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Ann Thorac Surg 1999;68:1815-1820
© 1999 The Society of Thoracic Surgeons


Original Articles

Fluoroscopy-aided thoracoscopic resection of pulmonary nodule localized with contrast media

Seok-Whan Moon, MDa, Young-Pil Wang, MDa, Keon-Hyon Jo, MDa, Moon-Sub Kwack, MDa, Se-Wha Kim, MDa, Ou-Kyoung Kwon, MDa, Hye-Suk Jang, MDa

a Departments of Thoracic and Cardiovascular Surgery, Anesthesiology, and Radiology, College of Medicine, The Catholic University of Korea, Seoul, South Korea

Address reprint requests to Dr Moon, Department of Thoracic and Cardiovascular Surgery, Kang Nam St Mary Hospital, 505 Banpo-Dong, Socho-Ku, Seoul 137-040, Republic of Korea
e-mail: swmoon{at}cmc.cuk.ac.kr


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. The pulmonary nodules have become the major indication of video-assisted thoracic surgery (VATS). Recently, several preoperative or intraoperative techniques for identifying small or deeply seated pulmonary nodules have facilitated thoracoscopic resection. We describe the new technique for detecting difficult lesions.

Methods. Preoperatively, we marked the visceral pleura near the pulmonary nodules with dye, simultaneously injected contrast media (1 water-soluble Optiray [Mallinckrodt Medical Inc, Quebec, Canada], 18 barium sulfate, 11 Lipiodol [Laboratoire Guerbet, Aulnay-sous-Bois, France]) into or around the nodule under computed tomography (CT) guidance. During VATS, we were able to easily and accurately detect and resect all the nodules localized with contrast media, of which the radiopacity was visualized on the portable fluoroscopic monitor.

Results. Between February 1996 and December 1998, we thoracoscopically resected 30 nodules in 28 patients (13 were women; age, 53 ± 14 years). The resected nodules were 17 ± 7.6 mm (range; 4 to 32 mm) in size, and 8.9 ± 8 mm (range, 2 to 34 mm) in depth. The pathologic diagnosis of the nodules was benign in 20 and malignant in 10 (six primary cancers of lung and four metastatic cancers). There were only minor complications related CT localization.

Conclusions. This new technique can help the surgeons detect and resect the difficult lesions with safety and rapidity by VATS without thoracotomy.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
The pulmonary nodule requires a percutaneous needle aspiration (PCNA) or excision biopsy for diagnosis, especially in the situation of high risk of malignancy, such as advanced age, lack of history of tuberculous or fungal infection, and presence of history of thoracic or extrathoracic malignant disease [1]. The importance of diagnostic excision as well as therapeutic excision of the pulmonary lesion is increased when the definite diagnosis by PCNA is unsuccessful or technically difficult. Development in endoscopic surgical equipment and attainment of thoracoscopic experiences have expanded the role of video-assisted thoracoscopic surgery (VATS) in thoracic diseases [2]. VATS has been a less morbid alternative to open thoracotomy for the pulmonary lesions. However, the inability to use bimanual palpation of the lung as a localizing technique has necessitated a new method to detect small or deeply seated lesions. Several methods, such as pleural marking by dye [3, 4] near the nodules or hook-wire localization [3, 59] under preoperative computed tomography (CT) guidance, and intraoperative sonography [1013] have facilitated intraoperative identification for the difficult lesions. The above-mentioned methods have varying degrees of success and necessitate one or more alternative methods for accurate localization.

We describe a new technique in which contrast media was injected into or around the nodules under preoperative CT guidance, which enabled us to detect them and perform successful thoracoscopic resections by fluoroscopic guidance.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
From February 1996 through December 1998, we thoracoscopically performed stapling resection of 30 nodules localized with our new method under informed consent. There were 15 men and 13 women. The average age was 53 ± 14 years with the youngest being 22 years and the oldest being 74 years.

Twenty-three of 28 patients had solitary nodules and 5 had multiple nodules as evident on chest CT scan. The indications leading to the election of VATS were as follows: 11 periodic radiologic follow-ups and eight medical check-ups, which include five symptomatic cases (chest pain in 2, episode of coughing in 2, spells of hemoptysis in 1). Ten patients were suspected of having metastatic pulmonary lesions spread from known visual malignant growths (two lymphomas, one gastric cancer, two bone tumors, one lung cancer, two uterine cervix carcinomas, one colon carcinoma, and one case of multiple masses of unknown origin). PCNA was done unsuccessfully in 18 patients, and was not done in 10 because we expected technical difficulty in the approach, and some of patients wanted to directly undergo VATS.

