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European Journal of Radiology 53 (2005) 463–470

Accuracy of transthoracic sonography in excluding post-interventional


pneumothorax and hydropneumothorax
Comparison to chest radiography
Angelika Reißig∗ , Claus Kroegel
Pneumology & Allergology, Department I, Medical University Clinics, Friedrich-Schiller-University, Erlanger Allee 101, D-07740 Jena, Germany

Received 13 February 2004; received in revised form 15 April 2004; accepted 19 April 2004

Abstract

Objective: Transthoracic sonography (TS) has evolved as an important imaging technique for diagnosing pleural and pulmonary conditions.
However, the value of TS in either excluding or diagnosing pneumothorax is still under debate. This study was conducted to examine whether
TS could replace chest radiography for the diagnosis of post-interventional pneumothorax and hydropneumothorax.
Methods: 53 patients (21 females, 32 males; median age 64 years, range 37–94 years), 35 of whom underwent transbronchial biopsy (TBB)
and 18 patients who had an ultrasound-guided chest tube placement (U-GCTP) were enrolled in the study. TS was performed three hours
after either TBB or removal of a chest tube, followed by postero-anterior chest radiograph (CRX). If any discrepancy between TS, the clinical
presentation and the CRX became apparent, either a lateral CRX or a computed tomography (CT) of the thorax was performed. TS was
assessed according to the presence of the following criteria: (1) “gliding sign” of the pleural line, (2) comet tail artifacts, (3) reverberation
artifacts, (4) air/fluid mirror, (5) hyperechoic reflectors within the pleural effusion and (6) “lung point”.
Results: In four out of the 53 patients (7.5%) a post-interventional pneumothorax or hydropneumothorax occurred. One out of the 35 patients
(2.9%) developed a pneumothorax after TBB, requiring chest tube placement. Three patients (16.7%) developed a hydropneumothorax due to
U-GCTP which was detected by sonography but was missed by postero-anterior CRX in one patient. The sensitivity, specificity and accuracy
of TS were 100% in excluding post-interventional pneumothorax/hydropneumothorax.
Conclusion: TS is a cost-effective and safe bed-side-method, allowing for an immediate exclusion or diagnosis of post-interventional pneu-
mothorax/hydropneumothorax in patients who have undergone TBB or U-GCTP. Thus, these preliminary results suggest that CXR may only
be required in patients with pneumothorax diagnosed by TS in order to assess its extension or to exclude any discrepancy between the TS-result
and the clinical presentation.
© 2004 Elsevier Ireland Ltd. All rights reserved.

Keywords: Pneumothorax; Hydropneumothorax; Transthoracic sonography; Transbronchial biopsy; Ultrasound-guided chest tube placement; Comet tail
artifacts

1. Introduction appropriate treatment or observation is required. Since most


post-interventional pneumothoraces develop within three
Transbronchial biopsy (TBB) during bronchoscopy as hours, a routine X-ray of the chest in expiration is usually
well as ultrasound-guided chest tube placement (U-GCTP) performed after this interval. However, a postero-anterior
may be complicated by a post-interventional pneumothorax, chest radiograph (CXR) will only show a large pneumotho-
irrespective of a correctly performed manipulation. This rax, whereas a small quantity of intrapleural air, especially
complication occurs in about 5.5% of the patients after TBB in supine patients, can escape detection. Thus, an additional
under X-ray-control [1] and in about 2.5 to 13.9% of the lateral view or even a computed tomography (CT) may be
patients after ultrasound-guided thoracentesis [2]. Depend- occasionally required.
ing on the volume of the intrapleural air, an immediate and To date, CT is considered the most sensitive method for
diagnosing both a pneumothorax or a hydropneumothorax.
∗ Corresponding author. Tel.: +49 3641 939 625; However, due to the potential risks associated with the ex-
fax: +49 3641 939 326. posure to ionising radiation, together with the considerable
E-mail address: angelika.reissig@med.uni-jena.de (A. Reißig). costs of the procedure, as well as the difficulties arising in

