Original Research
Chest Imaging
January 2007

Accuracy of Transthoracic Sonography in Detection of Pneumothorax After Sonographically Guided Lung Biopsy: Prospective Comparison with Chest Radiography

Abstract

OBJECTIVE. The purpose of this study was to prospectively evaluate the accuracy of transthoracic sonography in the detection of pneumothorax after transthoracic sonographically guided lung biopsy.
SUBJECTS AND METHODS. Transthoracic sonography was performed on 285 patients after transthoracic sonographically guided lung biopsy. Disappearance of the sliding lung and comettail artifacts and appearance of reverberation artifacts were considered evidence of pneumothorax. Upright chest radiography was performed within 30 minutes of transthoracic sonography. If a discrepancy between transthoracic sonographic and chest radiographic findings occurred, CT was performed. When it was diagnosed, pneumothorax was sonographically monitored. After visualization of resolution of pneumothorax, chest radiography was performed to confirm the resolution.
RESULTS. Pneumothorax occurred in eight (2.8%) of the patients. Transthoracic sonography depicted all cases of pneumothorax and excluded pneumothorax in the other cases. Chest radiography did not depict one case of pneumothorax, which was confirmed on CT. Sensitivity, specificity, positive predictive value, negative predictive value, and overall accuracy were all 100% for transthoracic sonography and 87.5%, 100%, 100%, 99.6%, and 99.6%, respectively, for chest radiography. The 95% confidence intervals (CI) of the differences in sensitivity, negative predictive value, and overall accuracy were -10% to 35%, -0.1 to 0.9%, and -0.1 to 0.9%. Transthoracic sonographic visualization of resolution of pneumothorax was always confirmed with chest radiography.
CONCLUSION. These preliminary results suggest that transthoracic sonography is as effective as chest radiography in the detection of pneumothorax after transthoracic sonographically guided lung biopsy and may become the method of choice for excluding, diagnosing, and monitoring pneumothorax after transthoracic sonographically guided biopsy. Chest radiography may be needed only for assessment of the extent of pulmonary collapse after transthoracic sonographic diagnosis of pneumothorax or in the presence of discrepancy between transthoracic sonographic findings and clinical presentation.

Introduction

The lung is usually considered poorly accessible by sonography. However, transthoracic sonography has been proven to be a useful method for the evaluation of pleural effusions, allowing detection of small volumes of pleural fluid [1, 2]. Transthoracic sonography has emerged as a diagnostic tool in various diffuse and focal pulmonary diseases [2-5] and in pneumothorax and hydropneumothorax [6-8]. Sonographic images of the lung are composed exclusively of artifacts because air prevents transmission of the ultrasound beam, but the artifacts in air-containing lungs differ from those induced by air in the pleural space [6]. In particular, in healthy lungs, respiration-dependent movement of the visceral pleura and lung surface with respect to the parietal pleura and chest wall can be easily visualized with real-time transthoracic sonography. This characteristic is known as lung sliding or the gliding sign [8-10]. At the boundary between the pleura and the ventilated lung, intensive bandlike reverberation echoes (comet-tail artifacts) are evoked during breathing movements [6, 9]. Comet-tail artifacts are generally sporadic in healthy lung and become more numerous in diffuse parenchymal diseases [2, 9]. The presence of air in the pleural space prevents sonographic visualization of visceral pleural movements, and the gliding sign and comet-tail artifacts disappear [2, 9, 10]. In addition, pleural air generates reverberation artifacts that form parallel horizontal echoic lines characterized by artifactual immobility during breathing movements. These artifacts (frozen echoes) are well documented with M-mode imaging [6, 9, 10]. With these main findings, bedside transthoracic sonography is widely used to detect pneumothorax in critically ill patients [11-14]. Conversely, the usefulness of transthoracic sonography in excluding and diagnosing postinterventional pneumothorax has scarcely been investigated. The few reports published are case reports [15] or trials in which a small number of patients were enrolled and conflicting results were obtained [10, 16]. This prospective study was planned to evaluate the accuracy of transthoracic sonography in the detection of pneumothorax after transthoracic sonographically guided biopsy of peripheral pulmonary lesions.
Fig. 1 53-year-old man with lung nodule extending to pleura. Longitudinal sonogram (5-MHz convex probe) of second left anterior intercostal space obtained after thoracic sonographically guided biopsy shows smooth and hyperechoic pleural line, representing pleura-aerated lung interface, and hypoechoic nodule with irregular margins (outline). Under real-time conditions, breath-dependent motion of pleural line (lung sliding) would be seen. One comet-tail artifact (arrows) is present near nodule, reflecting normally aerated lung. Postbiopsy pneumothorax can be excluded.
Fig. 2 66-year-old woman with pulmonary fibrosis. Longitudinal sonogram (5-MHz convex probe) shows irregular, fragmented, thickened pleural line with numerous comet-tail artifacts.

