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1 Vascular and Interventional Radiology Original Research Hiraki et al. Complications After CT Fluoroscopy Guided Lung Biopsy Vascular and Interventional Radiology Original Research Takao Hiraki 1 Hidefumi Mimura Hideo Gobara Kentaro Shibamoto Daisaku Inoue Yusuke Matsui Susumu Kanazawa Hiraki T, Mimura H, Gobara H, et al. Keywords: chest tube placement, complications, CT, lung biopsy, pneumothorax, pulmonary neoplasms DOI: /AJR Received June 24, 2009; accepted after revision August 24, All authors: Department of Radiology, Okayama University Medical School, Shikatacho, Okayama , Japan. Address correspondence to T. Hiraki (takaoh@tc4.so-net.ne.jp). AJR 2010; 194: X/10/ American Roentgen Ray Society Incidence of and Risk Factors for Pneumothorax and Chest Tube Placement After CT Fluoroscopy Guided Percutaneous Lung Biopsy: Retrospective Analysis of the Procedures Conducted Over a 9-Year Period OBJECTIVE. The objective of our study was to retrospectively evaluate the incidence of and the risk factors for pneumothorax and chest tube placement after CT fluoroscopy guided lung biopsy. MATERIALS AND METHODS. We analyzed 1,098 CT fluoroscopy guided lung biopsies conducted with 20-gauge coaxial cutting needles for 1,155 lesions in 1,033 patients. Apart from evaluating the incidence of pneumothorax and chest tube placement, the independent risk factors for pneumothorax and chest tube placement for pneumothorax were determined using multivariate logistic regression analysis. RESULTS. The overall incidence of pneumothorax was 42.3% (464/1,098). Chest tube placement was required for 11.9% (55/464) of pneumothoraces (5.0% [55/1,098] of the total number of procedures). The significant independent risk factors for pneumothorax were no prior pulmonary surgery (p = 0.001), lesions in the lower lobe (p < 0.001), greater lesion depth (p < 0.001), and a needle trajectory angle of < 45 (p = 0.014); those for chest tube placement for pneumothorax were pulmonary emphysema (p < 0.001) and greater lesion depth (p < 0.001). CONCLUSION. Pneumothorax frequently occurred and placement of a chest tube was occasionally required for pneumothorax after CT fluoroscopy guided lung biopsy. To reduce the risk of pneumothorax necessitating chest tube placement, physicians should adopt the shortest needle path to the lesion. C onventional CT-guided needle biopsy is an established method for the diagnosis of pulmonary lesions. Pneumothorax is a common complication of this procedure, and its incidence rate has been reported to be 12 45% [1 18]. In 1993, CT fluoroscopy for interventional procedures was introduced by Katada et al. [19]. Compared with conventional CT guidance, real-time image display with CT fluoroscopy has been shown to reduce the procedure time for the biopsy [20 23] and the number of times that the needle needs to be inserted [20]. Considering that the incidence of pneumothorax may be influenced by the procedural time [17] and the number of pleural punctures [18], we hypothesized that the use of CT fluoroscopy might affect the development of pneumothorax after the procedure. However, pneumothorax after CT fluoroscopy guided lung biopsy has not been fully investigated in large studies, to our knowledge. Thus, the purpose of our study was to evaluate the incidence of and risk factors for pneumothorax and chest tube placement after CT fluoroscopy guided lung biopsy in a large population. Materials and Methods We obtained informed consent of the patients for CT fluoroscopy guided lung biopsy. Our institutional review board did not require approval to report retrospective studies. Patients, Lesions, and Procedures Between April 2000 and March 2009, 1,098 CT fluoroscopy guided lung biopsy procedures were performed for 1,155 lesions in 1,033 patients (377 women and 656 men; mean age, 67.2 years) at our institution. All 1,098 procedures were performed percutaneously under CT fluoroscopy guidance (Asteion, Toshiba Medical Systems) by an experienced radiologist or a radiology trainee (resident or fellow) under the direct supervision of an experienced radiologist. The following settings were used when acquiring the CT fluoroscopic images: scanning speed, 0.75 second per rotation (360 ); tube voltage, 120 kv; current, 20 ma; and collimation, 5 mm. A coaxial needle system comprising a 19-gauge introducer needle and a 20-gauge AJR:194, March