0720-048X/$ – see front matter © 2004 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.ejrad.2004.04.014
464 A. Reißig, C. Kroegel / European Journal of Radiology 53 (2005) 463–470

transporting the patient, CT is not the method of choice for formed for further clarification. The study protocol followed
diagnosing pneumothorax. Thus, alternative methods that the guidelines of the local ethics committee. Informed con-
could substitute for radiological techniques in routine post- sent was obtained from all patients enrolled in the study.
interventional exclusion of pneumothorax are called for.
Transthoracic sonography (TS) has proved to be an ex- 2.3. Transthoracic sonography
tremely useful method for the evaluation of pleural effu-
sion and as a guidance for thoracentesis. In recent years, All patients underwent transthoracic examination using a
this technique has emerged as a diagnostic tool in vari- 5 MHz convex scanner (AU5 Harmonic, Esaote Biomedica;
ous pulmonary, pleural, and mediastinal conditions such as Munich, Germany), regularly supplemented by examina-
pulmonary embolism, carcinoma of the lung and diffuse tion with power colour Doppler mode, occasionally supple-
parenchymal lung disease [3–7]. Its main drawback is that mented by a 7.5 MHz linear scanner. Transthoracic sonogra-
the healthy lung parenchyma cannot be penetrated and im- phy was performed by an experienced pneumologist trained
aged by sonography. However, since the ultrasound pattern in chest sonography. The patients were examined in a seated
of the air-containing lung differs from the artifacts induced position from the anterior and the posterior aspect of the
by air within the pleural space [8], the diagnosis of pneu- chest. Selected sonographic images of major abnormalities
mothorax may be revealed by sonography. On the basis of were recorded on photographic film. Sonography was con-
these observations, the present prospective study was car- ducted via a systematic examination of the intercostal spaces
ried out to investigate the potential diagnostic value of TS at the biopsy or tube thoracostomy side. The sonographic
in post-interventional pneumothorax or hydropneumothorax findings of the left and right lung were compared. Further,
on a pneumological ward. the breath-dependent motion of the pleural line was care-
fully evaluated for about five respiratory cycles.
The following criteria were assessed for TS excluding
2. Materials and methods pneumothorax: (1) presence of “gliding sign” or “lung
sliding” of the pleural line and (2) presence of comet tail
2.1. Patients artifacts (CTA). When required, “lung sliding” was further
reviewed using power colour Doppler imaging, the so-called
A total of 53 consecutive patients (21 females, 32 males; “power slide”.
median age 64 years, range 37–94 years) were enrolled In addition, the following criteria were assessed for TS,
in this prospective study. Thirty-five patients underwent suggesting the presence of pneumothorax/hydropneumo-
transbronchial biopsy during bronchoscopy (16 females, 19 thorax: (3) occurrence of reverberation artifacts, (4) presence
males; median age 63 years, range 48–79 years). Eighteen of an air-fluid mirror, (5) presence of hyperechoic reflectors
patients (5 females, 13 males; median age 66.5 years, range within the pleural effusion [8–13] and (6) the “lung point”
37–94 years) were subjected to an ultrasound-guided chest was assessed in case of pneumothorax [14,15]. Furthermore,
tube placement for pleural effusion. Pleural fluid drainage TS was assessed for (7) pleural effusion in all patients.
using a small diameter tube was performed in all of these The diagnostic criteria of TS are defined as follows:
patients. In two of the 18 patients, pleural drainage was
inserted following pleural biopsy. (1) “Gliding sign” or “lung sliding” of the pleural line:
The final diagnosis of all patients (n = 53) enrolled in Under physiological conditions, the visceral pleura and
the study included squamous cell carcinoma of the lung (n lung surface form an echoic line, the so-called “pleu-
= 5), non small cell lung cancer (n = 10), adenocarcinoma ral line”. The respiration-dependent up- and down-
of the lung (n = 5), small cell lung cancer (n = 3), cervical movement of the “pleural line” is called “gliding sign”
carcinoma of the uterus (n = 1), squamous cell carcinoma of or “lung sliding”. This sign needs to be demonstrated
the upper jaw (n = 1), breast cancer (n = 1), ovarian cancer under real-time-conditions (Fig. 1A).
(n = 1), chronic pneumonia (n = 9), bronchiolitis obliterans “Power slide”: “Lung sliding” is made visible via
organising pneumonia (n = 2), congestive heart failure (n power colour Doppler imaging [14] (Fig. 1B).
= 5), aspergilloma (n = 2), empyema (n = 1), idiopathic (2) Presence of comet tail artifacts (CTA): CTA become
pulmonary fibrosis (n = 6), and leukemia (n = 1). visible when a marked difference in acoustic impedance
between an object and its surroundings exists, demar-
2.2. Study design cating the edge of the aerated normal lung [16]. These
artifacts are best visible under real-time conditions,
Three hours after transbronchial biopsy or removal of the since often their appearance is less striking on frozen
chest tube, respectively, the patients first underwent sono- sonograms. CTA are only generated by an intact lung
graphic examination followed by a clinical examination and surface. Thus, the presence of CTA excludes a pneu-
lastly a postero-anterior CRX. If any discrepancy between mothorax (Figs. 2 and 3).
TS, clinical presentation and result of the CRX became ap- (3) Occurrence of reverberation artifacts: Pneumothorax
parent, a CRX in a lateral view or a thoracic CT was per- is defined as the presence of air within the pleural
A. Reißig, C. Kroegel / European Journal of Radiology 53 (2005) 463–470 465

