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Ann Thorac Surg 2002;74:1635-1639
© 2002 The Society of Thoracic Surgeons

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Original article: general thoracic

"Early" peripheral lung cancer: prognostic significance of ground glass opacity on thin-section computed tomographic scan

^a Division of Thoracic Surgery National Cancer Center Hospital, Tokyo, Japan
^b Division of Diagnostic Radiology, National Cancer Center Hospital, Tokyo, Japan

Accepted for publication June 13, 2002.

* Address reprint requests to Dr Suzuki, Division of Thoracic Surgery, National Cancer Center Hospital, 1-1, Tsukiji 5-chome, Chuo-ku, Tokyo 104-0045, Japan.
e-mail: kjsuzuki{at}ncc.go.jp

	Abstract

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
BACKGROUND: The number of peripherally located lung cancers with an excellent prognosis has been increasing, possibly due to the introduction of computed tomography for lung cancer screening in Japan. The concept of peripherally located "early lung cancer" remains controversial.

METHODS: A retrospective study was conducted on 1,540 lung cancers resected at our institute between May 1992 and December 2000. The sizes of solid attenuation and ground glass opacity were evaluated radiologically and the relationships between radiologic findings and clinicopathologic features were investigated to define peripheral early lung cancer.

RESULTS: Sixty-nine (4.4%) lung cancers showed a large ground glass opacity component on thin-section computed tomographic scan. The maximum tumor dimension ranged from 6 to 41 mm, and all tumors were clinical stage I. Forty-seven patients were diagnosed as having bronchioloalveolar carcinoma pathologically. None of the tumors showed lymph node involvement or lymphatic invasion. Only two showed vascular invasion, but all were pathologic stage I disease. Most of the lung cancers that showed pure ground glass opacity were bronchioloalveolar carcinoma.

CONCLUSIONS: Peripheral lung nodules with a large ground glass opacity component on thin-section computed tomographic scan, which do not disappear during follow-up, tend to be bronchioloalveolar carcinomas or minimally invasive adenocarcinomas of the lung. These findings warrant a feasibility study of limited surgical resection for such lung tumors.

	Introduction

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The prognosis of resected lung cancer remains poor, and less than 80% of the patients with stage I disease are cured by surgical resection alone [1]. Because regional lymph node metastases are found in approximately 20% of primary lung adenocarcinomas of 2.0 cm or smaller [2, 3], major lung resection and locoregional lymph node dissection or sampling have been recommended even for small tumors [4]. The recent introduction of computed tomographic (CT) scan for screening has enabled the earlier detection of lung cancer in Japan. Most peripherally located lung cancers detected with CT scan have been stage I disease, and their surgical outcome has been excellent [5–9]. Such early lung cancer challenges the dogma that major lung resection and regional lymph node dissection or sampling is recommended even for small tumors.

We attempted to identify such favorable lung tumors based on information available at the time of operation.

