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Eur J Cardiothorac Surg 2007;32:843-847. doi:10.1016/j.ejcts.2007.09.002
Copyright © 2007, European Association for Cardio-thoracic Surgery. Published by Elsevier. All rights reserved.
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Thoracoscopic localization techniques for patients with solitary pulmonary nodule: hookwire versus radio-guided surgery

Alessandro Gonfiottia,*, Federico Davinia, Luca Vaggellib, Agostino De Franciscic, Adele Caldarellad, Paolo Maria Giglia, Alberto Jannia

a Thoracic Surgery Unit, University Hospital Careggi, Florence, Italy
b Division of Nuclear Medicine, University Hospital Careggi, Florence, Italy
c Department of Radiology, University Hospital Careggi, Florence, Italy
d Department of Human Pathology and Oncology, University Hospital Careggi, Florence, Italy

Received 17 May 2007; received in revised form 28 August 2007; accepted 3 September 2007.

* Corresponding author. Address: Thoracic Surgery Unit, University Hospital Careggi, Viale Pieraccini 17, Firenze 50100, Italy. Tel.: +39 055 7947935; fax: +39 055 7947935. (Email: agonfiotti{at}hotmail.com).


   Abstract
Top
 Abstract
1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
Objective: Our aim was to evaluate the best intrathoracoscopic localization technique between hookwire and radio-guided surgery, in patients with pulmonary nodule. Methods: From January 2000 to January 2005 we enrolled in this study 50 patients with a solitary pulmonary nodule, prospective randomized in two groups, well matched for diameter and depth of the pulmonary lesion. In 25 patients we performed the hookwire technique (Group A), whereas in the other 25 patients radio-guided localization was adopted (Group B). In both groups the localization technique was compared with finger palpation. In Group A, 9 lesions were in the left and 16 in the right lung; in Group B, 14 nodules were in the left lung and 11 in the right one. In both groups, the distance of the nodule from the pleural surface with lung inflated was 2.5 cm (1.5–2.5 cm in 12 patients, and >2.5 cm for the remaining 13). The mean size of the nodules in both groups was 1.1, range 0.6–1.9 (≤1 cm n = 18 patients, and >1 cm n = 7 patients). Results: All patients underwent thoracoscopic wedge resection, and 23 patients with a primary pulmonary lesion underwent thoracotomy for lobectomy and radical mediastinal lymphadenectomy. In Group A the hookwire technique localized the nodule in 21 of 25 patients (84%) whereas finger palpation localized it in 7 of 25 patients (28%). In Group B, radio-guided surgery localized the nodule in 24 of 25 patients (96%) whereas finger palpation localized it in 6 of 25 (24%). In Group A we registered 6 cases of pneumothorax compared to 1 case observed in the radio-guided group. Postoperative hospital stay required an average of 4 days in both groups. Conclusions: In our experience radio-guided surgery has therefore been proven efficacious in the diagnosis of solitary pulmonary nodule and video-assisted thoracoscopic surgery allows the removal of pulmonary nodules without complications. Hookwire was also shown to be efficacious but demonstrated complications linked primarily to external technical factors.

Key Words: Video-assisted thoracoscopic surgery • Solitary pulmonary nodule • Hookwire • Radio-guided surgery


   1. Introduction
Top
 Abstract
 1. Introduction
2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
The solitary pulmonary nodule (SPN) is defined as a single spherical lesion completely surrounded by pulmonary parenchyma without associated adenopathies or atelectases. The management of SPNs is closely tied to the probability that if the lesion is malignant, appropriate surgical treatment should be immediately implemented [1,2]. In the last decade, video-assisted thoracoscopic surgery (VATS) has become a useful minimally invasive tool in the diagnosis and treatment of pulmonary nodules, since it enables the entire nodule to be resected and histological analysis to be performed, with minimal pain and morbidity [3,4]. Unfortunately, thoracoscopic localization of small and central nodules into the lung may be difficult, although to localize a SPN is a fundamental step to plan a correct operative strategy and surgical tactics. A few localization techniques have been described, either preoperative (vital or blue dye, fluoroscopy-aided, needle wire) or intrathoracoscopic (finger palpation, intrathoracoscopic ultrasound, radio-guided surgery) [5,6].

This study was aimed at comparing the hookwire localization and the radio-guided surgery (still considered an innovative method); both methods are compared with finger palpation alone.