2 Hiraki et al. automated cutting biopsy needle with a 19-mm notch was used for all lesions (for the first 975 lesions: Super-Core, Medical Device Technologies; for the most recent 180 lesions: Temno Evolution, Cardinal Health). The patients were placed in the supine, prone, or lateral position according to the location of the lesion. CT images were obtained to locate the target lesion. A needle path avoiding interlobular fissures, visible bronchi, and relatively large vessels, when possible, was determined. After the administration of local anesthesia, the operator advanced the introducer needle under CT fluoroscopy guidance until its tip was in front of the lesion. To reduce radiation exposure, the operator used CT fluoroscopy intermittently that is, only to confirm the position of the needle and not while advancing the needle. Further, the operator held the needle with a pair of 19-cm-long forceps during CT fluoroscopy. The internal stylet of the introducer needle was replaced by the biopsy needle. The operator advanced the stylet of the biopsy needle into the lesion to obtain a specimen. Specimen acquisition was repeated until the operator thought that the specimens were adequate because no pathologist was available onsite. Immediately after acquisition of the specimens, chest CT images were obtained to evaluate complications. Any precaution against pneumothorax such as sealing the needle track and puncture site down patient positioning after the procedure was not applied. Patients were instructed to stay in bed for 3 hours after the procedure, but they were not instructed about their posture in bed. An upright posteroanterior chest radiograph was obtained 3 hours after the procedure and the next morning. The criterion for chest tube placement in our institution was symptomatic pneumothorax or pneumothorax occupying more than approximately 30 40% of the hemithorax. The chest tube was kept in place until air leakage ceased. Collection of Variables Multiple variables related to the patient, lesion, and procedure were collected to determine the risk factors for the occurrence of pneumothorax and those for the need for chest tube placement for pneumothorax. The patient variables were age, sex, presence of pulmonary emphysema in the vicinity of the lesion on CT images, and a history of surgery or radiation on the side of the lung on which the biopsy was performed. The lesion variables were size (long-axis diameter), lobar location (upper and middle lobes or lower lobe), contact with the pleura, and lesion depth. Lesion depth was measured from the pleura to the edge of the lesion along the needle path. The procedure variables were patient positioning (supine or prone), number of cutting specimens, and the angle of the needle trajectory (< 45 or 45 ). Lateral positioning of the patient was excluded from the analyses because it was quite rare. The angle of the needle trajectory was the smaller angle between the needle trajectory and the tangent line at the point at which the needle passed through the pleura. Statistical Analysis The risk factors for the occurrence of pneumothorax and those for the need for chest tube placement for pneumothorax were evaluated using lesions as the sampling unit. We excluded 40 lesions from the risk analyses because the biopsy procedure for those lesions targeted multiple lesions on the same side of the lung and, therefore, the lesion that was responsible for the occurrence of pneumothorax could not be determined. The remaining 1,115 lesions were divided into two groups according to whether pneumothorax occurred. The lesions for which the procedure was followed by pneumothorax were divided into two groups according to the need for chest tube placement. Furthermore, the lesions for which the procedure required chest tube placement were divided into two groups according to the duration of chest tube placement ( 3 days or > 3 days). The above-mentioned variables were compared between the two groups using univariate analysis with the two-sided Student s t test for numeric values and the chi-square test or Fisher s exact test for categoric values. Subsequently, the variables that were found to be significantly different by univariate analyses were subjected to multivariate logistic regression analysis to determine the independent risk factors for the occurrence of pneumothorax and those for the need for chest tube placement for pneumothorax. The variables that were determined to indicate a lower risk according to univariate analyses were used as the reference. An odds ratio (OR) of > 1.00 indicated a higher risk for the occurrence of pneumothorax or for the need for chest tube placement for pneumothorax. A p value of < 0.05 was considered to be statistically significant. Statistical analysis was performed using statistics software (SPSS version 11.0, SPSS). Results The characteristics of the patients, lesions, and procedures are shown in Table 1. Briefly, pulmonary emphysema in the vicinity of the lesion