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Eur J Cardiothorac Surg 2004;26:469-473
© 2004 Elsevier Science NL


Ultrasonographic evaluation of small nodules in the peripheral lung during video-assisted thoracic surgery (VATS)

Seiji Matsumotoa, Toshiki Hiratac, Eiji Ogawaa, Tatsuo Fukusea, Hiroyuki Uedab, Takashi Koyamab, Takayuki Nakamuraa, Hiromi Wadaa*

a Department of Thoracic Surgery, Graduate School of Medicine, Kyoto University, 54 Shogoin Kawara cho, Sakyo ku, Kyoto 606-8397, Japan
b Department of Radiology, Graduate School of Medicine, Kyoto University, 54 Shogoin Kawara cho, Sakyo ku, Kyoto 606-8397, Japan
c Department of Thoracic Surgery, Kishiwada City Hospital, 1001 Gakuhara cho Kishiwada, 569-8501 Osaka, Japan

Received 2 March 2004; received in revised form 5 May 2004; accepted 10 May 2004.

* Corresponding author. Tel.: +81-75-751-4975; fax: +81-75-751-4974
e-mail: wadah{at}kuhp.kyoto-u.ac.jp


    Abstract
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Comments
 References
 
Objective: We examined the possibility of intraoperative ultrasonography during video-assisted thoracic surgery (VATS) to localize and make a qualitative diagnosis of small peripheral pulmonary nodules. Methods: Ultrasonography during VATS and conventional thoractomy was performed on 25 and 18 nodules, respectively, all which were localized in the peripheral lung, were less than 30 mm in diameter and for which there was no definitive diagnosis. Results: All 25 nodules, including 10 invisible but palpable and three both invisible and non-palpable, could be localized by ultrasonography during VATS. If nodules were located less than 15 mm from the pleural surface, ultrasonography during VATS could detect nodules 10 mm or less in diameter. The rate of malignant tumors among 11 of 12 pulmonary nodules (91.6%) showing both heterogeneous and ill-defined patterns was significantly higher than 6 of 16 nodules (37.5%) showing both homogeneous and well-defined patterns on ultrasonography. Conclusions: Our study suggested that ultrasonography during VATS is useful for the detection of peripheral pulmonary nodules, even when they are not identified on video images or palpation, and may enable a differential diagnosis between malignant and non-malignant lesions.

Key Words: Video-assisted thoracic surgery • Ultrasonography • Pulmonary nodule


    1. Introduction
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Comments
 References
 
Video-assisted thoracic surgery (VATS) [1,2] is less invasive than conventional thoracotomy and is suitable for the resection of small peripheral lung nodules. However, small peripheral lung nodules often cannot be confirmed using a monitor or palpation with forceps during VATS. To solve this problem, previous investigators have reported that preoperative computed tomography (CT) guide marking [3,4] and pigment infusion [5] were useful to identify the location of peripheral nodules during VATS. However, this method has many potential problems such as pneumothorax or hemothorax, leaving in the hook wire, difficulty in direct confirmation of a lesion during surgery, and extra costs. Therefore, a procedure that can identify small peripheral nodules during VATS is essential.

Ultrasonography is widely used as a diagnostic tool in various clinical fields, such as percutaneous echoes [6], echoes during surgery [711] and transbronchial echoes. However, only a few researchers have reported that ultrasonography can identify peripheral pulmonary nodules [9,10]. Moreover, the ability of ultrasonography to facilitate qualitative diagnosis has not been clarified. Therefore, in this study, we examined whether ultrasonography during VATS can locate a nodule in real time and make a differential diagnosis in the peripheral lungs.


    2. Material and methods
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Comments
 References
 
We examined 43 nodules from 41 patients. Twenty-five nodules of 23 patients underwent VATS and 18 nodules of 18 patients underwent conventional thoracotomy at Kyoto University Hospital or Kishiwada City Hospital between April 2000 and April 2002. All 41 patients had small nodules located in the pulmonary peripheral side a one-third and smaller than 30 mm in diameter on chest CT, but preoperative diagnoses of all lesions were not confirmed.

When a small pulmonary nodule is identified on a chest X-ray or CT in an institution, a bronchoscopy is usually performed for diagnosis. If no pathological diagnosis is obtained, VATS is performed, followed by a conventional thracotomy if the pathological diagnosis reveals primary lung cancer.

However, in cases strongly suspected of lung cancer based on a chest X-ray, CT findings or a tumor marker of serum levels, a conventional thoracotomy is initially performed without VATS.

2.1. Preoperative evaluation
Preoperative chest X-ray and CT were performed to evaluate the location, number, longest dimension, shortest dimension, depth, appearance and internal predisposition of the affected nodules in the peripheral lung. The depth of nodules on chest CT was defined as the smallest distance from the nodules to the pulmonary surface. All the distances between the nodules and the lung surface in Section 3 are expressed as measured in the preoperative chest CT.

