CT-Guided Transthoracic Needle Aspiration Biopsy of Small ( 20 mm) Solitary Pulmonary Nodules

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1 Yoshiharu Ohno 1 Hiroto Hatabu 2 Daisuke Takenaka 1 Takanori Higashino 1 Hirokazu Watanabe 1 Chiho Ohbayashi 3 Kazuro Sugimura 1 Received May 16, 2002; accepted after revision October 30, Department of Radiology, Kobe University Graduate School of Medicine, Kusunoki-cho, Chuo-ku, Kobe, Hyogo , Japan. Address correspondence to Y. Ohno. 2 Department of Radiology, Beth Israel Deaconess Medical Center, 330 Brookline Ave., Boston, MA Division of Pathology, Kobe University Hospital, Kusanoki-cho, Chuo-ku, Kobe, Hyogo , Japan. AJR 2003;180: X/03/ American Roentgen Ray Society CT-Guided Transthoracic Needle Aspiration Biopsy of Small ( 20 mm) Solitary Pulmonary Nodules OBJECTIVE. The purpose of our study was to determine the diagnostic accuracy and to analyze the factors influencing the diagnostic accuracy and incidences of pneumothorax and chest tube insertion rates for percutaneous CT-guided needle biopsy of small ( 20 mm) solitary pulmonary nodules. SUBJECTS AND METHODS. One hundred sixty-two patients with 162 small solitary pulmonary nodules underwent CT-guided transthoracic needle aspiration biopsy. The overall diagnostic accuracy, pneumothorax rate, and chest tube insertion rate were calculated. Factors influencing the diagnostic accuracy and pneumothorax rate were statistically evaluated. Influencing factors, diagnostic accuracies, pneumothorax rates, and chest tube insertion rates were statistically compared. RESULTS. Overall diagnostic accuracy, pneumothorax rate, and chest tube insertion rate were 77.2%, 28.4%, and 2.5%, respectively. Diagnostic accuracy was significantly affected by length of needle path and lesion size ( p < 0.05). The pneumothorax rate was significantly affected by the percentage of predicted forced expiratory volume in 1 sec, the number of punctures, and the needle path length ( p < 0.05). The chest tube insertion rate was significantly affected by the number of punctures ( p < 0.05). For diagnostic accuracy, needle path lengths of 40 mm or less and lesion sizes greater than 10 mm were significantly more accurate than other factors ( p < 0.05). For pneumothorax rates, a percentage of predicted forced expiratory volume in 1 sec of greater than 70%, a single puncture, and a needle path length of 40 mm or less were significantly lower than other factors ( p < 0.05). CONCLUSION. CT-guided transthoracic needle aspiration biopsy is a useful diagnostic tool for small solitary pulmonary nodules smaller than 20 mm in diameter. The diagnostic accuracy is significantly improved for large (> 10 mm) lesion size and short ( 40 mm) needle path length. R ecently, academic and public interest in lung cancer screening using low-dose CT has grown drastically. With the increased use of lung cancer screening with helical CT, an increased incidence of small lung cancer, especially small adenocarcinoma, has been reported in some countries [1 4]. According to current reports of CT screening for early lung cancer, the detection of small lung cancers may improve the prognosis of lung cancer patients [5 9]. However, the increased number of small solitary pulmonary nodules detected at CT screening has created a new problem in management. Repeated CT examination with evaluation of volume change of the small solitary pulmonary nodule is one of the solutions for management of solitary pulmonary nodules [10, 11]. However, when an increase in solitary pulmonary nodule size is recognized on follow-up CT examination, a pathologic diagnosis is mandated. Data about diagnostic accuracy and incidences of pneumothorax and chest tube insertion of percutaneous CT-guided needle biopsy in these cases of small solitary pulmonary nodules would provide critical information as to how to manage each case with a growing small solitary pulmonary nodule of 2 cm or less in diameter. Percutaneous CT-guided needle biopsy of the lung is a relatively safe and accurate method of diagnosing benign and malignant lesions of the chest [12 19]. Various reports have analyzed factors thought to influence the diagnostic accuracy and the complication rate of CT-guided transthoracic needle aspiration biopsy [15 20]. The diagnostic accuracy and the frequency of pneumothorax in CT-guided transthoracic needle aspiration biopsy are affected by many fac- AJR:180, June

