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BJA Advance Access originally published online on March 8, 2007
British Journal of Anaesthesia 2007 98(4):442-446; doi:10.1093/bja/aem010
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© The Board of Management and Trustees of the British Journal of Anaesthesia 2007. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org

Transoesophageal echocardiography for the detection and quantification of pleural fluid in cardiac surgical patients

S. J. Capper1, J. J. Ross2, E. Sandström3, P. C. Braidley1 and N. J. Morgan-Hughes1,*

1 South Yorkshire Cardiothoracic Centre
2 University of Sheffield Academic Anaesthetic Unit, Northern General Hospital, Sheffield S5 7AU, UK
3 Department of Anaesthesia, Östersunds Hospital, Östersunds, Sweden

* Corresponding author: South Yorkshire Cardiothoracic Centre, Northern General Hospital, Sheffield S5 7AU, UK. E-mail: nick.morgan-hughes{at}sth.nhs.uk

Accepted for publication January 10, 2007.


    Abstract
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 
Background: Transoesophageal echocardiography (TOE) can image pleural fluid. Left pleural collections may be easier to detect than right, as the thoracic aorta serves as an acoustic window. Attempts to quantify pleural fluid using TOE are restricted to a case report in which volume was predicted by multiplying maximal cross-sectional area (CSAmax) by axial length (AL). A computed tomography (CT) derived formula for quantifying pleural effusions is maximal effusion depth squared (d2) multiplied by maximal effusion length.

Methods: Eight patients were studied before chest closure following coronary bypass surgery. Fifty millilitre saline aliquots were instilled into the pleural space until detected by TOE. Saline was then instilled up to the next 200 ml increment and further 200 ml aliquots added until it spilled from the pleural space. CSAmax, d and AL were measured for each stage and used to calculate pleural fluid volume.

Results: Median detection volume (range) was 125 ml (50–200) on the left and 225 ml (150–300) on the right (P = 0.016). Volume calculated by CSAmax x AL correlated strongly with actual volume (r2 = 0.93 left and 0.92 right) as did volume calculated by d2 x AL (r2 = 0.86 left and 0.89 right). Mean difference between volume calculated by CSAmax x AL and actual volume was – 51 ml on the left and 45 ml on the right vs – 253 ml on the left and – 212 ml on the right for volume calculated by d2 x AL.

Conclusions: TOE detects small volumes of pleural fluid on both sides of the chest. CSAmax x AL provides a reasonably accurate measure of pleural fluid volume.

Keywords: pleural effusion; pleural fluid; monitoring, transoesophageal echocardiography; surgery, cardiac


    Introduction
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 
Transoesophageal echocardiography (TOE) is an established monitoring technique for patients undergoing cardiac surgery. It is primarily used to provide information about cardiac function and guide surgical repair, but has other applications including identifying pleural fluid.

Intraoperatively fluid may accumulate either because of bleeding or the collection of irrigation fluid. Unrecognized pleural fluid can push the lungs up into the operative field and impede surgical access. Pleural fluid can compress lung parenchyma and cause basal atelectasis resulting in impaired gas exchange. An undetected pleural collection may also act as a potential focus for postoperative infection.

Orihashi et al.1 have described the TOE appearances of pleural fluid. When the patient is supine, fluid pools in the dorsal and caudal portions of the pleural space. The TOE probe is inserted ~30 cm from the incisors and a four-chamber view of the heart obtained. To examine the left pleural space, the probe is rotated counter clockwise from the four-chamber view in order to obtain the short-axis view of the descending aorta. The aorta is seen in the near field. In the absence of pleural fluid, the pleural space cannot be visualized because ultrasound is markedly reflected at the surface of the air-filled lung situated adjacent to the aorta. In the presence of fluid, a crescent-shaped, echo-free space, originating in the paraaortic region and extending to the far field is seen. The echo-free space is enclosed by the aorta, lung, and the posterior chest wall. The shape has been likened to a ‘tiger's claw’.2 To examine the right pleural space, the probe is rotated clockwise from the four-chamber view position. During rotation, the image of the right atrium in the four-chamber view moves to the right of the screen and disappears. In the absence of pleural fluid, the right pleural space cannot be seen because the ultrasound is markedly reflected by the lung, which is located adjacent to the oesophagus. Fluid appears as a crescent-shaped, echo-free space adjacent to the transducer enclosed by the lung and posterior chest wall.

The aorta appears to be helpful in visualizing the fluid located in the most dorsal portion of the left pleural space because it acts as an acoustic window. On the right side, it may be more difficult to detect pleural fluid because there is no acoustic window. Figure 1 shows the extent of visualization of the left and right pleural spaces using TOE superimposed on an axial computed tomography (CT) scan. Figure 2 demonstrates the TOE appearances of chronic left and right pleural effusions with associated atelectatic lung.


