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INVITED REVIEW

Video-Assisted Surgery for Lung Cancer. State of the Art and Personal Experience

Jesus Loscertales, MD, Rafael Jimenez-Merchan, MD, Miguel Congregado, MD, Francisco Javier Ayarra, MD, Gregorio Gallardo, MD, Ana Triviño, MD

General and Thoracic Surgery Department, Virgen Macarena University Hospital, Seville, Spain

Jesus Loscertales, MD, Tel: +34 955008205, Fax: +34 954372734, Email: jloscert{at}us.es, General and Thoracic Surgery Department, Virgen Macarena University Hospital, Av. Dr. Fedriani, 3. 41007 Seville, Spain.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 STAGING OF LUNG CANCER
 OUR SURGICAL TECHNIQUES
 RESULTS
 SOLITARY PULMONARY NODULE
 OUR EXPERIENCE OF VTS...
 MAJOR PULMONARY RESECTION USING...
 OUR EXPERIENCE OF VATS
 REFERENCES
 
This paper reviews the role of videothoracoscopy in lung cancer, highlighting its utility in definitive staging, diagnosis, and treatment. We show exploratory videothoracoscopy to be the perfect technique for last-minute staging, looking for tumor invasion, especially parietal T3 and vascular T4 (due to videopericardioscopy), management of solitary pulmonary nodules, and the possibility of radical treatment with video-assisted thoracoscopic lobectomy. We perform an overview of the literature and analyze our experience of 1,381 patients with lung cancer. In 1,277 of them, the final decision on resectability was made by exploratory videothoracoscopy, including 91 by videopericardioscopy (only 30 were considered non-resectable on videopericardioscopy). Solitary pulmonary nodules were diagnosed in 382 cases (190 were cancer), and we performed 260 major lung resections by video-assisted thoracoscopic surgery (22 pneumonectomies, 238 lobectomies/bilobectomies).

Key Words: Carcinoma • Bronchogenic • Lung Neoplasms • Pneumonectomy • Surgical Procedures • Minimally Invasive • Thoracic Surgery • Video-Assisted


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
STAGING OF LUNG CANCER
 OUR SURGICAL TECHNIQUES
 RESULTS
 SOLITARY PULMONARY NODULE
 OUR EXPERIENCE OF VTS...
 MAJOR PULMONARY RESECTION USING...
 OUR EXPERIENCE OF VATS
 REFERENCES
 
Over the last 15 years, advances in the field of minimally invasive surgery have radically transformed surgical practice. The first clinical application of thoracoscopy has been attributed to Hans Christian Jacobaeus who inserted a rigid cystoscope into the pleural cavity to cauterize adhesions and facilitate lung collapse in the treatment of tuberculosis in 1910.1 It was not until 1992 that Landreneau and colleagues2 laid the technical and strategic foundations of modern video-assisted thoracic surgery (VATS); thereafter, the rediscovery of thoracoscopy and its growing use enabled increasingly complex operations to be performed, which had hitherto only been possible by thoracotomy. At an international symposium on thoracoscopic surgery held in January 1993 in San Antonio, Texas, it became clear that many of the simplest videothoracoscopic surgical procedures would rapidly become the gold standard for the treatment of certain pathologies.3

Bronchogenic carcinoma is the leading cause of cancer-related death in men. Preoperative TNM staging of non-small-cell lung cancer is essential for establishing both the prognosis and therapeutic strategies available. Complete surgical resection, traditionally performed via thoracotomy, is considered the treatment of choice. However, recent progress in VATS has led to this approach assuming a major role in many aspects of the treatment of lung cancer. The objective of this paper is to examine the current indications for videothoracoscopy in the management of lung cancer. This minimally invasive technique can be used in the evaluation of solitary pulmonary nodules and final staging of tumors, pleural and lymph node metastases; staging includes intrapericardial tumor evaluation to determine the feasibility of tumor resection as a first step in lung cancer surgery. Finally, resection can be performed by thoracoscopic surgery in the early stages of lung cancer.


   STAGING OF LUNG CANCER
TOP
 ABSTRACT
 INTRODUCTION
 STAGING OF LUNG CANCER
OUR SURGICAL TECHNIQUES
 RESULTS
 SOLITARY PULMONARY NODULE
 OUR EXPERIENCE OF VTS...
 MAJOR PULMONARY RESECTION USING...
 OUR EXPERIENCE OF VATS
 REFERENCES
 
The TNM system used for clinical staging of lung cancer requires characterization of the primary tumor (T), of regional lymph node involvement (N), and of remote metastases (M). The main aims of staging are to rule out remote metastases and determine any local reasons for non-resectability; without the data thus obtained, treatment may often prove inappropriate. Despite advances in imaging techniques and various modes of mediastinoscopy, and despite the standardization of lung cancer staging, exploratory thoracotomies are still only performed in around 10% of patients.4–7 Computed tomography (CT) is currently the most widely used imaging technique for determining the T parameter. Although it defines the location, size, and anatomical features of the tumor, it is not always able to differentiate between simple contact and invasion of adjacent structures. Gdeedo and colleagues8 suggested that CT staging of bronchogenic carcinoma should not contraindicate therapy, due to the discrepancies observed between imaging TNM and postoperative pathological TNM. Their study recorded an agreement between the two in only 35.1% of patients; the primary T was correctly staged by CT in 54.1%, over-staged in 27%, and under-staged in 18.9%. The addition of positron-emission tomography to CT may improve the false-positive rate obtained by CT alone.9 Magnetic resonance imaging provides a clearer definition of soft-tissue planes than CT, and may be useful for defining possible nerve or bone invasion in superior sulcus tumors; however, it has no advantages over CT for the evaluation of mediastinal infiltration.10

From the outset, a number of surgeons led by Wain and colleagues11 in 1993, suggested that videothoracoscopy could be used for TNM staging. Later, Roviaro and colleagues,12 using the term "videothoracoscopic operative staging" and ourselves,13 preferring the term exploratory videothoracoscopy, reported that this method of evaluation was not only feasible but should become the first step in the surgical treatment of non-small-cell lung cancer. A major advantage of exploratory videothoracoscopy is that it minimizes the number of exploratory thoracotomies performed, by detecting cases of non-effusive pleural carcinomatosis not identifiable by diagnostic imaging methods, or by clearly confirming non-resectability where imaging results are unclear, particularly in cases of mediastinal invasion. Exploratory videothoracoscopy enables complete visual evaluation of local primary tumor involvement and invasion. The tumor can be not only inspected but also palpated, either digitally or with instruments inserted through the entry ports.