	Material and methods

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Between May 1992 and December 2000, 1,540 patients underwent lung resection for lung carcinoma at the National Cancer Center Hospital, Tokyo, Japan. Among them, 69 patients (4.4%) with peripheral lung cancer that showed a large ground glass opacity (GGO) component on thin-section CT were selected to be investigated retrospectively. The CT scan was performed using a TCT 900S or X-Vigor (Toshiba, Tokyo, Japan), and 10-mm-thick contiguous collimation was used to evaluate the entire lung. All primary tumors were evaluated with thin-section CT. Helical scans with 2-mm collimation were performed through the primary tumor. Images were reconstructed with a high-frequency algorithm, and photographed with a window level of -600 H and a window width of 2,000 H, as a "lung window." Radiologically, the following factors were evaluated by three independent observers on thin-section CT: the maximum tumor dimension, the size of GGO, and the size of solid attenuation. The GGO was defined as a hazy increase in lung attenuation without obscuring the underlying bronchial or vascular structures [10]. Solid attenuation was defined as an increase in lung attenuation obscuring the underlying structures. The ratio of the size of solid attenuation to the maximum tumor dimension (Cons/Tumor) was calculated in one dimension and tumors for which this ratio was less than 0.5 were selected to be investigated (Fig 1). The patients were divided into two groups: pure GGO and complex GGO. Pure GGO denoted a lung tumor that was composed of just GGO on thin-section CT scan (Fig 2), whereas complex GGO denoted lung tumor that was composed of GGO and solid attenuation on thin section CT scan (Fig 3). The cut-off line was based on our earlier experience [11]. The medical record of each patient was examined for age, gender, preoperative serum carcinoembryonic antigen level, the location of the primary tumor, clinical TNM status, histology, maximum tumor dimension, pathologic TNM status, pleural involvement (P0 versus P1 to P3), vascular invasion (positive versus negative), and operative procedure (pneumonectomy versus lobectomy or limited operation). The normal range for the carcinoembryonic antigen level at our institute was 5.0 ng/mL or less. Pleural involvement was classified as P0, P1, P2, or P3; P0 included tumor with no pleural involvement or reaching the visceral pleura but not extending beyond its elastic pleural layer; P1 included tumor reaching the visceral pleural elastic layer but not exposed on the pleural surface; P2 included tumor exposed on the pleural surface; and P3 included tumor invading the parietal pleura or chest wall [12]. Vascular invasion indicated tumor cells identifiable in a blood vessel lumen. Histologic typing was determined according to the World Health Organization classification [13]. All resected specimens were formalin-fixed and sliced at 5- to 10-mm intervals. Primary lung neoplasms and nodules were evaluated microscopically by conventional hematoxylin and eosin stain. The stage of the disease was based on the TNM classification of the International Union Against Cancer, 5th edition [14]. The extent of lymph node dissection or sampling was based on the report by Naruke and colleagues [15]. However, we modified the extent of lymph node dissection according to the report by Asamura and associates [16]. Thus, for tumors located in the upper lobes, dissection of the subcarinal lymph node was omitted if pretracheal lymph nodes were shown to be tumor-free by intraoperative frozen-section diagnosis, whereas for tumors in the lower lobes, dissection of superior mediastinal lymph nodes was omitted if hilar and subcarinal lymph nodes were shown to be tumor-free. The surgical procedure depended on the surgeon, and no definitive criteria for limited surgical resection or lymph node dissection were adopted. For instance, peripherally located small tumors in the left upper lobe might be resected by segmentectomy or partial resection.

View larger version (113K): [in this window] [in a new window]   Fig 1. Thin-section computed tomographic scan of lung carcinoma showing solid attenuation and ground glass attenuation. Largest dimension of tumor (line A) and solid attenuation (line B) were decided based on thin-section computed tomographic scan. The Cons/Tumor ratio is defined as line B/line A.

View larger version (122K): [in this window] [in a new window]   Fig 2. Thin-section computed tomographic scan of bronchioloalveolar carcinoma showing pure ground glass attenuation. The Cons/Tumor ratio was calculated to be zero for this patient.

View larger version (112K): [in this window] [in a new window]   Fig 3. Thin-section computed tomographic scan of lung adenocarcinoma showing solid and ground glass attenuation (so-called complex type). The Cons/Tumor ratio was calculated to be 0.33 for this patient.

	Results

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Extent of surgical resection and lymph node dissection or sampling
Major lung resection was performed in 43 patients (63%), whereas the other 26 patients (37%) underwent limited lung resection. Lymph node dissection was performed based on the description by Naruke and colleagues [15]. Complete hilar and mediastinal lymph node dissection was performed in 22 patients (32%), lymph node dissection up to the hilar region was performed in 29 (42%), and no sampling was conducted in 16 patients (23%). All of these latter patients were surgically evaluated as Nx status. The relationships between the extent of operation and clinicopathologic features are shown in Table 3 (see below).

Radiologic features of bronchioloalveolar carcinoma
Among 47 bronchioloalveolar carcinomas, 32 showed a pure GGO pattern on thin-section CT. Pure GGO lesions tended to be bronchioloalveolar carcinomas.

Histologic findings of lung cancer showing pure GGO on CT
Among the 38 peripherally located lung cancers that showed pure GGO on thin-section CT, six were diagnosed to be adenocarcinoma based on the recently re-vised World Health Organization criteria [13]. None of the pure GGOs showed vascular, lymphatic, or pleural invasion by tumor cells.

Survival data
The median follow-up period for patients alive has been 35 months. Thus far, we have not observed either local or distant failure. All of the patients are still alive without disease.

