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Original Research: Pulmonary Procedures |

Novel Use of Pleural Ultrasound Can Identify Malignant Entrapped Lung Prior to Effusion DrainageIdentification of Trapped Lung With Ultrasound FREE TO VIEW

Matthew R. Salamonsen, MBBS; Ada K. C. Lo, MAppSc; Arnold C. T. Ng, MBBS, PhD; Farzad Bashirzadeh, MBBS; William Y. S. Wang, MBBS; David I. K. Fielding, MD
Author and Funding Information

From the Department of Thoracic Medicine (Drs Salamonsen, Bashirzadeh, and Fielding) and Department of Cardiology (Ms Lo), Royal Brisbane and Women’s Hospital; and Department of Cardiology (Drs Ng and Wang), The Princess Alexandra Hospital, Brisbane, QLD, Australia.

CORRESPONDENCE TO: Matthew R. Salamonsen, MBBS, Department of Thoracic Medicine, Royal Brisbane and Women’s Hospital, Brisbane, Herston 4029, QLD, Australia; e-mail: mattsalamonsen@gmail.com


FUNDING/SUPPORT: Dr Salamonsen was supported by research scholarships from the National Health and Medical Research Council and the RBWH Foundation.

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details.


Chest. 2014;146(5):1286-1293. doi:10.1378/chest.13-2876
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BACKGROUND:  The presence of entrapped lung changes the appropriate management of malignant pleural effusion from pleurodesis to insertion of an indwelling pleural catheter. No methods currently exist to identify entrapped lung prior to effusion drainage. Our objectives were to develop a method to identify entrapped lung using tissue movement and deformation (strain) analysis with ultrasonography and compare it to the existing technique of pleural elastance (PEL).

METHODS:  Prior to drainage, 81 patients with suspected malignant pleural effusion underwent thoracic ultrasound using an echocardiogram machine. Images of the atelectatic lower lobe were acquired during breath hold, allowing motion and strain related to the cardiac impulse to be analyzed using motion mode (M mode) and speckle-tracking imaging, respectively. PEL was measured during effusion drainage. The gold-standard diagnosis of entrapped lung was the consensus opinion of two interventional pulmonologists according to postdrainage imaging. Participants were randomly divided into development and validation sets.

RESULTS:  Both total movement and strain were significantly reduced in entrapped lung. Using data from the development set, the area under the receiver-operating curves for the diagnosis of entrapped lung was 0.86 (speckle tracking), 0.79 (M mode), and 0.69 (PEL). Using respective cutoffs of 6%, 1 mm, and 19 cm H2O on the validation set, the sensitivity/specificity was 71%/85% (speckle tracking), 50%/85% (M mode), and 40%/100% (PEL).

CONCLUSIONS:  This novel ultrasound technique can identify entrapped lung prior to effusion drainage, which could allow appropriate choice of definitive management (pleurodesis vs indwelling catheter), reducing the number of interventions required to treat malignant pleural effusion.

Figures in this Article

Traditionally, the primary treatment of patients with a malignant pleural effusion is pleurodesis.1,2 The most common cause for pleurodesis failure is the presence of lung entrapment by tumor, which restricts expansion of the lung and prevents apposition of the visceral and parietal pleura.3,4 In the presence of entrapped lung, an indwelling pleural catheter (IPC) should be inserted. Currently, there are no methods to identify entrapped lung prior to drainage of a malignant pleural effusion5 and so many patients require more than one procedure for definitive management.

A number of ways exist to analyze the motion of tissue using ultrasonography, which could be used to identify a lung with restricted movement. Motion mode (M mode) quantifies tissue displacement and is widely available on current ultrasound machines.6 A more sophisticated technique, called elastography, quantifies tissue deformation, and expresses it as strain, which is a dimensionless measure of the change in length of a tissue with time.79

We hypothesized that an entrapped lung would less readily transmit the cardiac impulse, resulting in less motion and strain (deformation) as compared with a nonentrapped lung and, furthermore, that this would be identifiable with ultrasonography. This study aims to develop, and examine the diagnostic accuracy of, a method to diagnose entrapped lung using M mode and speckle tracking imaging (STI) strain analysis with pleural ultrasound, prior to pleural effusion drainage.

