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Vascular and Interventional Radiology |
1 From the Department of Radiology, Massachusetts General Hospital, Boston (J.P.K., J.O.S., E.A.D. S.L.A., E.H., T.C.M.); Barts and the London NHS Trust, England (A.S.); and the University of Texas M.D. Anderson Cancer Center, Houston (B.S.). From the 1999 RSNA scientific assembly. Received February 10, 2000; revision requested March 24; revision received May 5; accepted May 22. Address correspondence to J.P.K., Department of Radiology, NYU Medical Center, 560 1st Ave, New York, NY 10016 (e-mail: jane.ko@med.nyu.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: In 159 patients, 160 coaxial computed tomography (CT)-guided lung biopsies were performed. Dwell time, the time between pleural puncture and needle removal, was calculated. The smallest angle of the needle with the pleura ("needle-pleural angle") was measured. These and other variables were correlated with pneumothorax and chest tube rates.
RESULTS: One hundred fifty biopsies were included. There were 58 (39%) pneumothoraces (14 noted only at CT), with eight (5%) biopsies resulting in chest tube placement. Longer dwell times (mean, 29 minutes; range, 12–66 minutes) did not correlate with pneumothoraces (P = .81). Smaller needle-pleural angles (80°), decreased forced expiratory volume in 1 second to vital capacity ratio (<50%), lateral pleural puncture, and lesions along fissures were associated with lower pneumothorax rates (P < .05). Emphysema along the needle path, pulmonary function tests showing ventilatory obstruction, and lesions along fissures predisposed patients to chest tube placement (P < .05). Pleural thickening and prior surgery were associated with lower pneumothorax rates (P < .05).
CONCLUSION: Longer dwell times do not correlate with pneumothorax and should not influence the decision to obtain more biopsy samples. A shallow pleural puncture angle may increase the pneumothorax rate.
Index terms: Biopsies, complications, 60.732 • Computed tomography (CT), guidance, 60.12111 • Lung, biopsy, 60.1263 • Pneumothorax, 60.732
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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With coaxial biopsy systems, multiple fine-needle aspirates and core biopsy specimens can be obtained through an introducer needle, which remains within the lung parenchyma for a variable time. We refer to this time between pleural puncture and needle removal as "dwell time." To our knowledge, the relationship of dwell time to pneumothorax rate has not been studied extensively (1). Investigators (2) have shown that the incidence of pneumothorax is higher when performed with computed tomographic (CT) rather than fluoroscopic guidance because of the longer procedure duration and the fact that biopsy of smaller lesions is often performed under CT guidance (3). Smaller size (2) and greater depth (1) of lesions have been shown to correlate with an increase in pneumothorax frequency. It is unclear whether this increased rate is related to the amount of lung traversed, the number and angle of needle redirections, or longer dwell times related to biopsy difficulty. If longer dwell times do correlate with a higher pneumothorax rate, this fact may influence the biopsy strategy and decision to obtain more samples, particularly when on-site cytopathologic analysis is available.
The angle at which the needle enters the pleura, which we term the "needle-pleural angle," has not, to our knowledge, been extensively correlated with pneumothorax rate (4). The angle of pleural puncture may influence the shape and size of the pleural hole and therefore the pneumothorax rate (5).
The purpose of this prospective study was to examine variables that potentially affect the rate of pneumothorax and chest tube placement, with concentration on longer needle dwell times and shallower needle-pleural angles.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Experienced thoracic radiologists (J.P.K., J.O.S., E.A.D., S.L.A., T.C.M.) or radiology residents or fellows (A.S., B.S.) under the supervision of a thoracic radiologist performed the biopsies by following a standard protocol. A brief history and written informed consent were obtained. The patients were instructed to abstain from moving, coughing, talking, or deep breathing during the procedure and the 3-hour postprocedural period.
All biopsies were performed under CT guidance by using a model 9800 scanner (GE Medical Systems, Milwaukee, Wis) and a coaxial system composed of a 19-gauge ultrathin introducer and 22-gauge Greene Chiba–type aspiration needle (Cook, Bloomington, Ind). The safest and most direct route from the chest wall to the lesion was used to determine the patient’s position on the CT table. The optimal skin entry point was determined after a paper grid (E-Z-Em, Westbury, NY) was applied to the skin and 3-mm contiguous transverse CT sections were obtained through the lesion. The patient’s position was altered if it was necessary to change the biopsy approach.
