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Ann Thorac Surg 2002;74:170-173
© 2002 The Society of Thoracic Surgeons


Original article: general thoracic

Fluoroscopy-assisted thoracoscopic resection of lung nodules marked with lipiodol

Hiroaki Nomori, MD*a, Hirotoshi Horio, MDa, Tsuguo Naruke, MDa, Keiichi Suemasu, MDa

a Department of Thoracic Surgery, Saiseikai Central Hospital, Tokyo, Japan

Accepted for publication March 18, 2002.

* Address reprint requests to Dr Nomori, Department of Thoracic Surgery, Saiseikai Central Hospital, 1-4-17 Mita, Minato-ku, Tokyo 108-0073, Japan
e-mail: hnomori{at}qk9.so-net.ne.jp


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Background. To localize small and deeply situated pulmonary nodules under thoracoscopy with roentgenographic fluoroscopy, we developed a marking procedure that uses both lipiodol and colored collagen.

Methods. Pulmonary nodules were marked with 0.4 mL of lipiodol under computed tomography. The visceral pleura near each nodule was marked with 1 mL of colored collagen, ie, a mixture of atelocollagen and methylene blue. Nodules were marked more than 1 day before thoracoscopy. At thoracoscopy, C-arm-shaped roentgenographic fluoroscopy was used to detect the radiopaque nodules. Eighteen nodules in 16 patients were localized by this procedure. The nodules had an average diameter of 7 mm (range: 4 to 10 mm) and were located an average distance of 19 mm (range: 8 to 30 mm) from the pleural surface under computed tomographic measurement.

Results. There were no complications from the marking procedure except for pneumothorax in 1 patient who required chest tube drainage for additional marking. All 18 nodules could be easily localized at thoracoscopy. The colored collagen revealed the pleura near the nodules. The lipiodol showed the nodules on the fluoroscopic monitor, which was used to guide the forceps to grasp the nodules. All of the nodules could be resected completely under thoracoscopy without adding minithoracotomy. The pathologic diagnosis was malignant tumor in 9 patients, atypical adenomatous hyperplasia in 3, and benign lesion in 4.

Conclusions. A marking procedure that uses both lipiodol and colored collagen can localize small and deeply situated pulmonary nodules under fluoroscopy and facilitate safe and successful thoracoscopic resection.


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
In recent years, thoracoscopic surgical techniques have been used in diagnostic excisional biopsies of pulmonary nodules as well as in therapeutic resection of peripheral lung cancer. For small and deeply situated pulmonary nodules, however, a major factor limiting the success of thoracoscopic resection is the difficulty in locating the target nodule because it cannot be digitally palpated. To locate pulmonary nodules under thoracoscopy, several methods, such as pleural marking by dye [13], hook-wire technique [36], and coil [7], have been used. In 1996, we developed colored collagen for dye marking [8]. We used a mixture of methylene blue, atelocollagen, and water-soluble contrast medium. The colored collagen, because it stays at the injected site for a long time, solves the problem of the single-dye injection method, which requires the simultaneous use of both computed tomography (CT) scanning and an operating room because of the rapid diffusion of the dye after injection. However, the colored collagen is barely visible under fluoroscopy, because the contrast medium used in it is water soluble and vague under fluoroscopy. In fact, we once failed to resect a deeply situated pulmonary nodule 10 mm in diameter that was marked only with colored collagen. Since that case, we have developed a marking procedure that uses both lipiodol and colored collagen for fluoroscopy-assisted thoracoscopic resection. This study examined the usefulness of the marking procedure using both lipiodol and colored collagen for deeply situated small pulmonary nodules.


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Patients
Between January 1999 and December 2001, we used colored collagen to perform preoperative marking of small pulmonary nodules in 66 patients undergoing thoracoscopic biopsy. During that time, for all of 16 patients with 18 pulmonary nodules that were small and deeply situated, we used lipiodol (lipiodol ultra-fluid, Mitsui Pharmaceutical Co, Ltd, Tokyo, Japan) together with colored collagen (Table 1). The colored collagen was prepared as described previously [8]. Briefly, it is composed of 1% atelocollagen (Koken Co, Tokyo, Japan), 5% methylene blue, 32% nonionic contrast medium (iohexal), and 2% xylocaine. The maximum diameter of the nodules ranged from 4 to 10 mm, averaging 7 mm. As determined by CT scanning, the distance from the peripheral edge of the nodule to the nearest pleural surface ranged from 8 to 30 mm, averaging 19 mm. There were 10 men and 6 women, aged from 45 to 79 years. The nodules were located in the right upper lobe in 4 patients, right middle lobe in 4, right lower lobe in 3, left upper lobe in 3, and left lower lobe in 4. Informed consents for the risk of the marking procedure, including pneumothorax and embolism, were obtained from all of the patients.