Characteristics of pulmonary nodules
Thirty nodules to be resected were located in the right upper lobe in 7 patients, right middle lobe in 1, right lower lobe in 15, left upper lobe in 2, and left lower lobe in 5. The diameter of the nodules ranged from 4 to 32 mm with a mean of 17 ± 7.6 mm. The distance from the outer margin of the nodule to the nearest pleural surface ranged from 2 to 34 mm with a mean of 8.9 ± 8 mm.

Localization methods of pulmonary nodule
Chest CT was performed using a pulmonary protocol consisting of 8-mm scans through the thorax and 4-mm scans in the region of the nodule. If it was anticipated from preoperative examination of chest CT that there would be difficulty in locating the nodules during VATS, the patients selected for CT directed localization on the day or before the day of operation were taken to the CT scanner room. The patients were placed in a proper position, depending on the nodule location. The site of the needle insertion was determined by a radiopaque grid placed on the patient’s skin. The nodule to be localized was detected by 8-mm thick axial CT sections in inspiratory position. The lesion was then punctured with a 20-gauze Chiba needle (Calibrated Chiba Stylet needle, Manan Medical Products Inc, Northbrook, IL) into or near the nodule during suspended full inspiration after local anesthesia of the thoracic wall. Once the needle tip was identified to be within the nodule or just in contact with it, the stylet was removed from the needle and subsequent CT images were obtained after the procedure to confirm the localization. We injected 1 mL of contrast media solution (Fig 1), and as the needle was withdrawn, a small amount of indigo carmine (Inverin, Galway, Ireland), usually less than 0.5 mL, was injected at the visceral pleura near the nodule. All the lesions were successfully localized and marked by radiologist; 18 with barium sulfate (Solotop, Taejoon, Seoul, South Korea), 11 with iodized oil (Lipiodol Ultra Fluide, Laboratoire Guerbet, Aulnay-sous-Bois, France), and one with water-soluble contrast media (Optiray 320 Mallinckrodt Medical Inc, Quebec, Canada). The CT localization procedure itself took about 27.5 ± 11 minutes (range, 25 to 55 minutes per localization) to complete.



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Fig 1. Thoracic computed tomogram (CT) in a patient after injection with contrast media (barium sulfate) into the nodule under CT guidance. A solitary nodule (18 mm in diameter and 16 mm apart from the nearest visceral pleura) in the right lower lobe, and was localized by injecting 1 mL of barium sulfate into the nodule under CT guidance (arrow indicates radioopacity of contrast media).

 
Technique of thoracoscopic resection
There was a delay of several hours or a day between VATS and CT localization, depending on the operation schedule. General thoracoscopy was performed under one-lung anesthesia (double-lumen tube, Broncho-Cath, Mallinckrodt Medical Athlone, Ireland or Univent, Phygon Univent Fuji Systems Corporation, Tokyo, Japan) with three or four thoracoports, which were made for a 7-mm thoracoscope (Richard Wolf Medical Instruments Corporation, Rosemade, IL), and instruments or endostaplers. A C-arm-shaped portable fluoroscopic unit was equipped for detecting the nodule marked with contrast media. All the nodules were clearly visualized on fluoroscopic imaging except the nodule localized with water-soluble, radiopaque Optiray, which was poorly visualized. The radiopaque nodule was grasped (Fig 2) and resected with one or more endostaplers (Fig 3) (Multifire Endo GIA 60, Auto Suture International, USSC, Norwalk, CT and Endoscopic linear cutter 45 mm, Ethicon Endo-Surgery, Cincinnati, OH) simultaneously with the aid of fluoroscopic monitor and thoracoscopic monitor. Fluoroscopic imaging in one or another projection helped us guide the placement of the endostaplers and progression of cutting to safely encompass the whole lesion (Fig 4). The time concomitant of portable fluoroscopy personnel during VATS varied, and was sometimes lengthy (average, 45 ± 11.3 minutes, ranging 15 to 85 minutes).



