CT-Guided Fine-Needle Aspiration and Core Needle Biopsies of Pulmonary Lesions: A Single-Center Experience With 750 Biopsies in Japan

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1 Cardiopulmonary Imaging Original Research Takeshita et al. CT-Guided Biopsy of Pulmonary Lesions Cardiopulmonary Imaging Original Research Jumpei Takeshita 1 Katsuhiro Masago Ryoji Kato Akito Hata Reiko Kaji Shiro Fujita Nobuyuki Katakami Takeshita J, Masago K, Kato R, et al. Keywords: core needle biopsy, CT-guided lung biopsy, fine-needle aspiration, pneumothorax, pulmonary lesion DOI: /AJR Received May 2, 2014; accepted without revision June 15, Presented at the 15th World Conference on Lung Cancer, Sydney, Australia, October All authors: Division of Integrated Oncology, Institute of Biomedical Research and Innovation, 2-2, Minatojima- Minamimachi, Chuo-Ku, Kobe, Hyogo , Japan. Address correspondence to J. Takeshita (jumpeinr2tfm3@fbri.org). This article is available for credit. Supplemental Data Available online at AJR 2015; 204: X/15/ American Roentgen Ray Society CT-Guided Fine-Needle Aspiration and Core Needle Biopsies of Pulmonary Lesions: A Single-Center Experience With 750 Biopsies in Japan OBJECTIVE. CT-guided lung biopsy is a well-established diagnostic method for pulmonary lesions. The aim of our study was to evaluate the diagnostic outcomes and safety profile of conventional CT guided lung biopsies. MATERIALS AND METHODS. We retrospectively analyzed the results of CT-guided lung biopsies for 750 patients to determine the diagnostic accuracy, complication rates, and independent risk factors for diagnostic failure and severe pneumothorax. RESULTS. Diagnostic accuracy was 92.9%. Independent risk factors for diagnostic failure were malignant lesions (odds ratio [OR], 4.20; 95% CI, ; p = 0.001), lesions in the lower lobe (OR, 2.01; 95% CI, ; p = 0.011), lesions 2.0 cm or smaller (OR, 2.87; 95% CI, ; p < 0.001), and the presence of pneumothorax during the procedure (OR, 2.18; 95% CI, ; p = 0.004). Pneumothorax requiring drainage occurred in 7% of patients. Independent risk factors for pneumothorax requiring drainage were age of 73 years or older (OR, 2.19; 95% CI, ; p = 0.009), the presence of emphysema (OR, 4.29; 95% CI, ; p < 0.001), benign lesions (OR, 2.33; 95% CI, ; p = 0.012), supine positioning of the patient (OR, 2.61; 95% CI, ; p = 0.001), and length from the pleura to the lesion of 1.5 cm or greater (OR, 3.08; 95% CI, ; p < 0.001). CONCLUSION. CT-guided lung biopsy has a high diagnostic accuracy. Complication rates were acceptable and comparable to those of previous studies. T he increasingly widespread use of imaging in clinical practice, particularly CT, has led to a steep increase in incidental findings of asymptomatic solitary pulmonary nodules. In these situations, histologic analysis is needed to confirm the diagnosis, and examination by bronchofiberscopy is preferred. However, the diagnostic accuracy of bronchofiberscopy has been reported as 60%; therefore, many cases require a more reliable diagnostic method [1]. CT-guided lung biopsy is a well-established method for determining the diagnosis of pulmonary lesions [2 4], with a diagnostic accuracy of 64 97% [5 8]; however, pneumothorax is a common complication, occurring in 8 69% of patients [9 11]. A number of previous studies have analyzed factors thought to influence the diagnostic accuracy and complication rate of CT-guided lung biopsy [9 25]. In this retrospective analysis, we evaluated factors related to diagnostic accuracy and complications in a large series of patients who underwent conventional CT guided lung biopsy of a pulmonary lesion. We present the diagnostic outcomes and safety profile of CT-guided lung biopsy and independent risk factors for diagnostic failure and severe pneumothorax. Materials and Methods Patients We retrospectively analyzed the results of CTguided lung biopsies performed between March 2004 and July 2013 at the Institute of Biomedical Research and Innovation. All examinations were performed on the basis of clinical indications alone. We included patients referred to our department for the evaluation of suspicious lung lesions after nondiagnostic bronchoscopy, transbronchial biopsy, or lavage or for the evaluation of lesions for which bronchoscopic biopsy was considered not feasible. Before lung biopsy, all lesions were scanned using routine CT performed at a thickness of 2.5 mm (BrightSpeed, GE Healthcare). The maximum diameters of the lesions were measured on lung window settings. Normal platelet counts and coagulation parameters (e.g., prothrombin time or activated prothrombin time) AJR:204, January