In cases of chest wall invasion by T3 tumors, videothoracoscopy confirms invasion and helps to define the extent of enbloc resection required, as well as facilitating a decision on the type of thoracotomy needed, depending on the predicted difficulty.13,14 A further advance in assessment of the T parameter is videothor-acoscopic intrapericardial examination of pulmonary vessels. This procedure, which we have termed video-pericardioscopy, has been successfully used in patients with suspected invasion of the pulmonary hilum and/or intrapericardial vessel involvement, detected by CT, magnetic resonance imaging, or exploratory videothoracoscopy.15,16 Pericardioscopy, using a mediastinoscope through a subxiphoid pericardial window, enables diagnosis and treatment of pericardial effusions (inflammatory, infectious, neoplastic, traumatic) by allowing the removal and examination of pericardial fluid as well as pericardial and epicardial biopsies, even in cases of cardiac tamponade.17,18 This procedure differs from videopericardioscopy in the approach (subxiphoid pericardial window vs. thoracoscopy and pericardiotomy), the purpose (analysis and treatment of effusions vs. evaluation of T4 cancer with intrapericardial vessel invasion), and surgical technique (endoscopy and biopsy vs. thoracoscopic surgery). The development of thoracoscopic surgery has enabled this application of videopericardioscopy, which overcomes the limitations imposed by the conventional approach through a subxiphoid window.

Our team performed videopericardioscopy in 27 patients in 2002.16 Fifteen patients had previously undergone CT that disclosed suspected invasion (particularly of the artery), while in the other 12, invasion was confirmed by exploratory videothoracoscopy. Pulmonary resection was indicated in 21 patients after confirmation of the feasibility of intrapericardial ligation of the vessels. Pompeo and colleagues19 recently reported the use of flexible videopericardioscopy in patients with radiologic evidence of proximal vascular invasion observed by multislice CT. In 7 of 21 patients undergoing flexible videopericardioscopy, radical resection was carried out. A further technical modification of videopericardioscopy has been described by Ohno and colleagues20 who used an endothoracic sonographic probe to obtain a more accurate assessment of the posterior aspect of the pulmonary artery. Two of our patients who underwent exploratory thoracotomy had previously been examined by videopericardioscopy that allowed visualization of the anterior aspect of vessels, which were free, but not of the posterior aspect of the pulmonary artery trunk, which was invaded. This could perhaps have been avoided by intrapericardial ultrasonography. To date, we have performed 91 videopericardioscopies, with comparable results.

Exploratory videothoracoscopy is of great value in the diagnosis and treatment of T4 with pleural effusion. Around 40% of cytological findings obtained by thoracentesis in malignant pleural effusion are inconclusive.21 In contrast, exploratory videothoracoscopy provides 90% sensitivity in the diagnosis of unconfirmed pleural effusion in bronchogenic cancer.22 Exploratory videothoracoscopy determines whether pleural effusion is secondary to venous or lymphatic obstruction to the tumor process, in which case, surgical resection may be considered, or secondary to pleural infiltration by carcinomatosis, in which case, surgery can be followed by talc pleurodesis. Mediastinoscopy has traditionally been used to evaluate mediastinal lymph node involvement (N). A meta-analysis of 14 studies reported a specificity of up to 100%, although sensitivity was only 81%23. This may be due to the relatively high rate of false negatives (9%) because mediastinoscopy is unable to reach posterior and inferior lymph node stations, and access to the subcarinal region is awkward. Access to lymph node stations 5 and 6 (anterior mediastinum and aortopulmonary window) is only possible using anterior mediastinotomy according to Chamberlain and colleagues,24,25 or extended cervical mediastinoscopy as described by Ginsberg and colleagues,26 which not all surgeons are willing to perform. For the assessment of mediastinal lymph node involvement, VATS provides full access to the pleural cavity, thus enabling exploration of all ipsilateral lymph node regions, even those not accessible by standard mediastinoscopy.27,28 VATS has also been found to be 92%–100% effective for biopsying lymph node stations 5 and 6.29–31 Roberts and colleagues32 found that the technique was valuable for establishing a diagnosis of N2 due to involvement of lymph node stations 8 and 9, particularly in patients with lower-lobe tumors and negative mediastinoscopy. Biopsies obtained by VATS for histological examination are comparable to those obtained by lymph node dissection using thoracotomy.32 Despite these undoubted advantages, most chest surgery departments fail to perform a systematic evaluation of N by videothoracoscopy, and only a few reports have addressed its systematic use in the assessment of lymph node involvement.33–35 Mouroux and colleagues35 advocate a combination of standard cervical mediastinoscopy and VATS, which increases the detection of lymph node metastases in doubtful cases.

Regarding the detection of intrapleural metastases (M), exploratory videothoracoscopy enables complete visual and instrumental exploration of the whole pulmonary and pleural surface as well as the taking of biopsies, thus allowing the surgeon to establish the nature of any lesion observed. In cases of pleural carcinomatosis, pleural seeding is more readily appreciated using this technique. Exploratory thoracotomy can thus be avoided, and biopsies can be taken. Drainage and pleurodesis can also be performed at the time of exploration in cases of pleural effusion.13,36 Where nodules are located in a lobe other than that occupied by the primary tumor, VATS allows them to be visualized, digitally or instrumentally palpated, biopsied, and resected.14 Although use of exploratory videothoracoscopy in lung cancer staging is becoming more widespread, there are few reports of its routine use as a first step in all patients who are to undergo surgery for lung cancer.14,37,38 However, insertion of the videothoracoscope for what Sihoe and Yim39 term "last-minute staging" takes no more than a few minutes, does not incur morbidity, and may avoid a significant number of exploratory thoracotomies.