Study Design

This was a prospective multicenter cohort study, conducted between March 2012 and October 2013. The study was approved by the Human Research Ethics Committee at Royal Brisbane and Women’s Hospital (Queensland, Australia) (approval number: HREC/11/QRBW/452).

Consenting patients undergoing drainage of at least 500 mL for suspected malignant pleural effusion were recruited. The primary outcome was the ability of predrainage M mode and STI to identify entrapped lung as defined by postdrainage radiology and to compare this with pleural manometry.10 Secondary outcomes were the utility of these modalities to predict pleurodesis failure (defined as reaccumulation of the pleural effusion on chest radiograph during the study period) and the identification of factors that increase the chance of false-positive and false-negative results.

Methods

Prior to undergoing effusion drainage, a targeted pleural ultrasound of the ipsilateral lower lobe was performed using an echocardiogram machine (Vivid E9; GE Healthcare), by either a senior echocardiographer or a pulmonologist trained in the use of the cardiac equipment. Following identification of the diaphragm through the posterior chest wall, the probe was moved progressively superior until the first imaging of atelectatic lung was achieved. Cine loops were then acquired during breath hold at functional residual capacity for three or more cardiac cycles.

M Mode and Strain Analysis

M mode and strain analysis were performed offline (EchoPAC version 108.1.5; GE Vingmed, General Electric Co) by an experienced cardiologist, blinded to the clinical and radiologic details of each patient. Strain was measured with STI, a technique developed for assessing myocardial contractility11 (Fig 1). The software calculates the strain in a direction radially outward from the center of a manually inserted region of interest (ROI). To provide data for reliability testing, 20 ultrasound scans were also analyzed by two other doctors (one cardiologist and one pulmonologist) and for a second time by the primary cardiologist (2 months after the initial analysis), providing intertester and test-retest data, respectively.

Figure Jump LinkFigure 1 –  Calculation of myocardial radial strain with speckle tracking imaging (STI). A, Diagram detailing the cross-section of the heart, showing the direction of radial strain measurements (arrows). B, A region of interest (ROI), corresponding to the cross-section of the heart, is placed on the grayscale ultrasound image. C, The software calculates strain in a radial direction and produces six-color traces, corresponding to the six-color-coded areas in the ROI. Strain is expressed as a percentage.Grahic Jump Location
Pleural Manometry

During drainage of the pleural effusion, manometry was performed. Pleural elastance (PEL) was calculated, according to the well-established technique summarized by Feller-Kopman.10

Gold-Standard Scoring of Lung Entrapment on Postdrainage Radiology

The gold standard for the diagnosis of entrapped lung was the consensus opinion of two interventional pulmonologists, using postdrainage radiology and any available clinical details. Patients were allocated to one of five categories: 0, definitely free; 1, probably free; 2, definitely entrapped; 3, probably entrapped; and 4, unable to score (Fig 2).

Figure Jump LinkFigure 2 –  Entrapped lung scoring by radiograph (left images in each panel) and CT scan (right images in each panel). A, Definitely free. Complete apposition of parietal and visceral pleura (arrows). B, Probably free. Apposition of parietal and visceral pleura in most places but some residual pleural fluid (arrows). C, Definitely entrapped. Air separating the visceral and parietal pleura around the lower lobe (arrows) (a chest tube is also seen within the pleural space). D, Probably entrapped. Some air between visceral and parietal pleura in places around the lower lobe but residual pleural fluid obscuring some areas (arrows). E, Unable to score. Insufficient drainage of pleural fluid to allow designation in one of the prior categories (arrows).Grahic Jump Location
Statistical Analysis

