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Ann Thorac Surg 2006;81:413-419
© 2006 The Society of Thoracic Surgeons

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Original article: General thoracic

Radiologic Classification of Small Adenocarcinoma of the Lung: Radiologic-Pathologic Correlation and Its Prognostic Impact

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

Accepted for publication July 18, 2005.

^_* Address correspondence to Dr Suzuki, Thoracic Surgery Division, National Cancer Center Hospital, 1-1, Tsukiji 5-chome, Chuo-ku, Tokyo 104-0045, Japan (Email: kjsuzuki{at}ncc.go.jp).

General thoracic surgery: To participate in The Annals of Thoracic Surgery CME Program, please visit http://cme.ctsnetjournals.org.

 

	Abstract

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
BACKGROUND: A new radiologic classification for small adenocarcinoma is necessary for discussions of limited surgical resection for peripheral lung cancer.

METHODS: Between 1999 and 2003, 1,697 consecutive patients underwent pulmonary resection for lung cancer. Three hundred forty-nine of these patients with clinical stage IA lung cancer who had lung peripheral adenocarcinoma, 2 cm or less in size, were investigated retrospectively. Radiologic classification was based on the findings of thin-section computed tomographic scan such as the presence of solid and ground-glass opacity (GGO). Type 1 (n = 22), type 2 (n = 26), type 3 (n = 25), and type 4 (n = 43) show a simple GGO, an intermediate homogeneous increase in density, a halo, and a mixed area of GGO and a solid, respectively. Type 5 (n = 54) shows a solid tumor with GGO, and type 6 (n = 179) shows a solid tumor.

RESULTS: There was no difference in the maximum tumor dimension among the six groups. All but 1 patient had no lymph node metastases among type 1 to 4 tumors, whereas these were found in 5% and 24% of the patients with type 5 and 6 tumors, respectively. Lymphatic invasions were rarely found in patients with type 1 to 4 tumors (p < 0.001).

CONCLUSIONS: Types 1, 2, 3, and 4 are considered to be radiologic early adenocarcinoma of the lung, and their pathologic features were minimally invasive. On the other hand, type 5 and 6 tumors could have lymph node metastases and are considered to be invasive adenocarcinoma. Although limited surgical resection may be enough for type 1 to 4 tumors, anatomic pulmonary resection should be recommended for type 5 or 6 tumor.

Several authors have reported that the incidence of adenocarcinoma of the lung has been increasing [1, 2]. The introduction of computed tomography (CT) for screening of lung cancer has made it possible to detect smaller pulmonary nodules. Most of those pulmonary nodules are peripherally located adenocarcinoma of the lung, and such early detection may be associated with attainment of cure through early intervention [3, 4]. Although there is a general consensus regarding the pathologic diagnosis of early adenocarcinoma of the lung [5–8], the clinical and radiologic diagnosis of early adenocarcinoma with favorable prognosis is still controversial. Several authors have reported that adenocarcinoma of the lung that shows a wide area of ground-glass opacity (GGO) has a good prognosis [4, 9–15]. However, there is no generally accepted method for measuring the area of GGO, as it is sometimes difficult to divide peripherally located adenocarcinomas according to the existing classification. Thus, a new classification of peripherally located adenocarcinoma of the lung is necessary, and in this study we sought to determine how to best classify peripherally located adenocarcinoma of the lung retrospectively.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Patient Characteristics
Between January 1999 and December 2003, 1,697 consecutive patients underwent pulmonary resection for lung cancer. Among them, 349 patients with clinical stage IA lung cancer who had peripherally located adenocarcinoma of the lung 2 cm or less in size were investigated in this study. Patients who received preoperative treatment, such as radiotherapy or chemotherapy, or who had multiple lung cancers were excluded from the study. Informed consent was obtained from the patients. Of these, 167 were men and 182 were women. Their ages ranged from 23 to 89 years, with a median of 64 years.

Radiologic Evaluation
Contrast-enhanced 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 for preoperative staging. The size of tumors was determined digitally based on the findings of thin-section CT scan. We perform thin-section cuts for every lung tumor 2.0 cm or less in maximal dimension. All tumors were subsequently evaluated with thin-section CT scan. Helical scans with 2-mm collimation were performed through a 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." Radiologic findings were evaluated by two observers (M.K. and K.S.), who were not informed of the pathologic and prognostic outcome, on thin-section CT scan.