Fig. 2. Comet tail artifacts, sonogram (linear scanner) in idiopathic pul-


monary fibrosis in a 62-year-old woman with established idiopathic pul-
monary fibrosis. Examination with a linear scanner revealed an irregular,
fragmented and thickened pleural line with numerous comet tail artifacts.

Fig. 3. Reverberation-artifacts, sonogram (linear scanner) in a patient


with pneumothorax. Comparison to the unaffected contralateral lung.
Pneumothorax in a 65-year-old woman following transbronchial biopsy
for idiopathic pulmonary fibrosis. On the left side, a thickened, irregular
pleural surface with comet tail artifacts reflecting the interstitial lung
disease is seen. In contrast, on the contralateral side no comet tail artifact
Fig. 1. (A) “Gliding sign”, sonogram (linear scanner) in a patient with
can be detected, since reverberation-artifacts are present. Under real-time
unaffected pleura. The sonogram reveals a normal lung surface with a
conditions, the loss of the breath-dependent motion of the pleural line
smooth and regular hyperechoic “pleural line”. One single comet tail arti-
could be demonstrated.
fact is detectable reflecting a normally aerated lung. Under real-time con-
ditions, the breath-dependent motion of the pleural line can be seen (“glid-
ing sign”). (B) “Power slide”, sonogram (convex scanner supplemented
by power Doppler mode) in a patient with unaffected pleura. The sono- ral effusion may also become visible as hyperechogenic
gram shows a normal lung surface. Under real-time conditions, the power reflectors within the effusion [10,13] (Fig. 5).
colour Doppler signal along the pleural line reveals a breath-dependent (6) The “lung point”: In pneumothorax, the border be-
movement of the lung (“Power slide”).
tween aerated lung and pneumothorax is depicted as
“lung point” [15] (Fig. 6).
space preventing full expansion of the lung. The pleural (7) Pleural effusion: The presence of pleural effusion (E)
air generates reverberation artifacts that form parallel is demonstrated as an echo-poor or echo-free space
horizontal echoic lines (Fig. 3). between the pleura visceralis and parietalis, and is best
(4) Air-fluid mirror: In case of a hydropneumothorax an visible above the diaphragm (Fig. 7).
air/fluid level may develop, with air accumulating in
the upper zones of the thoracic cavity. The horizontal 2.4. Chest radiograph
line of the air/fluid-level has been designated as the
air-fluid mirror [10,13] (Fig. 4). Directly following a sonographic examination, all patients
(5) Hyperechoic reflectors: Air inclusions within the pleu- underwent a postero-anterior chest radiograph (Vertix Poly-
466 A. Reißig, C. Kroegel / European Journal of Radiology 53 (2005) 463–470

Fig. 4. Air-fluid mirror, sonogram (convex scanner) in a patient with Fig. 5. Hyperechoic reflectors within the effusion, sonogram (convex
a hydropneumothorax. The 58-year-old woman suffered from pleural scanner) in a patient with hydropneumothorax. The 77-year-old woman
effusion due to non small cell lung cancer. During the removal of the suffered from pleural effusion due to non small cell lung cancer. The
effusion, the sonogram revealed an air-fluid mirror that is suggestive of sonogram shows hyperechoic reflectors within the effusion representing
hydropneumothorax. hydropneumothorax.