   2. Materials and methods
Top
 Abstract
 1. Introduction
 2. Materials and methods
3. Results
 4. Discussion
 5. Conclusions
 References
 
From January 2000 to January 2005, 50 patients with SPN (32 males and 18 females, ranging from 21 to 74 years, average age 56.3 years) were enrolled following this inclusion criteria: a maximum nodule diameter less than 2 cm; a distance from the nearest pleural surface between 1.5 and 3 cm; signature of the informed consent form. Multiple pulmonary nodules, mediastinal lymphadenopathy, suspicion of metastases from a locally non-controlled primitive neoplasm have been exclusion criteria. All patients underwent the study protocol including: hemato-chemical exam, chest X-ray, chest CT, ECG, spirometry and bronchoscopy.

Patients were randomly assigned to hookwire technique (Group A) or to radio-guided technique (Group B) to locate the pulmonary nodule. In both group the localization technique was compared with finger palpation. Table 1 shows patients and SPN characteristics in Group A and B.


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  		Table 1 Patients, SPN characteristics and results
 
Patients in Group A, were taken to the radiology unit on the day of surgery just before their operation and were placed on the CT scan table possibly in a posterolateral thoracotomy position. After local anesthesia with lidocaine, a 20-gauge needle, 32 cm in length (Allegiance Healthcare Corporation, Inamed, Toulon, France), was placed percutaneously through the chest wall and through the pulmonary parenchyma near the nodule under CT scan guidance. A hookwire, 10 cm in length was then placed through the localizing needle into the nodule. When it was not possible to place the hookwire directly into the nodule, localization within 1 cm of the target lesion was considered good enough. The 20-gauge needle was then removed and the proximal end of the hookwire was positioned on the skin under gauze dressing. The wire was left free to follow the collapse of the lung for the following surgery. At the end of the localization procedure, patients were transferred to the operating room (an average of 4 h later, range 60 min to 6 h). Before resection, we attempted to locate the nodule by finger palpation. Wedge resections were performed using three ports.

The radio-guided technique (Group B) requires various phases. The pulmonary nodule is identified by means of a CT scan and then, following local anesthesia of the thoracic wall, the insertion of a Chiba 22-gauge needle. A CT scan carried out while the needle is in place confirms the exact needle position (intra-lesional or peri-lesional in case of a nodule <1 cm). At this point a solution composed of 0.3 ml of microspheres of human albumin serum labeled with 99mTc (5–10 MBq) and 0.2 ml of non-ionic contrast medium (to allow a following radiological control), is injected. This solution, available at any time in our institution, is contained in a special syringe protected by a lead container specific for radioprotection. A successive CT scan is done to confirm precise staining of the nodule. The patient is then transferred to the operating room. Surgery is carried out under general anesthesia with double lumen intubation and the patient placed in a lateral position.

Operations were performed 120 min to 16 h from the end of the radio-localization procedure. The first trocar was used for exploration of the pleural cavity using a 5 mm 30° video-thoracoscope while a second trocar was placed to introduce an 11 mm diameter magnetic probe connected to a gamma camera (Scinti Probe MR 100, Pol.hi.tech., L’Aquila, Italy); the radioactivity is converted from the system into audio signal. The probe is used to conduct a starting scan of all the pulmonary surfaces far from the suspected area, just to reset the system and to eliminate the background noise. The scan is therefore concentrated in proximity of the suspected area and once the site of major radioactivity is identified, the third trocar is placed to perform the wedge resection. Before this, a second surgeon attempts to locate the nodule by finger palpation, blinded to the results of the radio-guided technique. Then resection is performed and the suture margins are checked with the probe to reveal any residual hyper-absorption.

In both groups, when the nodule was not localized, thoracoscopy was converted in a sparing muscle thoracotomy.

All specimens underwent frozen section and in case of primary lung cancer a standard lobectomy and lymphadenectomy were performed through a thoracotomy; in such cases the conversion was considered as a necessary therapeutic procedure and not a failure of thoracoscopy.

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.


   3. Results
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
4. Discussion
 5. Conclusions
 References
 
In Group A, the hookwire technique localized the nodule in 21 of 25 patients (84%), while finger palpation localized it in 7 of 25 (28%, significant). In one case (4%) the metal guide protruding from the patient's thorax was dislocated while moving the patient from radiology to the operating room; in two cases (8%) dislocation happened at the time of thoracoscopy: in both these cases the nodules were located in the lower lobe, in his posterior aspect. In none of these patients was the nodule identifiable at thoracoscopy with finger palpation. In another case (4%), conversion to thoracotomy was necessary because of strong pleural adhesion; however the hookwire was dislodged before conversion, during the attempt of thoracoscopic debridement, so we considered this case a failure. In six cases (24%), also from this group, the hooked needle caused a small pneumothorax not requiring a chest tube. In no case of failure, finger palpation was able to locate the SPN.