Subjects and Methods

Patients

From January 1999 to June 2005, 288 patients with peripheral lung lesions extending to the pleura consecutively underwent transthoracic sonographically guided biopsy. During a transthoracic sonographic examination performed to assess the best acoustic window for the biopsy, the presence of lung sliding and comet-tail artifacts around the lesion and throughout the healthy parenchyma was assessed, because conditions such as thoracic wall emphysema, pleural adhesions, phrenic paralysis, and bullous emphysema can impair lung excursion and interfere with sonographic visualization of the pleural surfaces [10, 14]. Lung sliding and comet-tail artifacts were not identified in three patients. The other 285 patients (177 men, 108 women; mean age, 57 years; age range, 28-83 years) were enrolled in this prospective study. The study protocol followed the guidelines of our local ethics committee, and informed consent was obtained from all patients.

Study Design

Transthoracic sonographically guided biopsy was performed with an 18-gauge Menghini-modified (SureCut, Hospital Service) or semiautomated Tru-Cut needle (Precisa, Hospital Service). If the lung lesion disappeared during the procedure, systematic sonographic examination of the entire lung was performed immediately after biopsy to assess the presence of pneumothorax, and upright expiratory posteroanterior chest radiographs were obtained within 30 minutes. When necessary, an additional lateral chest radiograph was obtained. If the lesion did not disappear after biopsy, transthoracic sonography and chest radiography were repeated in 3 hours. All sonographic examinations were performed by the same experienced physician well trained in chest sonography. A real-time sonographic system with a 5-MHz convex transducer (SSA-370A, Toshiba Medical Systems) was used. If necessary, a 7.5-MHz linear probe also was used. When pneumothorax was suspected, M-mode images were obtained to document the presence of frozen echoes. All patients were examined in the supine and prone positions. When considered appropriate, the seated position also was used. Transthoracic sonography was performed as a systematic examination of the ventral and dorsal intercostal spaces, starting from the biopsy site. The following parameters were assessed to diagnose or exclude postbiopsy pneumothorax.
The boundary between visceral pleura and lung surface is visualized with transthoracic sonography as an echoic line, the so-called pleural line. Respiration-dependent up-and-down movement of the pleural line with respect to the parietal pleura and chest wall is called lung sliding or the gliding sign and can only be seen under real-time conditions (Fig. 1). Presence of lung sliding excludes pneumothorax.
Comet-tail artifacts become visible when a marked difference in acoustic impedance exists between an object and its surroundings. These artifacts are evoked only at the boundary between the visceral pleura and the aerated lung [9, 10]. It follows that the presence of comet-tail artifacts excludes the diagnosis of pneumothorax. Comet-tail artifacts are best visualized under real-time conditions, but they can be seen on frozen sonograms. These artifacts are sporadic in healthy lung (Fig. 1) and more numerous in diffuse parenchymal disease (Fig. 2).
Fig. 3A 69-year-old man with pneumothorax after transthoracic sonographically guided biopsy of pulmonary nodule. Longitudinal B-mode image (5-MHz convex probe) of right anterior third intercostal space shows horizontal reverberation artifacts. Loss of breath-dependent motion of pleural line is evident.
Fig. 3B 69-year-old man with pneumothorax after transthoracic sonographically guided biopsy of pulmonary nodule. M-mode image corresponding to A shows loss of breath-dependent motion of pleural line as artifactual immobility (frozen echoes).
Fig. 3C 69-year-old man with pneumothorax after transthoracic sonographically guided biopsy of pulmonary nodule. Longitudinal B-mode image obtained after resolution of pneumothorax shows pleural line.
Fig. 3D 69-year-old man with pneumothorax after transthoracic sonographically guided biopsy of pulmonary nodule. M-mode image obtained after resolution of pneumothorax shows breath-dependent movements as single, thin comet-tail artifact (arrow) quite different from frozen echoes of A and B.
When pneumothorax occurs, the presence of air within the pleural spaces prevents full expansion of the lung and generates parallel horizontal reverberation artifacts. The immobility of these artifacts during breathing movements is well documented as frozen echoes on M-mode images (Figs. 3A, 3B, 3C, and 3D).
When pneumothorax is diagnosed on the basis of the absence of the gliding sign and comet-tail artifacts and the presence of reverberation artifacts, the lung point, defined as the border between aerated lung and pneumothorax, is assessed (Fig. 4).
All chest radiographs were obtained within 30 minutes of transthoracic sonographic examination and were interpreted by a radiologist expert in chest radiology. The reviewer was unaware of the transthoracic sonographic findings but was informed about the number of the needle passes necessary to perform the biopsy. Concordance between the results of transthoracic sonography and chest radiography was considered sufficient for a diagnosis of or exclusion of pneumothorax. CT of the chest was performed only if discrepancy was found between the results of transthoracic sonography and chest radiography or between transthoracic sonographic and chest radiographic findings and clinical presentation. We and our ethics committee judged it unethical to expose patients to the ionizing radiation of routine CT when concordance between the two methods and clinical presentation made the likelihood of missed pneumothorax negligible and without consequence for the patient's clinical condition.
If pneumothorax was detected, whether or not it necessitated chest tube drainage, the lung was examined daily with transthoracic sonography. After sonographic visualization of resolution of pneumothorax, upright posteroanterior and lateral chest radiographs were obtained to confirm the resolution.