was identified in 302 patients. The mean long-axis diameter of the lesions was 22.7 mm. In 1,043 procedures, a single lesion was biopsied; in 55 procedures, multiple (two or three) lesions were biopsied. The mean number of specimens obtained per lesion was 2.7. For four lesions, the procedure was terminated before specimen acquisition because of rapidly progressive pneumothorax (n = 3) or intrapulmonary bleeding that obscured a small lesion with ground-glass opacity (n = 1). The use of the coaxial method allowed the acquisition of the specimen with a single pleural puncture for most lesions even when multiple specimens were obtained. The overall incidence of pneumothorax was 42.3% (464/1,098); it was 42.3% (441/1,043) for procedures that targeted a single lesion and 41.8% (23/55) for procedures that targeted multiple lesions. Chest tube placement was required for 11.9% (55/464) of the pneumothoraces (5.0% [55/1,098] of the total number of procedures). The duration of chest tube placement was 1 day in the case of 18 procedures; 2 days, 11 procedures; 3 days, three procedures; 4 6 days, 13 procedures; and 7 13 days, 10 procedures. From the results of univariate analyses, the significant risk factors for the occurrence of pneumothorax were no prior pulmonary surgery (p = 0.005), smaller lesion size (p = 0.004), lesions in the lower lobe (p < ), lesions away from the pleura (p = 0.005), greater lesion depth (p < ), and a needle trajectory angle of < 45 (p = 0.027) (Table 2). From the results of multivariate analysis, the significant independent risk factors were no prior pulmonary surgery (OR, 2.09; 95% CI, ; p = 0.001), lesions in the lower lobe (OR, 2.11; 95% CI, ; p < 0.001), greater lesion depth (OR, 1.02; 95% CI, ; p < 0.001), and a needle trajectory angle of < 45 (OR, 1.52; 95% CI, ; p = 0.014) (Table 3). From the results of univariate analyses, the significant risk factors for the need for chest tube placement for pneumothorax were male sex (p = 0.003), pulmonary emphysema (p < ), lesions in the upper and middle lobes (p = 0.007), greater lesion depth (p < ), and supine positioning (p = 0.002) (Table 2). From the results of multivariate analysis, the significant independent risk factors were pulmonary emphysema (OR, 3.52; 95% CI, ; p < 0.001) and greater lesion depth (OR, 1.04; 95% CI, ; p < 0.001) (Table 4). Men had a higher risk of the need for chest tube placement for pneumothorax than women, but the difference did not reach a statistically significant level (OR, 2.46; 95% CI, ; p = 0.052) (Table 4). From the results of univariate analyses, none of the variables was significantly related to the duration of chest tube placement (results not shown). 810 AJR:194, March 2010

3 Complications After CT Fluoroscopy Guided Lung Biopsy Discussion Large surveys [24, 25] show that the most common complication of percutaneous lung biopsy is pneumothorax. After conventional CT-guided lung biopsy, the incidence of pneumothorax ranges from 12% to 45% [1 18]; moreover, chest tube placement is required in 0 53% of pneumothorax cases and 0 15% of all biopsy cases [1 18]. Thus, the incidences of pneumothorax and of chest tube placement for pneumothorax in our study with the use of CT fluoroscopic guidance were comparable to those of the abovementioned studies. Regarding previous studies of CT fluoroscopy guided biopsy, Silit et al. [26] showed that pneumothorax developed in five (6%) of 81 patients with thoracic lesions. Yamagami et al. [27] showed that pneumothorax occurred in 104 (37%) of 283 lung biopsies and that chest tube placement was required in nine pneumothorax cases. Muehlstaedt et al. [28] showed that pneumothorax occurred in 21 (21%) of 98 biopsies for thoracic lesions and that chest tube TABLE 1: Characteristics of 1,033 Patients, 1,155 Lesions, and 1,098 Procedures Patient characteristics Age (y) Variable Value Mean ± SD 67.2 ± 11.2 Range Sex (no. of patients) Female/male 377/656 Emphysema (no. of patients) Yes/no 302/731 Prior surgery (no. of patients) Yes/no 96/937 Prior radiation (no. of patients) Yes/no 15/1,018 Lesion characteristics Size (mm) Mean ± SD 22.7 ± 15.0 Range Lobe (no. of lesions) Upper/middle/lower 615/79/461 Contact with pleura (no. of lesions) Yes/no 429/726 Lesion depth (mm) Mean ± SD 19.3 ± 15.7 Range 0 76 Procedure characteristics Positioning (no. of procedures) Supine/prone/lateral 498/596/4 No. of target lesions per procedure (no. of procedures) 1/2/3 1,043/51/4 No. of specimens obtained per lesion Mean ± SD 2.7 ± 1.0 Range 0 10 Needle trajectory angle (no. of procedures) 45 /< /189 placement was required in two pneumothorax cases. In several studies, investigators have compared the incidence of pneumothorax after