2 Takeshita et al. were confirmed to ensure that patients had taken no anticoagulants within 3 days before the procedure. All biopsies were performed by experienced physicians. This study was approved by our institutional review board (the Research Ethics Committee of the Institute of Biomedical Research and Innovation) and was conducted in accordance with the amended Declaration of Helsinki. Informed consent was obtained from all patients before all procedures. Procedures All procedures were performed percutaneously under conventional CT guidance using the coaxial method [21]. Patients were placed in the prone or supine position, depending on the lesion site, to provide the shortest route for lung biopsy. The patient was instructed to stop breathing after normal inspiration at functional residual capacity before the procedure. CT images were obtained from the lung apices to the diaphragm to detect the pulmonary lesion at end-inspiration. The center of the lesion was positioned at the CT landmark using a radiopaque skin grid on the patient s skin. CT images were obtained again, and the puncture point was determined after measuring the distance from the skin surface to the pleura, the needle path length, and the smallest angle between the vertical line and the needle. At the needle puncture site, 10 ml of 1% lidocaine hydrochloride (Xylocaine, Injection Polyamp 1%, AstraZeneca) was administered subcutaneously as local anesthesia. After skin incision, all biopsies were performed with a coaxial needle system consisting of a 19-gauge coaxial introducer needle (SuperCore Semi-Automatic Biopsy Instrument MCXS2015LY, Argon Medical Devices), a 22-gauge needle for fineneedle aspiration (Sonoguide PTC Needle Type B, Hakko Medical), and a 20-gauge automated cutting biopsy needle with 15- or 25-mm notches for core needle biopsy (Bard Magnum, Medicon) (Fig. 1). The initial puncture was performed without penetrating the pleura (Fig. 2). CT images were obtained to check the biopsy needle position, and biopsies were performed to avoid ribs, bullae, vessels, and fissures. If the lesion was on the extended course of the needle track, the biopsy procedure was continued; otherwise, the course or puncture site was changed. After the lesion was penetrated, the needle tip was checked, and the biopsy was repeated in the same session (Fig. 2). Specimens were immediately immersed in 10% formalin solution and were sent to the pathologist for examination. After the procedure, chest CT was routinely performed to detect pneumothorax or intrapulmonary hemorrhage. Patients with asymptomatic pneumothorax or intrapulmonary hemorrhage were treated conservatively by monitoring vital signs, and followup chest radiographs were obtained 2 and 5 hours after the procedure and again the next morning to confirm stability. We inserted a temporary drainage or indwelling chest tube in patients who had pneumothorax with signs of respiratory distress or shortness of breath. All patients were admitted to the hospital and discharged the day after an uneventful course. Pulmonary emphysema was diagnosed if centrilobular or panlobular emphysema, bullae, or blebs were detected on CT. Statistical Analysis To determine the diagnostic accuracy, we classified biopsy diagnoses as malignant, benign, or nondiagnostic. Results were considered nondiagnostic if the procedure was terminated before specimen acquisition because of complications during the procedure. Diagnoses of malignant and benign disease were considered positive and negative results, respectively. A final diagnosis of benign disease was classified as a true-negative result if it was confirmed in the surgical specimen, the lesion regressed without anticancer therapy, or the lesion was stable in size for at least 12 months. Follow-up CT for patients with benign disease was scheduled 3, 6, and 12 months after the biopsy. A final diagnosis of malignant disease was classified as a truepositive result. These malignant diagnoses were confirmed by the surgical specimen, similarities between the histology of the biopsy specimen and the patient s known malignancy of other organs, or postprocedural malignant processes. Atypical adenomatous hyperplasia was included in the final diagnosis of malignant disease. A positive biopsy result was considered to be false-positive if surgical resection yielded a benign diagnosis, the lesion subsequently disappeared or decreased in size before surgical resection, or the lesion remained stable on follow-up CT for at least 12 months for cases in which the patient did not agree to surgical resection. A negative biopsy result was considered to be false-negative if surgical resection yielded a malignant