2.5. Spiral computed tomography


dros SX 80, Siemens, Erlangen, Germany and Optimus Didi,
Philips, Hamburg, Germany). When necessary, an additional If any discrepancy between the results obtained from chest
CRX in a lateral view was obtained. CRX was interpreted sonography, clinical presentation and the CRX was present,
by an expert in chest radiology who was unaware of the re- a CT (Somatom Plus 4, Siemens, Erlangen, Germany) of the
sults obtained by TS. thorax was carried out for clarification purposes.

Fig. 6. “Lung point”, sonogram (linear scanner) in a patient with pneumothorax. The sonogram reveals the “lung point”, the border between aerated lung
and pneumothorax (arrow).
A. Reißig, C. Kroegel / European Journal of Radiology 53 (2005) 463–470 467

Table 1
Exclusion and depiction of pneumothorax and hydropneumothorax by
transthoracic sonography and postero-anterior chest radiography in 53
patients who underwent transbronchial biopsy (n = 35) and ultrasound-
guided tube thoracostomy (n = 18)
Patients (n = 53) Transthoracic Postero-anterior
sonography chest radiography
Without pneumothorax (n = 49) 49/49 49/49
With pneumothorax (n = 1) 1/1 1/1
With hydropneumothorax (n = 3) 3/3 2/3a
a In one case after positive findings by sonography, an additional CRX

in a lateral decubitus view was necessary to detect hydropneumothorax.

mirror (Fig. 4), which was detected by sonography during


fluid removal by means of a chest tube. In contrast, the
Fig. 7. Pleural effusion, sonogram (convex scanner): pleural effusion is postero-anterior chest radiograph did not depict a hydrop-
demonstrated as an echo-tree space between the pleura visceralis and neumothorax in this patient. Therefore, an additional lateral
parietalis, best visible above the diaphragm. A colour signal appears within
decubitus CRX was performed which confirmed the hydrop-
the fluid depending on respiratory and cardiac cycles. The sonogram also
shows an atelectasis (arrow). neumothorax diagnosed by sonography (Table 1). In all pa-
tients, there was no further necessity for performing CT for
any discrepancy between clinical presentation, chest sonog-
2.6. Statistics raphy and result of the CRX.
For thoracic ultrasound, a sensitivity of 100% (49/49), a
Data are given as percentage. The sensitivity, specificity specificity of 100% (4/4) as well as an accuracy of 100%
as well as accuracy of TS for diagnosing pneumotho- (53/53) were calculated in excluding post-interventional
rax/hydropneumothorax were calculated. pneumothorax/hydropneumothorax. In contrast, postero-
anterior CRX showed a sensitivity of 98% (48/49), a speci-
ficity of 100% (3/3) and an accuracy of 96.3% (51/53).
3. Results
3.1. Sonographic findings in TBB patients
In four out of the 53 patients (7.5%), a post-interventional
pneumothorax or hydropneumothorax was observed. One of Among the 35 patients who underwent TBB only one
the 35 patients (2.9%) who had undergone TBB developed (2.9%) developed pneumothorax. In this patient, the loss
a pneumothorax measuring approximately 20% of the tho- of “gliding sign”, “lung sliding” and comet tail artifacts
racic volume. A chest tube was inserted over a period of 4 were evident on sonography. However, neither pleural
days to remove the air from the pleural space and ensure effusion nor an air/fluid mirror was detected. Multiple re-
full extension of the lung. In these patients, pneumothorax verberation artifacts within the region of pneumothorax
was correctly diagnosed by TS (Fig. 3) as well as by CRX were observed and the “lung point”, i.e. the checkpoint to
(Table 1). In the remaining 34 out of 35 patients (97.1%), the aerated lung, was assessed. In a second patient suf-
pneumothorax was correctly excluded by means of TS. fering from pneumonia, pleural effusion was detected on
In the 18 patients in whom ultrasound-guided chest tube sonography.
placement was performed, there were no cases of pneu- In all other patients without a pneumothorax, the breath-
mothorax, but three patients developed a hydropneumotho- dependent motion of the pleural line (“gliding sign” or
rax (16.7%) (Fig. 5), which could be detected by TS. Only “lung sliding”) could be clearly demonstrated. Moreover,
one of these three patients was symptomatic, complaining of a small number of comet tail artifacts were also observed
nocturnal pleuritic pain. Another patient revealed an air/fluid (Table 2).

