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Ann Thorac Surg 2005;79:258-262
© 2005 The Society of Thoracic Surgeons


Original article: General thoracic

Thoracoscopic Localization Techniques for Patients With Solitary Pulmonary Nodule and History of Malignancy

Davide Sortini, MD*, Carlo V. Feo, MD, Paolo Carcoforo, MD, Giovanni Carrella, MD, Enzo Pozza, MD, Alberto Liboni, MD, Andrea Sortini, MD

Section of General Surgery, Department of Surgical, Anaesthesiological and Radiological Sciences, University of Ferrara, Ferrara, Italy

Accepted for publication June 2, 2004.

* Address reprint requests to Dr Sortini, Sezione di Chirurgia Generale, Dipartimento di Scienze Chirurgiche, Anestesiologiche e Radiologiche, Università di Ferrara, C.so Giovecca 203, 44100 Ferrara, Italy (E-mail: sors{at}libero.it).

Presented at the Poster Session of the Fortieth Annual Meeting of The Society of Thoracic Surgeons, San Antonio, TX, Jan 26–28, 2004.


    Abstract
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
BACKGROUND: Our aim was to evaluate the best intrathoracoscopic localization technique in patients with single pulmonary nodule and a history of malignancy.

METHODS: We divided 50 patients in two groups, well matched for diameter and depth of the pulmonary lesion. In 25 patients we performed intrathoracoscopic ultrasound to locate the pulmonary nodule (group A), whereas in the other 25 patients the radio-guided technique was adopted (group B). In both group A and group B, the localization techniques were compared with finger palpation. In group A, 12 nodules were in the left lung and 13 in the right one; in group B, 11 lesions were in the left and 14 in the right lung. In both groups, the distance of the nodule from the pleural surface was 2.6 ± 0.5 cm (2 to 2.5 cm in 14 patients, and >2.5 cm for the remaining 11). The diameter of the nodule was 1.26 ± 0.22 (≤1 cm in 10 patients, and 1 to 1.5 cm in 15) in both groups. All patients underwent thoracoscopic wedge resection, and 10 patients with a primary pulmonary lesion underwent posterior-lateral thoracotomy for lobectomy and mediastinal lymphadenectomy.

RESULTS: In group A, ultrasound localized the nodule in 24 of 25 patients (96%) whereas finger palpation localized it in 19 of 25 (76%; not significant). In group B, both the radio-guided and finger palpation techniques localized the nodule in 20 of 25 patients (80%; not significant). No complications were recorded with the ultrasound technique; however, 10 cases of pneumothorax were detected after the radio-guided technique (p < 0.01).

CONCLUSIONS: Both the ultrasound and radio-guided techniques are accurate to detect solitary pulmonary nodules, but the radio-guided method yields complications as compared with the ultrasound.


    Introduction
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
he diagnosis of a solitary pulmonary nodule in patients with a previous history of malignancy is more frequent than suspected. During their natural history the majority of patients with a malignant tumor will develop a pulmonary metastasis [1]. A few questions arise when the diagnosis of pulmonary nodule is established. First, the pathology of the nodule is extremely important in a patient who had a previous cancer, even if the nodule is small and peripheral. Chest roentgenogram, computerized tomography (CT), and bronchoscopy do not always ascertain the diagnosis of pulmonary nodules, as well as more invasive diagnostic procedures (eg, CT-guided fine-needle or transbronchial biopsy). The next step is a minimally invasive surgical technique to perform a biopsy of the tumor. Video-assisted thoracic surgery is considered the gold standard for the diagnosis and, in selected cases, for the treatment of pulmonary nodules [2–5]. However, thoracoscopic localization of small and central nodules of the lung may be difficult, although to localize a solitary pulmonary nodule is a fundamental step to plan a correct operative strategy and surgical tactics. A few localization techniques have been described, either preoperative (ie, vital or blue dye, fluoroscopy-aided, needle wire) or intrathoracoscopic (ie, finger palpation, intrathoracoscopic ultrasound, and the radio-guided technique) [6–20]. In this study, we compared the intrathoracoscopic ultrasound and radio-guided techniques with finger palpation to localize solitary pulmonary nodules in patients with a history of malignancy.