diagnosis; the lesion increased in size; or other proven metastases were diagnosed on CT, MRI, or bone scintigraphy. True-positive and true-negative cases were considered diagnosed cases. The overall diagnostic accuracy was calculated using the following formula: diagnostic accuracy (%) = number of cases accurately diagnosed (truepositive + true-negative) / total number of cases (excluding nondiagnostic cases). We calculated the overall sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) for the diagnosis of malignancy. The factors related to the patients, lesions, and procedures were evaluated by univariate analyses using the two-sided Student t test for numeric values and chi-square test for categoric values. The factors that were significant in the univariate analyses were used as variables in multivariate logistic regression to identify independent risk factors for severe pneumothorax and diagnostic failure (i.e., nondiagnostic, false-positive, and false-negative results). Odds ratios (ORs) with 95% CIs were calculated. Differences were considered significant at p < Statistical analyses were performed using statistics software (JMP, version 9.0.0, SAS Institute). Results Patient Characteristics We retrospectively analyzed 750 consecutive patients who underwent convention- Fig. 1 Biopsy needles. A, Photograph shows 22-gauge needle used for fine-needle aspiration (Sonoguide PTC Needle Type B, Hakko Medical). B, Photograph shows 20-gauge automated cutting biopsy gun and needle used for core needle biopsy (Bard Magnum, Medicon). C, Photograph shows 19-gauge coaxial introducer needle (SuperCore Semi- Automatic Biopsy Instrument MCXS2015LY, Argon Medical Devices). 30 AJR:204, January 2015

3 CT-Guided Biopsy of Pulmonary Lesions TABLE 1: Patient Characteristics Characteristic Value Age (y) Median 71 Range Sex, no. (%) of patients Male 450 (60) Female 300 (40) Lesion size (cm), 2.4 ± 1.5 mean ± SD Length from pleura to 1.6 ± 1.1 lesion (cm), mean ± SD Lobe, no. (%) of patients Upper 349 (46.5) Middle 111 (14.8) Lower 290 (38.7) al CT guided lung biopsies between March 2004 and July Patient characteristics are summarized in Table 1. Diagnostic Accuracy Nondiagnostic results were obtained in 10 of the 750 patients (1.3%) because the procedure was terminated before specimen acquisition due to progressive pneumothorax during the procedure. Of the remaining 740 patients (98.6%), 542 had positive results for malignancy, and 198 had negative results. The histologic diagnoses are shown in Table S1, which can be seen in the AJR electronic supplement to this article available at A final diagnosis of benign disease was made in 151 patients (20.1%) based on confirmations of the surgical specimen (n = 14), lesion regression without anticancer therapy (n = 43), or stable lesion size for at least 12 months (n = 94). A final diagnosis of malignant disease was made in 599 patients (79.9%). These malignant diagnoses were confirmed by the surgical specimen (n = 237), similarities between the histology of the biopsy specimen and a patient s known malignancy of the other organs (n = 36), or postprocedural malignant processes (n = 326). The diagnostic accuracy was 92.9% (688/740 patients). For the diagnosis of malignant disease the overall sensitivity was 91.3% (541/592), specificity was 99.3% (147/148), PPV was 99.8% (541/542), and NPV was 74.2% (147/198). The diagnostic success group (n = 688) consisted of 541 true-positive results and 147 true-negative results; the diagnostic failure group (n = 62) consisted of 51 false-negative results, 10 TABLE 2: Results of Univariate Analysis to Identify Risk Factors for Diagnostic Failure Factors Diagnostic Success a (n = 688) Diagnostic Failure b (n = 62) p Age (y) Mean ± SD 69.0 ± ± 2.61 Sex, no. of patients Female Male Smoking status, no. of patients Nonsmoker Smoker Emphysema, no. of patients Yes 64 8 No Final diagnosis, no. of patients Benign Malignant Lesion size (cm) Mean ± SD 2.50 ± ± 0.37 Lesion size cutoff, no. of patients < cm > 2.0 cm Location of lesion, no. of patients Upper lobe Middle lobe or lingula of left lung Lower lobe Patient positioning for procedure, no. of patients Supine Prone Length from pleura to lesion (cm) Mean ± SD 1.73 ± ± 0.30 Length from pleura to lesion cutoff, no. of patients < 1.5 cm cm Pneumothorax during procedure, no. of patients < Absent Present a Diagnostic success consists of true-positive and true-negative results. b Diagnostic failure consists of nondiagnostic, false-positive, and false-negative results. nondiagnostic results, and one false-positive result. In the one patient with a false-positive result, the biopsy diagnosis was adenocarcinoma, but the postoperative diagnosis was pulmonary inflammatory pseudotumor. Of the 51 patients with false-negative biopsy results, non small cell lung cancer was finally diagnosed in 40 cases, small cell lung cancer in one case, malignant lymphoma in three cases, and pulmonary metastases from other primary tumors in seven cases. The results of the univariate analysis to identify potential risk factors for diagnostic failure are shown in Table 2. Smoking (p = AJR:204, January