Figure 1
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Fig 1 Axial CT image of the thorax, cephalad to the diaphragm in a supine patient. Solid lines indicate the extent of visualization when examining the left (L) and right (R) pleural spaces using TOE. Pleural fluid (PF) pooling in the right dorsal pleural space and pulmonary atelectasis (AT) can be seen. The aorta (Ao) and vertebral body (V) are marked.

 


Figure 2
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Fig 2 TOE images demonstrating the ‘tiger's claw’ appearance of chronic left (L) and right (R) pleural effusions. The presence of pulmonary atelectasis (AT) means the full extent of the pleural fluid (PF) is visualized. The aorta (Ao) is marked.

 
Orihashi et al.1 concluded that further studies were needed to examine the quantitative measurement of pleural fluid in relation to TOE findings. The use of transthoracic echo to calculate the size of pleural effusions is described.3 Previous attempts to quantify pleural fluid using TOE are restricted to a single case report.4 In this report, the authors predicted the volume of a right-sided collection by multiplying the maximal cross-sectional area (CSAmax) by the axial length (AL). The ‘gold standard’ for assessment of pleural fluid volume is from three-dimensional (3D) reconstruction using helical CT examinations. Mergo et al.5 demonstrated that the effusion volume calculated as greatest effusion depth squared (d2) multiplied by maximal effusion length accurately correlated with 3D CT reconstruction volume.

The aims of this study were to identify the minimum detection volume of right and left pleural effusions using TOE, to determine whether there is a difference in the minimum detection volume between right and left effusions and to assess CSAmax x AL and d2 x AL as formulae to calculate pleural effusion volume.


    Methods
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 
Local Ethics Committee approval was obtained. The study took place between April 2003 and May 2004. Exclusion criteria were asthma, chest wall or thoracic spine deformity, radiographic evidence of left ventricular dilatation, pleural disease, emphysema or raised hemi diaphragm, hiatus hernia, and pharmacological or mechanical circulatory support. After written informed consent, eight male patients were recruited who were undergoing elective off-pump coronary artery bypass graft surgery. Mean age (range) was 56 yr (39–66). Other mean values (SD) were weight 86 (9) kg, height 178 (4) cm, FEV1 3.1 (0.8) litre and FVC 4.0 (0.9) litre. Intraoperative TOE monitoring pre- and post-grafting was routine.

TOE examination was performed using a Philips SONOS 4500 system with an OmniPlane II probe (Philips Medical Systems, Andover, MA, USA) following induction of anaesthesia, in accordance with current guidelines.6 Both pleura were opened routinely as part of the operative procedure.7 All TOE studies were performed by a single operator.

Protocol
Pleural effusion studies were undertaken following coronary artery bypass surgery immediately prior to chest closure. Intermittent positive pressure ventilation continued with a tidal volume of 7 ml kg – 1, a respiratory frequency of 12 bpm and a positive end expiratory pressure of 5 cm H2O. The fractional inspired oxygen concentration was maintained at 0.6.

A suction catheter was inserted into the left pleural space and any fluid that had accumulated intraoperatively removed. Saline at 37°C was instilled into the left pleural space in 50 ml aliquots until fluid was seen on TOE using the previously described examination technique.1 This initial volume was defined as the detection volume. A two beat echo loop was obtained, with recording timed to onset of expiration, demonstrating CSAmax of the detection volume. The probe depth at which CSAmax was obtained was noted. AL was measured using the centimetre marks on the TOE probe by determining the proximal and distal detection points relative to the patients' teeth. Fluid was then instilled up to the next 200 ml increment and a further two beat echo loop demonstrating CSAmax obtained and the measurements repeated. Further 200 ml increments were instilled and repeat measurements made after each aliquot. Infusion was discontinued, either when saline spilt from the pleural defect, or torsion or displacement of the mediastinum was noted by the surgeon. All the saline was then aspirated from the pleural space. The study sequence was then repeated on the right. CSAmax and d were formally measured by an independent observer using the freeze frame and trace facility on the TOE platform after the study was completed using the stored images. Figure 3 shows examples of the TOE appearances of a left and a right pleural effusion generated during the study.


Figure 3
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Fig 3 TOE images demonstrating the ‘tangerine segment’ appearance of acute left (L) and right (R) pleural effusions. The dotted line marks the circumference of the pleural fluid (PF). The area within the dotted line is the maximal cross-sectional area (CSAmax). The solid line represents the maximal depth of the pleural fluid (d). The aorta (Ao) is marked.