   OUR SURGICAL TECHNIQUES
TOP
 ABSTRACT
 INTRODUCTION
 STAGING OF LUNG CANCER
 OUR SURGICAL TECHNIQUES
RESULTS
 SOLITARY PULMONARY NODULE
 OUR EXPERIENCE OF VTS...
 MAJOR PULMONARY RESECTION USING...
 OUR EXPERIENCE OF VATS
 REFERENCES
 
EXPLORATORY VIDEOTHORACOSCOPY
Under general anesthesia and selective intubation, the patient is placed in the lateral decubitus position, as for a posterolateral thoracotomy. Conventional instruments are at hand so that open surgery may be performed if required. Video monitors are placed on either side of the patient, so they can be comfortably viewed by the surgeon and assistants. Unlike the position routinely preferred for conventional thoracotomy, for exploratory videothoracoscopy, the surgeon stands facing the patient, together with the scrub nurse, while two assistants are placed behind the patient. A first entry port is made (12-mm trocar) over the 7th or 8th intercostal space in the mid axillary line, to allow insertion of the 0° lens, and subsequently, placement of the posteroinferior pleural drain. When previously unsuspected pleural carcinomatosis is observed, the procedure ends with the taking of a biopsy, generally through another entry port at the 3rd/4th intercostal space in the anterior axillary line; the second drain can be placed here, if required. Otherwise, a 3rd entry port is placed over the line of the potential thoracotomy incision, below the tip of the scapula, to continue the exploration (Figure 1Go). Use of 3 entry ports allows visual and surgical exploration of the whole pleural cavity. Adhesions are detached surgically with electrocauterization of the wound or, more recently, using an ultrasonic scalpel. Exploration is then extended to the pleural, visceral, mediastinal, and diaphragm surfaces; fissures are examined for possible tumor infiltration, and ipsilateral lymph nodes are visualized and biopsied if necessary. Where there is doubt as to possible invasion, or where undiagnosed pulmonary nodules are found, biopsies can be taken intraoperatively to guide decision-making. Having completed the exploration, the surgeon can then proceed to videothoracoscopic surgery or thoracotomy that may be either lateral or posterolateral (mainly in cases of chest wall invasion). When exploring the mediastinum to check for possible invasion, it should be noted that good mediastinal mobility and flexibility generally suggest the absence of invasion, while vascular buckling (invisible to the naked eye but visible using a thoracoscope, a finding made during exploratory videothoracoscopy and confirmed intraoperatively) is indicative of invasion (Figure 2Go); in our department, this is known as the Loscertales sign. In cases of anterior mediastinal involvement and/or extrapericardial invasion of pulmonary vessels, where it is impossible to assess the feasibility of resection, the use of videopericardioscopy is indicated.


Figure 1
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  		Figure 1. Entry ports and lines showing position of lateral and posterolateral thoracotomies. The arrow indicates the site of a possible fourth entry port.

 

Figure 2
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  		Figure 2. Vascular buckling indicative of tumor invasion (Loscertales’ sign).

 
VIDEOPERICARDIOSCOPY
Using the same entry ports as for exploratory videothoracoscopy, with the possible addition of a 4th port on the line of the potential thoracotomy, this exploration can be performed comfortably and with little or no risk. The pericardium is opened at the pulmonary vein level, posterior to the phrenic nerve, to avoid damaging the nerve. The collapsed lung is retracted using endosurgical instruments inserted through the posterior entry port to expose the pericardium, which is gently separated from the myocardium. Using Endoshears or Endo-dissect forceps with monopolar cautery, a point on the pericardium is cauterized open; the opening is then extended 3–4 cm longitudinally in the direction of the pulmonary artery to enable intrapericardial exploration. In cases of intrapericardial effusion (indicated by pericardial tension), the fluid starts to flow after the initial opening, and specimens can be taken for cytological examination if required. The incision can then be widened to allow insertion of an aspirator. Once the pericardium is open, one border is retracted and the thoracoscope is inserted into the pericardial cavity. This maneuver may be facilitated using the aspirator, an instrument that not only keeps the cavity clean and helps to separate tissues, but may also be used as a measuring guide (it is 5 mm in diameter). At this stage, the length of tumor-free vessel can be determined, and thus the feasibility of surgery (intrapericardial pneumonectomy via thoracotomy) with intrapericardial vessel ligation.

It is easier to explore the artery from the left side (Figure 3AGo) than from the right side. The first structures encountered are the left atrium and left atrial appendage, followed by the pulmonary veins, which are clearly visible. Using the aspirator to depress the atrium, the pulmonary artery trunk and its bifurcation can be readily visualized. The maneuvers described earlier can be used to determine whether there is sufficient free space for intrapericardial ligation of the vessel. Using a right-sided approach, the first structures encountered are the right atrium and superior vena cava, together with the ascending aorta. Visualization of the pulmonary artery is more difficult because the superior vena cava has to be depressed and pushed forwards; this can be achieved with the aspirator, leaving the pulmonary artery clearly visible as it passes beneath (Figure 3BGo). If necessary, the thoracoscope can be switched from its initial entry port to the port located in the 3rd intercostal space to explore the inferior pulmonary vein, as the superior pulmonary vein is readily visible from the original camera port. At the end of the exploration, either a thoracotomy is performed for pulmonary resection or if resection is not feasible, an intrapericardial biopsy is taken when appropriate, and 1 or 2 pleural stents are placed in the inferior and anteroinferior entry ports (Figure 4Go).


Figure 3
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  		Figure 3. (A) Left videopericardioscopy, showing invasion-free left atrial appendage, upper pulmonary vein and pulmonary artery. (B) Right videopericardioscopy, showing the aspirator pushing the superior vena cava forward to check that the pulmonary artery has sufficient free margin to enable intrapericardial dissection.

 

Figure 4
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  		Figure 4. Intrapericardial biopsy of a tumor invading the left pulmonary artery.

