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* From the Division of Thoracic Oncology, National Cancer Center Hospital East, Chiba, Japan.
Abstract
Study objective: To determine the indications for preoperative localization of a small indeterminate pulmonary nodule.
Design: In this retrospective study, univariate and multivariate analyses were performed by the logistic regression procedure.
Setting: A single National Cancer Center Hospital in Japan.
Patients: A series of 92 consecutive patients who underwent video-assisted thoracoscopic surgery (VATS) at our institute between 1993 and 1996.
Interventions: The frequency and reasons for conversion to thoracotomy were assessed retrospectively. All preoperative CT scans were reviewed for eight radiologic features by two of the authors. These data were entered into univariate and multivariate analyses to identify the significant risk factors for a failure to detect a pulmonary nodule.
Measurements and results: Fifty
patients (54%) needed conversion to a thoracotomy. The most common
reason for the conversion was failure to localize nodules (46%).
Univariate and multivariate analyses of 11 variables revealed one
significant risk factor in the failure to detect nodules:
distance to the nearest pleural surface (p < 0.05). Tumor size on
radiograph remained marginally significant (p = 0.065) in
multivariate analyses. If the distance to the pleural surface was > 5
mm in cases of nodules 
10 mm in size, the probability of failure to
detect a nodule was 63%.
Conclusions: Our
results suggested the indications for preoperative localization of a
peripheral pulmonary nodule. Preoperative marking for a small
indeterminate pulmonary nodule should be considered when the distance
to the nearest pleural surface is > 5 mm in cases of lung nodules of
10 mm in size.
Key Words: detectability • distance to the pleural surface • indeterminate lung nodule • preoperative localization • thoracoscopy • tumor size • univariate and multivariate analysis
Small peripheral pulmonary nodules, which could not be detected by conventional radiography, have become detectable by helical CT screening.1 Conventional diagnostic modalities such as bronchoscopic or transthoracic needle biopsy are not very useful in the diagnosis of some of these small lung nodules, and video-assisted thoracoscopic surgery (VATS) has come to play a more important role. Although this technique has been reported to be safe and definitive,2 ,3 ,4 ,5 some lung nodules are difficult to identify thoracoscopically. The smaller the nodules are, the more difficult they are to localize. Preoperative marking of a pulmonary nodule is sometimes necessary if it is too small or too far from the pleural surface to be identified by thoracoscopy. Although there have been many articles on methods for preoperative marking,6 ,7 ,8 ,9 there has only been a single report that dealt with the indications for these methods.10
We assessed the probability of intraoperative detection of small peripheral pulmonary nodules during thoracoscopic exploration, based on the radiographic findings on preoperative CT images, in an attempt to clarify the indications for preoperative marking.
Materials and Methods
Between 1993 and 1996, 92 patients (47 men, 45 women) who underwent VATS at our institute had indeterminate lesions, despite preoperative transthoracic needle biopsy and/or transbronchial biopsy. Procedures performed before the decision to undergo a VATS biopsy are shown in Table 1 . Ages ranged from 14 to 82 years, with a median of 56 years. All patients underwent a chest CT scan preoperatively. Thoracoscopic surgery was performed under general anesthesia using single lung ventilation via a dual lumen endobronchial tube. The thoracoscope was inserted through a thoracic port in the seventh intercostal space on the midaxillary line in most cases. Additional intercostal incisions were made to visualize and manipulate the lesion as necessary. When a nodule was not visible thoracoscopically, palpation with thoracoscopic instruments was performed to localize it. When the palpation failed to localize the nodule, we converted to thoracotomy. Thoracoscopic wedge resection and/or needle aspiration biopsy/cytologic examination were performed for lesions that we localized. All specimens underwent immediate histologic/cytologic examination. When a nodule was found to be benign, a chest tube was inserted and the operation was finished. When a nodule was found to be malignant, we converted to thoracotomy and performed a lobectomy. The reasons for all the conversions to thoracotomy were assessed retrospectively.