Radiologic Criteria for Grouping
The radiologic findings evaluated were as follows: the maximal tumor dimension, the presence and extent of solid or GGO component in tumor, and homogeneity of tumor. The solid (or consolidation) component was defined as an area of increased opacification more than 5 mm in diameter, which completely obscured underlying vascular markings. Ground-glass opacity was defined as an area of a slight, homogeneous increase in density, which did not obscure underlying vascular markings. Semiconsolidation was defined as an area of an intermediate homogeneous increase in density, which did not obscure underlying vascular markings. A halo was an area that consisted of a solid part and a surrounding GGO halo. Mixed was an area with a heterogeneous increase in density, which consisted of GGO and a solid part with an air-bronchogram. We divided the 373 small adenocarcinomas of the lung into six groups based on the extent of the solid component, presence of GGO, and homogeneity of the tumors (Table 1, Fig 1). Type 1 and 2 tumors are homogeneous in density, and lack a solid component (Figs 2, 3). The density of the tumor distinguishes type 1 from type 2. Type 3 and 4 tumors are heterogeneous in density, and the solid component comprises less than 50% of its diameter. The patterns of the solid component and GGO distinguish type 3 from type 4 (Figs 4, 5). Type 5 and 6 tumors are those that predominantly have a solid component. The presence of GGO distinguishes type 5 from type 6 (Figs 6, 7).

View larger version (55K): [in this window] [in a new window]   Fig 1. Flow chart for the new classification of small adenocarcinoma of the lung. (GGO = ground-glass opacity; w/o = without.)

View larger version (146K): [in this window] [in a new window]   Fig 2. Type 1 tumor is homogeneous in density, and this tumor has been called "pure GGO" or "simple GGO." (GGO = ground-glass opacity.)

View larger version (137K): [in this window] [in a new window]   Fig 3. Type 2 tumor is homogeneous in density. It is too dense to call it "pure GGO." The density is much denser than type 1 tumor. (GGO = ground-glass opacity.)

View larger version (144K): [in this window] [in a new window]   Fig 4. Type 3 tumor is heterogeneous in density, and the solid component comprises less than 50% of its diameter, and is composed of solid and surrounding GGO. (GGO = ground-glass opacity.)

View larger version (157K): [in this window] [in a new window]   Fig 5. Type 4 tumor is heterogeneous in density, and the patterns of the solid component and GGO distinguish type 3 from type 4. (GGO = ground-glass opacity.)

View larger version (139K): [in this window] [in a new window]   Fig 6. Type 5 tumor predominantly has a solid component and surrounding GGO. (GGO = ground-glass opacity.)

View larger version (142K): [in this window] [in a new window]   Fig 7. Type 6 tumors predominantly have a solid component. This tumor is so-called pure solid.

	Results

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Clinical Characteristics by Radiologic Classifications
Patients with resected adenocarcinoma of the lung 2 cm or less in size were divided into six groups (Table 2). Type 1, 2, 3, 4, 5, and 6 tumors were found in 22 (5.9%), 26 (7.4%), 25 (7.2%), 43 (12.3%), 54 (15.5%), and 179 (51.3%) patients, respectively. With regard to sex differences, women outnumbered men in each category except type 6. The radiologic maximal tumor dimension ranged from 0.6 to 2.0 cm, with a mean of 1.5 cm, and there were no significant differences among the six categories. Although approximately 20% of patients with type 5 or 6 tumors did not have stage I disease, all but 1 patient with tumors in the other types had stage I disease (p < 0.001).