 

   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 STAGING OF LUNG CANCER
 OUR SURGICAL TECHNIQUES
 RESULTS
SOLITARY PULMONARY NODULE
 OUR EXPERIENCE OF VTS...
 MAJOR PULMONARY RESECTION USING...
 OUR EXPERIENCE OF VATS
 REFERENCES
 
Since July 1992, we have been performing exploratory videothoracoscopy as a first step in lung cancer treatment, with a view to final staging and evaluation of the feasibility of pulmonary excision. Until March 1993, patients underwent thoracotomy after exploratory videothoracoscopy, to confirm videothoracoscopic findings by conventional exploration. Thereafter, thoracotomy ceased to be performed in cases that exploratory videothoracoscopy had shown to be non-resectable. Between March 1993 and December 2007, 1,381 patients with bronchogenic carcinoma were treated in our department. In all cases, clinical staging had been carried out using routine methods (radiography, CT, bronchoscopy, fine-needle aspiration biopsy); mediastinoscopy is not systematically performed as we believe that final lymph node staging is more accurate using exploratory videothoracoscopy. In 1,277 patients, resectability was assessed and final staging completed by videothoracoscopy. This was not possible in the remaining 104 patients, largely due to firm pleural adhesions or evidence of invasion that could not be clarified by exploratory videothoracoscopy; 61 of them underwent resection after thoracotomy, but resection was not feasible in 43 (3.1% of patients undergoing exploratory thoracotomy). The reasons for exploratory thoracotomy in resectable patients were: pleural adhesions in 47; lung collapse preventing complete exploration in 6; intolerance of single-lung ventilation in 1; and in the other 7, suspected bronchial or posterior mediastinal invasion required thoracotomy to attempt resection, which was successful in all cases. In non-resectable patients, thoracotomy was performed due to firm pleural adhesions in 25 cases, failed lung collapse in 5, chest-wall infiltration preventing mobilization and thus exploration in 4, a further 8 patients could not be properly explored for bronchial invasion during exploratory videothoracoscopy, and resection was impossible in the remaining patient due to hemodynamic instability after clamping the pulmonary artery. Resection was not feasible in 36 patients with mediastinal invasion, in 4 with un-assessed carcinomatosis in whom exploratory videothoracoscopy was not possible, and in 3 with functional intolerance of the required pneumonectomy.

Exploratory videothoracoscopy was performed in 141 patients who were subsequently deemed unsuitable for surgery: 81 had mediastinal invasion that had been suspected after CT, 38 had non-effusive pleural carcinomatosis, 6 had both, and 16 displayed trans-fissure and vascular invasion that contraindicated lobectomy and even sleeve lobectomy; pneumonectomy was thus required in these patients, but was not tolerated due to functional contraindications. Exploratory thoracotomy was avoided in all these patients (10.2%). The mean duration of exploratory videothoracoscopy in the least complex cases, i.e., those in whom resectability was immediately seen as feasible (T1–T2 N0) or wholly unfeasible (e.g., pleural carcinomatosis), was 10–15 min, whilst in more complex cases, the procedure took 30–40 min. Generally speaking, more time was spent on non-resectable cases, which required a very thorough exploration before a decision was taken. Exploratory thoracotomy usually takes around 60 min, and the postoperative recovery is not always as satisfactory as one might wish. Because of the surgical wound, patients take longer to recover and experience twofold immunodepression because of the cancer and the surgical procedure. This is sometimes exacerbated by difficulties in postoperative lung inflation.

Videopericardioscopy was performed in 91 patients over the same period; it was indicated in 45 because CT suggested possible hilar and vascular invasion, and in 46 because invasion was confirmed by exploratory videothoracoscopy. In 61 of these 91 patients, pulmonary resection was undertaken after checking the feasibility of intrapericardial vessel ligation (4.4% of all exploratory videothoracoscopy patients, and 67% of those undergoing videopericardioscopy); 31 of these had been classified as non-resectable by CT (6 were assessed elsewhere and classified as totally non-resectable), these were assigned to surgery. In the other 30 patients undergoing resection, invasion was encountered during exploratory videothoracoscopy. There were 55 pneumonectomies, 4 upper right lobectomies, and 2 upper left lobectomies. Evaluation by exploratory videothoracoscopy was hindered in 3 right lobectomies by lack of lung mobility due to chest wall invasion, and in a further case, adhesions impeded evaluation of the hilum. One of the 2 patients undergoing upper left lobectomy had previously received neoadjuvant chemotherapy, and exploratory videothoracoscopy suggested mediastinal infiltration. In the other, there were doubts as to the feasibility of resection because of the hilar location of the tumor and aortopulmonary window lymph node involvement.

In all pneumonectomies, vascular and pericardial invasion was confirmed by histology, with no invasion of the resection margins. Two patients displayed distal intra-pericardial infiltration of the pulmonary artery, but there was sufficient margin for dissection and ligation; the section border was also free. In 30 patients, intrapericardial vessel invasion rendered dissection (and therefore resection) impossible. Invasion of the pulmonary artery was observed in 17 of these patients, invasion of both the artery and the upper pulmonary vein in 6, and of the pulmonary artery and superior vena cava in 2, evidently in right-sided tumors. The remaining 5 patients displayed considerable invasion of the left atrium and pulmonary veins, which prevented resection. The duration of videopericardioscopy ranged from 16 to 33 min (mean, 23 min). Thus the resection procedure was not significantly prolonged by videopericardioscopy, which reduced the number of exploratory thoracotomies required. The mean length of stay for patients undergoing videopericardioscopy without resection was 2.4 days. This allowed them to be referred very rapidly for neoadjuvant treatment, which would not have been possible if they had undergone exploratory thoracotomy. In patients undergoing resection, the length of postoperative stay is not relevant as it is due to lung resection via thoracotomy rather than to videopericardioscopy.


   SOLITARY PULMONARY NODULE
TOP
 ABSTRACT
 INTRODUCTION
 STAGING OF LUNG CANCER
 OUR SURGICAL TECHNIQUES
 RESULTS
 SOLITARY PULMONARY NODULE
OUR EXPERIENCE OF VTS...
 MAJOR PULMONARY RESECTION USING...
 OUR EXPERIENCE OF VATS
 REFERENCES
 
Technological progress in the development of lenses, videos, monitors, and surgical instruments (all specially adapted for endoscopic use) has enabled countless diagnostic and therapeutic procedures to be carried out, which would previously have been unthinkable. In every 500 chest radiographs, one new solitary pulmonary nodule is discovered; 9% of patients display no symptoms. Given that around half the nodules detected are malignant, the quest for early detection has assumed growing importance. High-resolution helical CT scanning has enabled the diagnosis of more and smaller nodules, many of which represent a major diagnostic and therapeutic dilemma40,41. A number of factors point to the potential malignancy of solitary pulmonary nodules, including age, tobacco use, nodule size, demonstrable growth in the interval between consecutive examinations, and history of malignant tumors. Where the tumor is accessible using a bronchoscopic approach, samples can be taken for histological analysis. Unfortunately, in most cases the solitary pulmonary nodules is either peripherally located and/or <1 cm, and bronchoscopy is futile. Other methods are therefore required to ensure accurate histological typing. Moreover, given the high malignancy rate among solitary pulmonary nodules, all nodules have to be considered malignant unless proved otherwise, and it is therefore essential to obtain an accurate histological diagnosis as quickly as possible. Schwarz and colleagues42 reported promising results using electromagnetic navigation based on virtual bronchoscopy and real-time 3-dimensional CT images, a technique that has been shown to be capable of reaching peripheral lung masses beyond the reach of the standard bronchoscope; however, sampling for subsequent histological examination has not been performed, and the patient series are still very small.