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Table 1. Characteristics of Pulmonary Nodules

 
Marking technique
We reviewed the original diagnostic CT studies to select the marker injection sites. The shortest distance from the nodule to the thoracic wall was selected as the injection site. The patient was placed on the CT table in a suitable position (supine or prone). The site for marker injection was marked on the skin, and the angle and depth of the needle required to reach the nodule were determined. After local anesthesia of the thoracic wall, a 21 or 23-gauge needle was introduced from the point marked on the skin to the nodule, according to the angle and depth measured (Fig 1). We drew back on the syringe to confirm that blood had not flowed backward, and then injected 0.4 mL of lipiodol with one shot. We then withdrew the needle tip to just beneath the visceral pleura and injected 1 mL of colored collagen to mark the pleural surface. The presence of the injected materials was confirmed by CT just after marking and again on the morning of operation. If pneumothorax occurred and made the marking unsuccessful, we introduced a chest drain and once more attempted the marking. Thoracoscopy was performed 1 to 3 days (mean: 1.5 days) after marking.



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Fig 1. Atypical adenomatous hyperplasia in the left upper lobe. (A) Computed tomography showed a deeply situated pulmonary nodule 4 mm in diameter in the left upper lobe (arrow). (B) The nodule was marked with lipiodol and colored collagen. (C) Chest roentgenogram the next morning revealed a radiopaque nodule.

 
Thoracoscopic resection technique
Thoracoscopy was performed under one-lung anesthesia, using a double-lumen tube (Broncho-Cath, Mallinckrodt Medical, Athlone, Ireland) with three thoracoports. A C-arm-shaped fluoroscopic unit was used to detect the radiopaque nodules. After finding the pleura dyed with the colored collagen, we introduced a ring-shaped forceps from the access port just above the site of the dyed pleura. The radiopaque nodule was grasped by the forceps under fluoroscopic imaging in multiple projections. The forceps was then moved in several directions under fluoroscopic monitor to confirm that the nodule was grasped within the forceps (Fig 2). The nodule was then resected with an endostapler (EZ-45, Ethicon Endo-Surgery, Cincinnati, OH) with the aid of the fluoroscopy monitor. The successive resection of the nodules were confirmed also by using the fluoroscopy monitor. The resected specimen was removed in a surgical bag. The specimen was histologically diagnosed by a routine intraoperative pathologic examination.



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Fig 2. The same patient as in Figure 1. Intraoperative fluoroscopic imaging showing the radiopaque nodule grasped with a ring-shaped forceps.

 

    Results
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
On CT examination, all 18 pulmonary nodules appeared to have been successfully marked with both the lipiodol and colored collagen. One patient required chest tube drainage and additional marking because the development of pneumothorax prevented successful marking on the first attempt. After chest tube drainage, the lung expanded, permitting successful marking at the second attempt. There was no complication associated with lipiodol or colored collagen. At thoracoscopy, the colored collagen could be easily seen through the pleura as a clear spot in each of the 18 nodules and was a great help in locating the nearby pleura. Fluoroscopy showed the radiopaque nodules clearly in all 18 cases. The average number of endostaplers used for resection was 3.4 ± 0.8 (range: 2 to 5). We were able to resect all of the nodules completely under thoracoscopy without adding a minithoracotomy. The pathologic diagnosis was primary lung cancer in 8 patients, atypical adenomatous hyperplasia in 3 inflammatory nodule in 2, metastatic lung cancer in 3, hamartoma in 1, and intrapulmonary lymph node in 1 (Table 1). There was no adverse effect of the materials injection on the histologic diagnosis. There was no postoperative pulmonary air leakage, and the chest tubes were removed on the same day of thoracoscopy in all of the patients who underwent wedge resection. These patients were discharged from the hospital within 3 days after thoracoscopy. Patients with primary lung cancer were given thoracoscopic lobectomy and mediastinal lymph node dissection on the same day and discharged from the hospital within 7 days after surgery.