    Material and Methods
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Between January 2001 and December 2003, 50 patients with a history of malignancy and a pulmonary nodule underwent intrathoracoscopic localization at our institution. We selected all patients with solitary pulmonary nodule and positive history of malignancy. Because we work in a general surgery unit and in our hospital there is also a thoracic surgery unit, we therefore only see patients with a history of malignancy.

We excluded all patients with nodules larger than 1.5 cm or less than 2 cm deep. Fifty consecutive patients were assigned to intrathoracoscopic ultrasound (group A) and radio-guided (group B) techniques to locate the pulmonary nodule. In 25 patients (group A), an attempt to localize the nodule was made by intrathoracoscopic ultrasound (Toshiba ECO-CEE with a linear scan multifrequency probe 5 to 8 MHz), whereas in the remaining 25 (group B), a radio-guided intrathoracoscopic technique (Scinti Probe MR 100; Polyvalent High Technology, Aquila, Italy) was adopted. In both group A and group B, finger palpation to locate the nodule was performed after the ultrasound or radio-guided localization techniques. The presence of the nodule was preoperatively shown by CT chest scan, and postoperatively confirmed by pathologic examination of the resected specimen. We did not randomize patients because we first used ultrasound and then, in a second time, we tried to localize the nodules adopting the radio-guided technique. The Ethical Committee of our university approved the study design, and we obtained an informed consent from each patient.

Patients
All patients had a history of malignancy, the previous tumor had been treated with a curative operation, and the pulmonary nodule was diagnosed during the follow-up. There were 27 men (54%) and 23 women (46%), and the mean age was 64.5 years (range, 41 to 80 years). As far the previous tumor is concerned, 30 patients (60%) had colorectal cancer, 12 had breast cancer (24%), and 8 had melanomas (16%). The mean follow-up at the diagnosis of the pulmonary nodule was 36 months (range, 23 to 50 months). The mean follow-up after the thoracoscopy was 12 months (range, 12 to 32 months; Table 1).


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Table 1. Patients and Nodule Characteristics
 
Lesion Characteristics
In all patients the diagnosis of pulmonary nodule was made by chest roentgenogram during the follow-up. All patients were asymptomatic. After the chest roentgenogram, a thoracic CT with fine-needle biopsy or bronchoscopy with bronchoalveolar lavage and biopsy were performed. The percutaneous needle aspiration and the bronchoalveolar lavage showed atypical cells of uncertain interpretation in 9 (18%) and 5 (10%) patients, respectively. In group A, 12 nodules were in the left lung and 13 in the right one, whereas in group B, 11 nodules were in the left and 14 in the right lung. The two groups were well matched for diameter and depth of the pulmonary lesion. In both groups A and B, the mean diameter of the nodule was 1.26 ± 0.22 cm (1 ± 0.14 cm in 10 patients and 1.4 ± 0.12 cm in the remaining 15 patients). The mean distance from the pleural surface was 2.6 ± 0.5 (14 nodules had a mean distance from the pleural surface of 2.2 ± 0.2 cm and 11 of 3.1 ± 0.13 cm) in both groups A and B.

Ultrasound Technique
We performed intrathoracoscopic ultrasound localization technique as described by Santambrogio and colleagues [13]. Patients were turned in the lateral decubitus position as for a thoracotomy. Operative scanning was performed immediately after the placement of thoracoscopic access. In all patients, three 10-mm trocars were set up in triangulate fashion according to the needs of strategic visibility and manipulation of the target lesion, usually between the fourth and eighth intercostal spaces. Pleural adhesions were lysed when present; no other surgical dissection was needed. After deflation of the lung the ultrasound probe was placed firmly on the area of the lesion, and when the nodule was identified, its relation to vessels and bronchi was also evaluated after a scan of the entire lung surface was done. No additional lesions were found with respect to the preoperative thoracic CT. After the ultrasound, a second thoracic surgeon attempted to locate the nodule by finger palpation, blinded to the result of the ultrasound localization technique.