Statistical Analysis

Estimates of sensitivity, specificity, positive predictive value, negative predictive value, and overall accuracy of transthoracic sonography and chest radiography were calculated. A statistical software program (SPSS 10, SPSS) was used to calculate 95% confidence intervals (CI) based on binomial distribution for sensitivity and specificity of transthoracic sonography and chest radiography and, if present, for the differences observed between transthoracic sonography and chest radiography.

Results

Postbiopsy pneumothorax occurred in eight (2.8%) of 285 patients. In seven cases, pneumothorax was asymptomatic and resolved spontaneously in 1 or 2 days. In one case, pneumothorax necessitated chest tube insertion and drainage for 3 days. In five cases, pneumothorax occurred immediately after biopsy; in three cases, it was documented 3 hours later. Transthoracic sonography correctly depicted all cases of pneumothorax and correctly excluded the presence of pneumothorax in 277 patients. Chest radiographs depicted seven cases of pneumothorax. In one case, transthoracic sonography showed disappearance of the lung lesion immediately after biopsy and depicted the lung point approximately 3 cm from the lesion, but chest radiographs did not depict pneumothorax immediately or 3 hours after biopsy. In this patient, thoracic CT findings confirmed the presence of a small pneumothorax limited to the surroundings of the biopsy site.
In all patients with pneumothorax, transthoracic sonography showed absence of lung sliding and comet-tail artifacts and presence of horizontal reverberation artifacts. The lung point was identified in seven patients, whereas it was not identified in the patient who needed chest tube insertion.
Fig. 4 72-year-old woman with pulmonary fibrosis and postbiopsy pneumothorax (PNX). Sonogram (7.5-MHz linear probe) shows lung point. Horizontal reverberation artifacts (vertical arrows) are interrupted by reappearance of irregular, fragmented, thickened pleural line with comet-tail artifacts (oblique arrows).
The sensitivity, specificity, positive predictive value, negative predictive value, and overall accuracy of transthoracic sonography were 100%. Chest radiography had a sensitivity of 87.5%, specificity of 100%, positive predictive value of 100%, negative predictive value of 99.6%, and overall accuracy of 99.6%. The 95% CIs for sensitivity and specificity of transthoracic sonography were 63-100% and 89.5-100%, respectively; those of chest radiography were 47.3-99.6% and 89.5-100%. The 95% CIs of the differences in sensitivity, negative predictive value, and overall accuracy between transthoracic sonography and chest radiography were -10 to 35%, -0.1 to 0.9%, and -0.1 to 0.9%.
Transthoracic sonographic monitoring of postbiopsy pneumothorax correctly showed resolution of pneumothorax in all cases, depicting reappearance of lung sliding and comet-tail artifacts and disappearance of horizontal reverberation artifacts and frozen echoes. There was 100% concordance with chest radiographic findings

