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Ann Thorac Surg 1999;68:2069-2073
© 1999 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Prognostic value of bronchiolo-alveolar carcinoma component of small lung adenocarcinoma

^a Departments of Department of Thoracic Surgery, Osaka Medical Center for Cancer and Cardiovascular Diseases, Osaka, Japan
^b Department of Pathology, Osaka Medical Center for Cancer and Cardiovascular Diseases, Osaka, Japan
^c Department of Radiology, Osaka Medical Center for Cancer and Cardiovascular Diseases, Osaka, Japan

Address reprint requests to Dr Higashiyama, Department of Thoracic Surgery, Osaka Medical Center for Cancer and Cardiovascular Diseases, Nakamichi 1-3-3, Higashinariku, Osaka 537-8511, Japan

Abstract

Background. Bronchiolo-alveolar carcinoma (BAC) is often observed in lung adenocarcinoma, but its clinicopathological and prognostic significance, especially in small peripheral lung adenocarcinoma, remains undetermined.

Methods. We assessed 206 consecutive cases of surgically resected small peripheral lung adenocarcinoma (less than 2 cm in diameter) recorded between 1973 and 1997. According to the component area of well differentiated BAC within maximally cut surface specimens of tumor tissue, we semiquantitatively classified the tumors into four types: those in which the BAC component comprised 0% (type I), 1% to 49% (type II), 50% to 99% (type III), and 100% (type IV) of the tumor tissue.

Results. Forty tumors were classified as type I, 75 as type II, 74 as type III, and 17 as type IV. The tumors with less BAC, especially type I and II, showed a significantly more aggressive nodal involvement and tumor stage, and consequently a worse prognosis, while type IV tumors had no nodal involvement and the most favorable prognosis. The patients with type III showed clinicopathological characteristics somewhere between those of type II and type IV patients. Among stage I patients, however, those with type II had the worst prognosis, while those with type I showed as good a prognosis as the other two groups.

Conclusions. This novel classification based on the degree of BAC involvement in small peripheral lung adenocarcinoma may reflect clinicopathological and prognostic characteristics. This classification may prove practical for planning therapeutic strategies, in particular surgical treatment.

With the recent dramatic increase in the incidence of small peripheral lung adenocarcinoma [1, 2], has come the need to assess the value of lung resection including segmentectomy, partial resection during open thoracotomy, and video-assisted endothoracic operation, as a limited form of surgical intervention for this disease [3–12]. At our institute, procedures of this type, especially segmentectomy using Nd:YAG (Dornier Medizintechnik Co, Ltd, Wessling, Germany) laser during open thoracotomy has been aggressively applied to the treatment of such diseases, with results not inferior to those of standard surgical procedures [11, 12]. Limited procedure, moreover, has the benefit of preserving postoperative quality of life (QOL) without loss of respiratory function [13].

In regard to node dissection, assessment of preoperative node status by computed tomography or mediastinoscopy, and intraoperative checks using frozen sections of lymph node are mandatory for limited procedures. However, the closest regional lymph nodes, such as lobar and segmental nodes, can not be completely removed, and even small adenocarcinomas 2 cm or less in size have considerable potential for lymph node metastasis [4, 7, 10, 14]. There have been several reports on the dangers of limited surgery [3–6]. Therefore, a more reliable indicator for node metastasis in this disease is needed.

Bronchiolo-alveolar carcinoma (BAC) in lung adenocarcinoma, in which tumor cells grow upon preexisting alveoli walls without damaging the underlying architecture of the lung [15], is often observed, but its clinicopathological and prognostic significance, especially in small peripheral lung adenocarcinoma remains undetermined. It was recently reported that localized pure BAC differed from other adenocarcinomas of the lung [16]. This type of tumor has a good prognosis without nodal involvement, suggesting that the BAC pattern within the tumor tissue can provide information as to surgical strategy in association with node metastasis and prognosis. The purpose of this study was to determine the value of BAC pattern within tumor tissue of small peripheral lung adenocarcinoma as a clinicopathological indicator, especially of the extent of nodal involvement and prognosis.