By using a sterile technique and lidocaine 1% (Xylocaine-MPF; Astra USA, Westborough, Mass) local anesthetic, the operator placed the introducer needle into the extrapleural soft tissues. When the introducer was passed through the pleura, the cytotechnologist was telephoned. Aspirates were obtained after the introducer was placed within the periphery of the lesion and the cytotechnologist was present. Imaging was performed after each aspirate was obtained. The cytotechnologist immediately analyzed the samples, which had been stained with hematoxylin (Gill-3; Shandon, Pittsburgh, Pa) and eosin 1% alcoholic (Eosin; Fisher Health Care, Houston, Tex). When the cytotechnologist decided that the sample was adequate, the pathologist was telephoned. On arrival, the pathologist rendered an opinion of the adequacy of the specimen and often rendered a diagnosis. Separate fine-needle aspirates were obtained for microbiologic examination when there was clinical or cytopathologic suspicion of infection. A core biopsy specimen was obtained with a 20-gauge automated cutting needle (Cook) if the cytopathologic diagnosis was uncertain and the radiologist determined that it was safe to obtain a core biopsy specimen.
After needle removal, the patient was monitored for 3 hours and positioned with the puncture side down. One- and 3-hour posteroanterior chest radiographs were obtained. Anteroposterior radiographs were obtained if the patient could not sit up. If there was pneumothorax on CT scans or chest radiographs, low-flow oxygen was administered through a nasal cannula. Any asymptomatic patient without a pneumothorax or with a small nonenlarging pneumothorax was discharged and instructed to seek medical attention if shortness of breath or chest pain developed. If there was a need to return to a hospital emergency department because of symptoms, the patient was asked to inform the thoracic radiology office. Any patient who lived far from a hospital, had no companion for the next 24 hours, or had a pneumothorax or symptoms that warranted observation was admitted for 23-hour observation. Patients with pneumothoraces that were enlarging or accompanied by symptoms and signs of shortness of breath, chest pain, or low oxygen saturation received chest tubes.
Data Collection
Biopsy time points were recorded on a standard form by the CT technologist who was present during biopsy. The same technologist assisted with 129 of the biopsies. Time points recorded were the initiation of procedure, which was defined as the time when the patient was placed on the CT table, and the time of pleural puncture, cytotechnologist arrival, telephone call to the pathologist, pathologist arrival, and needle removal.
The physician performing the biopsy completed forms with information regarding operator experience, biopsy technique, and the patient who underwent biopsy. The experience of the physician performing biopsy was separated into subsets of 0–1, 5–10, and greater than 10 years. Residents and fellows who performed a majority or crucial part of the procedure had their experience level (0–1 year) recorded. Patient position (prone, supine, oblique, or lateral decubitus), use of conscious sedation, site of pleural puncture, crossing of a fissure by the introducer needle, and the number of pleural punctures, aspirates or core biopsy samples obtained, and redirections of the introducer within the lung were noted. The patient’s age, sex, and inpatient or outpatient status were recorded in addition to the presence of general emphysema on CT scans, emphysema along the needle path, and history of prior cardiac or thoracic surgery on the side of the body on which biopsy was performed.
A pneumothorax was measured at the largest separation between the visceral and parietal pleura on chest radiographs and CT scans. A pneumothorax was considered small if it was less than or equal to 1 cm, medium if it was greater than 1 cm but less than or equal to 3 cm, or large if it was greater than 3 cm or associated with a lateral component that extended below the upper third of the thorax. Hemoptysis was considered major when the patient had hemodynamic or respiratory compromise.