Statistical analysis was performed using the computer package SPSS (IBM). All measurements (M mode, STI, PEL) were well approximated by a normal distribution. The probably and definitely categories of the gold-standard diagnosis were grouped so that all patients were classified as entrapped, free, or unable to score. Patients designated as unable to score were excluded from the analysis. The dataset was then randomly divided into a development and validation set by the statistical software. Data from the development set were used to construct receiver-operating curves describing the diagnostic accuracy of M mode, STI, and PEL to identify entrapped lung, and cutoffs were chosen to maximize sensitivity and specificity.12 For PEL, a cutoff of 19 cm H2O was selected, as this is the value most commonly used in the literature.13 Applying these cutoffs to the validation set, the sensitivity, specificity, positive predictive value, and negative predictive value of each method to identify entrapped lung and failed pleurodesis were calculated.

To identify factors associated with false positives (entrapped lung on ultrasound but free lung on postdrainage imaging) and false negatives (free lung on ultrasound but entrapped lung on postdrainage imaging), a multivariate logistic regression model was constructed and applied to the entire dataset. Variables entered were diagnosis, effusion size and side, drainage volume, full or partial atelectasis of the lower lobe, septations visible at ultrasound, left ventricular function, endobronchial obstruction or consolidation of the lower lobe on CT images, and the presence of through-plane motion on the ultrasound cine loops.14 To assess reliability between repeated analyses, mean differences and the intraclass correlation of test-retest and intertester results were calculated.

Eighty-three consecutive patients were recruited for the study; two were excluded as they were designated as not scorable on postdrainage radiology (Fig 2). Fifty-one were men, and the mean age was 66 years (62-70 years) (95% CI). The final diagnosis was pleural malignancy (59%), parapneumonic (8%), heart failure (4%), and other (29%). Mean pleural drainage volume was 1,351 mL (1,194-1,509 mL) (95% CI).

There were 34 patients in the development set and 47 in the validation set. The number of patients in each of the gold-standard diagnostic groups is shown in Table 1.

Table Graphic Jump Location
TABLE 1 ]   Patient Numbers in Gold-Standard Diagnostic Categories

The surrounding effusion provided a clear sonographic window to image the atelectatic lower lobe with ultrasonography. Typical M mode and STI appearances of entrapped and free lung are shown in Figure 3.

Figure Jump LinkFigure 3 –  A-B, Motion-mode (M-mode) analysis of free lung (A) showed greater cardiac-associated motion than entrapped lung (B). C-D, Strain measured with STI was greater for free lung (C) than entrapped lung (D). Note the relationship of movement and strain to the cardiac cycle (ECG). See Figure 1 legend for expansion of other abbreviations.Grahic Jump Location

Receiver-operating curves derived from the development set, demonstrating the diagnostic abilities of STI, M mode, and PEL to identify entrapped lung, are shown in Figure 4. The area under the curve was 0.86, 0.79, and 0.69 for STI, M mode, and PEL, respectively. Results were similar if only the definitely free and definitely entrapped categories of the gold standard were used (STI, 0.88; M mode, 0.76; and PEL, 0.70).

Figure Jump LinkFigure 4 –  Receiver-operating curves derived from the development set for STI (solid line), M mode (dashed line), and PEL (dotted line). AUCs for each methodology are shown. AUC = area under the curve; PEL = pleural elastance. See Figure 1 and 3 legends for expansion of other abbreviations.Grahic Jump Location

Table 2 shows the sensitivity, specificity, positive predictive values, and negative predictive values calculated from the validation set. Cutoffs used to delineate positive from negative results were 6% for STI, 1 mm for M mode, and 19 cm H2O for PEL.

Table Graphic Jump Location
TABLE 2 ]   Diagnostic Indexes to Diagnose Entrapped Lung

M mode = motion mode; NPV = negative predictive value; PEL = pleural elastance; PPV = positive predictive value; STI = speckle tracking imaging.