    Comment
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Several methods have been proposed for the localization of small pulmonary nodules under thoracoscopy. They include percutaneous injection of methylene blue solution [13], the hook-wire technique [36], micro-coil [7] and endoscopic ultrasound [9]. The original dye method, because of rapid diffusion around the tissue after injection, has the following faults: (1) marking must take place within 3 hours before thoracoscopy to enable the dye to be seen, therefore, simultaneous use of both CT and the operating room is needed [10]; and (2) the injection site appears blurred. Intraoperative ultrasound has a failure rate of 40% in locating nodules [9]. The hook-wire method carries the risk of pneumothorax, pulmonary hemorrhage, and dislodgement of the wire from the lung before thoracoscopy is performed [36]. Also recently, the hook-wire technique was reported to cause a massive gas embolism during hook-wire localization [11]. This report indicated that the massive embolism could have occurred by simultaneous injury of a bronchiole and the adjacent pulmonary vasculature by the hook apparatus (which was 9-mm long and 3-mm wide), thus allowing air to pass into the vasculature. To localize small pulmonary nodules, Lizza and colleagues used a micro-coil 15-mm long and 5-mm in diameter [7]. This was larger than the hook-wire and therefore could also have a risk for massive gas embolism, as did the hook-wire. We therefore consider that marking procedures that use coils or hook-wires are not suitable for pulmonary nodules. Okamura and associates demonstrated barium marking with CT-guided bronchoscopy in 21 patients [12]. However, their procedure was complicated in that it required simultaneous bronchoscopy and CT and took approximately 30 minutes (range: 15 to 60 minutes) to mark one nodule.

The marking procedure using lipiodol was first reported by Moon and coworkers, who had success in 10 patients [13]. They used indigo carmine to mark the pleural surface, but the indigo carmine tended to disappear within a few hours after injection because it was water soluble. We therefore used colored collagen to mark the pleural surface instead, as it can stay at the injection site for more than 10 days [8], making the marking available long before thoracoscopy. However, our procedure also has potential risks, such as embolism of lipiodol or colored collagen. We therefore routinely draw back on the syringe to confirm that blood has not flowed backward before injection. Moon and colleagues [13] used 1 mL of lipiodol, but we were able to reduce the volume to 0.4 mL to minimize the risk of embolism, which indeed did not eventuate in our series. It should be stressed that all marking materials used for fluoroscopy guidance have a risk of embolism. The hook-wire and coil have a risk of massive gas embolism as described above. While there have never been reports of embolism associated with the lipiodol or barium, those materials themselves also have a risk of embolism because they are water insoluble. However, we believe that our procedure is the simple, safe, and inexpensive one of the above procedures for localizing small and deeply situated pulmonary nodules.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

  1. 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]
  2. Kerrigan D.C., Spence P.A., Crittenden M.D., Tripp M.D. Methylene blue guidance for simplified resection of a lung lesion. Ann Thorac Surg 1992;53:163-164.[Abstract]
  3. Shah R.M., Spirn P.W., Salazar A.M., et al. Localization of peripheral pulmonary nodules for thoracoscopic excision. AJR Am J Roentgenol 1993;161:1279-1283.[Abstract/Free Full Text]
  4. 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]
  5. Mack M.J., Gordon M.J., Postma T.W., et al. Percutaneous localization of pulmonary nodules for thoracoscopic lung resection. Ann Thorac Surg 1992;53:1123-1124.[Abstract]
  6. Plunkett M.B., Peterson M.S., Landreneau R.J., Ferson P.F., Posner M.C. Peripheral pulmonary nodules: preoperative percutaneous needle localization with CT guidance. Radiology 1992;185:274-276.[Abstract/Free Full Text]
  7. Lizza N., Eucher P., Haxhe J.P., et al. Thoracoscopic resection of pulmonary nodules after computed tomographic-guided coil labeling. Ann Thorac Surg 2001;71:986-988.[Abstract/Free Full Text]
  8. Nomori H., Horio H. Colored collagen is a long-lasting point marker for small pulmonary nodules in thoracoscopic operations. Ann Thorac Surg 1996;61:1070-1073.[Abstract/Free Full Text]
  9. Shennib H., Bret P. Intraoperative transthoracic ultrasonographic localization of occult lung lesions. Ann Thorac Surg 1993;55:67-69.
  10. Vandoni R.E., Cuttat J.F., Wicky S., Suter M. CT-guided methylene-blue labeling before thoracoscopic resection of pulmonary nodules. Eur J Cardiothorac Surg 1998;14:265-270.[Abstract/Free Full Text]
  11. Horan T.A., Pinheiro P.M., Araujo L.M., Santiago F.F., Rodrigues M.R. Massive gas embolism during pulmonary nodule hook wire localization. Ann Thorac Surg 2002.
  12. Okamura T., Kondo H., Suzuki K., et al. Fluoroscopy-assisted thoracoscopic surgery after computed tomography-guided bronchoscopic barium marking. Ann Thorac Surg 2001;71:439-442.[Abstract/Free Full Text]
  13. Moon S.W., Wang Y.P., Jo K.H., et al. Fluoroscopy-aided thoracoscopic resection of pulmonary nodule localized with contrast media. Ann Thorac Surg 1999;68:1815-1820.[Abstract/Free Full Text]



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