One radiologist (J.P.K.) reviewed the biopsy CT scans, postbiopsy chest radiographs, and prebiopsy CT scans on hard copy or at an IMPAX picture archiving and communication system (PACS) workstation (AGFA, Ridgefield Park, NJ). Nonpulmonary lesions in which biopsy was not performed through the lung, in addition to patients with incomplete data sheets and preexistent chest tubes, were excluded. Lesion depth, as measured along the needle path, size, and location were recorded. If the lesion contacted the fissures or pleura, adjacent pleural disease or chest wall invasion was noted. The presence of diffuse pleural disease on the side of the body on which biopsy was performed was documented. Middle lobe, lingular, and lower lobe lesions were categorized as "lower"; upper lobe lesions, as "upper." An apical lesion was defined as one that contacted the lung apex or had more than half its cranial-caudal dimension within 4 cm of the apex.
An electronic caliper on the PACS unit or a goniometer was used to measure the smallest angle formed by the introducer needle and the pleura in the mediolateral direction. This angle was measured on the transverse 3-mm section that documented placement of the needle into the lesion. Also, the angle in the craniocaudal dimension was calculated by subtracting the gantry tilt from 90°. The smaller of the two angles was assigned the label "needle-pleural angle" (Figure). The maximal change in the direction of the needle when in the lung parenchyma was also calculated by subtracting changes in the mediolateral angles but was not calculated for the cranial-caudal dimension.
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Statistical Analyses
The two-tailed Fisher exact test and Student t test were performed to determine significant differences in dwell time, needle-pleural angle, and other variables between patients who did and those who did not have pneumothorax. Multiple regression analysis using Cochran-Mantel-Haenszel statistics was performed on significant variables. The same tests were applied in patients with and those without chest tubes. Associations with dwell time were also tested by means of Student t tests for all presence or absence indicators and the Pearson correlation coefficient for all numeric measures. These tests were performed by using SAS software (SAS Institute, Cary, NC) on a personal computer.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Complications
Fifty-eight (39%) of 150 patients developed pneumothoraces. Fourteen (24%) of 58 pneumothoraces were noted only on CT scans, whereas 28 (48%) were considered small; eight (14%), medium; and eight (14%), large on chest radiographs. On CT scans, a pneumothorax was noted to have developed during the procedure in 32 (21%) of 150 patients. Eight (5%) of 150 patients required chest tubes, including one who had a pneumothorax that enlarged 12 hours after the patient had been discharged with a small stable pneumothorax. Hemoptysis, five minor and one major episode, occurred in six (4%) of 150 patients. Two (1%) of 150 patients had vasovagal episodes. Twelve outpatients were admitted: six after chest tube placement, and two for close observation of a moderate pneumothorax. The remaining patients who were admitted either lacked someone to stay with them for the next 24 hours (three patients) or were recovering from a major vasovagal episode (one patient).
Needle Dwell Times
Dwell time did not correlate significantly with pneumothorax (P = .81) or chest tube (P = .56) rates (Table 1). The pneumothorax rate for dwell times longer than 50 minutes was lower than for other subsets. The pneumothorax rates for dwell time subsets were 42% (11 of 26 patients) for less than 20 minutes, 33% (20 of 61) for 20–29 minutes, 46% (17 of 37) for 30–39 minutes, 44% (seven of 16) for 40–49 minutes, and 30% (three of 10) for 50 minutes or greater. The overall mean dwell time was 29 minutes ± 11 (SD) (median, 25 minutes; range, 12–66 minutes).
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Patients who had diffuse pleural disease, prior cardiac or thoracic surgery on the side of the body on which biopsy was performed, or lesions with contiguous focal pleural disease or chest wall invasion had lower pneumothorax rates but not lower chest tube rates (P < .05) (Table 2). When patients who had pleural disease and other protective factors were subtracted from the analysis, no significant correlation between pneumothorax rate and dwell time was revealed.
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The presence of a pneumothorax during biopsy, as demonstrated on the CT images obtained during the procedure, did not correlate significantly with dwell time (P = .26).
Needle-Pleural Angle and Other Variables
Higher pneumothorax rates (Table 2) correlated with smaller needle-pleural angles, lesions along fissures, and lateral puncture site or lateral decubitus patient position (P < .05).
