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Ann Thorac Surg 1999;68:218-222
© 1999 The Society of Thoracic Surgeons

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Original Articles

Intraoperative ultrasound during thoracoscopic procedures for solitary pulmonary nodules

^a Clinica Chirurgica, Università di Milano, Osp. San Paolo and Ospedale Maggiore, IRCCS, Milano, Italy
^b Istituto di Chirurgia Generale e Oncologia Chirurgica, Università di Milano, Ospedale San Paolo and Ospedale Maggiore, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Milan, Italy

Address reprint requests to Dr Santambrogio, Via Natale Battaglia 34, 20127 Milan, Italy
e-mail: r.sant{at}imiucca.csi.unimi.it

	Abstract

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Background. Traditional nonoperative diagnostic approaches to the solitary pulmonary nodule (bronchoscopy and percutaneous needle biopsy) can be inconclusive. Video-assisted thoracic surgery (VATS) provides a minimally invasive way to diagnose and treat these nodules. We evaluated the use of a dedicated intraoperative ultrasound probe as an aid in localization of small pulmonary nodules during VATS.

Methods. An intraoperative ultrasound examination during a thoracoscopic procedure was performed on 18 patients to localize deep pulmonary nodules less than 20 mm in diameter without a definitive diagnosis by preoperative imaging techniques.

Results. In the 18 patients, all nodules were successfully identified by intraoperative ultrasound. A definitive pathologic diagnosis was obtained from thoracoscopic biopsy or resection. The final diagnoses were primary lung cancer in 5 patients, metastatic lesions in 4 patients, hamartoma or chondroma in 4, granuloma in 3, and interstitial fibrosis in 2 patients.

Conclusions. In our experience, intraoperative ultrasound can safely and effectively localize invisible or nonpalpable pulmonary nodules at the time of thoracoscopy. This may help surgeons perform minimally invasive lung resections with clear surgical margins.

	Introduction

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Over the last 5 years, video-assisted thoracic surgery (VATS) has been performed with increasing frequency. The role of VATS has been expanded to include the diagnosis and management of many intrathoracic pathologic conditions. The solitary pulmonary nodule represents the most common reason to use VATS in the majority of series [1–3]. Most lesions can easily be identified by inspection and tactile evaluation with a gentle instrumental probe [4]. However, in the difficult situation of deep or small lesions, additional techniques to facilitate identification of the nodule at the time of VATS can be required [5]. They include preoperative injection of methylene blue [6], colored collagen [7], and needle localization [8, 9]. However, these techniques carry the risks of pneumothorax, pulmonary hemorrhage, and dislodgment of the hook wire and can require both the computed tomographic facility and the operating room simultaneously [3, 6, 10].

The idea of using intraoperative ultrasound during VATS stemmed from the experience gained during laparoscopic procedures [11–13]. This new imaging technique has made it possible to detect nodules or structures too small to be visualized by other preoperative imaging modalities [14]. Here we present our preliminary results with the clinical application of thoracoscopic ultrasound (TUS) in the localization of small pulmonary nodules during VATS.

	Material and methods

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Since November 1993, TUS has been integrated into the routine preoperative and intraoperative examination protocol for all patients in whom a definitive diagnosis of a pulmonary lesion was not obtained by conventional preoperative techniques. An Aloka SSD-500 instrument (Tokyo, Japan) was used. The probes (either rigid or with a flexible tip) have a linear array transducer with a frequency of 7.5 MHz and are 10 mm in diameter and 50 cm in length (Fig 1). Ultrasonograms were video recorded.

View larger version (80K): [in this window] [in a new window]   Fig 1. Intraoperative ultrasound probe with a linear head of 7.5 MHz.

View larger version (122K): [in this window] [in a new window]   Fig 2. Intraoperative view using thoracoscope shows ultrasound probe over area of suspected pulmonary nodule.