 
Statistical analysis
A sample size calculation suggested that eight patients were required to demonstrate a 100 ml difference between left and right minimum detection volumes assuming an estimated detection volume SD of 70 ml, a power of 80%, and a significance level of P < 0.05. The Wilcoxon signed-rank test was used to compare left and right minimum detection volumes. Linear regression and Bland–Altman8 analysis were used to compare actual with calculated volume of pleural fluid. Bland–Altman plots were constructed by calculating differences as calculated volume minus actual volume instilled plotted against the actual volume.


    Results
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 
Detection volume
The median detection volume (range) was 125 ml (50–200) on the left and 225 ml (150–300) on the right. The detection volume on the left was significantly lower than on the right, P = 0.016. The median depth of probe insertion from the teeth (range), at CSAmax, for the minimum detection volume was 31 cm (27–35) on the left and 31 cm (29–36) on the right.

TOE volumes measured
The total volume infused ranged from 1000–1800 ml on the left and 1000–1600 ml on the right.

Volume calculated from the CSAmax x AL measurements correlated strongly with the actual volumes instilled for both the left and right sides (r2 = 0.93 and 0.92, respectively). Figure 4A and B shows the correlation of actual volume instilled plotted against the calculated TOE volume for the left and the right pleural spaces. Figure 5A and B shows the actual volume instilled plotted against the difference between the calculated TOE volume and actual volume for the left and the right sides. Bland–Altman analysis showed a mean difference (95% CI) between TOE and actual volume of – 51 ml (291 to – 393) on the left and 45 ml (528 to – 439) on the right. Inspection of the Bland–Altman plots revealed a tendency for TOE, using CSAmax x AL, to underestimate at low volume and overestimate at higher volume on both sides.


Figure 4
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Fig 4 Scatter plots showing actual volume of pleural fluid instilled against volume calculated using TOE. (A and B) TOE volume calculated using CSAmax x AL for left and right data, respectively. (C and D) TOE volume calculated using d2 x AL for left and right data, respectively.

 


Figure 5
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Fig 5 Bland–Altman plots showing the actual volume instilled against the difference between calculated TOE volume and actual volume instilled. (A and B) TOE volume calculated using CSAmax x AL for left and right data, respectively. (C and D) TOE volume calculated using d2 x AL for left and right data, respectively. The bold line represents the linear trend. The central dotted line represents mean bias. The upper and lower broken lines represent 95% CI.

 
Volume calculated from d2 x AL correlated with actual volume instilled for both left and right (r2 = 0.86, and 0.89 respectively). Figure 4C and D shows the correlation of actual volume instilled plotted against the calculated TOE volume for the left and the right pleural spaces. Figure 5C and D shows the actual volume instilled plotted against the difference between the calculated TOE volume and actual volume for the left and the right sides. Mean difference (95% CI) between TOE and actual volume was – 253 ml (79 to – 586) on the left and – 212 ml (101 to – 526) on the right. Inspection of the Bland–Altman plots revealed a tendency to underestimate at low volume on both left and right sides. The degree of this underestimate increased as volume increased on the left and decreased on the right.

Axial length
The mean caudad detection point remained relatively constant irrespective of the volume of fluid in the pleural space presumably reflecting the fixed demarcation between thoracic and abdominal cavities. In contrast, the mean cephalad detection point reduced steadily as the volume of fluid increased.


    Discussion
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 
There are a number of limitations to this study. The study design meant that the person obtaining the TOE images was not blinded to the volume of fluid in the pleura. To reduce this potential source of bias, measurements obtained from the images were made offline by an independent observer.

Random chance, and the higher incidence of coronary artery disease in males, resulted in all the patients in this study being male. Inter-sex differences in thoracic anatomy might limit the applicability of this study to female subjects.

This was a small study in terms of patient numbers; however, multiple measurements were taken from each subject as the pleural effusions increased in size. Previous quantitative studies have been based on the assessment of pre-existent effusions where each patient has contributed only one or two data points.3 5 The incremental design of this study meant that although only eight patients were studied, this resulted in many more data points than previous studies. It should be acknowledged, however, that our use of regression analysis fails to take into account the fact that repeated measures of volume were obtained from each patient.

The open pleura in this study meant that the lung tended to float on the pleural fluid. Also the acute onset of the effusion combined with the application of positive end expiratory pressure prevented atelectasis. Atelectasis is necessary to image the tip of the ‘tiger's claw’ as there is lung between the transducer and the fluid. Aerated lung will reflect ultrasound and prevent the full extent of the effusion from being seen. In our patients with open pleura and without atelectasis, the lung tended to float on the fluid and the effusions took on a ‘tangerine segment’ appearance (Fig. 3). A further study would be required to investigate the applicability of the formula CSAmax x AL to patients with chronic effusions and intact pleura. The assessment of other geometric models offers another potential avenue for study.

