http://www.cmaj.ca/cgi/content/abstract/179/12/1293? maxtoshow=&HITS=&hits=&RESULTFORMAT=1&andorexacttitle=and&fulltext=j ogging+and+pregnant+women %27&andorexactfulltext=and&searchid=1&FIRSTINDEX=0&sortspec=relevance&f date=1/1/2005&resourcetype=HWCIT harm http://chestjournal.chestpubs.org/content/133/4/881.

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Ultrasound vs CT in Detecting Chest Wall Invasion by Tumor*

A Prospective Study
1. 2. 3. 4. 5. 6. Venkata Bandi, MD, FCCP, William Lunn, MD, FCCP, Armin Ernst, MD, FCCP, Ralf Eberhardt, MD, Hans Hoffmann, MD, and Felix J. F. Herth, MD, FCCP

+ Author Affiliations 1.
*

From the Baylor College of Medicine (Drs. Bandi and Lunn), Houston, TX; Beth Israel Deaconess Medical Center (Dr. Ernst), Boston, MA; Thoraxklinik (Drs. Eberhardt, Hoffmann, and Herth), University of Heidelberg, Heidelberg, Germany.

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Abstract
Background: Lung cancer is one of the leading causes of cancer-related deaths worldwide. Accurate staging is important for patient management and clinical research. The recognition of chest wall involvement preoperatively is important for staging and surgical planning. Multiple modalities are available to assess the chest wall involvement preoperatively, including CT scanning, MRI, and ultrasound (US) examination. The purpose of this study was to evaluate the sensitivity and specificity of the US examination in determining the chest wall involvement of lung cancer compared to that of CT scan and surgery. Methods: A total of 136 patients with clinical suspicion of chest wall involvement were recruited. Ninety patients met the inclusion criteria and underwent CT scanning, transthoracic US, and surgical exploration. A final determination regarding chest wall involvement was made after reviewing the final pathology results and surgical staging.

Results: Chest wall invasion by tumor was noted in 26 patients during surgery and final pathologic examination of the tissue. Of these patients, US correctly identified 23 patients tumor invasion, while CT scanning identified 11 patients with tumor invasion. There were 3 false-positive results and 3 false-negative results with US examination, compared to 15 false-negative results and no false-positive results with CT scanning. Conclusions: US has better sensitivity (89%) and specificity (95%) in assessing chest wall involvement by a lung tumor compared to CT scan examination (sensitivity, 42%; specificity, 100%).

CT scan lung cancer staging surgery ultrasound

Lung cancer is one of the leading causes of cancer-related deaths in the world, causing more deaths than breast and prostate cancer together.1 the accurate staging of lung cancer is extremely important for patient management and in clinical research. Invasion of the parietal pleura, the subpleural soft tissue, or the bony structure of the chest wall occurs in 5 to 8% of patients with non-small cell lung cancer who are undergoing surgical treatment,23 and alters the TNM classification, staging, and planned treatment approaches.456 Therefore, it is important to determine the extent of disease prior to surgery, as this will directly impact disease management and prognosis. In the small subgroup of patients with pleural-based masses, a distinction needs to be made between tumor invasion of the chest wall or impression on the chest wall due to the proximity of the tumor. Visceral pleural involvement alone constitutes a T2 lesion with a 5-year survival rate of 58%. Those tumors with parietal pleura and or chest wall involvement are staged as a T3 lesion with a 5-year survival rate of 38%. Surgical exploration and examination is the best possible modality to assess for tumor invasion of the chest wall. En bloc resection of lung cancer invading the chest wall is safe but is associated with significant morbidity7 and expense. By knowing the extent of pleural and chest wall involvement preoperatively, the surgical and medical oncology teams can determine the surgical approach, the extent of resection, and the need for chest wall reconstruction.8 The American College of Chest Physicians has published guidelines9 with recommendations for the noninvasive staging of non-small cell cancer. The guidelines recommend MRI of the chest for suspected brachial plexus and vertebral body involvement in cases of superior sulcus tumor. However, they did not identify the best method for evaluating suspected tumor invasion of the chest wall. Until now, CT scanning has been used preoperatively to assess chest wall involvement, but it has a poor sensitivity. Ultrasound (US), MRI, and positron emission tomography may also be used. Because it is dynamic, US may be a better modality for the assessment of chest wall and pleural involvement.10 However, there are no head-to-head studies comparing the diagnostic accuracy of US vs other modalities. We conducted a study