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Fig 2. Intraoperative fluoroscopic imaging of the radiopaque nodule. The nodule localized with contrast media was easily seen on portable fluoroscopic monitor and was targeted between the endoscopic instruments at the time of thoracoscopy (T = thoracoscope; arrow = radioopacity of the nodule localized with contrast media).

 


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Fig 3. Placement of endostapler for resection of the radiopaque nodule under portable fluoroscopic imaging during thoracoscopy. The radioopacity of the nodule on fluoroscopic imaging gave us planning and guiding the placement of endostapler (E = endostapler; T = thoracoscope; arrow = the nodule to be marked with contrast media).

 


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Fig 4. Cut section of the whole nodule. This specimen showed a whitish and eccentric barium stained area (arrow head) within the nodule and revealed a metastasis on frozen section analysis and permanent examination (uterine cervix cancer).

 
The operative procedure was converted from VATS to open thoracotomy for anatomical resection in two of six primary cancers on frozen section analysis.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
We operated on 30 nodules in 28 patients by VATS and performed three anatomical resections and one subtotal gastrectomy. There was neither mortality nor any complication related to the operation, but there were four minor complications related to CT localization. Thoracoscopic resection required an average time (incision to dressing or the result of frozen section analysis) of 110.5 ± 33.9 minutes (range, 35 to 165 minutes). The average number of endostaplers used was 2.8 ± 1.2 (range, 1 to 5). The chest tube was removed on the third or fourth day (average; 3.4 ± 0.9 days, ranging 2 to 7 days), and the patients were discharged on the ninth postoperative day (average; 8.7 ± 2.1 days, ranging 5 to 17 days).

Pathologic examinations revealed that nineteen nodules (63%) were diagnosed as benign (three hamartomas, ten tuberculous granulomas, five chronic inflammatory granulomas, one leiomyoma). Six were primary lung cancers (three adenocarcinomas, two bronchoalveolar cell carcinomas, one squamous cell carcinoma), and four were pulmonary metastasis (two uterine cervix carcinomas, one colon carcinoma, one osteosarcoma). Because of severe pulmonary dysfunction in 1 patient the advanced age of another with pulmonary dysfunction, and pleural seeding in another, 3 patients with primary lung cancer did not undergo anatomic lobectomy. They received adjuvant chemotherapy and have been well without recurrence on follow-up (5 to 24 months). Two patients who underwent anatomical lobectomy have been well on follow-up (9 and 15 months). Ten patients with pulmonary tuberculosis received antituberculous medication for 3 to 6 months. Two patients with suspected metastatic pulmonary spread underwent subtotal gastrectomy and contralateral thoracotomy for lobectomy several days after VATS, respectively. Table 1 summarizes results from 28 patients who were operated on thoracoscopic resection.


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Table 1. Summary of 30 Procedures in 28 Patients Who Underwent Thoracoscopic Resection Using the New Localization Technique

 

    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
The pulmonary nodules will be diagnostic in 75% to 90% of malignant lesions and in 40% of benign nodules by PCNA [1]. Therefore, a definite pathologic diagnosis must be made by excision biopsy in case of no diagnostic results in PCNA.

With the advancements in endoscopic equipment, VATS is increasingly a useful modality for the diagnosis and management of many intrathoracic problems, especially pulmonary nodules [2].

Difficult lesions, that are too small (less than 1 cm) or too deeply seated (more than 2 cm from the pleural surface), limit the successful thoracoscopic resection without conversion to the open thoracotomy. The limiting factor is the inability to use bimanual palpation to identify the pulmonary lesion and the reason that the endoscopic visualization is possible only if the nodules are associated with pleural change, so called puckering, and become effaced as the lung is deflated. In fact, the main concerns for the surgeon are to localize the nodule with accuracy and to resect it with a sufficient margin, as in open thoracotomy. Therefore, the difficult lesions necessitate utilizing one or more localizing techniques such as pleural markings with dye [3, 4], hook-wire [3, 59] under preoperative CT guidance, and intraoperative sonography [1013]. Although effective for localizing, they have their limitations. Because the dye marker diffuses as time passes by, it requires a close coordination between the radiologist, the surgeon, and anesthesiolo-gist. Furthermore, the dye marking allows poor surface localization in case the lung is extremely blackened by anthracosis [4]. Hook-wire insertion has varying degrees of failure because of its dislodgment [68, 10]. Intraop-erative sonography helps the surgeon detect and guide planning the strategy of resections, but has a high failure rate only by itself, and may seem limited in cases of incomplete collapse of the lung, or in patients with obstructive emphysematous lung [12, 13].