In Group B, radio-guided surgery localized the nodule in 24 of 25 patients (96%) whereas finger palpation localized it in 6 of 25 (24%, significant); in this group we had 1 case of pneumothorax (4%) not requiring drainage. In one case of failure (4%) we experienced the contamination of pleural cavity with the contrast medium, due to a technical mistake during TC-guided injection. The fast diffusion of the radioactivity above the pleural surface was the reason of missed localization and also finger palpation was not able to localize the lesion.

No statistical significance could be demonstrated between the two groups in locating the nodule; both techniques are superior with statistical significance when compared to finger palpation alone. The average surgical time of the thoracoscopy was 41 min (range 24–98 min) in Group A and 43 min (range 20–85 min) in Group B. The mean time to detect the nodule with the scinti-probe was 9 min (range 3–15) including the first phase to reset the system; this phase does not prolong the overall time of the radio-guided technique versus the hookwire. In the latter the entire surgical procedure must be treated with care to avoid the dislodgement of the needle and this means a slower procedure. In both groups, failure was not correlated with the size of the nodule: in Group A the two nodules that escaped detection were <1 cm while the other two were >1 cm; in Group B the nodule that escaped detection was >1 cm.

Wedge resection was always feasible with at least 1 cm of tissue margin. The frozen section revealed a primary pulmonary tumor in 23 (46%) cases and a secondary lesion in 9 (18%) cases. The remaining 18 cases (36%) were pathologically benign (Table 2 ).


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  		Table 2 Histopathological findings
 
In patients with primitive pulmonary tumors, after wedge resection we performed a standard lobectomy with radical mediastinal lymphadenectomy (n = 23, 46%): after the anatomo-pathological exam, 18 patients were found to be T1N0 (78.3%), 4 patients T1N1 (17.4%) and 1 patient T1N2 (4.3%).

Postoperative hospital stay averaged 4 days (range 3–6) in both groups. No intra- or postoperative complications were detected.


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
5. Conclusions
 References
 
Improved imaging techniques such as high resolutions, single breath or spiral CT scanning, result in more frequent identification of small and often sub-centimetric SPN and they always represent a major diagnostic dilemma. Such lesions are usually peripheral making bronchoscopic approaches to diagnosis futile while accuracy of the CT-guided biopsy is hindered by the small diameter and by the patient's respiratory movements during the exam. Various studies have shown that positron emission tomography (PET) has a sensibility between 85% and 95% in the diagnosis of the malignancy of a SPN but in cases of nodules with a diameter less than 1 cm, specificity and sensitivity are not satisfactory [7,8].

For these reasons, surgery is considered to be at the same time both a diagnostic and therapeutic step that is unavoidable when confronted with a pulmonary nodule of uncertain significance. In such lesions VATS seems to be the best diagnostic tool (less morbidity as well as shorter hospitalization). On the other hand, this kind of lesion may be difficult to locate during thoracoscopy and this inability depends on the size and the depth of the lesion. Several authors report different results based on the characteristics of the nodules included in each study [3–5]; Suzuki et al. [6] reports a probability of failure to detect the lesion >50% if the distance to the pleural surface is >5 mm in case of lesions of ≤10 mm in size; they consider a preoperative marking as absolutely indicated when the distance is >10 mm. Several techniques for localization of SPN have been described and are well known in their positive or negative aspects: vital dye, intraoperative ultrasound, hookwire and radio-guided detection are the most common used.

Staining with methylene blue and hookwire can be done alone or in combination. A failure rate of around 13% for methylene blue injection alone has been reported due to either an excess of liquid injected or an error in nodule localization. The major problem of this technique is the time elapsed between methylene blue staining and thoracoscopy, which considerably reduces the density of coloration and therefore visualization of the target area [9]. Many authors advise thoracoscopy within 3 h of staining.

Intraoperative ultrasound detection can be limited by the presence of air in the lung when complete collapse is not feasible; this means low efficacy in emphysematous patients [10–12]. However ultrasound has been shown to be very sensitive in experienced hands and some authors describe a 96% success rate affirming that the presence of a small amount of air in the pulmonary parenchyma is useful to localize the SPN [13]. In addition ultrasound allows studying the structure surrounding the nodule (i.e. vessels, bronchi and lymph nodes) and may play a role predicting the pathologic status of the nodule. Obviously, ultrasound is strongly operator dependent and unfortunately at our institute the low availability of colleagues well experienced in thoracic intraoperative ultrasound does not allow us to plan this method as a routine strategy.