The formula CSAmax x AL assumes uniform cross-sectional area of collections from diaphragm to apex and that the oesophageal window allows accurate measurement of AL. Clearly, neither of these assumptions is correct. Nevertheless, the formula would appear to offer a clinically useful guide to effusion size, certainly within the context of an open chest and open pleura.

In their original description of pleural fluid, Orihashi et al. concluded that on the right side it is more difficult to detect pleural fluid because there is no acoustic window like the aorta and that fluid needs to accumulate to the level of the oesophagus to be detected by TOE. A study by Chirillo et al.9 to assess the usefulness of TOE in the recognition and management of cardiovascular injuries after blunt chest trauma offered indirect support to this point of view, identifying 39% of patients as having left-sided pleural collections but making no mention of right-sided collections.9 The significantly smaller detection volume on the left side of the chest compared with the right in this study supports the hypothesis that the aorta acts as an acoustic window making effusions easier to see on the left. However, although there is a statistical difference between the minimum detection volumes on the left and the right, this difference is small and unlikely to be clinically relevant. Furthermore, it fails to explain the absence of right-sided collections in the Chirillo study.

There is a greater correlation between actual volume instilled and the volume calculated using the formula CSAmax x AL than using d2 x AL. This is apparent for both left and right effusions. Bland–Altman analysis, certainly in terms of mean bias, also suggests that CSAmax x AL is more accurate in quantifying pleural fluid volume.

In conclusion, we have delineated the minimum volume of pleural fluid that can be detected with TOE on both sides of the chest. We have confirmed that a lesser volume of fluid can be seen on the left side compared with the right, but have also shown that in reality this difference is small and clinically irrelevant. Finally, we have confirmed that multiplying CSAmax by AL provides a reasonable estimate of effusion size, and could be used to guide clinical intervention particularly in the cardiac surgical population.


    Acknowledgements
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 
We would like to thank Dr David Woodward for performing the offline measurements of the TOE images and Dr Edward Casson, of the University of Sheffield Statistical Services Unit for statistical advice.


    References
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 
1 Orihashi K, Hong YW, Chung G, Sisto D, Goldiner PL, Oka Y. (1991) New applications of two-dimensional echocardiography in cardiac surgery. J Cardiothoracic Vasc Anaes 5:33–9.[CrossRef][Medline]

2 Scott DA and Sutton DC. (2003) Image planes and standard views. In Sidebotham D, Merry A, Legget M (Eds.). Practical Perioperative Transoesophageal Echocardiography(Elsevier, Philadelphia) pp. 61–2.

3 Eibenberger KL, Dock WI, Ammann ME, Dorffner R, Hörmann MF, Grabenwöger F. (1994) Quantification of pleural effusions: sonography versus radiography. Radiology 191:681–4.[Abstract/Free Full Text]

4 Swenson JD and Bull DA. (1999) Intraoperative diagnosis and treatment of pleural effusion based on transoesophageal echocardiographic findings. Anesth Analg 89:309–10.[Free Full Text]

5 Mergo PJ, Helmberger T, Didovic J, Cernigliaro J, Ros PR, Staab EV. (1999) New formula for quantification of pleural effusions from computed tomography. J Thorac Imaging 14:122–5.[ISI][Medline]

6 Shanewise JS, Cheung AT, Aronson S, et al. (1999) ASE/SCA guidelines for performing a comprehensive intraoperative multiplane transesophageal echocardiography examination: recommendations of the American Society of Echocardiography Council for Intraoperative Echocardiography and the Society of Cardiovascular Anesthesiologists Task Force for Certification in Perioperative Transesophageal Echocardiography. J Am Soc Echocardiogr 12:884–900.[CrossRef][ISI][Medline]

7 Baumgartner FJ, Gheissari A, Capouya ER, Panagiotides GP, Katouzian A, Yokoyama T. (1999) Technical aspects of total revascularization in off pump coronary bypass via sternotomy approach. Ann Thorac Surg 67:1653–8.[Abstract/Free Full Text]

8 Bland JM and Altman DG. (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1:307–10.[CrossRef][ISI][Medline]

9 Chirillo F, Totis O, Cavarzerani A, et al. (1996) Usefulness of transthoracic and transoesophageal echocardiography in recognition and management of cardiovascular injuries after blunt chest trauma. Heart 75:301–6.[Abstract/Free Full Text]


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This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow All Versions of this Article:
98/4/442    most recent
aem010v1
Right arrow E-Letters: Submit a response to the article
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