to determine the sensitivity, specificity, and accuracy of US in detecting chest wall involvement by lung cancer compared with CT scanning. Previous SectionNext Section

Materials and Methods

The study was conducted at the Thoraxklinik in Heidelberg, Germany, between January 2003 and November 2005. The study was approved by the institutional review board of the University of Heidelberg and informed consent was obtained from patients. Patients with a diagnosis of lung cancer and suspected chest wall involvement who were able to provide informed consent were prospectively recruited for the study. Patients with suspicion for Pancoast tumor and mesothelioma were excluded. Patients with N3 positive lymph nodes, known metastatic disease, and those who had received neoadjuvant chemotherapy were excluded. Patients with significant comorbidities precluding thoracic surgical intervention were also excluded. All patients underwent thoracic CT scanning (Multislice 4X-scanner; Siemens AG; Berlin, Germany) as a part of their staging workup. A dynamic US examination of the lung and chest wall was performed using a convex transducer probe (3.5 MHz; Hitachi; Ltd, Tokyo, Japan) and high-frequency (5 to 7.5 MHz) linear probes (Hitachi, Ltd) by one of the investigators, all of whom are pulmonologists with expertise in transthoracic and endoscopic US. Each investigator performs hundreds of diagnostic chest US examinations each year. US examination was performed with patients in the supine, sitting, or standing position, depending on the location of the lesion. The lungs and pleura were evaluated in modified longitudinal and oblique intercostal and subcostal transducer application.11 The apex of the lung was examined via the suprasternal, supraclavicular, and infraclavicular approaches. The average duration of such an examination was approximately 15 min. The CT scan was evaluated by the radiologist for signs of chest wall involvement, which was defined as an obtuse angle between the mass and chest wall, the obliteration of extrapleural fat, evidence of tumor growth in to the chest wall, and/or invasion of the ribs by tumor.121314 On transthoracic US examination, the chest wall was deemed to be involved when any two of the following criteria were met: (1) tumor growth into the chest wall; (2) interruption of the pleural reflection; (3) invasion of the ribs; and (4) impairment of movement with respiration. The CT scan and US examinations were performed a few days prior to surgery. The physicians performing thoracic US were blinded to the official reading of the CT scan. The CT scan reports were not available at the time of the US for the US physicians, but the scans themselves were available for review. Radiologists evaluating the CT scans were blinded to the results of the thoracic US. The surgical team had access to the CT scans and the CT scan interpretation, but was blinded to the US data. Patients were followed up through surgery and a note was made of chest wall involvement or the lack thereof intraoperatively. Chest wall involvement or the lack thereof was determined by both intraoperative findings and final pathology. The radiologists and the US physicians were blinded to the results of surgical and pathologic TNM staging data until the completion of the study.

During the study period, 136 patients presented with possible chest wall involvement. Table 1 outlines the patient demographics. Of these, 90 patients underwent surgical resection or exploration. Forty-six patients were excluded from the study due to metastatic disease, positive N3 nodes, comorbidities, lack of informed consent, or the administration of preoperative chemotherapy (Table 2 ). The data were prospectively collected. Data were analyzed using a statistical software package (STATA, version 8.0; Stata Corp; College Station, TX). Sensitivity, specificity, and accuracy were calculated for US and CT scan diagnosis. Paired data were compared with the McNemar test for correlated proportions. A p value of < 0.05 was considered to be significant in all statistical analyses. Previous SectionNext Section