Patients and methods

From 1973 through 1997, 1590 lung cancer patients underwent surgical resection of the lung at our institute, Osaka Medical Center for Cancer and Cardiovascular Diseases in Japan. Of these, the records of 206 patients (13%) with small peripheral lung adenocarcinoma, 2 cm or less in maximum dimension on resection, were studied retrospectively. The mean patient age was 59.9 years, and the male to female ratio was 1.26 (115 to 91). The cases were classified according to the TNM classification and the International Staging System for Lung Cancer [17].

Surgical treatment of these patients included the following: standard resection, including pneumonectomy and lobectomy was done in 3 and 123 cases, respectively, while limited resection, including segmentectomy [11, 12] and partial resection was done in 60 and 20 cases, respectively; mediastinohilar node dissection was performed in 158 cases, whereas incomplete hilar node dissection was done in 26; 12 patients underwent limited resection without node dissection, among whom 2 underwent video-assisted thoracoscopic wedge resection; consequently, 190 patients underwent potentially curative operation, while noncurative operation was performed in 16 cases, 14 for pleural dissemination and 2 for residue in the surgical margin.

The surgically resected tumors were fixed routinely in 10% formalin and embedded in paraffin. Four micrometer sections, including the largest piece cut from the surface of the tumor in each case, were stained with hematoxylin and eosin and elastica van Gieson, and then examined by light microscopy.

The tumors of these patients were classified by histological examination into four types according to the area occupied by well differentiated BAC within the whole tumor tissue; those in which the BAC component comprised 0% (type I), 1% to 49% (type II), 50% to 99% (type III) and 100% (type IV) of the tumor tissue (Fig 1). These analyses were performed semiquantitatively by 2 or 3 observers. When the BAC component area could not be analyzed on the hematoxylin and eosin stained section, for example due to insufficient preservation by limited lung resection, the elastic fiber pattern was assessed on the elastica stained section.

View larger version (141K): [in this window] [in a new window]   Fig 1. Classification based on the extent of well differentiated bronchiolo-alveolar carcinoma (BAC) within the tumor tissue. (A) Type I, tumor has no BAC component (0%). (B) Type II, tumor less than 50% BAC. (C) Type III, more than 50% BAC. (D) Type IV 100% BAC. The right-upper corner shows a high-power magnification of each tumor tissue.

Results

Of the 206 patients with small peripheral lung adenocarcinoma, 40 patients (19%) had tumors of type I, 75 (36%) of type II, 74 (36%) of type III, and 17 (8%) of type IV. Table 1 shows a summary of the association between each type and the clinicopathological factors.

Results of postoperative survival analyses for all the patients are shown in Figure 2. The 5-year overall survival rate was 60% for type I, 57% for type II, 88% for type III, and 100% for type IV (Fig 2A). Also, the 5-year disease-free survival rate among the patients undergoing potentially curative operations was 60% for type I, 55% for type II, 90% for type III, and 100% for type IV (Fig 2B). Thus, those patients with less extensive BAC involvement showed a significantly poorer prognosis (overall survival, p = 0.0009; DFS, p < 0.0001).

View larger version (12K): [in this window] [in a new window]   Fig 2. (A) Postoperative overall survival among all the patients (n = 206). (B) Postoperative disease-free survival (DFS) among the patients undergoing potentially curative operation (n = 190). The groups with less of a BAC component showed a significantly worse prognosis (overall survival, p = 0.0009; DFS, p < 0.0001).

View larger version (13K): [in this window] [in a new window]   Fig 3. (A) Postoperative overall survival among the patients with stage I disease (n = 151). (B) Postoperative disease-free survival (DFS) among the stage I patients undergoing potentially curative operation (n = 149). Type II patients showed a significantly worst prognosis (overall survival, p = 0.0007; DFS, p < 0.0001). In contrast, type I patients showed rather the same prognosis as type III patients.