The use of a metal guide in the localization of a SPN is widely used; tension on the wire during thoracoscopy permits exposure of the area containing the nodule [14]. It is, nevertheless, evident how the metal guide protruding from the thorax of a patient can dislocate while moving the patient from radiology to the operating room or during positioning of the patient on the operating table, not to mention the possible consequence of pulmonary collapse caused by the surgical maneuvers itself. The failure of these methods, therefore, is tied to the dislocation of the guide and occur in 6–10% of the cases [15,16]. The needle-wire technique is also associated with several complications, with pneumothorax being the most frequent one, reported in some series as occurring in 30–50% of cases [17]. We chose to localize SPN by this technique in Group A: the small distance between us and the radiology unit and the chance to perform the procedure just before surgery has made this technique safe (4% of dislodgement during this step), but with an incidence of pneumothorax in 24% of the patients even without the need of a chest tube. We tried to reduce the chance of dislodgement by positioning the patients on the CT scan table in a posterolateral thoracotomy position and maintaining an adequate length of the hookwire outside the chest, thus allowing the wire to follow the deflated lung during single lung ventilation; all the surgical maneuvers must be careful to avoid wire dislodgement. Despite these precautions we had a 16% rate of failure, higher than the 8% rate of dislodgement shown in most literature [15], but much lower than the failure rate of 47% reported by Bernard in a multicenter study due to hookwire dislodgement, mistaken nodule localization or subpleural hematoma [4]. This could be referred to the characteristic of our sample (higher distance from the nearest pleural surface and smaller diameter compared to other studies) [14–16]. In two cases (8%), the dislodgement of the hookwire happened while pulling the lung during the maneuvers to resect nodules located in the posterior aspect of lower lobe; we think that SPNs in this position are particularly at risk for hookwire dislodgement during thoracoscopy.

The radio-guided methods we used in Group B allowed us to overcome these limitations. The technique necessitates the injection of CT-guided radioactive dye but, differing from the hookwire technique, there is no risk of dislocation. It is without a doubt easier on the patient and there are no problems caused by the time between staining and the operation [18,19]. In our case studies we had two patients that were operated on at a relative distance of 16 h without any problem occurring in radio-localization. What differs in these cases is the absolute value of the absorption (peaks/min), but it is useful to remember that the resection is guided by the difference in absorption existing between the parenchyma zones containing the injected nodule and the surrounding area, represented by the absorption on the parenchyma far from the nodule. Because of the characteristics of the nodules (i.e. a maximum distance from the visceral pleura of 3 cm), we did not register any anatomical location inaccessible to scintigraphic detection or marking. Success with this radio-guided procedure was achieved in 96% of the cases. An ulterior advantage of the radio-guided method is the control of the suture seams at the end of the procedure to check for possible residual hyper-absorption indicating the immediate need to perfect the resection. Furthermore, whereas the dose of radio-labeled solution is minimal (5–10 MBq) even if compared to a standard scintigraphy, we do not need any special exposure reading for personnel involved in the procedure [18,19]. Although no statistical significance could be demonstrated among Group A and Group B, the radio-guided method seems to be superior for detecting SPN (96% vs 84%) also with less complications (24% vs 4%). Finger palpation, 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 [3,4,13]. The main limit of finger palpation is the difficulty in inserting the entire finger through the port; usually only the first two phalanges enter through the hole for a 5 mm thoracoport. Another drawback of finger palpation is the impossibility and difficulty of moving the deflated lung under the finger, so that the palpation is limited to the underlying parenchyma. We excluded patients with nodules larger than 2 cm and less than 1.5 cm from the pleural surface with the goal of avoiding redundant localization procedures in nodules easily palpable or visible under the pleural surface. In our experience, finger palpation is a low efficacy method for localization of SPN with these characteristics.

As collateral data, we have to underline the role of VATS resection of SPN in early diagnosis of lung cancer. In the general population only 5% of SPN discovered by a routine radiographic survey are carcinoma; however, in series in which resections have been performed, about 50% of SPN in patients over 50 years of age, are carcinomas [1–6]. In our series 46% of patients presented an unsuspected lung cancer and thoracoscopic resection led to an early diagnosis in 78.3% (stage IA); unfortunately 24.7% of patients with primary lung cancer presented a lymph node evolvement.


   5. Conclusions
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusions
References
 
No difference in accuracy could be detected among hookwire and radio-guided techniques. We think the identification of the best localization technique is strongly related to the background of the surgical team. Based on our experience, we conclude that radio-guided surgery appears to be a safe procedure, with fewer complications and failures than hookwire technique. Nevertheless, we must also stress that hookwire was also shown to be efficacious, with complications linked primarily to external technical factors.


   Footnotes
 
\#9734; Presented at the joint 20th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 14th Annual Meeting of the European Society of Thoracic Surgeons, Stockholm, Sweden, September 10–13, 2006.


   References
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 

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  8. Hagberg RC, Segall GM, Stark P, Burdon TA, Pompili MF. Characterization of pulmonary nodules and mediastinal staging of bronchogenic carcinoma with F-18 fluorodeoxyglucose positron emission tomography. Eur J Cardiothorac Surg 1997;12:92-97.[Abstract]
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