Table 2
Sonographic criteria in patients without pneumothorax, with pneumothorax and with hydropneumothorax, who underwent transbronchial biopsy (n = 35)
and ultrasound-guided tube thoracostomy (n = 18)
“Gliding sign”/ Comet tail Reverberation Air-fluid Hyperechoic reflectors “Lung Pleural
“power slide” artifacts artifacts mirror within the effusion point” effusion
Without pneumothorax (n = 49) 49/49 47/49 0/49 0/49 0/49 0/49 15/49
Pneumothorax (n = 1) 0/1 0/1 1/1 0/1 0/1 1/1 0/1
Hydropneumothorax (n = 3) 0/3 0/3 3/3 3/3 1/3 3/3 3/3
468 A. Reißig, C. Kroegel / European Journal of Radiology 53 (2005) 463–470

3.2. Sonographic findings in ultrasound-guided chest tube risk of developing a post-interventional hydropneumotho-
placement patients rax irrespective of a correctly performed ultrasound-guided
procedure.
Among the 18 patients who underwent tube thoracostomy, The lung is usually considered poorly accessible to ultra-
none developed a pneumothorax. However, in three patients sound. Indeed, the ultrasound image is herein exclusively
(16.7%) a hydropneumothorax was depicted in association composed of artifacts, because air prevents the transmis-
with persistent pleural effusion. In these patients, at least one sion of the ultrasound beam. However, as a vital organ the
air/fluid mirror as well as the loss of the “gliding sign” and respiration-dependent movement of the visceral pleura sur-
comet tail artifacts within the area of hydropneumothorax face along the parietal pleura synchronous with respiration
were observed. Moreover, hyperechoic reflections within the (“lung sliding”) can be easily visualised by its characteris-
pleural effusion could be detected in one patient (Table 2). tic artifacts [24]. The disappearance of this movement was
The 15 patients without pneumothorax revealed an unim- originally observed in animal and man [8,11,25,26]. Early
paired breath-dependent motion of the pleural line (“gliding sonographic investigations showed that pneumothorax may
sign” or “lung sliding”), and in 14 cases a small pleural ef- be detectable by sonography [8,11]. In these studies, TS
fusion persisted after removal of the chest tube (Table 2). was performed after the diagnosis of pneumothorax had
been established either by X-ray or CT. In contrast, the
present investigation was performed prospectively with the
4. Discussion radiological images being performed after obtaining the
sonographic findings.
To date, the method of choice for the exclusion of a post- The most characteristic sonographic alterations associ-
interventional pneumothorax is an erect expiratory CRX per- ated with pneumothorax are the occurrence of reverberation-
formed approximately 3 h following the diagnostic proce- artifacts, which are defined as exclusive horizontal echoic
dure. However, this investigation requires a transport of the lines. In addition, the “lung point” designated as point of dis-
patients to the investigation site, and administration of ion- tinction between aerated lung and area of pneumothorax [15]
ising radiation. In addition, small pneumothoraces may be has proved to be useful as it confirms the existence of a pneu-
missed, and severely ill or traumatised patients can only mothorax and provides an estimate of the size of the lung col-
be radiographed in recumbent position, which makes di- lapse. Further, in patients suffering from diffuse parenchy-
agnosis of a pneumothorax by CRX even more difficult. mal lung disease in whom TBB is often performed another
Because of this, the purpose of this prospective investiga- sign can be applied. When examined by TS, these conditions
tion was to determine the accuracy of transthoracic sonogra- are characterised by the manifestation of multiple CTAs dis-
phy in excluding/diagnosing post-interventional pneumoth- tributed over the whole lung surface and combined with a
orax or hydropneumothorax in patients who underwent di- thickened and irregular and fragmented pleural line [27]. In
agnostic transbronchial biopsy or ultrasound-guided chest pneumothorax, the CTAs disappear. In other words, the de-