Needle-pleural angles less than 80° were associated with a higher percentage of pneumothoraces, whereas the less than 50° subset had the highest percentage overall (Table 3). The assigned needle-pleural angle represented the craniocaudal and mediolateral pleural angle in seven and 143 biopsies, respectively. Eight of the nine patients with a lateral pleural puncture were also in the lateral decubitus position. No difference in pneumothorax rate was revealed for upper lung lesions, as compared with lower lung lesions (Table 2).
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Multiple regression analysis showed that, when controlling for a lateral pleural puncture site, there was a significant additional risk for pneumothorax with a shallow needle-pleural angle (P = .023) and lesions along fissures (P = .032).
The initial significant correlation of greater lesion depth (P = .88) and smaller lesion size (P = .21) was lost when 58 patients with protective factors of focal or diffuse pleural disease, chest wall invasion, and surgical history were excluded.
There were significant differences in pulmonary function test results, more specifically, FEV1 percentage, FEV1/VC, and FEV1/VC percentage, between patients who received chest tubes and those who did not (P < .05). Emphysema along the needle path (P = .012) and lesions along fissures (P = .034) were associated with a higher chest tube rate (Table 4). Thirty-three percent (three of 10) of patients with a FEV1 percentage less than 40% required chest tubes, as compared with 4% (two of 51) with a FEV1 percentage greater than or equal to 40%. Patients with FEV1/VC less than 50% had a 28% (two of seven) chest tube rate, as compared with those with a FEV1/VC greater than or equal to 50%, who had a 6% (three of 54) rate. Patients with a FEV1/VC percentage less than 70% had a 33% (four of 12) chest tube rate, whereas those with a FEV1/VC percentage greater than or equal to 70% had a 2% (one of 49) chest tube rate. Four patients who had chest tubes and emphysema along the needle track also had pulmonary function tests that demonstrated ventilatory obstruction.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Our study results showed no significant difference in dwell times between CT-guided biopsies complicated by pneumothoraces or chest tubes and those without these complications. The small number of biopsies that had dwell times equal to or longer than 50 minutes could have contributed to the lack of association between pneumothorax and dwell time. Our findings correlate with those of the study by Laurent et al (1), which demonstrated no significant difference in dwell times between their patients who did and those who did not have pneumothorax.
Dwell times in our study were 12–66 minutes, but most were 20–40 minutes. Longer dwell times resulted from a higher number of aspirates, core biopsies, and needle redirections in the lung parenchyma. We found that those patients who had undergone prior thoracic surgery and had focal and diffuse pleural disease and chest wall invasion were less likely to have a pneumothorax. The exclusion of patients with protective factors did not unmask any significant correlation of dwell time with pneumothorax rate.
An oblique biopsy-needle path has been advocated to secure needle placement in subpleural nodules (4,5). A craniocaudal gantry tilt may enable better access to a lesion; the entire needle trajectory may be visualized when an intervening rib is present (8). An angled approach may therefore be preferable in many instances; however, its correlation with pneumothorax rate has not been extensively studied (4).
We observed a significant association between small needle-pleural angles and pneumothorax rate but not chest tube requirement. Needle-pleural angles less than 80° and, in particular, less than 50°, were associated with a higher pneumothorax rate. In their study concentrating on the success rate of CT-guided biopsy of 61 subpleural lesions, Tanaka et al (4) noted a pneumothorax rate of 12.5% for biopsies performed with an oblique approach, as compared with a rate of 20% with a near 90° approach. Our study included a larger number of biopsies and did not focus solely on subpleural lesions; this may explain the differences in our results, as compared with theirs. The pleural hole created by a needle entering the pleura at a shallow angle may be elongated and therefore potentially increase the risk of pneumothorax. Moore et al (5,9) have noted that the shape of the pleural hole affects the amount of air leakage from the lungs. A simple pinhole can withstand a larger pressure challenge than can a visible pleural tear. The number and angle of needle redirections could also widen the pleural hole and change its shape, but we did not observe any association with increased pneumothorax rates.
