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Evolution of Peripheral Lung Adenocarcinomas

CT Findings Correlated with Histology and Tumor Doubling Time

¹ Department of Radiology, University of Occupational and Environmental Health School of Medicine, Yahatanishi-ku, Kitakyushu-shi, 807-8555 Japan.
² Department of Pathology and Oncology, University of Occupational and Environmental Health School of Medicine, Kitakyushu-shi, 807-8555 Japan.
³ Department of 2nd Surgery, University of Occupational and Environmental Health School of Medicine, Kitakyushu-shi, 807-8555 Japan.
⁴ Department of Respiratory Disease, University of Occupational and Environmental Health School of Medicine, Kitakyushu-shi, 807-8555 Japan.

Received April 20, 1999; accepted after revision August 12, 1999.

 
Address correspondence to T. Aoki.

Abstract

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OBJECTIVE. This study was performed to evaluate the evolution of peripheral lung adenocarcinomas using CT findings and histologic classification related to tumor doubling time.

MATERIALS AND METHODS. The subjects were 34 patients, each with an adenocarcinoma smaller than 3 cm. All patients underwent chest radiography and 10 of them had previously undergone CT more than 6 months before surgery. Tumor doubling time was estimated by examining sequential radiographs using the method originally described by Schwartz. Tumor growth was also observed by studying the changes on CT in the 10 patients who had previously undergone CT. The histologic classification (types A-F) was evaluated according to the criteria of Noguchi et al.

RESULTS. Five (83%) of the six adenocarcinomas with tumor types A or B showed localized ground-glass opacity on high-resolution CT. All six tumors had a tumor doubling time of more than 1 year. Fifteen (71%) of the 21 tumors with type C showed partial ground-glass opacity mixed with localized solid attenuation on high-resolution CT. Ten (48%) of these 21 type C tumors had a tumor doubling time of more than 1 year. In types B and C, the solid component or the development of pleural indentation and vascular convergence increased during observation before surgery. All seven tumors with types D, E, and F showed mostly solid attenuation, and the tumor doubling time was less than 1 year in six (87%) of the seven tumors.

CONCLUSION. Two main types of peripheral lung adenocarcinoma exist. The first type appears on CT as a localized ground-glass opacity with slow growth, and the other appears as a solid attenuation with rapid growth.

Introduction

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Adenocarcinoma is the most common histologic type of lung cancer in many countries, and its incidence has increased over the last 30 years [1,2,3]. Most patients with early-stage adenocarcinoma are asymptomatic; the common initial finding is a peripheral nodule detected by a routine radiologic examination [4]. The central scar of peripheral lung adenocarcinoma was formerly considered to be a result of a preexisting pulmonary lesion [5,6,7]. Although several conditions resulting in chronic pulmonary interstitial fibrosis are certainly associated with the development of cancer later, many of the scars are currently considered to be desmoplastic reactions to the tumor that are formed during tumor growth [8,9]. Noguchi et al. [10] reported that active fibroblastic proliferation plays an important role in tumor progression because the event histologically distinguishes the advanced from the in situ tumors in small lung adenocarcinoma. These researchers proposed a new histologic subclassification of adenocarcinoma of the lung for tumors smaller than 2 cm that shows a good correlation with the prognosis.

Many studies have documented the radiographic and CT findings of peripheral lung adenocarcinomas [11,12,13,14,15], but the correlation of these CT findings with the histologic growth pattern has not been fully explored. The aim of this study was to evaluate the evolution of peripheral adenocarcinomas of the lung using CT findings and the histologic classification of Noguchi et al. [10] related to tumor doubling time.

Materials and Methods

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We retrospectively reviewed the records and images of 34 patients who had surgically resected peripheral adenocarcinomas smaller than 3 cm between 1990 and 1997 and who underwent CT and chest radiography before surgery. All patients underwent chest radiography and 10 of them had undergone previous CT more than 6 months before surgery. The patients were 19 men and 15 women (age range, 48-81 years; mean, 69 years) who were histologically classified with six types of tumors on the basis of the tumor growth pattern using the criteria of Noguchi et al. [10]: type A (n = 3), localized bronchioloalveolar carcinoma; type B (n = 3), localized bronchioloalveolar carcinoma with foci of structural collapse of alveoli; type C (n = 21), localized bronchioloalveolar carcinoma with active fibroblastic proliferation; type D (n = 3), poorly differentiated adenocarcinoma; type E (n = 1), tubular adenocarcinoma; and type F (n = 3), papillary adenocarcinoma with a compressive growth pattern.