Small lesions not accessible to the bronchoscope may be reached using CT-guided percutaneous fine-needle aspiration biopsy, although this avoids surgery in only 10% of cases, because if the nodule has to be removed, or if the diagnosis is inconclusive, an excisional biopsy is still considered the most reasonable option to obtain a sample for histological examination.43 There is some controversy regarding the use of fine-needle aspiration biopsy in the diagnosis of solitary pulmonary nodules, due to the high rate of false negatives, reportedly up to 29%, the occurrence of pneumothorax in roughly 30% of cases, although it often requires no specific therapeutic maneuvers, and the philosophical belief that it is an expensive procedure associated with considerable morbidity and with limited influence on therapeutic decision-making.22,44,45

Since 1992, a number of studies have suggested that videothoracoscopic surgery (VTS) may be an ideal procedure for the diagnosis and therapeutic management of solitary pulmonary nodules.46 Thoracoscopic Nd:YAG laser resection has been successfully used for various clearly benign nodules (hamartomas).47 VTS has become an increasingly routine procedure in the management of solitary pulmonary nodules, largely because it obviates the need for thoracotomy; results have been published for large series of patients.48–51 However, even among experienced surgeons, a common problem is the difficulty in locating the solitary pulmonary nodule during VTS, particularly if it is only around 1 cm in diameter and/or located deep in the pulmonary parenchyma (3–4 cm from the visceral pleura). A number of techniques have been developed to enable preoperative nodule localization, including visual inspection with instrumental or digital palpation (the finger is inserted through one of the entry ports), injection of dyes or radiotracers into the nodule, use of a hookwire, or intraoperative sonography (all guided by preoperative CT). Studies suggest that all these techniques yield similar results.51,52

One widely used technique is the immediately preoperative insertion of a CT-guided hookwire.41,48,49,53–55 This has proved to be highly effective if the nodule is small and/or located deep within the parenchyma, but great caution is required in handling the hookwire as it could work loose during transport of the patient from the X-ray Department to the operating theater, or once there, while changing the patient’s position, and it could also work loose during lung collapse, a finding reported in 4% to 47% of patients.41,54–57 To avoid hookwire detachment during lung collapse, once the patient has been placed in the lateral decubitus position, we insert the wire 3–4 cm into the pleural cavity and section it flush with the skin, so that as it collapses, the lung pulls the wire into the pleural cavity. It is easier to do this than to detach the wire from the nodule; hookwire detachment has thus only occurred in 6.7% of cases, all of which were among the first 150 patients in whom this technique was used. Use of a CT-guided hookwire has enabled localization and removal of nodules in almost 100% of patients, because even if it is detached, the wire tends to leave a small bruise mark on the lung, which itself facilitates nodule localization.48,49,55

Another widely used method for solitary pulmonary nodules localization is CT-guided percutaneous staining with methylene blue.58 Although excellent results have been reported, the technique is becoming less common because even better results are obtained with the hookwire. Intraoperative sonography is used to locate solitary pulmonary nodules during VTS, as it is able to pinpoint invisible non-palpable nodules.59 The drawback is that it is not available in all hospitals. Excellent results have been reported for nodule localization using CT-guided percutaneous injection of a radiotracer (technetium 99 m gamma-emitting solution, technetium 99 m macro-aggregated albumin), although the technique requires use of an intraoperative radio-probe not available in all hospitals.22 Grogan and colleagues60 located 95% of solitary pulmonary nodules using this technique, and recommend its use even in open surgery to locate small or deep-seated nodules. Gonfiotti and colleagues41 and Davini and colleagues61 reported better results and fewer complications with a radiotracer than with the hookwire.

Another sophisticated technique for nodule localization is CT-guided marking using a Lasermarker. Klöppel and colleagues62 suggested that this is a promising approach, reporting 100% positive results in a small patient series; but here again, the limited availability of the Lasermarker in hospitals will limit its use. Although not strictly intended for nodule localization but rather for histological examination, fine-needle aspiration biopsy during VTS enables wedge resection to be avoided and surgery to be performed directly, using either VATS or an open approach.63 Our team has for many years performed a cutting-needle biopsy (Tru-Cut; Baxter Healthcare Corporation) to obtain a tissue cylinder from the nodule; this enables accurate diagnosis and obviates the need for wedge resection.48 This technique is of particular value where the nodule is difficult to locate or is close to large vessels, and wedge resection is thus considered unsafe. Nevertheless, we still consider wedge resection the best method of ensuring an accurate diagnosis. In fact, most surgeons use more than one method for locating nodules, depending on their size, depth, and anatomical site. A number of surgeons routinely use a combination of hookwire, preoperative injection of methylene blue or radiotracer, visualization, and intraoperative instrumental or digital palpation.46,48,64 Sortini and colleagues65 suggested that intraoperative sonography yields better results than either digital palpation or radiotracer injection, and is associated with fewer complications than radiotracer injection.