Radio-Guided Technique
We used the same radio-guided localization technique used in breast surgery (radioguided occult lesion localization) [17, 18]. Early morning on the day of operation the patients underwent radiolabeled localization. Under local anesthesia 0.3 mL of a solution composed of 0.2 mL of 99mTc-labeled human serum albumin microspheres, 80 nm in diameter, and 0.1 mL of nonionic contrast was injected through the thoracic wall with a 22G needle into the lesion or just in contact with it. Then the patient was transferred to the operating room after the introduction of a trocar for videothoracoscopy exploration, usually in the sixth or seventh intercostal space along the midaxillary line. A second incision of 2 cm was performed. This second incision was planned according to the radiologic site of nodule and the position of the lobes on thoracoscopic vision. First an area of the lung far from the suspected one was scanned to reset the system, then we approached the pleural surface of the target area to localize the radioactive source. Once the area with the higher value of radioactivity was identified, a third trocar was placed, and a wedge resection was performed. Before the wedge resection a second thoracic surgeon attempted to locate the nodule by finger palpation, blinded to the results of the radioguided technique. After the wedge resection, any residual radioactivity was searched with the probe.

Statistical Analysis
All data are expressed as mean ± standard deviation (range). The {chi}2 test, analysis of variance, and the two-tailed unpaired Student's t test were used when appropriate to compare the results between groups. Differences were considered significant when p was less than 0.05.


    Results
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
In group A, the intrathoracoscopic ultrasound localized the pulmonary nodule in 24 of 25 patients (96%) and finger palpation in 19 of 25 patients (76%; not significant); in group B, both radio-guided and finger palpation techniques localized the lesion in 20 of 25 patients (80%). Although no statistical significance could be demonstrated among different localization methods, the intrathoracoscopic ultrasound seems to be superior for detecting solitary pulmonary nodules as compared with both the radio-guided and finger palpation localization techniques (96% versus 80%; not significant). Obviously when the nodule was not localized we converted into a thoracotomy.

The mean time to detect the nodule with the ultrasound was 8 minutes (range, 6 to 17 minutes), including a complete ultrasound scan of the lung; the mean time for the radio-guided localization was 21 minutes (range, 18 to 40 minutes); finally, the mean time for the finger palpation was 6 minutes (range, 4 to 15 minutes). Therefore, the intrathoracoscopic ultrasound and finger palpation techniques were faster than the radio-guided one in localizing the nodule (p < 0.05).

No complications were detected with the ultrasound, whereas radio-guided technique was associated with 10 cases of preoperative pneumothorax (p < 0.05).

In both groups A and B, we always performed a thoracoscopic wedge resection with a frozen section of the specimen after the intraoperative localization of the lesion. In 10 patients, an adenocarcinoma was detected, and we converted the operation into a posterolateral thoracotomy for lobectomy and mediastinal lymphadenectomy. In 32 patients the frozen section showed a metastasis, and in 8 a benign nodule; thus, we did not perform any further treatment in these patients. The final pathologic diagnosis confirmed that 32 nodules were pulmonary metastases (18 from colon cancers, 8 from malignant melanomas, and 6 from breast cancers), 10 were primary malignant pulmonary tumors (all adenocarcinomas T1N0M0), 2 hamartomas, and 6 inflammatory nodules. Interestingly, the final pathologic diagnosis showed six cases of perinodular inflammation, probably as a result of the contrast medium injection. Clean margins were obtained on all resected nodules both for primary lung cancers and metastatic nodules.

The mean postoperative hospital stay was 6 days (range, 5 to 8 days) compared with 5 days (range, 4 to 6 days) after a thoracoscopic wedge resection.

No intraoperative complications were detected, and the only postoperative complication was a case of air leakage that was successfully treated by prolonging the chest drainage to the sixth postoperative day.

All 50 patients are still alive, disease free, and undergoing follow-up. The 2 patients with benign lesions are also included in the follow-up as they had colon and breast cancers.