2 TABLE 1 Characteristics of 97 Male and 65 Female Patients Characteristic No. Lesion size (mm) > 80 7 Distance to pleura (mm) Needle approach Patient supine 86 Patient prone 76 Location Right upper lobe 36 Right middle lobe 18 Right lower lobe 37 Left upper lobe 38 Left lower lobe 33 Needle pleural angle ( ) No. of punctures % of predicted forced expiratory volume in 1 sec > Note. Patients were years old (mean ± SD, 66.6 ± 11.9 years). Ohno et al. tors, including size, depth, and number of needle paths. However, to our knowledge no major reports have evaluated factors influencing the diagnostic accuracy and the pneumothorax rate of small solitary nodules less than 20 mm in diameter. The purpose of our study was to provide basic data about diagnostic accuracy and incidence of pneumothorax and chest tube insertion with respect to percutaneous CT-guided needle biopsy of small solitary pulmonary nodules of 20 mm or less in diameter. Subjects and Methods Patients One hundred sixty-two patients with 162 small solitary pulmonary nodules with diameters of less than 20 mm 97 men and 65 women who were years old (mean ± SD, 67 ± 12 years) underwent CT-guided transthoracic needle aspiration biopsy in our hospital between April 1996 and July Patients characteristics are shown in Table 1. Diameters of all nodules, including adjacent ground-glass opacities, were measured on lung window settings. All patients underwent posteroanterior and lateral chest radiography in the erect position before the biopsy procedures. Follow-up erect posteroanterior and lateral chest radiographs were obtained immediately after biopsy, 2 4 hr later, and 24 hr later for evaluation of pneumothorax. The placement of a chest catheter or tube was considered in the event a patient became symptomatic or a large (> 30%) pneumothorax was found. Patients were generally observed, and the size of the pneumothorax was reevaluated every 7 days after the last follow-up examination if the patient was asymptomatic. However, if the pneumothorax increased (> 30%) on follow-up chest radiographs or if the patient became symptomatic or was found to have a large pneumothorax, a chest catheter or tube was placed. Pneumothorax size was determined on the basis of the criteria established by Rhea et al. [21]. Pulmonary function tests were performed according to American Thoracic Society standards [22, 23]. Pulmonary function tests and electrocardiography were performed before the CT-guided biopsy procedure (mean, 7 ± 2 days). The institutional review board approved the study, and informed consent was obtained from all patients before biopsy. CT-Guided Biopsy Techniques and Procedures For CT-guided biopsy, 62 examinations were conducted on a nonhelical CT scanner (TCT 300, Toshiba, Tokyo, Japan), and 100 examinations were conducted on a single-detector helical CT scanner (Somatom Plus 4 VB 40, Siemens, Forchheim, Germany) by two radiologists experienced in thoracic and interventional radiology. The scanning parameters of the TCT 300 scanner were 120 kvp, 200 ma, 3- to 5-mm collimation, and 3- to 5-mm section thickness. The scanning parameters of the Somatom Plus 4 VB 40 scanner were 120 kvp, ma, 3- to 5-mm collimation, 3- to 5-mm section thickness, and a table speed of 3 10 mm/sec (pitch, 1 2). Thirty-five biopsies were performed with IV-injected contrast media to avoid necrotic tissue, and cystic lesions were identified using prior diagnostic contrast-enhanced CT. A total of 40 ml of iodinated contrast agent (Omnipaque 300 [iohexol], Daiichi Seiyaku, Tokyo, Japan) was administrated IV at 2 ml/sec by a power injector (Auto Enhance-50, Nemoto, Tokyo, Japan) with a scanning delay of 20 sec on conventional CT. The remaining 60 ml of iodinated contrast agent was administrated at 1 ml/ sec during the initial puncture and check of the needle tip in the tumor. Unenhanced CT scans were reviewed with a lung window setting (window width, 1600 H; window level, 600 H) or with a mediastinal window setting (window width, 450 H; window level, 30 H). The contrast-enhanced CT scans were reviewed with a mediastinal window setting (window width, 450 H; window level, 40 H) for evaluation of the relationship between needle tip and intratumoral necrosis. All CT-guided aspiration cytologic examinations were performed with 9- to 15-cm, 22-gauge Westcott needles (MD TECH, Gainesville, FL). All biopsies were performed with the patient prone or supine, depending on the proximity of the lesion to the chest wall and considering the number of pleural surfaces to be crossed by the needle in choosing the biopsy route. With the patient in the prone position, the shoulders were abducted to move the scapulae laterally. A pillow was routinely placed under the patient s chest to open the intercostal spaces posteriorly, thereby permitting easier access to the lesions. The patient was instructed to stop breathing after normal inspiration at functional residual capacity. The importance of breath-holding was explained to each patient, and the technique was practiced before the procedure. The CT-guided biopsy procedure was as follows. CT images were obtained from the lung apices to the diaphragm for the detection of solitary pulmonary nodules at end-inspiration. The center of the lesion was positioned at the CT landmark using a radiopaque grid on the patient s skin. CT images were obtained again, and the puncture point was determined after we measured the distance from the skin surface to the pleura, the length of needle path, and the smallest angle between the pleura and the needle on the cathode-ray tube monitor of the imager (Fig. 1A). The needle path length was the length between the skin surface and the center of the solitary pulmonary nodule. The distance to the pleura was the distance from the skin surface of the initial puncture to the pleura. The needle pleural angle was formed between the skin surface of the initial puncture and the biopsy needle. The initial puncture was performed without penetrating the pleura. CT images were obtained to check the course of the biopsy needle (Fig. 1B). If the nodule was on the extended course of the needle track, the biopsy procedure was continued. If the nodule was not on the extended course of the needle track, the course or puncture site was changed. When the nodule was penetrated, the needle tip was checked and an aspiration specimen was obtained (Fig. 1C). The specimen was placed in 99% ethyl alcohol for cytologic examination. Then the on-site cytologist evalu AJR:180, June 2003

3 CT-Guided Biopsy of Solitary Pulmonary Nodules dicted forced expiratory volume in 1 sec ( 50%, 51 60%, 61 70%, 71 80%, and 81%). All quantitative data were evaluated on the cathode-ray tube monitor of the CT imager by two radiologists. The mean value was accepted for all quantitative data. Diagnostic accuracy and pneumothorax rate were statistically compared for each influencing factor using analysis of variance followed by Fisher s protected least significant difference test. A p value of less than 0.05 was determined to be significant. Statistical Analysis In our study, aspiration specimens were cytologically diagnosed into three groups by consensus among a cytologist and two pathologists as follows: negative for malignant cells, atypical cell with indeterminate or unknown malignant potential, and atypical cells suggestive of or positive for malignancy. Negative for malignant cells was considered the group for benign lesions, insufficient component was considered the group for atypical cells with indeterminate or unknown malignant potential, and malignant lesion was considered the group for atypical cells suggestive of or positive for malignancy. The overall diagnostic accuracy, pneumothorax rate, and chest tube insertion rate were determined. Positive findings at transthoracic needle aspiration biopsy of a solitary pulmonary nodule (including suspected malignancy) were considered to be true-positive in cases with surgical confirmation, when biopsy of another site revealed cancer with the same histologic characteristics, or when the lesion increased in size and other proven metastases were found. Negative findings at transthoracic needle aspiration biopsy were considered to be true-negative in cases with surgical confirmation, when the lesion subsequently disappeared or decreased in size with or without the administration of