	Comment

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

Among the six types of peripheral small-sized adenocarcinoma, women were predominant in all types except among patients with type 6 tumors. This is an unexpected finding. Traditionally, lung cancer is found more often in men than women. There was no significant difference among the types with regard to the maximal tumor dimension. Regarding small-sized adenocarcinoma of the lung, Noguchi and colleagues [6] investigated prognostic factors based on the findings of central fibrosis. They stated that type A or B tumors should be considered "in-situ" adenocarcinoma of the lung. It is probably safe to say that segmental resection or wide wedge resection is sufficient for such tumors because of their minimally invasive nature. Type 1 tumor is also known as pure GGO or simple GGO [18]. Among 22 type 1 tumors, there was no lymph node metastasis, and pathologic findings showed minimal invasion. There were 15 (68%) tumors that were equivalent to the type A or B tumors of Noguchi and colleagues [6], ie, roughly bronchioloalveolar carcinoma. Type 2 tumor is denser than type 1 tumor on thin-section CT scan. This tumor is not a solid tumor because we can see the underlying bronchovascular structure. No lymph node metastasis was noted, and 11 tumors were similar to the type A or B tumors of Noguchi and colleagues [6]. The difference in their density is probably related to the difference in the amount of air contained in the tumor, ie, differences in alveolar space histologically. Type 3 tumor is also known as GGO halo. One tumor had metastasized to the intrapulmonary lymph node, ie, N1 node, but 15 tumors were still diagnosed as being equivalent to the type A or B tumor of Noguchi and colleagues [6]. Type 4 tumor is actually defined by our original definition. This tumor consists of a mixture of GGO and a solid part containing air, roughly air-bronchogram. There was no lymph node metastasis and no lymphatic invasion. Basically, lung adenocarcinoma in the above four types is thought to be "minimally invasive" adenocarcinoma. A limited anatomic resection of the lung could be the standard surgical procedure for such tumors in the near future.

Type 5 and 6 tumors are considered to exhibit a "solid" course. Lymph node metastasis was found in roughly 5% of type 5 tumors, and 27% of type 6 tumors. Traditionally, lymph node metastasis is found in approximately 15% of small adenocarcinoma 2.0 cm or less in size. According to our results, however, lymph node metastasis was found mostly in type 6, which meant that if peripheral lung adenocarcinoma showed GGO on thin-section CT, the probability of lymph node metastasis was less than 5%. These "solid" tumors could be divided into several subgroups by means of positron emission tomography. If the solid tumors show positive results by positron emission tomography, they may be associated with a high frequency of lymph node metastasis and a poor prognosis.

One of the important objectives of this study is to determine the indication for limited surgical resection for lung adenocarcinomas. From this concept, the classification became simpler if the classification was composed with groups, ie, types 1 through 4 and types 5 and 6. If a tumor belongs to types 1 through 4, the patient would be a candidate for limited surgical resection, whereas a tumor belonging to group 5 or 6 warrants major lung resection with systematic lymph node dissection necessary. However, we believe the six classifications proposed in this study remain important for the surgeon to plan for the management of peripheral lung cancer. For instance, most of the type 1 tumors are bronchioloalveolar carcinoma, and some of them might be indolent tumors. On the contrary, type 2 tumors tend to be adenocarcinoma with invasive foci pathologically and grow in size. Actually we made a plan for a prospective follow-up study for type 1 tumors, not for type 2 tumors. Thus, clinical strategy depends on the six classifications, and we hope to leave the classification intact.

As to the surgical indications for pure GGO tumors, we resected the tumor if it is stable or increased in size. However, from our data, tumors belonging to type 1 could be bronchioloalveolar carcinoma, and are sometimes indolent. Thus, recently we just monitor such type 1 tumors without surgical interventions if the radiologic maximal tumor dimension is less than 15 mm. If radiologic findings suggest the tumor as lung cancer, preoperative CT-guided fine-needle biopsies are not always performed because of the high rate of a false-negative result for GGO tumors.

In conclusion, a new radiologic classification of small-sized adenocarcinoma of the lung has been proposed. Because this is the retrospective study, there may be numerous levels of bias. Therefore, we are planning to perform a prospective study of the management of peripheral small adenocarcinoma of the lung. Using the classification, we can easily classify peripheral adenocarcinoma of the lung into six categories, and the classification is significantly associated with pathologic prognostic factors. Future treatment strategies for small-sized adenocarcinoma of the lung may be based on this new radiologic classification.

	Acknowledgments

Top Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
The authors thank Dr Etsuo Miyaoka, PhD, a professor of Tokyo University of Science, for his technical support for statistical analysis. This work was supported in part by a Grant-in-Aid for Cancer Research from the Ministry of Health and Welfare.

	References

Top Abstract Introduction Patients 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 Author home page(s): Kenji Suzuki Ryosuke Tsuchiya Hisao Asamura Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Suzuki, K. Articles by Asamura, H. Search for Related Content PubMed PubMed Citation Articles by Suzuki, K. Articles by Asamura, H. Related Collections Lung - cancer