CT fluoroscopy guided lung biopsy with that after conventional CT-guided lung biopsy. Heck et al. [29] showed that the incidence of pneumothorax was 26% (15/57) after CT fluoroscopy guided lung biopsy, which was not significantly different from that after conventional CT-guided lung biopsy (38%, 16/42). In that study, chest tube placement was required in one pneumothorax case after CT fluoroscopy guided lung biopsy, whereas it was required in four pneumothorax cases after conventional CT-guided biopsy. Kirchner et al. [22] showed that the incidence of pneumothorax was 38% (8/21) after CT fluoroscopy guided biopsy for lung lesions and 38% (3/8) after conventional CT-guided biopsy. Gianfelice et al. [21] showed that the incidence of pneumothorax was 25% (15/59) after CT fluoroscopy guided lung biopsy and 29% (7/24) after conventional CT-guided lung biopsy. Considering the outcomes in our study and those in previous studies, the use of CT fluoroscopy does not seem to affect the development of postprocedural pneumothorax significantly. Although the use of CT fluoroscopy has been shown to reduce the procedure time for biopsy [20 23] and the number of times that the needle needs to be inserted [20], we assume that the reduction may not be considerable enough to significantly reduce the incidence of pneumothorax. For drawing a final conclusion, however, a large comparison study is necessary. Despite the unlikelihood that CT fluoroscopy confers a significant reduction of the risk of pneumothorax, we prefer to use CT fluoroscopy for lung biopsy procedures. Unlike conventional CT, CT fluoroscopy enables operators to obtain the images anytime by themselves. Further, the images are rapidly reconstructed and displayed. We think that this capability may considerably reduce physicians stress and facilitate the procedure, especially for the biopsy of small lesions. A recent large study on the diagnostic yield achieved by CT fluoroscopy guided lung biopsy [30] showed high diagnostic accuracy even for small lesions (92.7% [140/151] for lesions measuring 1.0 cm). In contrast, a major disadvantage of CT fluoroscopy is increased radiation exposure [22]. Thus, we minimize the use of CT fluoroscopy. Moreover, during CT fluoroscopy, the operator holds the needle with a pair of 19-cm-long forceps. AJR:194, March

4 Hiraki et al. TABLE 2: Results of Univariate Analyses to Determine Risk Factors for Pneumothorax and Chest Tube Placement for Pneumothorax Patient factors Variable In previous studies, investigators have reported a variety of risk factors for the occurrence of pneumothorax after CT-guided lung biopsy. Among them, smaller lesion size [1 4, 7, 8, 10, 11, 14, 16] and greater lesion depth [1 3, 5, 7 9, 11, 15 18] were common risk factors. In our study, smaller lesion size was Pneumothorax Chest Tube Placement Needed for Pneumothorax No (n = 663) Yes (n = 452) p No (n = 398) Yes (n = 54) p Age (y) Mean ± SD 67.3 ± ± ± ± 8.4 Sex Female Male Emphysema 0.38 < Yes No Prior surgery Yes No Prior radiation Yes No Lesion factors Size (mm) Mean ± SD 24.1 ± ± ± ± 11.7 Lobe < Upper and middle Lower Contact with pleura Yes No Lesion depth (mm) < Mean ± SD 17.7 ± ± ± ± 16.5 Procedure factors Positioning a Prone Supine No. of specimens Mean ± SD 27.7 ± ± ± ± 1.2 Needle trajectory angle < a Lateral positioning for four lesions are excluded from the analysis. determined to be a significant risk factor for pneumothorax by univariate analysis; however, when subjected to multivariate analysis, this factor was found to be not significant. The results of multivariate analysis showed that greater lesion depth was an independent risk factor for both the occurrence of pneumothorax and the need for chest tube placement for pneumothorax. It seems that the deeper the lesion, the more difficult it is to maneuver the needle into the lesion. Thus, more redirections of the needle may be required, which could probably result in greater tearing of the pleura and longer procedure time. 812 AJR:194, March 2010