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Univariate and Multivariate Analyses
Univariate and multivariate analyses were performed by the
logistic regression procedure11
using the software
Statistica 4.1J (Apple Computer, Inc; Cupertino, CA) to identify the
significant risk factors for a failure to identify the lesions
thoracoscopically. The 11 variables included in the analyses were as
follows: age; gender; histology (adenocarcinoma or not); size of the
lesion on radiograph; distance to the nearest pleural surface; and
presence or absence of vascular convergence, spiculation, pleural tail,
cavitation, smooth nodular edge, and calcification. In multivariate
analyses, forward and backward stepwise procedures were used to
determine the combination of factors that was important to predict a
failure to detect the lesions. Statistical analysis was considered to
be significant at p < 0.05.
Results
Histologic Findings and Size of Indeterminate Pulmonary Nodules
A definitive diagnosis was obtained in all patients (Table 2
).
Thirty-seven patients (40%) had malignant disease. Among them, 26
patients (28%) had primary lung adenocarcinomas, 10 (11%) had
metastatic lung cancer, and 1 (1%) had malignant lymphoma. The other
patients had benign disease. Granuloma was proven in 19 patients (21%)
and intrapulmonary lymph node in 12 patients (13%). Pulmonary nodules
< 10 mm in size tended to be benign tumor. However, 3 of 26 primary
lung adenocarcinomas were < 10 mm in maximum tumor dimension.
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Probability of Failure to Detect the Lesions
We evaluated the probability of failure to detect the lesions
based on two parameters: tumor size and distance to the pleural surface
(Table 7 ).
In both patients whose lesions were < 10 mm in diameter, and the
distance to the pleural surface was > 10 mm, the lesions were not
detected. If the distance to the pleural surface was > 5 mm in cases
of lesions of 10 mm in size, the probability of failure to detect
was 63%.
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In Japan, screening for lung tumor with spiral CT has become available and many otherwise undetectable small lung nodules have been detected.1 Conventional diagnostic modalities are not very useful in the diagnosis of such small lung nodules, and VATS biopsy plays an important role. In most cases in this study, we performed preoperative bronchoscopy and/or percutaneous needle biopsy, with or without CT guidance. These techniques are less invasive, but often fail to diagnose the nodule as benign. In contrast, VATS offers a minimally invasive approach for the diagnosis of lung nodules and virtually 100% sensitivity and specificity without serious complications.12 ,13 Although the value of the thoracoscopic approach remains controversial, thoracoscopy has been considered to be less invasive than conventional thoracotomy. To accomplish this procedure without converting to a thoracotomy, localization of the lung nodule is mandatory. If the lung nodule is small and deeply located, preoperative intrapulmonary marking should be considered. Guidelines for the indications for preoperative marking have rarely been reported, and decisions have been made based on the experiences of the thoracic surgeons in charge. Although it may be impossible to establish an absolutely objective guideline, our results would be helpful in such a clinical setting.
Our approach to the small indeterminate pulmonary nodule includes not only video-assisted thoracoscopic biopsy, but also transbronchial lung biopsy, and/or CT-guided transthoracic needle biopsy (Fig 1 ). VATS biopsy is performed only when the other conventional biopsy modalities have failed to diagnose the indeterminate nodules or have not been indicated. To our knowledge, it is not possible to arrive at a consensus on the proper management of an indeterminate pulmonary nodule. Munden et al14 reported that a considerable number of small pulmonary nodules < 1 cm in size were malignant. Small peripheral pulmonary nodules, which could not be detected by conventional radiography, have become detectable by helical CT screening in Japan.1 Considering this situation, we attempt to obtain a definitive diagnosis of small indeterminate pulmonary nodules as often as possible. As a result, we obtained a definitive diagnosis for all indeterminate pulmonary nodules, and 37 cases (40%) were diagnosed to have a malignant tumor. Of course, we followed up on a number of patients with indeterminate pulmonary nodules instead of obtaining a definitive diagnosis. Although a definitive criteria for the following up of patients does not exist, we exclude many patients with indeterminate pulmonary nodules based on the findings of benign calcification pattern, stable size of tumor for 2 years, and so on.
