interpretation, M.J.W., S.K.; statistical analysis, M.J.W., L.D.B.; manuscript definition of intellectual content and editing, M.J.W., S.K., S.G.; manuscript preparation, revision/review, and final version approval, M.J.W.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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