Twenty-nine patients underwent pleurodesis following complete effusion drainage. The decision of whether to undergo pleurodesis was made by the treating clinician according to clinical information available at the time. Of those who underwent pleurodesis, there was reaccumulation of the pleural fluid in 12. The sensitivity and specificity (using the previous diagnostic cutoffs) to predict pleurodesis failure were 60% and 93% for STI, 60% and 93% for M mode, and 25% and 100% for PEL.

Details of significant variables identified in the multiple regression analysis, which are associated with false-negative (ie, free lung on ultrasound but entrapped lung on postdrainage imaging) or false-positive (ie, entrapped lung on ultrasound but free lung on postdrainage imaging) classifications, are shown in Tables 3 and 4. Reliability was high, with small differences in repeated results and a high intraclass correlation coefficient (Table 5).

Table Graphic Jump Location
TABLE 3 ]   Patient Numbers for Variables Associated With False-Negative or False-Positive Diagnoses

OOPM = out-of-plane motion of the imaged atelectatic lung through the ultrasound image.

Table Graphic Jump Location
TABLE 4 ]   Variables Associated With False-Negative or False-Positive Diagnoses

Incomp Atel = incomplete atelectasis of the imaged lower lobe; Right side = right-sided pleural effusion. See Table 2 and 3 legends for expansion of other abbreviations.

Table Graphic Jump Location
TABLE 5 ]   Test-Retest and Intertester Reliability of Ultrasound Measures

ICC = intraclass correlation coefficient. See Table 2 legend for expansion of other abbreviations.

This study documents a novel approach to the identification of malignant entrapped lung, using preprocedure ultrasonography. M mode and STI strain analysis of the atelectatic lung gave very favorable results for diagnostic parameters, and measurements demonstrated a high level of reliability. Although some features can suggest the presence of entrapped lung (thickening of the visceral pleura at ultrasound, elevated PEL, or basilar pneumothorax on postdrainage imaging), it is often very difficult to detect this important clinical phenomenon prior to effusion drainage. Pleural fluid frequently obscures the visceral pleura, chest radiograph can be inadequate to show isolated entrapment of the lower lobe, and the chronicity of the effusion may not be clear. This new method offers a noninvasive way to reliably identify lung entrapment before any drainage procedure is performed.

The identification of entrapped lung early in the management of malignant pleural effusion could allow for streamlining of patient care directly to insertion of an IPC. In our experience, the appreciation of lung entrapment often does not occur until following the discharge of a patient postpleurodesis, when the effusion and symptoms return. Not only does this delay the appropriate insertion of an IPC, but it also results in an additional procedure. Furthermore, if the patient does not live locally, the opportunity to definitively manage his or her problem may be lost. In line with this, IPCs are becoming more widely used as an upfront treatment option for malignant pleural effusion, however, there are resource issues with IPCs, particularly with follow-up, in those who live remotely and in patients with a life expectancy > 6 weeks.15,16 Better case selection for IPC insertion, confined more to those just with entrapped lung, may lead to improved patient care and resource utilization.

Although this article only addressed the use of these new ultrasound techniques to guide management of malignant pleural effusion, it is possible that with further study, they could be applied to assist in other areas of pleural effusion management, such as thoracentesis (eg, to limit drainage volume in the setting of entrapped lung, preventing symptom development, or a postdrainage pneumothorax ex vacuo) or to indicate when surgery is required in the management of pleural infection.

