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Ann Thorac Surg 2007;84:1680-1684. doi:10.1016/j.athoracsur.2007.06.005
© 2007 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Is Finger Palpation at Operation Indispensable for Pulmonary Metastasectomy in Colorectal Cancer?

Jun Nakajima, MD, DMedSc*, Tomohiro Murakawa, MD, DMedSc, Takeshi Fukami, MD, DMedSc, Atsushi Sano, MD, Miki Sugiura, MD, Shinichi Takamoto, MD, DMedSc

Department of Cardiothoracic Surgery, Graduate School of Medicine, the University of Tokyo, Tokyo, Japan

Accepted for publication June 1, 2007.

* Address correspondence to Dr Nakajima, Department of Cardiothoracic Surgery, Graduate School of Medicine, the University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, 113-8655 Tokyo, Japan (Email: nakajima-tho{at}h.u-tokyo.ac.jp).


   Abstract
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 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: The use of thoracoscopic techniques for pulmonary metastasectomy is controversial because small metastatic foci might be missed without thorough finger palpation of the lung.

Methods: We retrospectively examined preoperative findings of helical computed tomography and pathologic findings of pulmonary nodules obtained by open thoracotomy, including median sternotomy or thoracoscopy, in patients thought to have pulmonary metastasis from colorectal cancer.

Results: We performed 122 pulmonary metastasectomies (43 thoracotomies and 79 thoracoscopies) in 102 patients from 1999 to 2005. Repeat metastasectomies were excluded. Preoperative evaluation revealed 219 pulmonary nodules suspicious for pulmonary metastasis, and 250 nodules were resected; however, pathologic examination revealed that 47 (18.8%) of 250 nodules were not metastases. When the diameters of the pulmonary nodules were small, the rates of metastasis were also significantly lower. Finally, 4 thoracotomy (9.3%) and 5 thoracoscopy patients (6.3%) were found to have additional pulmonary metastases at operation. Recurrent pulmonary metastases were found at the ipsilateral side of the metastasectomy in 27 (34.2%) of 79 thoracoscopies and 27 (62.8%) of 43 open thoracotomies (p = 0.0023) within 2 years after the pulmonary surgery. These metastatic foci might have been missed at the time of pulmonary metastasectomy.

Conclusions: The ability to detect pulmonary metastases in patients with colorectal cancer is limited by preoperative evaluation with computed tomography and surgical techniques, including open thoracotomy with bimanual palpation. Pulmonary metastasectomy by open thoracotomy or thoracoscopy may be a suboptimal intervention to remove metastatic foci in the lungs.


   Introduction
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 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Chest computed tomography (CT) is now routinely performed for the preoperative assessment of the number, location, and size of pulmonary nodules in patients with pulmonary metastases. The number of metastatic nodules is critical in the determination of the resectability of pulmonary metastases and postoperative prognosis. CT, however, is limited in its ability to detect pulmonary metastases accurately. Small metastatic foci are often missed, and small nonmetastatic nodules are often misdiagnosed as pulmonary metastases. Overestimation of the number of intrapulmonary nodules has recently become more problematic with the use of high-resolution images from helical CT.

Thoracoscopy plays an important role for pulmonary metastasectomy. Pulmonary wedge resection is a standard surgical procedure for the treatment of pulmonary metastasis and can be easily performed through thoracoscopy. However, bimanual palpation of the whole lung, which allows for detection of pulmonary nodules intraoperatively, cannot be accomplished by thoracoscopy because of its small access into the thorax.

We thus tried to determine the clinicopathologic characteristics of suspicious pulmonary nodules found in patients with a history of colorectal cancer. We focused on colorectal carcinoma to minimize the diverse characteristics of pulmonary metastases from other organs. We also examined the postoperative course to determine if other pulmonary metastases that had been missed at the time of operation developed in patients.


   Patients and Methods
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 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
We retrospectively enrolled patients with a history of colorectal carcinoma who underwent pulmonary resection for suspected pulmonary metastasis between 1999 and 2005. This study protocol was examined and approved by the departmental Research Review Board. All patients provided informed consent before operation.

Helical chest CT (5-mm slice) with contrast medium was performed before chest operation. The interval between the CT and operation was a mean ± standard deviation of 14.9 ± 12.9 days (range, 0 to 49 days). We excluded patients who had previously undergone ipsilateral pulmonary operation for metastasectomy and those who had undergone incomplete pulmonary metastasectomies.