In our study, lateral pleural puncture and lateral decubitus patient position strongly correlated with a higher pneumothorax rate but not with chest tube placement. Lateral pleural puncture and lateral decubitus position did not influence pneumothorax rate independently, because most of the patients with a lateral puncture site underwent biopsy in the lateral decubitus position. To our knowledge, lateral pleural puncture has not previously been mentioned in the literature, although Miller and colleagues (10) demonstrated a higher pneumothorax rate with an anterior needle approach in six of 50 biopsies. Differences in pneumothorax rate with different pleural puncture sites may be secondary to the increased motion of the anterior and lateral chest walls during respiration. In a similar manner, it could be postulated that respiratory motion could increase the risk of pneumothorax during the biopsy of lower lobe lesions; however, we did not demonstrate a higher pneumothorax rate in lower lobe lesions.
Our study results have shown that patients with lesions along the fissure are prone to higher rates of pneumothorax and chest tube placement. The introducer needle did not pass through the fissure in any of the patients in this series; however, the aspiration needle may have unintentionally punctured the fissure.
Our data confirm the association of obstructive lung disease with chest tube placement. The FEV1/VC ratio is the primary parameter for differentiating obstructive from nonobstructive patterns, whereas the severity of airway obstruction is determined with FEV1 (11). Lower FEV1 (12,13), FEV1 percentage (12), and FEV1/VC (12,13) have been associated with higher pneumothorax rates. In our study, patients who received a chest tube had a significantly lower FEV1 percentage, FEV1/VC, and FEV1/VC percentage, although there was no significant correlation with a lower FEV1. All of the patients who had chest tubes and emphysema along the needle path on CT scans also had pulmonary function tests that showed ventilatory obstruction; therefore, the individual contribution of this CT finding was not determined.
The pneumothorax rate was 29% (44 of 150 patients) when only the pneumothoraces visible on chest radiographs were included and 39% when those identified on CT scans alone were included. This falls within the range of 8% (14) to 64% (15) previously quoted in the literature. After being discharged with a small stable pneumothorax, one patient returned 12 hours later with a large pneumothorax. The true incidence of delayed pneumothorax, a pneumothorax enlarging after 24 hours, is unknown. Although it is rare, it can be life threatening and has been reported after transbronchial (16) and transthoracic (17) lung biopsy. Therefore, it is imperative to warn patients who are discharged about the importance of seeking medical attention if shortness of breath or chest pain develops.
In our study, many pneumothoraces, some moderate, did not require evacuation with a chest tube; this may have been secondary to our use of precautionary procedures. These procedures include positioning patients with the puncture site down after biopsy; discouraging talking, coughing, and deep breathing; and administering oxygen through a nasal cavity when a pneumothorax is identified at imaging (18).
There were some limitations to this study. We confirmed that, even in patients with lateral pleural punctures or lateral decubitus positioning, an additional risk was incurred by having a smaller needle-pleural angle and a lesion adjacent to a fissure. However, because of our small sample size, multiple regression analysis could not be performed to assess variables in relation to chest tube placement and to assess some variables in relation to pneumothorax. Measurement of the needle-pleural angle also is subject to variation, in particular for drawing the line tangential to the pleura.
In conclusion, longer dwell times do not correlate with higher rates of pneumothorax or chest tube placement but do correlate with the number of aspirates and core biopsy samples obtained. Therefore, the decision to obtain more aspirates and core biopsy samples should not be influenced by concerns for increasing pneumothorax rate, in particular if there is focal or diffuse pleural thickening, chest wall invasion, or a prior history of thoracic surgery. A smaller needle-pleural angle is associated with a higher rate of pneumothorax. This may be related to elongation or widening of the pleural hole by the needle.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, J.P.K.; study concepts, J.P.K., J.O.S.; study design, J.P.K., J.O.S., E.A.D.; definition of intellectual content, J.P.K., J.O.S., E.A.D., T.C.M.; literature research, J.P.K., E.A.D., J.O.S.; clinical studies, J.P.K., J.O.S., E.A.D., S.L.A., A.S., B.S., T.C.M.; data acquisition, J.P.K., J.O.S., E.A.D., S.L.A., A.S., B.S., T.C.M.; data analysis, J.P.K., E.H.; statistical analysis, E.H.; manuscript preparation, J.P.K.; manuscript editing and review, all authors.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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