It is of note that pleural manometry performed less well in this study than elsewhere published as a method to diagnose entrapped lung.17 This highlights one of the key differences between pleural manometry and this new ultrasound technique. PEL reflects the changing pressure within the entire hemithorax, whereas ultrasound analysis is specific to the segment of lung analyzed. In this study, entrapped lung was defined as entrapment of the lower lobe only. In the cases where the other lobes were not entrapped and expanded normally, the impact on PEL would be less marked. We believe this is why pleural manometry, in this study, had a lower sensitivity than in previous publications where lung entrapment was defined as separation of the parietal and visceral pleura throughout the whole hemithorax.17

The amount of displacement and strain of any given piece of lung depends on the magnitude of the force applied to it (in this case from the transmitted cardiac impulse).9 Therefore, the distance of the imaged lung segment from the heart and also how well the lung transmits the impulse could affect strain. Results from the multivariate analysis were consistent with this. The magnitude of displacement and strain was reduced for the right lower lobe compared with the left lower lobe (as the left lower lobe rests closer to the heart) and also if the lung was only partially atelectatic (as aerated lung acts as a capacitor, absorbing some of the kinetic energy from the transmitted cardiac impulse). Both these factors were associated with false-positive results (ie, misclassification of free lung as entrapped). In other areas of the body, this problem is overcome by taking the ratio of the strain in the diseased tissue to that in nondiseased adjacent tissue.18 This has the effect of standardizing the force applied in any given region of the body. This is not possible in the case of atelectatic lung, as there is no adjacent “normal” tissue that is equally distant from the heart (aerated lung cannot be imaged with ultrasound). Another limitation particular to STI is that out-of-plane motion of the atelectatic lung through the two-dimensional ultrasound image affects the measurements.14,19 STI works by tracking clusters of pixels within the image. If the atelectatic lung swings out of plane through the ultrasound image, it is incorrectly analyzed by the software as tissue deformation. This is reflected in its association with false negatives seen on the multivariate analysis (all four patients with entrapped lung and out-of-plane motion on ultrasound were incorrectly classified as free). Three-dimensional STI would overcome this problem.20

Our results could suggest an approach whereby if the ultrasound strongly suggests entrapped lung (strain < 5% [STI] or displacement < 0.8 mm [M mode]), an IPC should be inserted. If the lung is clearly free (strain > 7% [STI] or displacement > 1.2 mm [M mode]), then a pleurodesis is appropriate. However, if the ultrasound analysis is close to the cutoff between free and trapped lung (strain 5% to 7% [STI] or displacement 0.8-1.2 mm), then a chest tube should be inserted and the decision of whether to pleurodese or insert an IPC should be made once postdrainage radiology confirms the presence or absence of entrapped lung. It may be that applying catheter suction is appropriate in these cases.

There are a number of limitations to the design of this study. The identification of isolated lower lobe entrapment can be difficult and some patients may have been misclassified. For a diagnosis of entrapped lung to be made, there had to be air between the visceral and parietal pleura around the lower lobe, in the absence of an air leak through the chest catheter. However, following effusion drainage, sometimes there is initial separation of the visceral and parietal pleura that resolves in time and represents lung that is slow to reexpand but is not entrapped. Furthermore, in some cases, there was incomplete drainage of fluid from the pleural space such that it was not clear if the lung would fully reexpand had the fluid been completely drained. To address this uncertainty, probably entrapped and probably free categories for postdrainage assessment were created. When scoring patients to these categories, the judgers were able to gather other clues to support or reject the presence of entrapped lung, such as thickening of the visceral pleura, volume loss in or mediastinal shift toward the ipsilateral hemithorax, persistence in the shape of the visceral pleural silhouette on chest radiograph predrainage and postdrainage, or the appearance of the lung at pleuroscopy when these images were available. They were also allowed to use any follow-up radiology available at the time of scoring, which in some cases was more than a year following the procedure. Another point of note is that strain analysis, such as that found in many respiratory departments, is not currently available on most portable ultrasound machines. It is, however, quickly finding its place in clinical management and will probably be available as a standard feature on most machines soon.8,9

In summary, this study offers a significant contribution to the assessment of malignant entrapped lung, a clinical entity traditionally difficult to identify prior to pleural effusion drainage. This noninvasive technique may be able to guide decision-making about the timing of pleural interventions and prompt the early insertion of an IPC in cases of malignant entrapped lung. Although there are limitations to this technique that require further investigation to fully elucidate, this study serves as an introduction and “proof of concept.” It could lead to a reduction in the number of procedures required to treat malignant pleural effusion.