2.2. Ultrasonography during VATS
The patient was initially ventilated via a double-lumen endotracheal tube under general anesthesia, turned into the lateral decubitus position and three 11.5 mm trocars were set up. After the lung was deflated, we localized the nodules by visualization using a thoracosope monitor and by palpation with forceps.

Isotonic sodium chloride solution at 37 °C was poured into the thoracic cavity and the ultrasonography probe (a linear array transducer, an Aloka UST-5530, 7.5 MHz probe) was placed on the pulmonary surface suspected of having a pulmonary nodule. The location, longest dimension, shortest dimension, margin and internal predisposition of the nodules were evaluated by ultrasonography. Ultrasonographic signs were recorded as a hard copy and videotape.

After the completion of ultrasonography, partial resection of the lung and frozen-section histopathological diagnosis were performed immediately. When intraoperative diagnosis by a frozen-section suggested malignant nodules, thoracotomy and pulmonary lobectomy were performed after VATS. However, when intraoperative diagnosis suggested benign nodules, partial resection by VATS alone was performed without thoracotomy and pathological diagnosis using formalin embedded specimens was performed.

2.3. Ultrasonography during conventional thoractomy
We added 18 nodules from 18 patients who underwent an initial conventional thoracotomy for small peripheral nodules, which were located in the pulmonary periphery side a one-third, smaller than 30 mm in diameter and highly suspected of lung cancer.

The patient was initially ventilated via a double-lumen endotracheal tube under general anesthesia, then turned to the lateral decubitus position. After thoracotomy, the lung was deflated. Isotonic sodium chloride solution at 37 °C was poured into the thoracic cavity and the ultrasonography probe was placed on the pulmonary surface suspected of a pulmonary nodule

After completion of the ultrasonography, partial resection of the lung and a frozen-section histopathological diagnosis were performed immediately. If the nodule was determined to be primary lung cancer, a lobectomy was performed.

The images from both VATS and the thoracotomy were reviewed by a thoracic surgeon and two radiologists during surgery.

2.4. Statistical analysis
Statistical analysis was performed by StatView software (version 5.0, SAS Institute Inc, NC).

The relationships between the detection rate and the depth of the nodules, and the detection rate and the nodule diameter, and the correlation between malignant tumors and benign tumors were evaluated by Fisher's exact probability test. A P value less than 0.05 was taken to indicate a significant difference.


    3. Results
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Comments
 References
 
3.1. Patient characteristics
The VATS cases involved 25 nodules: 13 were malignant tumors and 12 were benign tumors. The thoracotomy cases involved 18 nodules: 17 malignant tumors and one benign tumor (Table 1).


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Table 1. Patient characteristics

 
3.2. Analysis of the VATS cases
3.2.1. Detection rate of nodules by video imaging, palpation, and ultrasonography
Of the 25 nodules treated by VATS, 15 (60%) were visible and identified on video images through a thoracoscope. The other 10 nodules were not identified on video images, and three were not palpable. Using ultrasonography, however, all 25 nodules were recognized during VATS. The detection rates of pulmonary nodules by ultrasonography were significantly higher than by video imaging (P=0.0006) (Table 2).


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Table 2. Detection rate of pulmonary nodules by video image, palpation, and ultrasonography

 
3.2.2. Detection rate, depth and diameter of the nodules
Among nodules located at a depth of more than 5 mm from the pleural surface, detection by ultrasonography was significantly higher than by video imaging (P=0.006) (Fig. 1 A).



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Fig. 1. Detection rate and nodule diameter. The solid bar shows the detection rate with video images. The hatched bar shows the detection rate with palpation. The outlined bar shows the detection rate with ultrasonography.

 
For nodules with a diameter less than 10 mm on the chest CT, the detection rate by ultrasonography was significantly higher than by video imaging (P=0.012) (Fig. 1B).

3.3. Differential diagnosis of pulmonary nodules (combination analysis of the 25 VATS cases and 18 thoracotomy cases)
3.3.1. Ultrasonographic classification of nodule (Fig. 2A, B)
Ultrasonographic findings were divided into the following two patterns.



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Fig. 2. Ultrasonographic classification of the findings. (A) Homogeneous pattern: the inside of the lesion showed a homogeneous and low echoic pattern. The pathological diagnosis was pulmonary tuberculosis. (B) Heterogeneous pattern: the inside of the lesion was heterogeneous, with a punctile-like hyperechoic spot. The pathological diagnosis was adenocarcinoma of the lung. (C) Well-defined pattern: the margin of the nodule was clear. Pulmonary tuberculosis. (D) Ill-defined pattern: the margin of the nodule was unclear. Metastaststic lung cancer from colorectal cancer.

 
Homogeneous pattern. The interior of the lesion was homogeneous with a low echoic pattern, for example, Fig. 2A , pulmonary tuberculosis.