Most CT was performed with a TCT-900S helical scanner (Toshiba Medical, Tokyo, Japan). Routine scanning of the whole lung (120 kVp, 150 mA) was first performed using a helical mode with a table speed of 10 mm/sec and a 10-mm collimation. Images were printed as fixed settings (lung window center, -700 H; lung window width, 1500 H; mediastinum window center, 35 H; mediastinum window width, 360 H). Additional high-resolution CT with 2.0-mm collimation (120 kVp, 250 mA, and 1.0 sec scanning time) covering the tumor was performed in all patients. High-resolution CT images were reconstructed with a high-spatial-frequency algorithm and were printed at fixed settings (window center, -700 H; window width, 1500 H). All scans were obtained with the patients in the supine position and at end-inspiration. The interval between CT and surgery ranged from 2 to 45 days.

High-resolution CT findings and the serial changes of the CT and radiographic images were analyzed retrospectively by two chest radiologists, and a final consensus on the findings was reached. All surgical specimens were fixed in the inflated state by transpleural and transbronchial infusion of formalin. The specimens were sliced at the center of the tumor to provide optimal correlation with the CT images, after which all specimens were reviewed by a lung pathologist. The internal characteristics of the tumors assessed by high-resolution CT were correlated with the pathologic specimens. The high-resolution CT-pathologic correlations were decided by consensus of one pathologist and one chest radiologist. The volume doubling times were calculated using the method originally described by Schwartz [16]:

(1)

where Td = tumor doubling time, t = time lapse between two measurements, Dt = mean tumor diameter at the final measurement, and D₀ = mean tumor diameter at the initial measurement. The longest and shortest diameters of the tumor were measured by initial and final chest radiography in all but one case. In one type A tumor, serial CT scans were obtained to measure the tumor size because no abnormality was detected on chest radiography, and the diameters were estimated on optimal axial CT slices. The changes in appearance on CT were also studied in the 10 patients who had previously undergone CT for observation. Ten-millimeter-thick slices were mostly used with high-resolution CT for reference because matching the same areas was difficult by thin-slice high-resolution CT alone.

Results

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High-Resolution CT Findings
The results of the high-resolution CT findings are summarized in Table 1. Five of the six tumors with types A or B, except for one goblet cell type, showed a nodule with marked ground-glass opacity, and air bronchogram was observed in all six tumors (Figs. 1A and 2A). A focal area of increased attenuation was seen at the center of type B tumors. Fifteen (71%) of the 21 type C tumors showed partial ground-glass opacity mixed with localized solid attenuation. The areas of ground-glass opacity were smaller than those in types A and B (Fig. 3A). A pleural tag was observed both in types B and C, but not in type A. Both spiculation and air bronchogram were seen in 10 (48%) of 21 type C tumors. No spiculation was seen in tumor type A or B. All seven tumors with types D, E, or F showed mostly solid attenuation (Fig. 4A). Air bronchogram was observed in only one of these tumors.

View larger version (85K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —Type A adenocarcinoma in 53-year-old man (tumor doubling time, 662 days). High-resolution CT scan shows 12 x 12 mm area completely occupied by ground-glass opacity.

View larger version (113K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —Type B adenocarcinoma in 74-year-old woman (tumor doubling time, 695 days). High-resolution CT scan shows 18 x 24 mm area with marked ground-glass opacity containing focal area of increased attenuation. Single pleural tag and air bronchogram are also present.

View larger version (96K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —Type C adenocarcinoma in 72-year-old woman (tumor doubling time, 249 days). High-resolution CT scan shows 20 x 28 mm nodule with ground-glass opacity only at periphery. Three pleural tags and air bronchogram are visible.

View larger version (125K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —Type D adenocarcinoma in 67-year-old woman (tumor doubling time, 245 days). High-resolution CT scan shows 20 x 24 mm nodule with mostly solid attenuation and well-defined margin.