5 Complications After CT Fluoroscopy Guided Lung Biopsy Previous surgery causes adhesion between the parietal and visceral pleura that may work as interference for the occurrence of pneumothorax. Thus, no prior pulmonary surgery was an independent risk factor for pneumothorax; this finding is in agreement with the outcome of previous studies [4, 6]. Similar to the results of previous studies [6, 8], shallow needle angle was also found to be an independent risk factor for pneumothorax. Inserting the needle at a shallow angle may result in an elongated and larger pleural hole than would have been created if the needle had been inserted perpendicular to the pleura. Further, advancing the needle in such a manner may possibly result in tearing of the pleura. To date, the significance of the lobar location of lesions with regard to the development of pneumothorax has not been fully investigated. According to the results of univariate analyses, lesions in the lower lobe indicated a higher risk of pneumothorax, whereas lesions in the upper and middle lobes indicated a higher risk of the need for chest tube placement once pneumothorax had occurred. Multivariate analysis showed that lesions in the lower lobe were also an independent risk factor for pneumothorax. It is possible that greater respiratory motion occurs in the lower lobe. Greater respiratory motion of the lung may make the procedure more difficult, necessitating more redirections of the needle to reach the lesion and prolonging the procedure time. Further, the pleural hole made by the needle may enlarge as a result of greater respiratory motion of the lung during the procedure. According to the results of previous studies, the presence of obstructive airway disease was also a common risk factor for both the occurrence of pneumothorax [5, 6, 8, 10, 11, 14, 15, 18] and the need for chest tube placement for pneumothorax [2, 3, 6, 11]. In our study, the presence of pulmonary emphysema was a significant independent risk factor for the need for chest tube placement for pneumothorax. The persistent air leakage that necessitates chest tube placement may also be explained by increased airway pressure in pulmonary emphysema. Although statistically insignificant, men had a higher risk of the need for chest tube placement. Greater forced vital capacity has been shown to be significantly related to a greater likelihood of the occurrence of pneumothorax [8]. Thus, men may be at a higher risk of persistent air leakage than women because men have greater vital capacity, which causes greater air ventilation and respiratory lung movement. TABLE 3: Results of Multivariate Analysis to Determine Independent Risk Factors for Pneumothorax Variables p Odds Ratio (95% CI) No prior pulmonary surgery ( ) Smaller lesion size ( ) Lesions in lower lobe < ( ) Lesions apart from pleura ( ) Greater lesion depth < ( ) Needle angle trajectory of < ( ) TABLE 4: Results of Multivariate Analysis to Determine Independent Risk Factors for Chest Tube Placement for Pneumothorax Variables p Odds Ratio (95% CI) Male sex ( ) Pulmonary emphysema < ( ) Lesions in upper and middle lobes ( ) Greater lesion depth < ( ) Supine position ( ) Precautions against pneumothorax after CT-guided lung biopsy have been reported. Several studies showed that sealing the needle track using autologous blood clot [31], NaCl [32], or fibrin glue [33] was helpful to reduce the incidence or the severity of pneumothorax. On the other hand, other researchers failed to show usefulness of the blood patch technique [34, 35]. Puncture site down positioning during or after the procedure may also be a useful technique [36, 37]. There are limitations of this study. This study was retrospective with an unknown bias. Pulmonary function was not evaluated in the risk analyses because the pulmonary function test is not usually performed before lung biopsy at our institution. Our study indicates that the incidence rate of pneumothorax after CT fluoroscopy guided lung biopsy was similar to the reported incidence rates after conventional CT-guided lung biopsy. However, our study was not designed to compare CT fluoroscopy with conventional CT in the development of postprocedural pneumothorax. Although a previous study [1] showed that less experienced operators were significantly associated with higher incidence of pneumothorax, we could not evaluate the effect of operators experience of the procedure on pneumothorax because of missing data regarding the operator. Multiple testing for multiple variables, as conducted here, is necessarily associated with an inflated type I error rate. In conclusion, pneumothorax occurred in 42.3% (464/1,098) of procedures after CT fluoroscopy guided lung biopsy procedures; a chest tube was placed for 11.9% (55/464) of the pneumothoraces (5.0% [55/1,098] of the total number of procedures). Compared with the previously reported incidence of pneumothorax after conventional CT-guided lung biopsy, the use of CT fluoroscopy does not seem to affect the incidence of pneumothorax. Postprocedural pneumothorax was significantly associated with no prior pulmonary surgery, lesions in the lower lobe, greater lesion depth, and a needle trajectory angle of < 45. The need for chest tube placement for pneumothorax was significantly associated with pulmonary emphysema and greater lesion depth. 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