Another key issue is the management of the nodule once located. Most surgeons prefer to perform wedge resection using an Endostapler, a procedure ensuring accurate histological typing of the solitary pulmonary nodules; benign solitary pulmonary nodules can then be left untreated, and malignant nodules can be removed immediately, by either VATS or conventional open surgery.40,44,47,48,56,57,61,62,65 As we have suggested, wedge resection can be bypassed by intraoperative fine-needle or cutting-needle biopsy.48,64 Others have performed both wedge resection using an Endostapler (72% of cases) and Nd:YAG laser resection (18% of cases), reporting comparably good results; the two techniques have also been used jointly (10% of cases).66 However, laser resection has never become a popular technique. VTS is now perhaps the most widely used technique for diagnosis and treatment of solitary pulmonary nodules as it is highly effective and associated with low risk.48,67–69 However, some cases may require a minithoracotomy (the procedure is then termed VATS rather than VTS), or conversion to thoracotomy due to the impossibility of locating and/or removing the nodule, particularly if it is located deep in the parenchyma, but such cases are rare.48,55 Mack and colleagues66 and Hazelrigg and colleagues69 reported that thoracoscopy provides a minimally invasive approach for the diagnosis and treatment of solitary pulmonary nodules, with almost 100% sensitivity, 100% specificity, minimum morbidity, and no mortality. In a comparison of percutaneous biopsy and videothoracoscopy, Mitruka and colleagues70 found that VTS afforded may advantages, including more accurate diagnosis of resectable nodules. Finally, wide-margin wedge resection appears to be an effective method of treating certain pulmonary carcinomas presenting as solitary pulmonary nodules in patients with poor cardiorespiratory status, although delayed recurrence rates were greater than in those undergoing lobectomy; nevertheless, perioperative mortality was 0% for wide-margin wedge resection, compared to 2.3% for lobectomy.71 Five-year survival rates were 61.1% and 82.5%, respectively, suggesting that lobectomy should still be the procedure of choice, even though wide-margin wedge resection may be preferable in patients with impaired cardiorespiratory function.


   OUR EXPERIENCE OF VTS IN SOLITARY PULMONARY NODULES
TOP
 ABSTRACT
 INTRODUCTION
 STAGING OF LUNG CANCER
 OUR SURGICAL TECHNIQUES
 RESULTS
 SOLITARY PULMONARY NODULE
 OUR EXPERIENCE OF VTS...
MAJOR PULMONARY RESECTION USING...
 OUR EXPERIENCE OF VATS
 REFERENCES
 
We first performed VTS in 1992. Since then, we have examined 382 cases of solitary pulmonary nodules; VTS was attempted in all, but conversion to thoracotomy was required in 15 patients in whom VTS was unable to locate a small nodule situated deep in the pulmonary parenchyma. These cases are thus excluded from the total number of solitary pulmonary nodules treated by VTS. The surgical technique was as described for exploratory videothoracoscopy with regard to entry ports for the camera and working instruments. A 4th entry port may also be placed in the 6th intercostal space, over the hypothetical thoracotomy incision line. This port can be used for digital palpation, for the Endostapler (if the other 2 ports are being used for forceps), and for supporting the lung or the forceps (if the Endostapler is inserted through one of the more usual upper entry ports). The final decision on port deployment will depend largely on the location and size of the nodule. In 60 patients with small (around 1 cm diameter) and/or deep-seated nodules, location was achieved by CT-guided hookwire on the morning of surgery, with the protruding part of the wire attached as firmly as possible to the skin using a plaster to prevent it from working loose. At first, surgery was started following selective intubation, as soon as the patient was placed in the lateral decubitus position; however, it soon became evident that the hookwire tended to become detached from the lung at the moment of lung collapse, due to either entry of air into the pleural cavity or to maneuvers intended to position the patient for wedge resection; this occurred in 4 cases (6.7% of 60 hookwires implanted). Thereafter, the hookwire was inserted 3–4 cm into the chest before any incision was made, and sectioned flush with the skin, as indicated earlier. Since then, there has been no detachment of the hookwire from a tumor. In the remaining cases, the nodule was localized by instrumental palpation and visualization in 203 patients, and by digital palpation in 104.

We have always had a clear preference for wedge resection, which we have so far performed in 363 cases using the Endogia blue cartridge Endostapler (Tyco Healthcare), together with Seamguard bioabsorbable staple line reinforcement (WL Gore & Associates) for the last 6 years, which helps to minimize postoperative air leaks; this has not been associated with any form of morbidity. In the remaining 4 cases, a Tru-Cut cutting-needle biopsy was undertaken due to the proximity of the nodule to lobar vessels. Histological classification of the resected nodules is shown in Tables 1Go and 2Go. VTS enabled accurate histological diagnosis in all cases, i.e., it yielded 100% sensitivity and 100% specificity (Table 3Go). Oncological procedures performed in these patients are shown in Table 4Go. None of the 367 patients died, and morbidity was both mild and infrequent, mostly in the form of air leaks (less common now that the Seamguard is used), leading to subcutaneous emphysema and small pneumothorax responding to prolonged drainage. Mean hospital stay (including only patients undergoing wedge resection but not those undergoing major pulmonary resection, whose stay was determined by the resection rather than VTS) was 2.3 days (range, 1–9 days). It may thus be concluded that VTS is an extremely valuable procedure for the diagnosis and treatment of solitary pulmonary nodules, offering 100% specificity and sensitivity, limited mild morbidity, and no mortality. It should therefore be the procedure of choice for solitary pulmonary nodules of unknown etiology.


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  		Table 1. Malignant histology in 247 patients
 

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  		Table 2. Benign histology in 120 patients
 

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  		Table 3. Diagnostic surgery in 367 patients
 

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  		Table 4. Oncological resections in 190 patients
 

   MAJOR PULMONARY RESECTION USING VATS
TOP
 ABSTRACT
 INTRODUCTION
 STAGING OF LUNG CANCER
 OUR SURGICAL TECHNIQUES
 RESULTS
 SOLITARY PULMONARY NODULE
 OUR EXPERIENCE OF VTS...
 MAJOR PULMONARY RESECTION USING...
OUR EXPERIENCE OF VATS
 REFERENCES
 
Major pulmonary resection using VATS is a widely accepted and wholly feasible procedure for the treatment of early stage non-small-cell bronchogenic carcinoma and benign lung pathologies. Reports of VATS major resections, covering increasingly large patient groups, are constantly being published worldwide, particularly in North America, Europe, and Asia.72,73,75 However, a number of concerns have been expressed regarding this relatively new procedure, particularly on the lack of absolute indications and a standardized surgical technique, with significant differences in technique from one center to another. Major pulmonary resections (chiefly lobectomies, but also pneumonectomies and sleeve lobectomies) are considered to be among the most complex procedures performed using minimally invasive surgery.75 At present, only a few specialist centers consider this the procedure of choice for the treatment of early stage lung cancer.