The CT images were examined by at least 2 radiologists and chest surgeons, and the number, the size, and the location of pulmonary metastases were determined. A pulmonary solid nodule, occasionally with a cavity, was suspected to be a pulmonary metastasis if the diameter of the nodule was 5 mm or greater, there was no calcification, or the nodule appeared de novo or enlarged in serial CT images, even if its diameter was less than 5 mm.

We performed thoracoscopy or open thoracotomy to resect pulmonary nodules in the patients suspected of having pulmonary metastases if they had resectable metastatic pulmonary neoplasms without uncontrollable tumor foci in other organs and if they were in reasonably good general physical condition. Open lateral thoracotomy or median sternotomy was often performed when the patient had multiple or bilateral pulmonary nodules, respectively. We palpated the whole lung to detect all nodules before pulmonary resection at open operation.

Thoracoscopy was performed if the patient had a solitary nodule located in the periphery of the lung. The thoracoscopic operation procedure that was used has been described elsewhere [1]. Briefly, under general anesthesia and separated ventilation with a double-lumen tube, the patient was placed in the recumbent position. Three small skin incisions, approximately 1 cm, 1 cm, and 2 cm long, were made, and three trocar ports were inserted. Video-assisted pulmonary resection, segmentectomy, or lobectomy was performed through the trocar ports. After the resection was completed, the specimen was wrapped in a disposable plastic bag (EndoPouch, Ethicon Endosurgery, Cincinnati, OH) and removed from a port. A chest tube was inserted and the wounds closed.

We performed percutaneous marking of the lung if the nodule was small or located deep in the parenchyma. We tried to touch the lung surface with a finger through thoracoscopy access ports as much as possible to detect additional pulmonary nodules.

Either through open thoracotomy or thoracoscopy, pulmonary wedge resection was performed to resect peripherally located pulmonary nodules with a safety margin. If the pulmonary nodule was located deep in the parenchyma, we performed lobectomy or segmentectomy to remove the nodule either through thoracotomy or thoracoscopy.

We retrospectively examined the number of pulmonary nodules suspicious for pulmonary metastasis by chest CT, the number of resected nodules at operation, and the number of pulmonary metastases diagnosed pathologically by one surgical procedure. The pulmonary operation events were divided into two groups, the open thoracotomy group, including conventional lateral thoracotomy and median sternotomy, and the thoracoscopy group. If two operations were sequentially performed on patients with multiple metastases in both lungs, the number of the procedures was counted as one. If the pulmonary metastasectomy was performed on the contralateral lung to remove new nodules during postoperative follow-up, the number of the operations was counted as two.

Patients were followed up with chest CT every 3 to 6 months postoperatively. "Surgically underestimated pulmonary metastasis" was defined as a new nodule that appeared in the previously operated lung within 2 years after the metastasectomy or at the time of the recurrence in other organs.

The {chi}2 test for independence and the Student t test were used for statistical analyses. A result was considered significant at a value of p < 0.05.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Between 1999 and 2005, 122 operations on 102 patients with pulmonary nodules suspicious for metastatic colorectal cancer were performed through 43 open thoracotomies (35.2%). Thirteen median sternotomies, three sequential bilateral open thoracotomies, and four sequential bilateral thoracoscopies for bilateral pulmonary metastasectomy were included in open thoracotomy operations. Thoracoscopy was used for 79 metastasectomies (64.8%). Twenty patients who were found to have new metastases in the contralateral naïve lung underwent a total of two metastasectomies each (Table 1).


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  		Table 1 Clinical Characteristics of Surgical Cases for Pulmonary Metastasis From Colorectal Cancer
 
The number of pulmonary nodules in each patient by CT was 1.78 ± 1.41 (range, 1 to 8 nodules), and 219 nodules were suspicious for pulmonary metastases preoperatively. During the 122 metastasectomies, additional pulmonary nodules that had not been detected by CT were found in 11 (25.6%) of 43 open thoracotomies and 10 (12.7%) of 79 thoracoscopies (p = 0.071, NS). Preoperatively, metastasectomy of a solitary pulmonary nodule was scheduled in 77 operations. More pulmonary nodules were found in six (7.8%) of these procedures. At the same time, more pulmonary nodules were found in 15 (33.3%) of the 45 operations for multiple metastasectomies. More nodules were found if the patient was thought to have multiple pulmonary nodules preoperatively (p < 0.001; Table 2).


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  		Table 2 Number of Pulmonary Metastases Diagnosed by Computed Tomography, Resected, Diagnosed Pathologically, and Detected Postoperatively
 
In two open thoracotomies with multiple pulmonary nodules diagnosed by CT preoperatively, the number of resected pulmonary nodules was less than that preoperatively diagnosed (n = 3 in total) because these nodules were apparently different than pulmonary metastases and the resections were cancelled at operation.