    Comment
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Preoperative localization techniques of pulmonary nodules have been extensively studied, and their pros and cons are well established. The needle-wire technique is associated with several complications [9–11], with dislodgment of the needle being the most important one. The latter generally occurs during transportation of the patient to the operating room or during the surgical procedure, either when the lung is deflated or during the resection of the nodule, as the surgeon will often apply gentle retraction on the wire. Other complications are pneumothorax, pleuritic pain, lung hemorrhages or hematoma, and pleural bleeding. The vital dye technique of pulmonary nodule localization has shown a high rate of complications such as pneumothorax, pleuritic pain, pulmonary bleeding, and fits of coughing [6–8]. The major problem related to this technique is the time elapsed between the location of the nodule and the surgical operation; in fact, the longer the time interval, the greater the diffusion of contrast medium into the pulmonary parenchyma surrounding the nodule. Thus, we focused our attention on more innovative techniques, which need to be developed and improved. We did not perform radio-guided and ultrasound procedures in the same patients because one method can influence the other, ie, injection of microspheres can provoke localized hematoma over the pleural surface and guide ultrasound localization.

Our study shows that intrathoracoscopic ultrasound seems to be superior to radio-guided and finger palpation techniques to locate single pulmonary nodules, and we suggest the use of intraoperative ultrasound to identify single pulmonary nodules.

The intrathoracoscopic ultrasound technique has been shown, in experienced hands, to be very sensitive for the localization of pulmonary nodules [13]. In addition, intrathoracoscopic ultrasound is less expansive than the radio-guided technique and it allows studying the structures surrounding the nodule (ie, vessels, bronchi, and lymph nodes). Furthermore, intrathoracoscopic ultrasound may play a role predicting the pathologic status of the nodule. In fact, in all patients the lesion appeared as a homogeneous hypoechoic pattern with the sonographic disappearance of the hyperechoic pulmonary surface. Heterogeneous echogenicity of the lesion was observed in 2 patients because of air bronchogram, presence of different tissue, or hamartoma. This ultrasound pattern, however, was not able to distinguish between malignant or benign lesion [13, 19]. Incomplete pulmonary exclusion and less air in the pulmonary parenchyma help to localize the nodule that has a hypoechoic ultrasound pattern in contrast with the hyperechoic surrounding pulmonary parenchyma. Thus, the presence of a small amount of air in the pulmonary parenchyma is useful to localize the pulmonary nodules [21].

The localization of pulmonary nodules by radio-guided technique has been shown to be reliable, revealing, however, some drawbacks [1]. Most important is the notable and fast diffusion of contrast medium in the pulmonary parenchyma surrounding the nodule owing to the rich vascularization of the lung. A second problem is locating deep and posterior nodules because of the size and structure of the probe that cannot move freely in the thorax. In fact, we report three cases of missed localization as a result of posterior location of the nodule in 1 patient and presence of an intense radioactivity emission of the pulmonary parenchyma around the nodule related to a fast diffusion of the contrast medium in 2 patients. Another problem with the radio-guided technique is pneumothorax; in fact in our series, as well as in others [9–11], we have found a high number of asymptomatic pneumothorax. Other factors, such as dimension or pathologic status of the nodule, did not seem to influence the radio-guided localization. Unfortunately, the radio-guided technique does not give any additional information about the pathologic status of the nodule.

Finger palpation [22], although safe, sensitive, quick, reliable, and inexpensive, is a subjective recording on the basis of the sensitivity of the surgeon and the consistency of the lesion. The main limit of finger palpation is the difficulty in inserting the entire finger through the port, but usually only the first two phalanges enter through the Thoracoport. Another drawback of finger palpation is the impossibility and difficulty of moving the deflated lung parenchyma under the finger. By contrast, the ultrasound localization is an objective method to detect the lesion. Obviously, ultrasound is strongly operator dependent; fortunately, at our institution there are very experienced colleagues in ultrasound imaging as our experience started many years ago with laparoscopic ultrasound [23]. Unfortunately, we have not a comparable experience in CT radio-labeled localization because it is a newer technique, with fewer applications than ultrasound. Moreover, the radio-guided occult lesion localization is a more recent technique than ultrasound, and thus the experience developed with this technique is less. Probably our experience in ultrasound did contribute to the fact that we recorded 96% sensitivity. No difference in accuracy could be detected among different pulmonary nodule localization techniques. Thus, we think that currently it is impossible to identify one localization technique as the gold standard. Based on our experience, we prefer ultrasound, although it has not shown higher accuracy than radio-guided. The main advantage of ultrasound, however, is the absence of complications.


    References
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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