Based on the results using the proposed system for classifying small peripheral lung adenocarcinoma, tumors with less BAC, namely types I and II showed significantly more aggressive nodal involvement (p < 0.0001). The incidence of node-positive cases amounted to 38% for type I and 35% for type II, as opposed to just 9% for type III, and interestingly 0% for type IV. Nevertheless, there was a problem regarding the background of patients in our series, as patients underwent various types of surgical treatment for lung cancer. Of particular importance, complete mediastinohilar node dissection was not performed in all patients. However, only 2 patients with type II tumors showed local recurrence in the regional lymph nodes following limited operation so far (data not shown). Therefore, our results concerning nodal involvement status in each group in this study seem to be reliable.

The proposed system of classification for this disease may be suggestive of the outcome of surgical intervention. Based on these findings, patients with type III and IV appear to be candidates for limited surgical procedure. In particular, partial resection without node dissection may be possible in the type IV patients. Therefore, some of the patients from these two groups may be able to undergo video-associated endoscopic thoracic operation [7–9]. In contrast, standard resection with node dissection would appear to be a reasonable surgical modality for type I and II patients.

Our results, regarding the prognosis for small lung adenocarcinoma, are also of interest. In the overall and DFS analyses using all patients, type I showed the same prognosis as type II, which had the worst clinical outcome, while the 5-year-survival rate for type IV was 100%. In contrast, type III showed a clinical course somewhere between that of type I or II and type IV. Considering the association between each type and the node status or stage in these series, such prognostic results may be regarded as reasonable. Among stage I patients, however, although those with type II tumors had a poor prognosis, those with type I showed rather as good a prognosis as the patients of the other groups. This finding is apparently paradoxical, but may be suggestive of oncobiological characteristics, possibly patients with type I do not show bad characteristics early on, but once their tumors metastasize, for example into the regional nodes, their biological characteristics may change and the tumor may take on an extremely aggressive clinical course.

This novel classification may be closely associated with conventional histological subtype of lung adenocarcinoma [15, 16]. The type IV tumors were purely well differentiated bronchiolo-alveolar adenocarcinoma, while the type I tumors were usually a poorly differentiated, tubular, and pure papillary type of lung adenocarcinoma. In contrast, the majority of type II and III tumors were usually a papillary subtype with an extensive BAC involvement and a wide range of biological characteristics. Noguchi and colleagues [16] recently created a new system for classifying small peripheral lung adenocarcinoma, which reflected clinicopathological and prognostic factors. Our classification is strongly correlated with Noguchi and colleagues [16]: type IV being included in his type A and a part of type B, type I usually in types D, E, and F, and types II and III in type C and a majority of type B, respectively. However, our system is based on BAC component area within the whole tumor tissue, and in particular, was of value in the distinction of clinicopathological and prognostic behaviors between types II and III, which account for the majority of small peripheral lung adenocarcinomas. There are often difficulties in distinguishing between type B or C using Noguchi’s classification [16], because of misjudgment as to the occurrence of active fibroblast proliferation within the tumor tissue. Thus, our classification seems to be more practical and clinically useful.

As described above, our classification for small peripheral lung adenocarcinoma may be applied as a surgical indicator, but because postoperative pathological analysis uses resected materials, unfortunately it cannot be used as a preoperative tool. Nevertheless, computed tomography (CT) scans, especially thin-section CT scans, have enabled small lung adenocarcinoma to be diagnosed, and interestingly, the extent of ground-glass opacity (GGO) may be well correlated with that of bronchiolo-alveolar growth of lung adenocarcinoma [18–20]. The percentage of GGO areas within the tumor tissue was greatest in patients with nonreplacement growth pattern adenocarcinoma, replacement growth pattern adenocarcinoma, and localized BAC, respectively. Therefore, the radiologic appearance of thin-section CT scans in this disease may be useful in surgical planning and prognostic diagnosis [20].

In conclusion, this novel classification based on the semiquantitative analysis of BAC component area in small peripheral lung adenocarcinoma may reflect clinicopathological and prognostic characteristics of the tumor. Therefore, it may be a useful tool for planning therapeutic strategies, particularly for surgical treatment and prognosis. In order to better apply our data preoperatively, preoperative quantitative analysis of the BAC area on thin-section CT may be prospectively needed.

Acknowledgments

This work was supported in part by a Grant-in-Aid for Cancer Research (9-18) from the Ministry of Health and Welfare, Japan.

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