antibiotics, or when the lesion remained stable on follow-up CT for 24 months. Follow-up CT for cases with negative findings was scheduled 3, 6, 12, 18, and 24 months after the biopsy, during which changes in lesion size were assessed. Positive findings at transthoracic needle aspiration biopsy were considered to be false-positive if surgical resection yielded a benign diagnosis, if the lesion subsequently disappeared or decreased in size before surgical resection, or if the lesion remained stable on the follow-up CT for at least 24 months in cases in which the patient did not agree to surgical resection. Negative findings at transthoracic needle aspiration biopsy were considered to be false-negative if surgical resection yielded a malignant diagnosis; if the lesion increased in size; if other proven metastases were diagnosed on CT, MR imaging, or bone scintigraphy and proven by histologic examination of the biopsy specimen or resection; or if the specimen of transthoracic needle aspiration biopsy was insufficient. True-positive and true-negative cases were considered diagnosed cases. Falsepositive and false-negative cases were considered nondiagnosed cases. The overall diagnostic accuracy was calculated using the following formula: diagnostic accuracy (%) = number of solitary pulmonary nodules accurately diagnosed (true-positive + true-negative) / total number of solitary pulmonary nodules. Overall diagnostic accuracy, pneumothorax rate, and chest tube insertion rate of transthoracic biopsy were statistically evaluated with stepwise regression analysis with respect to the following factors: age, lesion size ( 10, 11 15, and mm), needle path length (the distance from the visceral pleura to the center of the lesion: 10, 11 20, 21 30, 31 40, 41 50, 51 60, 61 70, 71 80, and 81 mm), distance from the skin surface to the pleura (distance to pleura: 10, 11 20, 21 30, 31 40, and 41 mm), patient position (prone or supine) during needle approach, location of solitary pulmonary nodules (right upper, right middle, right lower, left upper, or left lower lobe), the smallest angle between the pleura and the needle (needle pleural angle: 10, 11 20, 21 30, 31 40, 41 50, 51 60, 61 70, 71 80, and ), number of puncture attempts, and percentage of pre- The overall diagnostic accuracy of CTguided transthoracic needle aspiration biopsy of small solitary pulmonary nodules was 77.2%. Of the 162 solitary pulmonary nodules, 103 diagnosed as malignant and 22 diagnosed as benign were true-positive and true-negative cases, respectively. The remaining 37 solitary pulmonary nodules (15 malignant, 22 benign) were false-positive and false-negative cases, respectively, and were correctly diagnosed at video-assisted thoracic surgery (n = 8), open lung biopsy (n = 9), sputum cytology (n = 7), and follow-up examination (n = 14). The false-positive cases included 17 organizing pneumonias and five active inflammations. The overall pneumothorax rate of CT-guided transthoracic needle aspiration biopsy of small solitary pulmonary nodules was 28.4%. The overall chest tube insertion rate was 2.5% In stepwise regression analysis, diagnostic accuracy was significantly affected by the needle path length and the lesion size (r = 0.54, r 2 = 0.29, p < 0.05). The pneumothorax rate was A B C ated whether the quantity of the specimen was sufficient for diagnosis. If the specimen quantity was sufficient, the procedure was finished. If the specimen was not sufficient, another puncture was performed until a sufficient specimen was obtained. Results Fig year-old woman with adenocarcinoma in right upper lobe diagnosed at conventional CT-guided biopsy (conventional method). CT images were obtained with radiopaque grid. 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 pleura and needle (α) on cathode-ray tube monitor of imager. B, Initial puncture was performed without penetrating pleura. CT images were obtained to check course of biopsy needle. C, When solitary pulmonary nodule was penetrated, needle tip was checked and aspiration or histologic specimen was obtained. AJR:180, June