Heterogeneous pattern. The interior of the lesion was heterogeneous, with a punctile hyperechoic pattern, for example, Fig. 2B, lung cancer.

3.3.2. Ultrasonographic classification of nodule margin findings (Fig. 2C, D)
Ultrasonographic margin findings were divided into the following two patterns.

Well-defined pattern. The margin of the nodule was distinct, for example, Fig. 2C, pulmonary tuberculosis.

Ill-defined pattern. The margin of the nodule was unclear, for example, Fig. 2D, metastatic lung tumor from colorectal cancer.

3.4. Differential diagnosis based on internal patterns and the margin of the nodules
We defined primary lung cancer and metastatic lung tumor as malignant tumors and other tumors, e.g. tuberculosis, as benign tumors. The rate of malignant tumors among nodules showing both a heterogeneous pattern and an ill-defined margin (91.6%) was significantly higher than nodules showing a homogeneous pattern with a well-defined margin (37.5%) (P=0.0043). In homogenous patterns, an ill-defined margin indicated a malignant tumor (90.0%) stronger than a well-defined margin (37.5%) (P=0.0097) (Table 3).


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Table 3. Differential diagnosis by internal findings and findings from the nodule margins

 

    4. Comments
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Comments
 References
 
In our study, small nodules less than 10 mm in diameter on preoperative chest CT could be detected by ultrasonography during VATS if they were located at a depth less than 15 mm from the pleural surface. The number of nodules detected by preoperative CT was identical with the number of nodules detected by intraoperative ultrasonography in all patients.

Santambrogio et al. [9] performed ultrasonography during VATS on 18 cases with a pulmonary nodule diameter of 20 mm or less and reported that they could detect pulmonary nodules with a minimum diameter of 5 mm by ultrasonography. Greenfield et al. [10] detected 12 nodules by ultrasonography during VATS in 13 peripheral lung nodules with a minimum diameter of 4 mm and at a maximum depth of 20 mm from the pleural surface. Our results supported these results.

Our study also revealed that ultrasonography during VATS could detect 7 of 25 invisible and palpable pulmonary nodules, and moreover, 3 both invisible and non-palpable pulmonary nodules. Ultrasonography facilitated the discrimination of three non-palpable lesions; two patients had adenocarcinoma, and one patient a tuberculous nodule. In the patient with a tuberculous nodule, ultrasonography made it possible to avoid unnecessary thoracotomy for detecting nodules.

The results demonstrated the usefulness of ultrasonography during VATS in detecting peripheral pulmonary nodules.

In the use of ultrasonography to detect nodules in other areas, the detection rate of hepatocellular carcinomas in hepatic cirrhosis patients by ultrasonography was 33–96% [1216]. Bennett et al. [16] reported that the sizes of eight hepatocellular carcinomas detected by ultrasonography ranged from 1.2 to 7.5 cm, but no hepatocellular carcinomas less than 1 cm were detected. Endoscopic ultrasonography is the most sensitive method for the detection of pancreatic tumors, with a sensitivity of 90% [17]. Ultrasonography during VATS was not only effective for locating the pulmonary nodules, but also for determining the incision line, because it shows the longitudinal axis of pulmonary nodules.

An analysis of all 43 cases of ultrasonography during VATS and conventional thoracotomy showed that in a patient with homogenous patterns, an ill-defined margin indicated a malignant tumor (90.0%) more than a well-defined margin (37.5%) (P=0.0097). Moreover, the rate of malignant tumors among nodules showing both a heterogeneous and an ill-defined margin pattern (91.6%) was significantly higher than nodules showing both a homogeneous and well-defined margin pattern (37.5%) (P=0.0043) (Table 3). This result suggested that ultrasonography might be useful for differential diagnosis of lung nodules.

In our study, palpation with forceps during VATS was also a reliable technique for locating and confirming pulmonary nodules with a diameter less than 10 mm. However, Hayashi et al. [18] compared conventional resection techniques and a non-touch isolation technique, and concluded that the non-touch isolation technique prevented the dissemination of cancer cells into the portal blood system during surgery. If malignancy is strongly suspected by ultrasonography during VATS, it may be possible to avoid unnecessary palpation and prevent the dissemination of cancer cells.

Mean operative time of VATS is 2 h 33 min and ultrasonography during VATS can be performed with an average of 7 min, and the technique is relatively simple. The clinical application of this procedure is not likely to be difficult. If ultrasonography can be performed during VATS, preoperative marking with chest CT guidance would become unnecessary, resulting in the elimination of complications and extra expenses.

In conclusion, our study suggested that ultrasonography during VATS may be useful for detecting small peripheral pulmonary nodules that cannot be identified on video images or by palpation, and may enable differential diagnosis between malignant and benign tumors.


    References
 Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Comments
 References
 

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