tube placement. The results demonstrate, that TS is a non- tection of CTAs excludes the presence of a pneumothorax.
invasive and safe bed-side-method which allows an imme- Although sonographic exclusion of a pneumothorax is
diate exclusion/diagnosis of post-interventional pneumoth- performed with a standard ultrasound unit and equipment,
orax/hydropneumothorax. a few aspects of the examination should be emphasised. A
Pneumothorax or hydropneumothorax are potentially life- 3.5–5 MHz probe in combination with a high-frequent linear
threatening post-interventional complications that need to be transducer (within the 7–10 MHz pulse transmission range)
addressed in daily routine. Prospective studies without direct is preferred. The 5 MHz convex probe yields a clearer image
imaging guidance following thoracentesis revealed an inci- of more distant tissue regions. In contrast, the high-frequent
dence of pneumothorax of between 4.0 and 30.3%, with up to linear transducer allows a more detailed assessment of the
50% of these patients requiring chest tube drainage [17–20]. proximal tissue zones including the chest wall, lung surface
The frequency of pneumothorax for ultrasound-guided tho- and pleura. In addition, TS scan of the unaffected contralat-
racentesis ranged from 2.5 to 13.9%, with less than 1% eral lung is strongly recommended to confirm or exclude
of the patients requiring chest tube drainage [2,21–23]. In the presence of “lung sliding” [28]. This comparison of the
contrast, approximately 5–6% of the patients developed affected site with the respective area of the contralateral un-
a pneumothorax as a complication of transbronchial lung affected lung reduces the risk of missing a pneumothorax
biopsy [1]. In the present study, a comparable rate of post- [29]. Moreover, the position-dependent location of the air
interventional pneumothorax or hydropneumothorax was within the pleural space has to be taken into consideration
observed. Following TBB and transthoracic tube thora- during TS examination. Attention should focus on the upper
costomy, a post-interventional complication developed in part of the lung in seated patients and on the ventral lung
2.9% (1/35 patients) and 16.7% (3/18 patients), respec- regions in supine patients.
tively. Interestingly, in two patients, a hydropneumothorax There are only limited data available on the use of ul-
occurred ex vacuo supporting the previous notion that air- trasound in excluding/diagnosing post-interventional pneu-
way obstruction (i.e. due to tumour occlusion) increases the mothorax. Among the few reports published, no study dealt
A. Reißig, C. Kroegel / European Journal of Radiology 53 (2005) 463–470 469

with pneumothorax as a complication following TBB. Ul- tary CRX would only be required (1) for assessing extent
trasound detection of pneumothorax following computed of the pulmonary collapse or (2) under conditions of dis-
tomography-guided biopsy of pulmonary lesions was inves- crepancy between the TS-result and the clinical appearance.
tigated by Goodman et al. [29]. However, they had failed to However, future prospective studies comparing TS and CRX
detect five of 13 pneumothoraces because areas distant from in a larger number of patients with pneumothorax/hydrop-
the biopsy site were not examined sonographically. These neumothorax are warranted to substantiate our observations.
data suggest that it is insufficient to restrict sonographic ex-
amination solely to the needle entry site.
A prospective study comparing sonographic with radio- Acknowledgements
graphic detection of traumatic pneumothorax on 11 out of
27 patients showed a sensitivity of 100% (36%), a speci- The authors are indebted to N. Kroegel, B.Sc. for review-
ficity of 94% (100%) as well as a positive predictive value ing the manuscript.
of 92% (100%) and a negative predictive value of 100%
(70%), respectively [30]. In contrast, in the present study
a sensitivity of 100% (98%), a specificity of 100% (100%)
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