Discussion

Transthoracic needle biopsy is a well-established technique for diagnosing pulmonary lesions, and transthoracic sonographic guidance has been found as effective as CT guidance for lesions in contact with pleura [17-19]. Pneumothorax is the most common complication of transthoracic sonographically guided pulmonary biopsy, the frequency ranging from 1.6% to 5% [18, 20-22]. Chest radiography is routinely performed 3 hours after the procedure to assess development of pneumothorax, but small quantities of intrapleural air can escape detection [10]. CT is the most sensitive method for diagnosing pneumothorax, but it cannot be considered the method of choice in clinical practice because of the high exposure to ionizing radiation, considerable cost, and difficulties arising in transporting patients [10, 14]. Therefore there is increasing interest in alternative techniques in routine postinterventional exclusion of pneumothorax [10, 16] and detection of pneumothorax in trauma and critical illness [11-14].
Sonograms of the lung are exclusively composed of artifacts, but the artifacts generated by healthy lung can differ from those of several pulmonary pathologic conditions [2-5, 9]. Results of some studies [6, 8] have suggested that transthoracic sonography may be useful in the detection of pneumothorax. In particular, disappearance of lung sliding and comet-tail artifacts and detection of horizontal reverberation artifacts have been shown to be reliable signs of pneumothorax. More recent prospective studies [10, 14] confirmed these findings, and we have documented them in 100% of cases of pneumothorax in our study group.
Transthoracic sonography has been reported to have a high negative predictive value in detection of pneumothorax. The positive predictive value may be slightly lower, because a number of coexisting situations can hamper sonographic examination and cause false-positive findings [14]. In particular, bullous emphysema, pachypleuritis with pleural adhesions, and phrenic paralysis may impair lung excursion and prevent visualization of lung sliding, simulating the presence of pneumothorax [10, 14, 23, 24]. In our study, patients were enrolled after prebiopsy sonographic assessment of lung sliding and comettail artifacts, and no false-positive findings were observed after transthoracic sonographically guided pulmonary biopsy. Consequently, to exclude the presence of coexisting conditions that could hamper the diagnostic accuracy of transthoracic sonography, we recommend that preliminary assessment of these signs be performed immediately before patients undergo transthoracic sonographically guided interventional procedures. In this limited number of cases (in our experience, 1%), chest radiography should be preferred to transthoracic sonography.
Transthoracic sonography is considered a promising technique for detection and exclusion of pneumothorax in critically ill and trauma patients [11-14, 25]. Conversely, there are only limited and conflicting data available on the use of transthoracic sonography in the diagnosis of postinterventional pneumothorax. In an early case study, transthoracic sonography depicted two cases of pneumothorax after transthoracic sonographically guided biopsy of peripheral lung lesions [15]. In a subsequent study, however, transthoracic sonography did not depict five of 13 cases of postinterventional pneumothorax [16]. In that study, however, sonographic examination was restricted to the area around the needle entry site, and that methodologic limitation is likely to have hampered the diagnostic accuracy of transthoracic sonography. When transthoracic sonographic examination was extended to the entire anterior chest wall, the sensitivity and specificity of transthoracic sonography were 80% and 94% in an evaluation of pneumothorax after fluoroscopically guided lung biopsy [23]. Reissig and Kroegel [10] studied the accuracy of transthoracic sonography in detection of pneumothorax in 53 patients undergoing transbronchial biopsy or chest tube placement. Conducting systematic sonographic examination of the anterior and posterior intercostal spaces on the side of biopsy or tube thoracostomy, those authors found 100% sensitivity and 100% specificity of transthoracic sonography in the diagnosis or exclusion of postinterventional pneumothorax. Our study design was similar to that of Reissig and Kroegel, and our findings confirm their results but with a substantially larger number of patients. Moreover, our results suggest that transthoracic sonography can be helpful in documenting resolution of pneumothorax, replacing chest radiographic monitoring and avoiding patient exposure to ionizing radiation.