Lobectomy or segmentectomy was adapted for resection of nodules deeply located in lung parenchyma at nine open thoracotomies (20.9%) and 13 thoracoscopies (16.5%, p = 0.54, NS). Bilateral pulmonary metastasectomies performed simultaneously were more frequently performed through thoracotomies (n = 14) than through thoracoscopy (n = 1, p < 0.001; Table 3).


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  		Table 3 Comparison of Wedge Resection Versus Lobectomy or Segmentectomy, and Number of Bilateral Resections Performed Simultaneously
 
A total of 250 pulmonary nodules were resected, and 203 (81.2%) were pathologically diagnosed as pulmonary metastases from colorectal cancer. Pathologic findings of the other 47 pulmonary nodules were 3 primary lung adenocarcinomas, 1 solitary fibrous tumor of the pleura, 3 chondromatous hamartomas, 20 granulomas, 3 organizing pneumonias, 3 intrapulmonary lymph nodes, and 14 nonspecific fibrotic or hyalinizing foci.

The diameter of the pulmonary nodules correlated significantly with the diagnosis of a pulmonary metastasis. If the diameter of the nodules was more than 5 mm, 158 (91.3%) of 173 were pathologically diagnosed as pulmonary metastases from colorectal cancer. However, only 45 (58.4%) of 77 pulmonary nodules with a diameter of 5 mm or smaller were metastases (p < 0.001; Fig 1).


Figure 1
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  		Fig 1. Distribution of the diameter of resected pulmonary nodules in those with pulmonary metastasis (Pulm Meta; black bars) and others (clear bars). The rate of pulmonary metastasis (triangles) is plotted at each size.

 
Of the 77 operations for solitary metastasis preoperatively diagnosed by CT, 17 were performed through open thoracotomy and 60 were performed through thoracoscopy. Preoperative placement of percutaneous needle markers was performed in 14 thoracoscopic procedures. In all operations, the solitary pulmonary nodule was successfully resected. In 71 of 77 operations, the resected specimen was pathologically diagnosed as pulmonary metastasis from colorectal cancer. In the other six operations, the pulmonary nodules were found to be 2 chondromatous hamartomas, 1 solitary fibrous tumor, 1 bronchioloalveolar cell carcinoma of the lung, 1 granuloma, and 1 fibrotic focus. In two of 17 open thoracotomies and in four of 60 thoracoscopies, more pulmonary nodules were found during operation. In one of two thoracotomies and two of four thoracoscopies, these nodules newly found during operation were pathologically diagnosed as pulmonary metastases from colorectal cancer. Thus pulmonary metastases were underestimated in 3 (3.9%) of 77 patients with solitary pulmonary metastasis as diagnosed by CT preoperatively.

Of the 45 operations for multiple metastases preoperatively diagnosed by CT, 26 were performed through open thoracotomy and 19 were performed through thoracoscopy. In nine (34.6%) of 26 open thoracotomies and in six (31.6%) of 19 thoracoscopies, more pulmonary nodules were found during operation (p = 0.83, NS). In three of nine open thoracotomies and three of six thoracoscopies, these nodules newly found during operation were pathologically determined to be pulmonary metastases from colorectal cancer. Thus, pulmonary metastases were underestimated in at least six (13.3%) of 45 cases of multiple pulmonary metastases as preoperatively diagnosed by CT.

The mean diameter of 35 pulmonary nodules newly found and resected at operation was 3.7 ± 2.0 mm, significantly smaller than the other 215 nodules identified preoperatively (11.9 ± 9.6 mm, p < 0.001). Of the 35 nodules, only 15 (42.9%) were pulmonary metastases, whereas 188 (87.4%) of 215 preoperatively identified nodules were pathologically diagnosed as pulmonary metastases (p < 0.001).

Within 2 years of the operation, recurrent pulmonary metastases were found at the ipsilateral side of the metastasectomy in 27 (34.2%) of 79 thoracoscopies and 27 (62.8%) of 43 open thoracotomies (p = 0.0023). In 14 (18.2%) of 77 metastasectomies for solitary metastasis diagnosed by CT and 40 (88.9%, of 45 metastasectomies (p < 0.001) for multiple metastases, the patients had recurrent pulmonary metastases at the ipsilateral side of the previous operation.