A review of the literature and of our own experience suggests the following indications for VATS major pulmonary resection. First, the tumor should measure <4 cm, so that it can be extracted through the mini-thoracotomy. This is the ideal maximum size, although occasionally tumors up to 6 cm have been successfully extracted.76 Second, the tumor should be peripheral. McKenna and colleagues72 suggested that the tumor should be at least 1 cm from the fissure, although we feel that VATS lobectomy may be indicated even if the tumor is closer to the fissure. Third, the tumor should be early stage, particularly stage 1 (cN0), although this is not a totally exclusive criterion. Contraindications include invasion of the chest wall, tumor spread across the fissure, invasion of the pericardium or diaphragm, and also prior neoadjuvant radiotherapy or chemotherapy.74,77 Intraoperative discovery of small N2 lymph nodes does not necessarily signify that VATS resection should be abandoned, although Roviaro and colleagues78 recommend conversion to thoracotomy, regardless of the operative stage at which the discovery is made. This may reflect a desire to ensure a homogeneous N0 series and enable comparison of results, rather than the impossibility of proceeding with VATS lobectomy and lymph node removal. Finally, fissures should be open rather than fused, although this is not essential for certain lobectomies, for example those involving the right upper lobe.

Although there is no single standardized technique for VATS lobectomy, variations between schools are generally slight. The greatest differences are in the placing of the trocars and the utility minithoracotomy, which will prompt differences in the dissection of hilar and lobar structures, and positioning of the surgeon behind or in front of the patient. Most surgeons perform lobectomy with anatomical dissection of vascular and bronchial structures;72–4,79 however, Lewis and colleagues80 reported excellent results with non-rib spreading simultaneously stapled lobectomy. We achieved a similarly successful outcome with this technique on 4 occasions. The main features of our habitual surgical technique are outlined below.

The patient is placed in the lateral decubitus position with selective intubation. Three entry ports are made, as for exploratory videothoracoscopy. Once the feasibility of the procedure has been confirmed, a 4–5-cm anterior utility minithoracotomy is made at the 5th intercostal space, with no rib spreading, through which surgical instruments are inserted for vascular and bronchial dissection. A 0° 10-mm thoracoscope is used, and although the lower entry port is usually reserved for the camera, the port sometimes has to be changed to enable frontal visualization, particularly to the upper anterior port for artery dissection in upper lobectomies and to the minithoracotomy, so that the Endostapler can be inserted through the lower port. We recommend systematic anatomical dissection of hilar structures, except on rare occasions when technical difficulties require block sectioning and suture of the fissure, bronchus, and artery, using the technique that Lewis and colleagues80 term "simultaneously stapled lobectomy". Dissection of the vessels and bronchus is mainly performed via the utility minithoracotomy using endoscopic and conventional material. The whole procedure is carried out watching the video monitor, since nothing can be seen through the minithoracotomy when a rib spreader is not used (except occasionally for a brief interval at the end of surgery to allow extraction of the tumor). Those lobectomies in which the surgeon mainly operates looking through the a-VATS (assisted endoscopic lobectomy) minithoracotomy are not VATS lobectomies, as Yim and colleagues81 noted, but more properly minithoracotomies with video assistance, and do not share the advantages of c-VATS (complete endoscopic lobectomies).

The advantages of VATS lobectomy over conventional thoracotomy have been highlighted in a number of studies. Whitson and colleagues82 found that VATS patients, despite having more comorbidities (chronic renal insufficiency, hypertension, previous malignancies), had fewer postoperative complications, and concluded that VATS lobectomy appeared to be a less morbid operation. A review of the literature suggests that VATS patients experience less postoperative pain and require fewer analgesics.83,84 Postoperative length of stay is also considerably shorter. McKenna and colleagues85 recently reported that using a fast-tracking protocol, VATS lobectomy with anatomic dissection can be performed with minimal complications, a short postoperative length of stay, and reduced costs. Functional recovery is faster, which helps to maintain or preserve lung function; for that reason, a number of researchers, including Cattaneo and colleagues,86 particularly recommend this technique for elderly patients or those with poor lung function. In a multi-institutional study comparing c-VATS with a-VATS and conventional thoracotomy, Shigemura and colleagues87 found that patients undergoing c-VATS had less blood loss, faster recovery, shorter hospitalization, and a faster return to work than patients undergoing lobectomy with a-VATS and open approaches. VATS has other major advantages in the immediate postoperative period, including a less marked inflammatory response: patients undergoing VATS displayed significantly lower levels of interleukins (IL-6, IL-8, IL-10) and C-reactive protein than those undergoing conventional open surgery.88,89 Craig and colleagues90 studied levels of C-reactive protein, IL-6, tumor necrosis factor (TNF), TNF receptors (TNF-Sr55, TNF-sr75), P-Selectin and phagocyte reactive oxygen species in 24 patients (12 treated with VATS and 12 with thoracotomy) and found that open surgery increased the acute phase inflammatory response, while VATS was associated with lower C-reactive protein and IL-6 levels, and thoracotomy with an increase in reactive oxygen species in neutrophils; they concluded that pulmonary lobectomy was associated with reduced perioperative changes in acute phase responses. In a study of the postoperative changes in leukocytes, lymphocyte subsets, B cells, T cells, and natural killer cells in patients undergoing lung resection with VATS versus thoracotomy approaches, Ng and colleagues91 found significantly increased total white cell numbers, compared with preoperative values on postoperative day 1, 3, and 7 in all patients. On postoperative day 1, although T8 cells and natural killer cells were reduced in both groups, total T cell, T4 cell, and lymphocyte numbers were significantly reduced only in the thoracotomy group. On postoperative day 7, natural killer cell numbers were significantly lower in the thoracotomy group than in the VATS group. The latter recovered better and faster from postoperative immunosuppression. The same group found that VATS patients had higher circulating levels of insulin-like growth factor binding protein-3 and lower levels of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 early postoperatively, thus ensuring improved postoperative tumor immunosurveillance.92

Lobectomies using minimally invasive surgical techniques are also associated with a lower incidence of atrial fibrillation than those performed by thoracotomy.93 Regarding the outcome of different surgical techniques, it was initially argued that mortality and morbidity were greater with VATS than with conventional surgery; however, the procedure has undergone constant refinement, and the publication of increasingly large series (Table 5Go) shows that mortality rates are very low, ranging from 0.4% reported by Yim and colleagues95 to 3.7% recorded by Daniels and colleagues,93 and that morbidity is similar or lower than that in open surgery.