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10 mm in
size, the probability of failure to detect the lesions is > 50%.
Therefore, preoperative marking should be considered in such a clinical
setting. Furthermore, preoperative marking would be absolutely
indicated when the distance is > 10 mm, since the failure probability
was 100% in such cases. Adenocarcinoma is likely to be more detectable than other lung histologic findings, as it is often accompanied by some pleural changes, such as pleural indentation. In this study, however, adenocarcinoma showed only a marginally significant difference in detectability. One of our adenocarcinoma cases could not be palpated. The histopathologic subtype of the tumor was found to be localized bronchioloalveolar carcinoma (LBAC).15 This type of adenocarcinoma shows replacement growth of atypical cells with minimal or mild thickening of the alveolar septa. Fibrotic foci, pleural tail, and/or spiculation are often lacking. These histologic features often make an LBAC difficult to palpate, as it may show no more rigidity than the normal lung tissue. No matter how near to the pleural surface or how large a LBAC may be, surgeons may fail to palpate the lesion. Peripheral hyperplastic lesions, such as atypical adenomatous hyperplasias or type II pneumocyte hyperplasias, have similar morphologic characteristics to LBAC.16 ,17 Therefore, it would also be difficult to palpate these lesions digitally. These histologic factors should be taken into account when using the indications for preoperative marking proposed in this study.
We studied patients who underwent thoracoscopic surgery between 1993 and 1996 in this report. These cases were from our initial experiences in thoracoscopic surgery at our institute. We did not perform thoracoscopic surgery for patients with small, deeply situated, indeterminate lung tumors during this period. There may have been some bias in patient selection in this study. Nevertheless, we chose this time frame because we began to perform preoperative marking with several methods during the period. Although the results are based on our experiences in the learning curve period and may contain bias, we are sure that they will offer some help in indicating preoperative marking. Additional studies are necessary to determine what factors would be predictive for the detectability of lung nodules in a recent group of patients.
We attempted to clarify the detectability of intrapulmonary nodules in the study. Furthermore, it might also be possible to determine the indication for surgical intervention in indeterminate pulmonary nodules. For instance, nodules < 10 mm in size tended to be benign, and VATS for these small nodules might not be indicated. However, 3 of 26 primary lung adenocarcinoma were < 10 mm in size in this study, and Munden et al14 reported that small pulmonary nodules could be malignant. Therefore, such small nodules should not be necessarily excluded from surgical intervention to obtain the definitive diagnosis. Further prospective studies are needed to clarify the indication of biopsy.
Conclusions
The indications for preoperative marking of small peripheral
pulmonary nodules were proposed in this study. The probability of
failure to localize a lung nodule was significantly associated with the
distance between the nearest pleural surface and the nodule, and was
marginally associated with tumor size on radiograph. In conclusion, the
indications of preoperative marking are as follows: 1. Absolute
indications: when the distance to the nearest pleural surface is > 10
mm in cases of lung nodules 10 mm in size. 2. Relative indications:
when the distance to the nearest pleural surface is > 5 mm in cases
of lung nodules 10 mm in size.
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ACKNOWLEDGMENT: We thank Satoshi Sasaki, Epidemiology and Biostatistics Divisions, National Cancer Center Research Institute East, for his technical support in statistical analyses. We also thank Professor J. Patrick Barron, International Medical Communications Center, Tokyo Medical College, for reviewing the English manuscript.
Footnotes
Supported in part by a Grant-in-Aid for Cancer Research from the Ministry of Health and Welfare.
Correspondence to: Kenji Suzuki, MD, Division of Thoracic Oncology, National Cancer Center Hospital East, 6-5-1, Kashiwanoha, Kashiwa, Chiba, 277 Japan; e-mail: kjsuzuki@east.ncc.go.jp
Abbreviations: LBAC = localized bronchioloalveolar carcinoma; VATS = video-assisted thoracoscopic surgery
Received for publication November 18, 1997. Accepted for publication June 8, 1998.
References
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