Author contributions: M. R. S. takes responsibility for the accuracy of data and manuscript content. M. R. S. contributed to study design and patient recruitment, assisted with ultrasound scans, analyzed data, and wrote the manuscript; A. K. C. L. contributed by performing ultrasound scans; A. C. T. N. contributed to the analysis of the ultrasound images; F. B. contributed to postdrainage radiology scoring; W. Y. S. W. contributed to the analysis of ultrasound images for reliability testing; D. I. K. F. contributed to study design and postdrainage radiology scoring; and M. R. S., A. K. C. L., A. C. T. N., F. B., W. Y. S. W., and D. I. K. F. contributed to the revision and editing of the manuscript.

Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Role of sponsors: The sponsors had no role in the design of the study, the collection and analysis of the data, or the preparation of the manuscript.

IPC

indwelling pleural catheter

M mode

motion mode

PEL

pleural elastance

ROI

region of interest

STI

speckle tracking imaging

Roberts ME, Neville E, Berrisford RG, Antunes G, Ali NJ; BTS Pleural Disease Guideline Group. Management of a malignant pleural effusion: British thoracic society pleural disease guideline 2010. Thorax. 2010;65(suppl 2):ii32-ii40. [CrossRef] [PubMed]
 
Hausheer FH, Yarbro JW. Diagnosis and treatment of malignant pleural effusion. Semin Oncol. 1985;12(1):54-75. [PubMed]
 
American Thoracic Society. Management of malignant pleural effusions. Am J Respir Crit Care Med. 2000;162(5):1987-2001. [CrossRef] [PubMed]
 
Huggins JT, Doelken P, Sahn SA. Intrapleural therapy. Respirology. 2011;16(6):891-899. [CrossRef] [PubMed]
 
Burgers JA. Pleurodesis or not. International Pleural Newsletter. Perth, Australia: International Pleural Network; 2010;:19.
 
Gerscovich EO, Cronan M, McGahan JP, Jain K, Jones CD, McDonald C. Ultrasonographic evaluation of diaphragmatic motion. J Ultrasound Med. 2001;20(6):597-604. [PubMed]
 
Paterson S, Duthie F, Stanley AJ. Endoscopic ultrasound-guided elastography in the nodal staging of oesophageal cancer. World J Gastroenterol. 2012;18(9):889-895. [CrossRef] [PubMed]
 
Sparchez Z. Real-time ultrasound prostate elastography. An increasing role in prost ate cancer detection? Medical Ultrasonography. 2011;13:3-4. [PubMed]
 
Dewall RJ. Ultrasound elastography: principles, techniques, and clinical applications. Crit Rev Biomed Eng. 2013;41(1):1-19. [CrossRef] [PubMed]
 
Feller-Kopman D. Therapeutic thoracentesis: the role of ultrasound and pleural manometry. Curr Opin Pulm Med. 2007;13(4):312-318. [CrossRef] [PubMed]
 
Blessberger H, Binder T. NON-invasive imaging: two dimensional speckle tracking echocardiography: basic principles. Heart. 2010;96(9):716-722. [CrossRef] [PubMed]
 
Akobeng AK. Understanding diagnostic tests 3: receiver operating characteristic curves. Acta Paediatr. 2007;96(5):644-647. [CrossRef] [PubMed]
 
Huggins JT, Sahn SA, Heidecker J, Ravenel JG, Doelken P. Characteristics of trapped lung: pleural fluid analysis, manometry, and air-contrast chest CT. Chest. 2007;131(1):206-213. [CrossRef] [PubMed]
 
Artis NJ, Oxborough DL, Williams G, Pepper CB, Tan LB. Two-dimensional strain imaging: a new echocardiographic advance with research and clinical applications. Int J Cardiol. 2008;123(3):240-248. [CrossRef] [PubMed]
 