4 Ohno et al. Diagnostic Accuracy for TABLE 2 Each Range of Influencing Factors Factor Accuracy (%) a a a a a Lesion size (mm) b b a Significantly different from needle path lengths 40 mm (p < 0.05). b Significantly different from lesion sizes 10 mm (p < 0.05). significantly affected by the following three factors: percentage of predicted forced expiratory volume per 1 sec, the number of punctures, and needle path length (r = 0.59, r 2 = 0.35, p < 0.05). The chest tube insertion rate was significantly affected by the number of punctures (r = 0.43, r 2 = 0.23, p < 0.05). Diagnostic accuracies for each range of length of the needle path and lesion size are shown in Table 2. Diagnostic accuracy for needle path lengths of 40 mm or less was significantly greater than that for lengths greater than 40 mm (p < 0.05). Diagnostic accuracy for lesion size of 10 mm or less (52.0%) was significantly less than that of other sizes (11 15 mm, 74.4%; mm, 91.5%; p < 0.05). In the 10- mm-or-less group, 13 (nine malignant and four benign) of 25 solitary pulmonary nodules were true-positive and true-negative cases, respectively. The remaining 12 solitary pulmonary nodules (six malignant, six benign) were falsepositive and false-negative cases, respectively. In the more-than-10-mm and 15-mm-or-less groups, 58 (46 malignant and 12 benign) of 78 solitary pulmonary nodules were true-positive and true-negative cases, respectively. The remaining 20 solitary pulmonary nodules (seven malignant, 13 benign) were false-positive and false-negative cases, respectively. In the morethan-15-mm and 20-mm-or-less groups, 54 (48 malignant and six benign) of 59 solitary pulmonary nodules were true-positive and truenegative cases, respectively. The remaining five solitary pulmonary nodules (two malignant, three benign) were false-positive and false-negative cases, respectively. The pneumothorax rates for the percentage of predicted forced expiratory volume per 1 sec, number of punctures, and length of the needle path are shown in Table 3. The pneumothorax rate for patients whose percentage of predicted forced expiratory volume per 1 sec was greater than 70% was significantly lower than that for patients with a percentage of 70% or less ( p < 0.05). The pneumothorax rate for patients with single punctures was significantly lower than that for patients with more than one puncture ( p < ). Pneumothorax rates of patients who had needle path lengths of 40 mm or less were significantly lower than those of patients with lengths greater than 80 mm ( p < 0.05). The chest tube insertion rate for patients with three punctures (50%) was significantly greater than that of other groups (one puncture, 0.0%; two punctures, 0.3%; p < 0.05). Discussion Since Haaga and Alfidi [12] reported the first CT-guided biopsy in 1976, improved techniques have expanded the scope of thoracic lesions that are amenable to transthoracic biopsy [12 19, 24 32]. Percutaneous needle aspiration biopsy is a relatively safe and accurate means of diagnosing benign and malignant lesions of the chest [12 19, 24 32]. How to manage patients with growing solitary pulmonary nodules that are 20 mm or smaller is the ultimate question for radiologists and clinicians. The decisions depend on multiple factors including age, life style, coexisting medical problems, and experiences in each medical institution. When radiologists and clinicians consider using CT-guided transthoracic needle aspiration biopsy for small solitary pulmonary nodules, they should consider the impact that lesion size and the expected needle path length have on diagnostic accuracy. When transthoracic needle aspiration biopsy is performed, its accuracy must be explained carefully to the patients and referring physicians. Additionally, the association of pneumothorax rate with percentage of predicted forced expiratory volume in 1 sec, number of needle passes, and length of the needle path should be considered. The overall diagnostic accuracy (77.2%), pneumothorax rate (28.5%), and chest tube insertion rate (2.5%) of CT-guided transthoracic needle aspiration biopsy of small solitary pulmonary nodules were within the ranges of results of CT-guided biopsy reported in the literature, which include any size of solitary pulmonary nodule [12 19, 24 32]. Moreover, the diagnostic accuracy of small solitary pulmonary nodules smaller than 20 mm in diameter in our study was greater than that of fiberoptic bronchoscopy [33]. Our