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Ann Thorac Surg 2005;80:439-442
© 2005 The Society of Thoracic Surgeons


Original article: General thoracic

Preoperative Detection of Pleural Adhesions by Chest Ultrasonography

Masato Sasaki, MD, PhD * , Masakazu Kawabe, MD, Seiya Hirai, MD, Narihisa Yamada, MD, Kouichi Morioka, MD, PhD, Akio Ihaya, MD, PhD, Kuniyoshi Tanaka, MD, PhD

Department of Surgery (II), University of Fukui Faculty of Medical Sciences, Fukui, Japan

Accepted for publication March 4, 2005.

* Addresss reprint requests to Dr Sasaki, Department of Surgery (II), University of Fukui, Faculty of Medical Sciences, 23-3 Shimoaizuki, Matsuoka Fukui, Japan 911-1104 (Email: masato{at}fmsrsa.fukui-med.ac.jp).


    Abstract
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BACKGROUND: The presence of pleural adhesions may render video-assisted thoracoscopic surgery difficult or impossible. The aim of this study was to assess the value of chest ultrasonography in the detection of pleural adhesions prior to thoracotomy.

METHODS: Between October 2001 and September 2002, 42 consecutive patients undergoing thoracotomies (including video-assisted thoracic surgery) were evaluated with chest ultrasonography. These patients underwent a preoperative ultrasonic examination of the chest wall using a 7-MHz linear ultrasound probe at 7 points along the chest wall. We measured the movement of the visceral pleural slide.

RESULTS: When restricted viscera sliding was defined as less than 1 cm of excursion at the upper thoracic wall during exaggerated respirations, ultrasonography demonstrated a sensitivity of 63.6%, a specificity of 79.4%, a negative predictive value of 87.7%, a positive predictive value of 50.0%, and an overall accuracy of 75.6%. When restricted viscera sliding was defined as less than 2 cm of excursion at the lower thoracic wall during exaggerated respirations, ultrasonography demonstrated a sensitivity of 81.5%, a specificity of 81.0%, a negative predictive value of 96.0%, a positive predictive value of 44.0%, and an overall accuracy of 81.0%.

CONCLUSIONS: Chest ultrasonography is moderately accurate in detecting the presence and location of pleural adhesions. Use of preoperative chest sonographic findings to plan trocar placement and to determine the need for an open approach is valuable in helping prevent visceral injury and facilitating video-assisted thoracoscopic surgery.


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Video-assisted thoracoscopic surgery (VATS) has become an important tool for the thoracic surgeon and has gained widespread acceptance. But pleural adhesions between the visceral and parietal pleura prevent the lung from collapsing at the start of thoracoscopy, increase the risk of lung injury from the video-telescope, and in severe cases prevent access to the pleural space, requiring conversion to an open thoracotomy. Therefore, if we can detect pleural adhesions during preoperative evaluation, thoracoscopic surgery is optimized. It is very difficult to evaluate adhesions between the visceral and parietal pleura, even based on pleural thickness on chest computed tomography (CT) [1]. For laparoscopic surgery, there are several reports describing the use of preoperative abdominal ultrasound for detecting peritoneal adhesions based on the excursion of visceral slide [2–5]. It has been determined that a visceral slide less than 2 cm is diagnostic for the presence of adhesion.

However, there are no reports of whether the excursion of the visceral slide can be used to detect pleural adhesions, although there is one report of the use of preoperative ultrasound for detecting pleural adhesions [6]. The purpose of this study was to evaluate the use of preoperative ultrasound mapping of pleural adhesions on the chest wall in order to provide safe initial thoracoscopic access and to guide the placement of subsequent trocars, facilitating VATS.


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Patients
This study was designed as a prospective study. The ultrasound study was performed within 1 week prior to the scheduled surgery. Patients were selected on the basis of two indications. First, all patients were to have surgical procedures that would allow the examination of the pleural space to confirm the presence of pleural adhesions. Second, patients were excluded if they had a history of prior chest surgery. Between October 2001 and September 2002, 42 consecutive patients who were scheduled for a thoracotomy or VATS underwent a preoperative visceral slide ultrasound examination of the chest wall. The patient characteristics are summarized in Table 1. All patients were examined in the sitting position using a 7-MHz linear ultrasound probe at 7 points in intercostal spaces (ICS) during exaggerated respiration. We measured the movement of the visceral pleural slide. Three points were used in the upper thoracic wall. The second ICS in the midclavicular line, the third ICS in the midaxillary line, and the third ICS in the paravertebral line were defined as the upper thoracic wall. Four points were used in the lower thoracic wall. The seventh ICS in the midaxillary line, the fifth ICS in the scapular line, the ninth ICS in the scapular line and the seventh ICS in the midclavicular line were defined as lower thoracic wall (Fig. 1). The ultrasound system used for the viscera slide studies was a LOGIQ500 MR3plus (GE Yokogawa Medical Systems, Tokyo, Japan) 7-MHz array B-mode scanner. A linear-array type of transducer was used to scan the intercostal spaces at a 45 degree angle relative to the longitudinal direction. A distinct focal point in the image of the viscera, usually several hyperechoic points, was observed as the visceral pleura moved during respiration (Fig 2). The distance of the longitudinal excursion of the selected point was measured in relation to the chest wall. An electronic scale on the ultrasound screen was used to measure the exact distance transversed by the focal point. Preoperative scans were interpreted by the consensus read of two thoracic specialists. When we began this study, chest ultrasonography was interpreted by the consensus read of one thoracic surgeon and one radiologist at three patients. Afterwards, this examination was performed by two thoracic surgeons for the remaining 39 patients.