Once the nodule or lymph node was localized, a wedge resection or a biopsy was done. Thoracoscopic biopsies were performed on large-sized lesions or on nodules whose location did not allow easy resection. In these patients, the biopsy was done with an endoscopic microknife or a 16-gauge needle. All specimens were withdrawn after they had been inserted into a retrieval bag. On the basis of the results of frozen section, it was sometimes necessary to proceed with a conventional pulmonary lobectomy.

	Results

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Eighteen patients underwent TUS. There were 12 men and 6 women with a mean age of 63 ± 11 years (range, 28 to 79 years). In 14 patients, the primary indication was localization of a small pulmonary nodule for which the preoperative diagnosis was inconclusive (group 1). In the other 4, besides nodule localization, the indication was suspected involvement of mediastinal organs (group 2).

The patients in group 1 represented 8% of the 181 patients examined in the same period in whom preoperative techniques led to a correct diagnosis of either a malignant or a benign lesion. All patients had plain chest radiography and thoracic computed tomography with contrast enhancement. Six of the 14 patients had undergone percutaneous computed tomographic–guided biopsy of the lesion without diagnostic results. The remaining 8 patients had undergone preoperative fiberoptic bronchoscopy without the establishment of a conclusive diagnosis. Eight patients had no history of previous neoplasm, and 6 had previously been treated for carcinoma of the breast (n = 2), colon (n = 1), stomach (n = 1), kidney (n = 1), or for melanoma (n = 1).

In group 2, the pulmonary nodule was associated with suspected mediastinal masses. Two patients had a small lung cancer with a solitary brain metastatic lesion already treated by surgical resection in 1 and with an apparently complete response to neoadjuvant treatment in the other. In the other 2 patients in group 2, the indication for TUS was an inconclusive diagnosis with preoperative techniques. A young woman had recently undergone surgical resection of a melanoma, and the TUS–guided approach was necessary to obtain an adequate biopsy specimen of a small left hilar lesion for histologic study. A man had a small lesion that was thought to be associated with involvement of mediastinal organs.

The time required for TUS was 10 ± 4 minutes (range, 6 to 20 minutes). No complications occurred as a result of the intraoperative ultrasound technique. A single nodule was found in 14 patients, two nodules were located in 3, and multiple nodules were found in 1 patient. The nodules ranged from 5 to 19 mm in diameter (mean size, 13.9 ± 4.4 mm). All nodules were localized at the time of TUS, and a definitive diagnosis was obtained in all patients. No nodule was superficial, and therefore none were visible by simple thoracoscopic exploration. Further, palpation with the probe suggested but did not prove the exact site of the lesion in 5 patients, and in the other 13, only TUS was able to localize the lesion.

Benign disease was diagnosed in 9 patients, and malignant disease was found in the other 9 patients. The definitive diagnoses were hamartoma or chondroma in 4 patients, granuloma in 3, interstitial fibrosis in 2, primary lung cancer in 5, and metastatic lesions in 4. Six patients with malignant disease required conversion to a muscle-sparing thoracotomy for pulmonary lobectomy. Ten thoracoscopic wedge resections were performed. In the remaining 2 patients, a TUS–guided biopsy confirmed the diagnosis.

In regard to ultrasonic patterns, all patients had abnormal sonographic findings. Pulmonary lesions showed a homogeneous hypoechoic pattern in 13 patients (Fig 3). In 5 patients, heterogeneous echogenicity was observed (Fig 4) and was due to air bronchograms; this pattern was not associated with the criteria of malignancy. All lesions were identified by the "interruption" of the normal lung surface, recognized by its linear hyperechogenicity with reverberation artifacts. Hyperechogenicity of the posterior margins was observed in all patients with an apparent enhancement of the echo artifacts deep to the lesion.

View larger version (113K): [in this window] [in a new window]   Fig 3. Intraoperative ultrasound shows hypoechoic lesion (arrow). Because of the collapse of the lung during thoracoscopy, the nodule is seen close to the pleural surface.

View larger version (113K): [in this window] [in a new window]   Fig 4. Intraoperative ultrasound shows heterogeneous pulmonary nodule (arrow).