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  		Table 5. Morbidity and mortality rates in large series of patients undergoing video-assisted thoracoscopic surgery
 
Another area of initial controversy was operating time. In our experience, the mean duration is 153 min;74 in the early days, operations clearly took longer and this has undoubtedly affected calculation of mean operating time, but today our own mean is <120 min (median, 95 min); given that the time required to open and close a thoracotomy, the overall operating time with VATS is thus similar to or (for experienced surgeons) even slightly shorter than that of conventional thoracotomy. Ferguson and colleagues99 suggested that as the technique becomes standardized in greater detail, and as more specialist centers offer the opportunity for practical training, the learning curve involved will gradually disappear.

Last, but not least, a number of papers have examined oncological outcomes in large patient groups. Kaseda and colleagues98 reported 5-year survival rates as high as 97%, although survival rates are generally very similar to those achieved with open surgery. Even so, certain groups, including Roviaro and colleagues,100 claim "the results of VATS lobectomy are on a par with the best data obtained after conventional surgery". Minimally invasive surgery limits tissue damage and reduces postoperative immunological depression. Both VATS and conventional thoracotomy enable radical oncological surgery. Survival rates for cancer patients undergoing VATS versus thoracotomy are: T1N0, 83.5% vs. 70.21%; T2N0, 71.13% vs. 66.12%. Thomas and colleagues101 reported that "VATS lung resection with lymph node dissection achieved a 5-year survival similar to that achieved by the conventional approach. VATS is a valuable option for the management of selected patients with an early stage NSCLC". Shiraishi and colleagues102 concluded that overall 5-year survival rates associated with the thoracoscopic and standard procedure were 89.1% and 77.7%, respectively. Our findings suggest that thoracoscopic surgery is not inferior in its ability to achieve locoregional control in comparison with the standard procedure.

Naturally, if resection is complete and fulfills the criteria for oncological surgery, and if there is full removal of mediastinal lymph nodes, there is no reason why the surgical approach should modify long-term patient survival rates, although the better results reported for VATS may be due to the better immunological results associated with this technique. Iwasaki and colleagues103 reported that VATS resection with removal of mediastinal lymph nodes yielded a 5-year-survival rate of 77.3% in stage I and II patients. Sugi and colleagues96 performed lymph node dissections in a similar manner in VATS and conventional surgery groups, with no significant differences in the number of dissected lymph nodes. Survival rates were similar: 85% for the thoracotomy group and 90% for the VATS group.


   OUR EXPERIENCE OF VATS
TOP
 ABSTRACT
 INTRODUCTION
 STAGING OF LUNG CANCER
 OUR SURGICAL TECHNIQUES
 RESULTS
 SOLITARY PULMONARY NODULE
 OUR EXPERIENCE OF VTS...
 MAJOR PULMONARY RESECTION USING...
 OUR EXPERIENCE OF VATS
REFERENCES
 
From March 1993 to February 2007, we performed 260 major pulmonary resections using VATS. Thirty-nine patients were female. Mean patient age was 62.3 years (range, 12–83 years; median, 63 years; mode, 61 years). Non-small-cell bronchogenic carcinoma was diagnosed in 224 cases, benign lung pathologies in 26 (pulmonary sequestration, cystic adenomatoid malformation, bronchiectasis, aspergilloma), and carcinoid tumor in 5; the remaining 5 had metastases that could not be treated by wedge resection and required lobectomy. Twenty-two pneumonectomies were carried out (13 right, 9 left). The frequency of lobe involvement was: right upper lobe 76, left upper lobe 49, left lower lobe 42, and right lower lobe 41; medial lobectomy was performed in 11 cases, lower bilobectomy in 8, and upper bilobectomy in 9 cases. The conversion rate, which was higher when the technique was first used, was 9.2% (24 patients), conversion to open surgery being due to bleeding in 12 cases, technical difficulties in 11; and in the remaining case, invasion of the pulmonary artery was confirmed after vein dissection. Mean operating time for this patient series is currently 120 min, but the median time is 95 min, as the operation took longer in the early days of the technique, which it is now fully mastered and takes less time. Mean postoperative stay is 4.1 days. The morbidity rate is 15%, mostly involving readily resolved minor complications. The most common complication is air leak >4 days. Perioperative (30-day) mortality is 2% (2 cases of sepsis, 1 acute myocardial infarction, 1 pulmonary thromboembolism, 1 bronchopleural fistula with heart failure). The current actuarial 5-year survival rate is 77.7% for cancer patients. Follow-up detected mediastinal recurrence in 3 patients, cerebral and costal metastasis in 1, metachromic tumors in 2, same-lung metastasis in 3, cerebral metastasis in 7, multiple metastases in 7, acute myocardial infarction in 2, and others in 3.

In conclusion, provided that patients are properly selected, VATS lobectomy performed by experienced surgeons is a safe and viable procedure that meets oncological criteria for lung cancer surgery, because, as in conventional surgery, mediastinal lymph nodes can be removed simultaneously. Our own data and other reported results suggest that VATS lobectomy is associated with lower morbidity and mortality rates than conventional surgery; postoperative recovery is faster, and perhaps most importantly, survival rates are similar to those of open surgery. This procedure should be the treatment of choice for a number of benign lung pathologies and for bronchogenic carcinomas T1–T2 N0 M0. Randomized prospective studies are required to provide further evidence for this recommendation.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 STAGING OF LUNG CANCER
 OUR SURGICAL TECHNIQUES
 RESULTS
 SOLITARY PULMONARY NODULE
 OUR EXPERIENCE OF VTS...
 MAJOR PULMONARY RESECTION USING...
 OUR EXPERIENCE OF VATS
 REFERENCES
 

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Asian Cardiovasc Thorac Ann 2009; 17:313-326
© 2009 by SAGE Publications
DOI: 10.1177/0218492309104747



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