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Table 1. Patient Profiles
 


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Fig 1. Schematic diagram showing the measurement locations of the 7 points for chest ultrasonography.

 


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Fig 2. (A) Chest ultrasonography in the seventh intercostal space in the midaxillary line. The linear-array type of transducer is held at 45 degrees related to the longitudinal direction. (B) Chest ultrasonographic images; the arrow indicates pleura and the triangle indicates the distinct focal point. The distinct focal point in the visceral pleura is observed as it moved during several respirations.

 
Statistical Analysis
The ultrasonographic-predicted and VATS-detected adhesions were used to determine the sensitivity and specificity of ultrasonography for detecting adhesions, using lesion-by-lesion analysis. In lesion-by-lesion analysis, the simple presence or absence of adhesions for each lesion was used to categorize true positive and true negative findings. If adhesions were falsely suggested by sonography, the lesion was categorized as a false positive in the lesion-by-lesion analysis. A false negative finding occurred if one or more adhesions were found during VATS and the sonography revealed no lesions. A true positive finding was recorded if both sonography and VATS demonstrated pleural adhesions. All data are expressed as the mean ± standard deviation. Excursion values were analyzed using the unpaired Student’s t test and a p value less than 0.05 was considered significant.


    Results
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In the first consecutive 32 patients (220 lesions) we compared the excursion of the visceral slide with the findings from operation for every lesion. In the upper thoracic wall, the mean excursion where there was an adhesion was 0.70 ± 0.82 cm (n = 24), and the excursion where there was no adhesion was 1.52 ± 1.00 cm (n = 74, vs 0.70 ± 0.82 cm, p = 0.0006). Restricted visceral sliding in the upper thoracic wall was defined as less than 1 cm of excursion during exaggerated respiration. In the lower thoracic wall, the mean excursion where there was an adhesion was 1.13 ± 0.97 cm (n = 20), and the excursion where there was no adhesion was 2.38 ± 0.90 cm (n = 102, vs 1.13 ± 0.97 cm, p < 0.001). Restricted visceral sliding in the lower thoracic wall was defined as less than 2 cm of excursion during exaggerated respiration. We analyzed the accuracy of visceral sliding in the detection of chest wall adhesions in 43 consecutive patients (322 lesions) based on these results (Table 2). Nine locations could not be assessed due to disagreement between the two thoracic specialists or inability to image the area because of upper extremity immobility. Therefore, 313 lesions were evaluated in this study. In the upper thoracic wall, a total of 33 adhesions were found at VATS in the 15 patients. The detection of adhesions by visceral slide sonography revealed 21 true positive, 12 false negative, 21 false positive, and 81 true negative findings (sensitivity, 63.6%; specificity, 79.4%; accuracy, 75.6%). In the lower thoracic wall, 27 adhesions were found at VATS in 10 patients. The detection of adhesions by visceral slide sonography revealed 22 true positive, 5 false negative, 28 false positive, and 119 true negative findings (sensitivity, 81.5%; specificity, 81.0%; accuracy, 81.0%). The negative predictive value was 87.0% for the upper thoracic wall and 96.0% for the lower thoracic wall.


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Table 2. Results of Visceral Slide Ultrasonography in Detecting Pleural Adhesions
 