In our series, we inject contrast media within or around the nodule with or without dye marking on the pleura near the nodule under CT guidance. As a result, this radiopacity not only gives us accurate and quick identification of the nodule, but also helps us determine adequate margins of resections on fluoroscopic imaging in one or another projection. Because the water-soluble contrast media within the nodule was diffused after several hours of localization, it provided poor imaging on fluoroscopic monitor during VATS. Now we use the water-insoluble contrast media such as barium sulfate or Lipiodol for the better imaging of the nodule on the intraoperative fluoroscopic monitor, which will be totally removed with the pulmonary lesion. With the exception of the lengthy CT time and time concomitant of portable fluoroscopy personnel, this method is acceptable to patients and the staff because there is also less pressure on the radiology staff for the operating schedule.

In summary, we found that this new method was safe and effective in resecting the difficult lesions by VATS even though our cases were small in number.


    Acknowledgments
 
This study was supported in part by the Clinical Research Fund of The College of Medicine, The Catholic University of Korea.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Lillington G.A. Pulmonary nodules. Clin Chest Med 1982;3:361-367.[Medline]
  2. Coltharp W.H., Arnold J.H., Alford W.C. Videothoracoscopy improved technique and expanded indications. Ann Thorac Surg 1992;53:776-779.[Abstract]
  3. Landreneau R.J., Hazelrigg S.R., Ferson P.F., et al. Thoracoscopic resection of 85 pulmonary lesions. Ann Thorac Surg 1992;54:415-420.[Abstract]
  4. Wicky S., Mayor B., Cuttat J.F., Schnyder P. CT-guided localizations of pulmonary nodules with methylene blue injections for thoracoscopic resections. Chest 1994;106:1326-1328.[Abstract/Free Full Text]
  5. Mack M.J., Gordon M.J., Postma T.W., Berger M.S., Aronoff R.J., Acuff T.E. Percutaneous localization of pulmonary nodules for thoracoscopic lung resection. Ann Thorac Surg 1992;53:1123-1124.[Abstract]
  6. Gossot D., Miaux Y., Guermazi A., Celerier M., Frija J. The hook-wire technique for localization of pulmonary nodules during thoracoscopic resection. Chest 1994;105:1467-1469.[Abstract/Free Full Text]
  7. Garuti E., Vanzulli A., Varagona R., Negeri G., Zannini P., Del Maschio A. Use of CT-guided metal wires in pre-thoracoscopic localization of peripheral pulmonary nodules. Radiol Med (Torino) 1995;90:470-474.[Medline]
  8. Sartoris F., Cittadini G., Saitta S., et al. CT-guided needle localization of lung nodules for thoracoscopic resection. Eur Radiol 1996;6:420-424.[Medline]
  9. Sortini A., Benea G., Santini S., Navarra G., Occhionorelli S., Sartori A. Video-assisted atypical resection of peripheral lung nodules localized using CT-guided wires. First clinical experiences. Chir Ital 1995;47:27-29.[Medline]
  10. Mack M.J., Shennib H., Landreneau R.J., Hazelrigg S.R. Techniques for localization of pulmonary nodules for thoracoscopic resection. J Thorac Cardiovasc Surg 1992;106:550-553.[Abstract]
  11. Shennib H., Bret P. Intraoperative transthoracic ultrasonographic localization of occult lung lesions. Ann Thorac Surg 1993;55:767-769.[Abstract]
  12. Greenfield A.L., Steiner R.M., Liu J.B., et al. Sonographic guidance for the localization of peripheral pulmonary nodules during thoracoscopy. AJR 1997;168:1057-1060.[Abstract/Free Full Text]
  13. Mulder D.G., Shennib H. Localization technique for thoracoscopic resection of solitary pulmonary nodules. Surg Endosc 1993;7:246.
Accepted for publication April 15, 1999.




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