Results
At surgery, chest wall invasion by tumor was found in 26 of 90 patients (the tumor invasion group). Parietal and visceral pleura were not involved in 64 of the 90 patients (the tumor impression group). Tumor invasion data from US examinations, CT scans, and surgery are outlined in Table 3 . Of the 90 patients, CT scans identified 11 patients with tumor invasion and 79 patients with tumor impression. US identified 26 patients with tumor invasion and 64 patients with tumor impression. CT scanning correctly identified 11 of 26 patients as having tumor invasion, with 15 false-negative findings and 11 true-positive findings. US identified 26 patients as having tumor invasion, with 23 true-positive findings, 3 false-positive findings, and 3 false-negative findings. Table 4 outlines sensitivity, specificity, and accuracy data. Previous SectionNext Section

Discussion
Chest wall invasion is not a contraindication for surgery. Long-term survival after resection depends on the completeness of resection and absence of mediastinal and distant metastases.8 Numerous studies have evaluated the role of imaging in the diagnosis of chest wall invasion. However, there is no consensus on the best diagnostic approach. Indeed, the latest American College of Chest Physicians guidelines on the noninvasive staging of non-small cell cancer do not address this particular issue.915 Transthoracic US can be performed with any modern US unit including most of the widely available portable US units. A curvilinear probe of 2 to 5 MHz allows the visualization of deeper structures, and the sector scan field allows a wider field of view through a small acoustic window. The chest wall, pleura, and lungs can be quickly surveyed with the curvilinear probe. Once an abnormality has been identified, a high-resolution, linear, high-resolution probe of 7.5 to 10 MHz can provide detailed views of various layers of chest wall, pleura, and peripheral lung abnormalities16 (Fig 1 ). US has also been used for assessing invasion of the chest wall by tumor.171819 US is known to have a variety of uses for the imaging of malignant pulmonary lesions. It

can detect peripheral pulmonary metastases, which appear as multiple, subpleural, echogenic nodules that are 1 to 2 cm in size. Doppler US studies can evaluate vascular flow within lesions and distinguish benign from malignant pulmonary masses.2021 US may be superior to CT scans in the assessment of superior sulcus tumors,22 because visualization of these tumors on CT scans may be limited by the orientation of the scanning plane. Compared with MRI and positron emission tomography scanning, US units are widely available, do not have the added burden of radiation exposure, and provide a dynamic picture. Although US, by virtue of its real-time imaging, is an excellent tool for the detection of chest wall invasion (Fig 2 , 3 ), it has been underutilized because of better access to newer generation CT scanners and MRI devices. In 1988, Sugama and colleagues23 were the first to report the use of thoracic US in 65 patients with lung cancer with suspected chest wall invasion. In this study, they found an overall diagnostic accuracy of 77% with US, compared to a historical CT scan accuracy of 39%. Later that year, Saito and colleagues24 reported that US-guided needle aspiration can be utilized to evaluate and diagnose chest wall tumors. Suzuki et al25 retrospectively reviewed the charts of 120 patients who underwent CT scanning, US studies, and surgical exploration over a period of 9 years. They reported sensitivities of 100% and 68%, respectively, for US and CT scanning. This study is the first prospective investigation evaluating CT scanning and thoracic US in detecting chest wall invasion by lung cancer and comparing it to the gold standard, surgical evaluation. Unlike the study by Suzuki et al,25 this study was completed in a relatively short period of time, and there are no missing data points. The accuracy of US is comparable to that of the few smaller published studies. The sensitivity is significantly better than that of CT scanning and is comparable to that of MRI. Indeed, Padovani et al26 examined the utility of MRI in detecting chest wall invasion by bronchogenic carcinoma in 34 patients, and reported a sensitivity of 90% and a specificity of 86%. In the present study, US was falsely positive for chest wall invasion in three instances. In all three cases, dense adhesions, which were discovered intraoperatively, may have interfered with the assessment of pleural movement during the US examination. In three patients, the US finding was falsely negative. An adequate acoustic window is needed for the proper and thorough examination of the chest wall and pleura by US. Because of the tumor locations (two located behind the scapula and one in a paravertebral location) and proximity to nonconducting bone, all three false-negative examinations had poor acoustic windows. Interestingly, the sensitivity of CT scanning for the detection of chest wall invasion in this study is 42%, which is comparable to those of previously published studies.27 Thin-section CT scanning with multiplanar image reconstruction was shown to improve sensitivity to approximately 70% in a small trial28 assessing chest wall invasion. Our study shows that US is a superior modality for investigating chest wall and pleural invasion by lung cancer. As evidenced by the false-positive and false-negative US examination results, US assessment may be limited in certain situations. Such circumstances include when tumors are located near or behind bone and when other processes, such as adhesions,