    Comment
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Thoracoscopic approaches in thoracic surgery have become extremely popular during the past decade, due principally to the reduced pain and discomfort associated with the operation, as well as the shortened period of recovery. One of the pitfalls of this approach is the possibility of visceral injury during initial trocar placement due to pleural adhesions. Therefore, if we can detect pleural adhesions during preoperative evaluation, the risk of complication during thoracoscopic surgery can be decreased. In a field of laparoscopic surgery, there are several reports of the usefulness of ultrasonography for the evaluation of preoperative peritoneal adhesions [2–5]. Kodama and colleagues [2] reported the usefulness of ultrasonography in the preoperative identification and localization of abdominal wall adhesions prior to laparoscopy or laparotomy. Operations were performed on 18 patients, which confirmed the fact that restriction of ultrasonically detected viscera slide identified abdominal wall adhesions in all cases, but no adhesions were found in patients with normal visceral slide. Furthermore, Kolecki and colleagues [3] reported that only one patient with previous abdominal surgery or a history of peritonitis demonstrated adhesions. The sensitivity and specificity of visceral slide ultrasonography in predicting adhesions are 90% and 92%, respectively. In the field of thoracic surgery, Tateishi and colleagues [6] described the preoperative evaluation of pleural adhesions by ultrasonography and found a sensitivity of 75% and a specificity of 93%. However, that study did not report cutoff values for the pleural excursion. In this study, we demonstrated that there were no adhesions if the pleural excursion was greater than 2 cm in the lower thoracic wall and greater than 1 cm in the upper thoracic wall. The detection of pleural adhesions prior to surgery has received little attention in the radiology literature. Mason and colleagues [1] detected pleural adhesions by chest CT in 1999. This study had a sensitivity of 72% and a specificity of 71% on a patient-by-patient basis and a sensitivity of 46% and a specificity of 38% on a lesion-by-lesion basis. We hypothesize that our better results with sonography may be related to the real-time capability of chest ultrasonography, which is essential in observing the changing contour of the pleura during respiration. The main problem in this study was the presence of false negative findings. Almost all of the false negative lesions had minor adhesions. Therefore, we confirmed the excursion of visceral pleura on chest ultrasonography by slight pleural movement at the time of surgery. We were easily able to perform blunt dissection of these adhesions during VATS. In contrast, most of the false positive results were based on misinterpretations of images of the upper thorax. There are two possible reasons for these misinterpretations. First, these may have occurred because the visceral pleura in the upper thorax is more distant from the diaphragm, and therefore is exposed to less pronounced force, resulting in shorter longitudinal excursions than the visceral pleura in the lower thorax. The sensitivity for detecting adhesions in the upper thorax was lower than in the lower thorax. For example, it was difficult to detect pleural excursion in patients with emphysema or obesity because the pleural excursion is shorter. Second, because we cannot confirm pleural slide in a lesion that does not have a focal point, this can easily become a false negative finding.

In the future, we would like to compare the evaluation of adhesions by chest CT with chest wall ultrasonography. Furthermore, we would like to determine cutoff values for obese patients and patients with pulmonary emphysema. We believe that chest wall ultrasonography is useful for preoperative evaluation of pleural adhesions in patients undergoing thoracoscopic surgery.


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Each month, we select an article from the The Annals of Thoracic Surgery for discussion within the Surgeon’s Forum of the CTSNet Discussion Forum Section. The articles chosen rotate among the six dilemma topics covered under the Surgeon’s Forum, which include: General Thoracic Surgery, Adult Cardiac Surgery, Pediatric Cardiac Surgery, Cardiac Transplantation, Lung Transplantation, and Aortic and Vascular Surgery.

Once the article selected for discussion is published in the online version of The Annals, we will post a notice on the CTSNet home page (http://www.ctsnet.org) with a FREE LINK to the full-text article. Readers wishing to comment can post their own commentary in the discussion forum for that article, which will be informally moderated by The Annals Internet Editor. We encourage all surgeons to participate in this interesting exchange and to avail themselves of the other valuable features of the CTSNet Discussion Forum and Web site.

For August, the article chosen for discussion under the Adult Cardiac Dilemma Section of the Discussion forum is: Early Postoperative Use of Unfractionated Heparin or Enoxaparin is Associated with Increased Surgical Re-Exploration for Bleeding

Heath U. Jones, BS, Joseph B. Muhlestein, MD, Kent W. Jones, MD, Dale G. Renlund, MD, Tami L. Bair, BS, T. Jared Bunch, MD, Benjamin D. Horne, MStat, MPH, Donald L. Lappé, MD, Jeffrey L. Anderson, MD, and Donald B. Doty, MD

Tom R. Karl, MD

The Annals Internet Editor

UCSF Children’s Hospital

Pediatric Cardiac Surgical Unit

505 Parnassus Ave, Room S-549

San Francisco, CA 94143-0118

Phone: (415) 476-3501

Fax: (212) 202-3622

e-mail: mailto:karlt{at}surgery.ucsf.edu


    References
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 Patients and Methods
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  1. Mason AC, Miller BH, Krasna MJ, White CS. Accuracy of CT for the detection of pleural adhesionscorrelation with video-assisted thoracoscopic surgery. Chest 1999;115:423-427.[Abstract/Free Full Text]
  2. Kodama I, Loiacono LA, Sigel B, et al. Ultrasonic detection of visceral slide as an indicator of abdominal wall adhesions J Clin Ultrasound 1992;20:375-380.[Medline]
  3. Kolecki RV, Golub RM, Sigel B, et al. Accuracy of visceral slide detection of abdominal wall adhesions by ultrasound Surg Endosc 1994;8:871-874.[Medline]
  4. Borzellino G, De Manzoni G, Ricci F, Guglielmi A, Laterza E. Ultrasonography mapping of peritoneal adhesions Radiol Med (Torino) 1996;92:390-393.
  5. Borzellino G, De Manzoni G, Ricci F. Detection of abdominal adhesions in laparoscopic surgery. A controlled study of 130 cases Surg Laparosc Endosc 1998;8:273-276.[Medline]
  6. Tateishi U, Morikawa T, Miyasaka K. Detection of pleural adhesions with sonography J Clin Ultrasound 2001;29:61-62.[Medline]



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