Despite its sensitivity in detection of pneumothorax, transthoracic sonography is not considered a reliable tool for estimating the volume of pneumothorax [14, 26]. Although the size of pneumothorax can be roughly approximated by assessment of the lung point, the depth of pulmonary collapse cannot be evaluated. Chest radiography is necessary to determine the extent of pneumothorax when the lung point is identified far from the biopsy site [10]. For this reason, we did not attempt sonographic estimation of the size of postbiopsy pneumothorax. An interesting finding, however, was that we identified the lung point in all cases of pneumothorax except the one necessitating chest tube drainage. Although anecdotal, this observation also has been reported by other authors [23] and suggests that unsuccessful detection of the lung point may be a sign of deep pulmonary collapse and be an indication for mandatory prompt performance of chest radiography. Further confirmation with a larger number of patients is needed to substantiate such a hypothesis.
Our study had two limitations. First, CT was performed only when discrepancies were found between transthoracic sonographic and chest radiographic findings. Consequently, it is possible, although unlikely, that small, asymptomatic cases of pneumothorax were not detected with both transthoracic sonography and chest radiography and that the diagnostic accuracy of transthoracic sonography was overestimated but without consequence for the patients' clinical conditions. The second limitation was caused by the low prevalence of pneumothorax after transthoracic sonographically guided pulmonary biopsy [18, 20-22]. In our series the prevalence was 2.8%. It follows that despite the large number of patients enrolled, the low number of cases of pneumothorax detected may make the estimate of sensitivity questionable and decrease the ability to generalize the data. This limitation makes evaluation of sensitivity in larger series of cases of pneumothorax mandatory before any definitive conclusion can be drawn.
Despite the limitations, according to several reports [10-14, 23, 25], our results suggest that transthoracic sonography, performed by trained physicians, is an accurate tool for exclusion of the presence of pneumothorax. It is a safe and noninvasive bedside method, is at least as accurate as chest radiography, and does not expose patients to ionizing radiation. Moreover, the technique has been reported to have good interobserver reproducibility when the operators are skilled [23].
If further prospective studies confirm our findings, transthoracic sonography should be considered the method of choice in clinical practice for excluding, diagnosing, and monitoring pneumothorax after transthoracic sonographically guided interventional procedures. Chest radiography may be needed only for assessment of the extent of pulmonary collapse after pneumothorax has been diagnosed with transthoracic sonography and the lung point has been identified far from the biopsy site or in the presence of a discrepancy between transthoracic sonographic findings and the patient's clinical condition.

Footnote

Address correspondence to S. Sartori ([email protected]).

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Information & Authors

Information

Published In

American Journal of Roentgenology
Pages: 37 - 41
PubMed: 17179343

History

Submitted: September 27, 2005
Accepted: December 7, 2005
First published: November 23, 2012

Keywords

  1. biopsy
  2. interventional radiology
  3. lung
  4. sonography

Authors

Affiliations

Sergio Sartori
Section of Interventional Ultrasound, Department of Internal Medicine, St. Anna Hospital, corso Giovecca 203, 44100 Ferrara, Italy.
Paola Tombesi
Section of Interventional Ultrasound, Department of Internal Medicine, St. Anna Hospital, corso Giovecca 203, 44100 Ferrara, Italy.
Lucio Trevisani
Department of Internal Medicine, St. Anna Hospital, 44100 Ferrara, Italy.
Ingrid Nielsen
Department of Internal Medicine, St. Anna Hospital, 44100 Ferrara, Italy.
Davide Tassinari
Division of Oncology, City Hospital, 47900 Rimini, Italy.
Vincenzo Abbasciano
Department of Internal Medicine, St. Anna Hospital, 44100 Ferrara, Italy.

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