Lee YC, Fysh ET. Indwelling pleural catheter: changing the paradigm of malignant effusion management. J Thorac Oncol. 2011;6(4):655-657. [CrossRef] [PubMed]
 
MacEachern P, Tremblay A. Pleural controversy: pleurodesis versus indwelling pleural catheters for malignant effusions. Respirology. 2011;16(5):747-754. [CrossRef] [PubMed]
 
Lan RS, Lo SK, Chuang ML, Yang CT, Tsao TC, Lee CH. Elastance of the pleural space: a predictor for the outcome of pleurodesis in patients with malignant pleural effusion. Ann Intern Med. 1997;126(10):768-774. [CrossRef] [PubMed]
 
Cui XW, Jenssen C, Saftoiu A, Ignee A, Dietrich CF. New ultrasound techniques for lymph node evaluation. World J Gastroenterol. 2013;19(30):4850-4860. [CrossRef] [PubMed]
 
Notomi Y, Lysyansky P, Setser RM, et al. Measurement of ventricular torsion by two-dimensional ultrasound speckle tracking imaging. J Am Coll Cardiol. 2005;45(12):2034-2041. [CrossRef] [PubMed]
 
Saito K, Okura H, Watanabe N, et al. Comprehensive evaluation of left ventricular strain using speckle tracking echocardiography in normal adults: comparison of three-dimensional and two-dimensional approaches. J Am Soc Echocardiogr. 2009;22(9):1025-1030. [CrossRef] [PubMed]
 

Figures

Figure Jump LinkFigure 1 –  Calculation of myocardial radial strain with speckle tracking imaging (STI). A, Diagram detailing the cross-section of the heart, showing the direction of radial strain measurements (arrows). B, A region of interest (ROI), corresponding to the cross-section of the heart, is placed on the grayscale ultrasound image. C, The software calculates strain in a radial direction and produces six-color traces, corresponding to the six-color-coded areas in the ROI. Strain is expressed as a percentage.Grahic Jump Location
Figure Jump LinkFigure 2 –  Entrapped lung scoring by radiograph (left images in each panel) and CT scan (right images in each panel). A, Definitely free. Complete apposition of parietal and visceral pleura (arrows). B, Probably free. Apposition of parietal and visceral pleura in most places but some residual pleural fluid (arrows). C, Definitely entrapped. Air separating the visceral and parietal pleura around the lower lobe (arrows) (a chest tube is also seen within the pleural space). D, Probably entrapped. Some air between visceral and parietal pleura in places around the lower lobe but residual pleural fluid obscuring some areas (arrows). E, Unable to score. Insufficient drainage of pleural fluid to allow designation in one of the prior categories (arrows).Grahic Jump Location
Figure Jump LinkFigure 3 –  A-B, Motion-mode (M-mode) analysis of free lung (A) showed greater cardiac-associated motion than entrapped lung (B). C-D, Strain measured with STI was greater for free lung (C) than entrapped lung (D). Note the relationship of movement and strain to the cardiac cycle (ECG). See Figure 1 legend for expansion of other abbreviations.Grahic Jump Location
Figure Jump LinkFigure 4 –  Receiver-operating curves derived from the development set for STI (solid line), M mode (dashed line), and PEL (dotted line). AUCs for each methodology are shown. AUC = area under the curve; PEL = pleural elastance. See Figure 1 and 3 legends for expansion of other abbreviations.Grahic Jump Location

Tables

Table Graphic Jump Location
TABLE 1 ]   Patient Numbers in Gold-Standard Diagnostic Categories
Table Graphic Jump Location
TABLE 2 ]   Diagnostic Indexes to Diagnose Entrapped Lung

M mode = motion mode; NPV = negative predictive value; PEL = pleural elastance; PPV = positive predictive value; STI = speckle tracking imaging.

Table Graphic Jump Location
TABLE 3 ]   Patient Numbers for Variables Associated With False-Negative or False-Positive Diagnoses

OOPM = out-of-plane motion of the imaged atelectatic lung through the ultrasound image.