4 Takeshita et al ), malignant lesions (p = 0.005), lesions in the lower lobe (p = 0.009), and the presence of pneumothorax (p < 0.001) were significantly associated with diagnostic failure. Lesion size also had a significant effect when the analysis was performed using numeric values (p = 0.001) or using categoric values (p < 0.001). The results of the multivariate logistic regression analysis identified the following independent risk factors: malignant lesions (OR, 4.20; 95% CI, ; p = 0.001), lesions in the lower lobe (OR, 2.01; 95% CI, ; p = 0.011), lesions 2.0 cm or smaller (OR, 2.87; 95% CI, ; p < 0.001), and the presence of pneumothorax during the procedure (OR, 2.18; 95% CI, ; p = 0.004) (Table 3). Complications Pneumothorax was the most common complication, occurring in 276 patients (36.8%). Pneumothorax requiring temporal drainage or chest tube insertion occurred in 56 patients (7%), and tension pneumothorax occurred in two patients (0.2%). There were 27 patients (3.6%) with pulmonary hemorrhage; 63 patients (8.4%) with hemoptysis; two patients (0.2%) with air embolism; five patients (0.6%) with hypertension requiring antihypertensive treatment; one patient (0.1%) with posterior reversible encephalopathy syndrome; and eight patients (1.0%) with other complications, including pain, shock, subcutaneous emphysema, subcutaneous hematoma, epilepsy, and bradycardia or tachycardia. Of the 13 patients with severe complications, 12 patients recovered without TABLE 3: Results of Multivariate Analysis to Identify Risk Factors for Diagnostic Failure and to Identify Risk Factors for Pneumothorax Requiring Drainage Variables Reference Value p Odds Ratio 95% CI Potential risk factors for diagnostic failure Smoker Nonsmoker Final diagnosis, malignant lesion Benign Lesion size 2.0 cm > 2.0 cm < Lesion located in lower lobe Upper or middle lobe Pneumothorax present during procedure Absence of pneumothorax Potential risk factors for pneumothorax requiring drainage Age 73 y < 73 y Sex, male Female Emphysema present Absence < Final diagnosis, benign Malignant Patient positioning during procedure, Prone position supine Length from pleura to lesion of 1.5 cm < 1.5 cm < sequelae; however, one patient recovered but developed paraplegia due to spinal cord infarction. No patients died. The results of the univariate and multivariate logistic regression analyses to identify independent risk factors for pneumothorax requiring drainage are shown in Tables 3 and 4. Significant independent risk factors were age of 73 years or older (OR, 2.19; 95% CI, ; p = 0.009), the presence of emphysema (OR, 4.29; 95% CI, ; p < 0.001), benign lesions (OR, 2.33; 95% CI, ; p = 0.012), supine positioning of the patient for the procedure (OR, 2.61; 95% CI, ; p = 0.001), and length from the pleura to the lesion of 1.5 cm or greater (OR, 3.08; 95% CI, ; p < 0.001). Discussion In this retrospective analysis of CT-guided lung biopsies of 750 patients, we evaluated diagnostic accuracy, complication rates, and independent risk factors for diagnostic fail- A B C Fig year-old woman with adenocarcinoma in right lower lobe diagnosed at conventional CT guided biopsy. A, Puncture point was determined after measuring distance from skin surface to pleura (distance between a and b), needle path length (distance between b and c), and smallest angle between needle and thin vertical line (α) on CT image. Long thick line = puncture direction, short thick line = horizontal line. B, CT image shows needle after initial puncture, which was performed without penetrating pleura. During procedure, CT images were obtained to check position of biopsy needle. C, CT image shows needle is penetrating pulmonary lesion. After pulmonary lesion was penetrated, needle tip was checked, and aspiration for cytology or specimen for histologic analysis was obtained. 32 AJR:204, January 2015