	Comment

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
The concept of "early" lung cancer is well known for centrally located squamous cell carcinoma of the lung, but has not yet been widely accepted for peripherally located lung cancer, although some investigators have reported that bronchioloalveolar carcinoma without fibrotic scarring could be considered early adenocarcinoma of the lung, so-called in-situ peripheral lung carcinoma [12, 17–21]. However, their criteria were based on postoperative pathologic findings, which means that the definition can only be determined after resection, and therefore, could not have a strong impact on the choice of treatment. Therefore, we need criteria that are available preoperatively to define early minimally invasive lung cancer. Our present results show that peripheral lung carcinomas with a large GGO component on thin-section CT scan tend to show a minimally invasive nature pathologically and can be defined as early peripheral lung cancer.

Although many researchers have tried to define invasiveness pathologically, few acceptable definitions are available for lung cancer [12, 17–20, 22]. Furthermore, because these definitions are based on pathologic findings, they are not available preoperatively. Thus, these definitions have made little impact on surgical practice. However, if such early peripheral lung cancer could be diagnosed preoperatively, it would have an enormous impact. Surgical resection theoretically could be minimized, or even careful follow-up might be indicated, for such early peripheral lung cancer. The indications for surgical intervention for indeterminate lung nodules showing a GGO appearance on thin-section CT remain controversial. Some GGOs disappear on follow-up, whereas others remain stable or get bigger. We have not decided on the absolute indications for operation for GGO. However, when we find GGO, we observe the tumor for at least 3 months to determine whether or not it disappears. If the tumor disappears or gets smaller, we abandon surgical resection. If the tumor gets bigger, surgical resection is indicated. If the tumor remains stable, we previously performed surgical resection. Most of the tumors were adenocarcinoma or bronchioloalveolar carcinoma pathologically, although we do not know the exact numbers. However, we now often observe such tumors if they show a pure GGO appearance on thin-section CT scan and the maximum dimension of the tumor is 1.5 cm or less to investigate the natural history of such lung tumors.

Our present study was retrospective and there were many limitations. Thus, we are planning to conduct a prospective study on the natural history of GGO to answer the following important questions: (1) What is the population at risk for this condition? (2) What is the prevalence of this condition in the at-risk group? (3) What are the sensitivity and specificity of the screen?

We previously reported that the size of central fibrosis in peripherally located adenocarcinoma of the lung has prognostic significance [21]: a smaller central fibrosis of lung adenocarcinoma is associated with a better prognosis. The newly defined clinical prognostic factor is different from other conventional pathologic prognostic factors in that it can be evaluated preoperatively. Ground glass opacity and hazy attenuation on high-resolution CT have been reported to be comparable to pathologic lepidic tumor growth [23, 24], which means that if a lung tumor shows focal GGO on CT, we can know the area of pathologic lepidic tumor growth, and then predict the size of central fibrosis. Thus, our present study confirmed our previous results, that is, peripheral lung cancer with a small area of solid attenuation surrounded by a large GGO component on thin-section CT scan should show an excellent prognosis and have favorable pathologic characteristics. Such lung tumor can be defined as surgically curable early lung cancer.

Major lung resection has been accepted as the standard operative procedure, even for small lung cancer based on the results of a phase III trial conducted by the Lung Cancer Study Group (ie, comparison of limited surgical resection with major lung resection for stage IA nonsmall cell lung cancer) [25]. This trial clearly showed the inferiority of limited surgical resection in terms of locoregional relapse or prognosis, and failed to show the feasibility of limited surgical resection for stage IA lung cancer. We believe that a similar trial could be instituted for selected patients with stage IA lung cancer, using preoperative CT findings to establish the criteria for patient selection. Lung cancer showing small solid attenuation with a surrounding large GGO component on CT scan would have favorable pathologic features (ie, a minimally invasive nature), and patients with such lung cancer are possible candidates for limited surgical resection or minimized hilar and mediastinal lymph node sampling.

Our present study showed that the extent of the GGO component on thin-section CT scan has prognostic significance. Peripheral lung nodules with a large GGO component on thin-section CT, which do not disappear during follow-up, tend to be bronchioloalveolar carcinomas or minimally invasive adenocarcinomas of the lung. If such tumors are small and located in the peripheral region, segmentectomy or partial resection might be enough to achieve a cure. Otherwise, observation without operation might be an option. A prospective study is needed to give more conclusive results.

	Acknowledgments

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
The work was supported in part by a Grant-in-Aid for Cancer Research from the Ministry of Health and Welfare, Tokyo, Japan.

	References

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Suzuki, K. Articles by Tsuchiya, R. Search for Related Content PubMed PubMed Citation Articles by Suzuki, K. Articles by Tsuchiya, R.