   Comment
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 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
Pulmonary metastasis represents the systemic involvement of malignant neoplasms. Thomford and colleagues [2] advocated pulmonary metastasectomy for possible curative treatment if the pulmonary metastasis could be resected, the patient could tolerate the operation, and the primary lesion did not show any local recurrence. A recent multiinstitutional study also justified pulmonary metastasectomy for patients with pulmonary metastasis, showing that the postoperative 5-year survival rate was 36% to 48% [3, 4]. The diversity of the primary site of the neoplasms has disrupted the clinical outcome of metastasectomy because the postoperative prognosis depends on the malignancy of the primary lesion. Thus, we enrolled patients with pulmonary metastasis only from colorectal cancer.

Surgical treatment for patients with pulmonary metastasis from colorectal cancer has been well documented, with a 5-year survival of about 30% to 40% [5–16]. Among these reports, the extent of the primary lesion, serum titer of carcinoembryonic antigen, disease-free interval between treatment of the primary lesion and detection of the pulmonary metastasis, and the presence of hilar and mediastinal lymph nodal metastases were discussed as factors influencing postoperative survival of pulmonary metastasectomy in colorectal carcinoma. Most reports found that the number of pulmonary metastases and completeness of resection were factors influencing the survival rate after pulmonary metastasectomy [5–16].

Chest CT has been a crucial preoperative diagnostic for identifying the number, location, and size of the pulmonary metastases; however, it often cannot detect small nodules. Retrospective and prospective studies have shown that intraoperative bimanual palpation through thoracotomy can detect additional small pulmonary nodules that were not detected by the chest CT [17–19]. The authors of these studies commented that pulmonary metastasectomy would be incomplete without bimanual palpation through thoracoscopy. Mutsaerts and colleagues [20] supported this opinion in their prospective study that found more pulmonary metastasis at open thoracotomy after thoracoscopic metastasectomy. Younes and colleagues [21] evaluated the preoperative assessment with a brand-new helical CT and suggested that CT could not identify small pulmonary metastases. Parsons and colleagues [22] also reported that they missed 22% of pulmonary metastases even when they had evaluated pulmonary nodules by helical CT preoperatively.

In this study, however, we demonstrated that pulmonary nodules smaller than 5 mm in diameter that were detected by CT were often not pulmonary metastases. Finger palpation may detect more nonmetastatic pulmonary nodules during the operation. We also stress that finger palpation of the lung is also limited in the detection of small nodules. The number of pulmonary metastases detected by finger palpation may range between the number detected by preoperative CT and the true number of metastatic pulmonary nodules. Waters and colleagues [23] performed meticulous analysis of CT and pathologic findings of multiple pulmonary metastases in canine osteosarcoma. They suggest that many small metastatic nodules that were misdiagnosed by CT might also be missed by finger palpation because they are often less than 1 mm in diameter.

We found 34.2% of thoracoscopies and 62.8% of open thoracotomies yielded new pulmonary metastases at the same side of the operation within 2 years postoperatively. We thus suggest that pulmonary metastasectomy may be suboptimal regardless of whether it is performed by thoracoscopy or open thoracotomy. In fact, our retrospective study on the postoperative survival rates and nonrecurrence survival rates of pulmonary metastasectomy through thoracoscopy versus open thoracotomy postulated that the outcome of thoracoscopic operation is not inferior to open thoracotomy [24].

The thoracoscopic operation is more advantageous than open thoracotomy for treatment of pulmonary metastasis because the metastatic nodules are often located in the periphery of the lung. Wedge resection is a standard mode of resection in pulmonary metastasis, which is easily performed with staplers through thoracoscopy. Thoracoscopic operation is less invasive owing to less postoperative derangement of respiratory function and postsurgical pain and improved postoperative quality of life than open thoracotomy [25]. Furthermore, repeat surgery is feasible with thoracoscopy. Jaklitsch and colleagues [26] reported that repeat metastasectomy does not worsen the postsurgical prognosis.

We conclude that finger palpation for detecting additional pulmonary nodules at metastasectomy might play a limited role in improving postoperative outcome of the patients with pulmonary metastasis from colorectal cancer. We suggest that thoracoscopic surgery for pulmonary metastasectomy may be justified because all pulmonary metastatic foci are not resected through open thoracotomy with finger palpation.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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J. Nakajima, T. Murakawa, T. Fukami, and S. Takamoto
Is thoracoscopic surgery justified to treat pulmonary metastasis from colorectal cancer?
Interactive CardioVascular and Thoracic Surgery, April 1, 2008; 7(2): 212 - 217.
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