interfere with pleural movement. However, the real-time imaging of chest wall and pleural movement in addition to visual evidence of chest wall and/or rib invasion likely account for the increased sensitivity of US compared with CT scanning. We believe that the type of diagnostic chest US examination described herein is certainly well within the capability of the pulmonary medicine clinician to perform and can be valuable in managing patients with thoracic malignancy. Issues of training and credentialing for US are fraught with controversy, and are outside the scope of this discussion. However, it is reasonable to conclude that formal training and proctoring of this technique should take place, either in fellowship training or in postgraduate courses. Our combined experience in teaching house officers has taught us that the learning curve for chest US is steep, with proficiency developing rapidly after approximately 4 h of training followed by 20 proctored examinations. The interested reader is referred to other studies2930 for a more detailed discussion of US training. Since the diagnostic value of any test depends on the prevalence of disease in the population of patients tested, we propose that chest US be employed in patients with suspicion of malignancy known to invade the chest wall, pleuritic or chest wall pain, and abnormal chest radiograph or chest CT scan findings with soft-tissue density extending to the pleura. Our data suggest that such patients, if otherwise deemed to be surgical candidates, should have diagnostic chest US. Those without involvement of the chest wall by US criteria may be referred for surgical resection with more confidence than those who meet the US criteria for involvement of the chest wall. Previous SectionNext Section

Conclusion
US is more sensitive than CT scanning in the evaluation of chest wall invasion and compliments CT scan data. The extension of tumor beyond the parietal pleura into the chest wall can be confidently determined if the mass is seen to breech the pleura, with loss of the movement of the mass with respiration. We hope that more clinicians will start using thoracic US in the near future. Previous SectionNext Section View this table:

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Table 1. Patient Demographics View this table:

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Table 2. Reason for Exclusion View this table:

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Table 3. Tumor Invasion vs Impression View this table:

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Table 4. Comparison of CT Scanning, US, and Surgery in the Assessment of Chest Wall Invasion*

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Figure 1. Image obtained with a linear probe revealing various chest wall layers, pleura, and aerated lung. In real time, one can visualize the pleura gliding back and forth with respirations.

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Figure 2. CT scan and US images of lung cancer. Top, A: CT image revealing a mass in the left upper lobe. Bottom, B: one can visualize the loss of the visceral and parietal pleural reflections and the mass invading the chest wall.

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Figure 3. CT scan and US images of a left upper lobe mass. Top, A: CT scan detailing an anterior segment mass. Bottom, B: US image revealing tumor invasion of the chest wall. Previous SectionNext Section

Footnotes

Abbreviation: US = ultrasound All work was performed at Thoraxklinik, University of Heidelberg, Heidelberg, Germany. Dr. Lunn has taught ultrasound courses that were partially supported by manufacturers of ultrasound equipment including SonoSite and Hitachi. Dr. Ernst has directed and taught ultrasound courses that were partially supported by manufacturers of ultrasound equipment including SonoSite and Hitachi. Dr. Herth has directed and taught ultrasound courses that were partially supported by manufacturers of ultrasound equipment including SonoSite and Hitachi. Drs. Bandi, Eberhardt, Hoffmann have reported to the ACCP that no significant conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.
o o

Accepted September 15, 2007. Received July 3, 2007.

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