stepwise regression analysis suggested important factors that affect the diagnostic accuracy, pneumothorax rate, and chest tube insertion rate. Needle path length and lesion size significantly affect the diagnostic accuracy of CT-guided transthoracic needle aspiration biopsy of small solitary pulmonary nodules. Other factors did not contribute to improved diagnostic accuracy. Moreover, needle path length influenced diagnostic accuracy more than lesion size did. In published reports, many investigators indicate that diagnostic accuracies of CTguided biopsies were influenced mainly by lesion size [15 19, 24 32]. To our knowledge, no major reports suggest that needle path length is a more important factor in diagnostic accuracy of CT-guided transthoracic needle aspiration biopsy. In addition, our results suggest that the solitary pulmonary nodules of 10 mm or less in diameter should be followed up by repeated CT because the diagnostic accuracy for these nodules is significantly lower than that for larger solitary pulmonary nodules. The percentage of predicted forced expiratory volume in 1 sec, the number of punctures, and the needle path length significantly affected pneumothorax rate; and the number of punctures significantly affected the chest tube insertion rate. The pneumothorax rate of CT-guided transthoracic needle aspiration biopsy of small solitary pulmonary nodules in our study was not influenced by other factors, although some investigators have suggested that lesion size, needle pleural angle, location of the nodule, and needle approach influence pneumothorax rates [15 20]. The percentage of predicted forced expiratory volume in 1 sec suggests the degree of chronic obstructive pulmonary disease in patients [23]. A lower percentage of predicted forced expiratory volume in 1 sec has been suggested as a factor influencing pneumothorax rates [16, 20, 34]. In our study, patients whose percentage of predicted forced expiratory volume in 1 sec was 70% or less had a greater risk of pneumothorax, which is compatible with previous reports [16, 20, 34]. However, in our study, the number of punctures and the needle path length also significantly affected the pneumothorax rate. In addition, the number of punctures significantly affected the chest tube insertion rate AJR:180, June 2003

5 CT-Guided Biopsy of Solitary Pulmonary Nodules Rate of Pneumothorax for TABLE 3 Each Range of Influencing Factors Pneumothorax Factor Rate (%) % of predicted forced expiratory volume in 1 sec a a a No. of punctures b b c a Significantly different from percentage of predicted forced expiratory volume in 1 sec of > 70% ( p < 0.05). b Significantly different from single puncture ( p < 0.05). c Significantly different from needle path length of 40 mm ( p < 0.05). These facts are not compatible with previous results [15 20]. Recently, some investigators applied a coaxial technique for CT-guided biopsy. In our study, we did not adapt a coaxial technique. Therefore, the number of punctures may have directly affected the pneumothorax rate and chest tube insertion rate in our study. In 122 of 164 cases, the on-site cytologist evaluated the specimen from a single puncture as being sufficient for diagnosis. However, in the remaining 40 cases, 12 specimens from single punctures were not sufficient for diagnosis, and the other 28 cases were evaluated as inaccurate targeting of the lesion on the cathode-ray tube monitor. In these cases, we had to repuncture to obtain another specimen. In these situations, the increased number of punctures increases the risk of pneumothorax and the necessity of chest tube insertion. The needle path length must be considered because a longer needle path tends to damage a larger part of the lung parenchyma between the pleura and the solitary pulmonary nodule. Therefore, needle path length may significantly increase the risk of pneumothorax. Hence, it is preferable to try an accurate single puncture of a small solitary pulmonary nodule and to plan the needle trajectory (path) to be 40 mm or less. In conclusion, CT-guided transthoracic needle aspiration biopsy is useful as a diagnostic tool for small solitary pulmonary nodules with diameters of less than 20 mm. 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