	Comment

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Problems in nodule localization are well known in the surgical literature [5]. In fact, Hsu and associates [18] reported that in 5 of 42 patients with pulmonary nodules, the procedure was completed with a minithoracotomy because of inability to identify the lesion during VATS. Hazelrigg and coworkers [1], in a multicenter study, found that the inability to locate the lung nodule was a frustrating problem occurring in 7.5% (65 of 865) of patients with a nodule and resulting in thoracotomy. The techniques of localization include preoperative injection of methylene blue [6], colored collagen [7], and needle localization [8, 9]. However, these techniques carry the risk of pneumothorax, pulmonary hemorrhage, or dislodgment of the hook wire from the lung and the problem of requiring both the computed tomographic facility and the operating room simultaneously [6, 19]. In a multicenter study [3], the failure rate of the methylene blue localization technique was 13%, which was explained by either too large a quantity of liquid injected or an error in nodule localization, and the failure rate of the hook wire technique was 47%, which was due to removal of the hook wire, a mistake in nodule localization, or subpleural hematoma.

Our pilot study was designed to evaluate the feasibility of intraoperative ultrasound to localize small solitary nodules in the lung where the presence of air usually prevents adequate ultrasound exploration. No complications related to TUS occurred in our patients, and the use of high-frequency ultrasound probes is very accurate in the localization of small pulmonary nodules of 20 mm or less [20–22]. Although it is commonly believed that ultrasound is not feasible on the inflated lung [20, 23], we demonstrated that the lesion can be visualized even when it is not possible to entirely deflate the lung. However, complete collapse of the lung is useful and can be accomplished by careful suction of the airways. Applying gentle pressure on the parenchyma with the probe reduces residual air below the transducer and makes it possible to localize the lesion. Very small nodules can be easy to identify if they are less deep, fixed in position, and hard; a large but soft nodule could be more difficult to localize.

In 13 patients, the lesion appeared as a homogeneous hypoechoic pattern with the sonographic disappearance of the hyperechoic pulmonary surface (see Fig 3); because air totally reflects sound waves, the aerated lung appears only as a hyperechoic line producing a large area of air echo artifacts [24]. "Sonographic interruption" of this hyperechoic pulmonary surface was observed in all patients. The hyperechoic posterior margin generating apparent enhancement artifacts was visualized in every patient. Heterogeneous echogenicity of the lesion was observed in 5 patients (see Fig 4). This can be due to air bronchograms, presence of different tissues, or hamartoma. However, this ultrasound pattern was not able to distinguish between malignant and benign lesions. The lateral margins of the lesion can be partially masked by air within superficial alveolar spaces, reflecting sound waves, but with gentle pressure and a multiplanar approach, it is possible to detect the whole tumor with tapered edges. Filling the pleural cavity with saline solution can improve the surface contact of the transducer and result in better resolution. Further, use of the probe with a flexible tip allows multiplanar scanning of the area of interest.

Finally, the ultrasound probe can be used to guide both the placement of linear staplers and the excision procedure to safely encompass the whole lesion. In fact, visualization of the relationship between the lesion and important vascular and bronchial structures can determine the direction of linear stapling. For solitary nodules that prove to be granulomas or hamartomas, no further treatment is necessary. On the other hand, in most cases of primary lung cancer, some groups [25] think thoracoscopic resection is inadequate and conventional pulmonary resection is indicated to decrease the incidence of local recurrence. The use of TUS could be helpful in detecting the pulmonary nodule and in defining cardiovascular invasion and lymph node (Fig 5) and liver metastasis to make the choice of surgical procedure easier and to avoid unnecessary tissue dissection [21, 26–30].

View larger version (110K): [in this window] [in a new window]   Fig 5. Intraoperative ultrasound clearly shows enlarged lymph nodes (arrows).

In conclusion, our preliminary experience, although favorable, needs to be confirmed with a larger number of patients. We believe that intraoperative ultrasound can safely and effectively localize invisible or nonpalpable pulmonary nodules at the time of thoracoscopy and that this may help surgeons perform minimally invasive lung resections with clear surgical margins.

	References

Top Abstract Introduction Material and methods Results Comment References

 

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