Table Graphic Jump Location
TABLE 4 ]   Variables Associated With False-Negative or False-Positive Diagnoses

Incomp Atel = incomplete atelectasis of the imaged lower lobe; Right side = right-sided pleural effusion. See Table 2 and 3 legends for expansion of other abbreviations.

Table Graphic Jump Location
TABLE 5 ]   Test-Retest and Intertester Reliability of Ultrasound Measures

ICC = intraclass correlation coefficient. See Table 2 legend for expansion of other abbreviations.

References

Roberts ME, Neville E, Berrisford RG, Antunes G, Ali NJ; BTS Pleural Disease Guideline Group. Management of a malignant pleural effusion: British thoracic society pleural disease guideline 2010. Thorax. 2010;65(suppl 2):ii32-ii40. [CrossRef] [PubMed]
 
Hausheer FH, Yarbro JW. Diagnosis and treatment of malignant pleural effusion. Semin Oncol. 1985;12(1):54-75. [PubMed]
 
American Thoracic Society. Management of malignant pleural effusions. Am J Respir Crit Care Med. 2000;162(5):1987-2001. [CrossRef] [PubMed]
 
Huggins JT, Doelken P, Sahn SA. Intrapleural therapy. Respirology. 2011;16(6):891-899. [CrossRef] [PubMed]
 
Burgers JA. Pleurodesis or not. International Pleural Newsletter. Perth, Australia: International Pleural Network; 2010;:19.
 
Gerscovich EO, Cronan M, McGahan JP, Jain K, Jones CD, McDonald C. Ultrasonographic evaluation of diaphragmatic motion. J Ultrasound Med. 2001;20(6):597-604. [PubMed]
 
Paterson S, Duthie F, Stanley AJ. Endoscopic ultrasound-guided elastography in the nodal staging of oesophageal cancer. World J Gastroenterol. 2012;18(9):889-895. [CrossRef] [PubMed]
 
Sparchez Z. Real-time ultrasound prostate elastography. An increasing role in prost ate cancer detection? Medical Ultrasonography. 2011;13:3-4. [PubMed]
 
Dewall RJ. Ultrasound elastography: principles, techniques, and clinical applications. Crit Rev Biomed Eng. 2013;41(1):1-19. [CrossRef] [PubMed]
 
Feller-Kopman D. Therapeutic thoracentesis: the role of ultrasound and pleural manometry. Curr Opin Pulm Med. 2007;13(4):312-318. [CrossRef] [PubMed]
 
Blessberger H, Binder T. NON-invasive imaging: two dimensional speckle tracking echocardiography: basic principles. Heart. 2010;96(9):716-722. [CrossRef] [PubMed]
 
Akobeng AK. Understanding diagnostic tests 3: receiver operating characteristic curves. Acta Paediatr. 2007;96(5):644-647. [CrossRef] [PubMed]
 
Huggins JT, Sahn SA, Heidecker J, Ravenel JG, Doelken P. Characteristics of trapped lung: pleural fluid analysis, manometry, and air-contrast chest CT. Chest. 2007;131(1):206-213. [CrossRef] [PubMed]
 
Artis NJ, Oxborough DL, Williams G, Pepper CB, Tan LB. Two-dimensional strain imaging: a new echocardiographic advance with research and clinical applications. Int J Cardiol. 2008;123(3):240-248. [CrossRef] [PubMed]
 
Lee YC, Fysh ET. Indwelling pleural catheter: changing the paradigm of malignant effusion management. J Thorac Oncol. 2011;6(4):655-657. [CrossRef] [PubMed]
 
MacEachern P, Tremblay A. Pleural controversy: pleurodesis versus indwelling pleural catheters for malignant effusions. Respirology. 2011;16(5):747-754. [CrossRef] [PubMed]
 
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    Print ISSN: 0012-3692
    Online ISSN: 1931-3543