5 ure and severe pneumothorax. Our findings were comparable to those of previous studies evaluating the diagnostic outcomes of conventional CT guided lung biopsy [5, 26 28] (Table S2, which can be seen in the AJR electronic supplement to this article available at We found that lesion size ( 2.0 cm) is one independent risk factor for diagnostic failure. Tsukada et al. [6] reported diagnostic accuracies of 67% for lesions measuring 1.0 cm or smaller and 79% for lesions measuring cm, and Hiraki et al. [5] reported diagnostic accuracies of 92.7% for lesions measuring 1.0 cm or smaller and 96.1% for lesions measuring cm. In our study, diagnostic accuracies were 90.3% for lesions measuring 1.0 cm or smaller (56/62 lesions) and 87.5% for lesions measuring cm (288/329 lesions), which were considerably higher than those of Tsukada et al., who evaluated the results of conventional CT guided needle biopsy, but are lower than those of Hiraki et al., who evaluated the results of CT fluoroscopy guided biopsy. CT fluoroscopy guided biopsy can provide real-time visualization of the needle tip or lesion site; however, a major drawback of this technique is the high radiation exposure to the operator s hand [29, 30]. We assume that our use of MDCT, which shortens procedure time and minimizes the effect of patient movement due to breathing, contributed to the relatively high diagnostic accuracy for conventional CT guided needle biopsy. The diagnostic failure group consisted mainly of false-negative results; therefore, the risk of diagnostic failure was higher for malignant lesions than for benign lesions. The higher risk of diagnostic failure associated with lesions in the lower lobe may be explained by breathing during the procedure. Increased motion of the lower lobe during respiration can cause displacement of the biopsy needle. This motion can be a problem particularly for women older than 65 years and men older than 75 years who have decreased respiratory muscle strength and difficulty holding their breath for long periods [31]. In the patients who developed pneumothorax, diagnostic failure was due to termination of the biopsy procedure. In previous studies [9 11], pneumothorax occurred in 8 69% of patients undergoing CT-guided lung biopsy, and pneumothorax requiring drainage occurred in 7 15% of patients. In our study, 36.8% of patients developed pneumothorax; however, we included cases of small asymptomatic pneumothorax, CT-Guided Biopsy of Pulmonary Lesions TABLE 4: Results of Univariate Analysis to Identify Risk Factors for Pneumothorax Requiring Drainage Factors Patients Without Pneumothorax Patients With Pneumothorax Requiring Drainage Requiring Drainage (n = 694) (n = 56) p Age (y) Mean ± SD 68.7 ± ± 2.74 Age, no. of patients < 73 y y Sex, no. of patients Female Male Smoking status, no. of patients Smoker Nonsmoker Emphysema, no. of patients < Yes No Final diagnosis, no. of patients Benign Malignant Lesion size (cm) Mean ± SD 2.47 ± ± 0.39 Lesion size, no. of patients cm > 2.0 cm Location of lesion, no. of patients Upper lobe Middle lobe or lingula of left lung Lower lobe Patient positioning during procedure, no. of patients < Supine Prone Length from pleura to lesion (cm) < Mean ± SD 1.66 ± ± 0.31 Length from pleura to lesion, no. of patients < < 1.5 cm cm which may have overestimated the pneumothorax rate. Pneumothorax requiring drainage occurred in 9.6% of patients in our study, which is similar to the results of previous studies [9 11]. Several studies have suggested that emphysema and deep lesion location increase the risk of pneumothorax [9 11]. In our study, risk factors for pneumothorax requiring drainage were age ( 73 years) and benign lesions. Elderly patients have a more difficult time following the breath-holding directions for our procedure than young and middle-aged patients. Thirteen of the 19 benign lesions in patients with pneumothorax requiring drainage yielded nondiagnostic results, indicating biopsy of normal lung tissue. AJR:204, January

6 Takeshita et al. The study limitations include its retrospective design with unknown bias. In addition, multiple testing is associated with an inflated type 1 error rate. The final diagnosis for negative cases could not be established for most patients unless they underwent surgery. Conclusions In this study, we found that conventional CT guided lung biopsy has a high diagnostic yield, but malignant lesions, lesions in the lower lobe, small lesions ( 2.0 cm), and pneumothorax during the procedure are significantly associated with diagnostic failure. Complication rates were acceptable; pneumothorax requiring drainage was associated with patient age ( 73 years), emphysema, benign lesions, supine position of the patient during the procedure, and length from the pleura to the lesion of 1.5 cm or greater. References 1. Baaklini WA, Reinoso MA, Gorin AB, et al. Diagnostic yield of fiberoptic bronchoscopy in evaluating solitary pulmonary nodules. 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