Correlation of High-Resolution CT and Pathologic Findings
The growth pattern involving replacement of alveolar lining cells accounted for the ground-glass opacity of type A (Fig. 1B) and that at the periphery of the nodules in types B and C (Figs. 2B and 3B). The central zone of higher attenuation in types B and C corresponded to the fibrotic foci as a result of alveolar collapse and a compact cellular growth pattern with active fibroblast, respectively. Types D, E, and F showed an expanding and compressive growth pattern without replacement of alveolar lining cells (Fig. 4B), which was mostly reflected as solid attenuation with a well-defined margin on high-resolution CT.

View larger version (178K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —Type A adenocarcinoma in 53-year-old man (tumor doubling time, 662 days). Photomicrograph of histologic specimen reveals localized bronchioloalveolar carcinoma growing by replacement of alveolar lining cells. Note minimal thickening of alveolar septa.

View larger version (198K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —Type B adenocarcinoma in 74-year-old woman (tumor doubling time, 695 days). Photomicrograph of histologic specimen reveals replacement growth pattern with fibrotic foci as result of collapse of alveolar structure in center.

View larger version (201K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —Type C adenocarcinoma in 72-year-old woman (tumor doubling time, 249 days). Photomicrograph of histologic specimen shows replacement growth pattern at periphery with cellular growth pattern in central zone.

View larger version (179K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —Type D adenocarcinoma in 67-year-old woman (tumor doubling time, 245 days). Photomicrograph of histologic specimen reveals solid growth and distinct boundary between tumor and nontumorous parenchyma.

Tumor Doubling Time and Changes of CT Appearances
The tumor doubling times according to tumor type are shown in Figure 5. All six tumors of types A or B had tumor doubling times of more than 1 year, which ranged from 662 to 1486 days, with a mean of 880 days. Those of type C ranged from 42 to 1346 days. The tumor doubling times of types D, E, and F ranged from 124 to 402 days, with a mean of 252 days. The difference in the tumor doubling time between the group of types A and B and the group of types D, E, and F was significant (Mann-Whitney test, p < 0.01). The changes on CT were also evaluated in the 10 patients who had previously undergone CT. Two type A tumors gradually increased in size, maintaining groundglass opacity in all areas. In types B and C, the solid component or the development of pleural indentation and vascular convergence increased during observation before surgery (183-1162 days; mean, 693 days) (Figs. 6A,6B and 7A,7B). Tumor type E and F and one case of type C showed mostly solid attenuation throughout with increased pleural indentation and vascular convergence (Fig. 8A,8B). A vascular convergence was considered to be present if there was retraction of the lung adjacent to the tumor and the vessels were closer, more curved toward the tumor, or both on follow-up CT.

View larger version (12K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5. —Graph shows tumor doubling times according to tumor type. Difference in tumor doubling time between group of types A and B and group of types D, E, and F was significant (p < 0.01). Those of type C varied widely, ranging from 42 to 1346 days.

View larger version (95K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6A. —Type B adenocarcinoma in 74-year-old man (tumor doubling time, 750 days). Initial CT scan shows localized 22 x 22 mm ground-glass opacity in left lower lobe of lung.

View larger version (114K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6B. —Type B adenocarcinoma in 74-year-old man (tumor doubling time, 750 days). CT scan obtained 349 days after initial CT scan shows increase in size (to 23 x 26 mm) and development of vascular convergence. Attenuation at center of tumor is slightly increased.

View larger version (106K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7A. —Type C adenocarcinoma in 64-year-old man (tumor doubling time, 447 days). Initial CT scan shows tiny solid nodule (arrow) with minimal adjacent ground-glass opacity (15 x 10 mm) in right middle lobe.

View larger version (111K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7B. —Type C adenocarcinoma in 64-year-old man (tumor doubling time, 447 days). CT scan obtained 1137 days after initial CT scan shows increase in size (25 x 20 mm) and vascular convergence. Area of solid attenuation is also increased.

View larger version (91K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 8A. —Type F adenocarcinoma in 75-year-old woman (tumor doubling time, 124 days). Initial CT scan shows 4 x 5 mm solid nodule in lingula.

View larger version (102K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 8B. —Type F adenocarcinoma in 75-year-old woman (tumor doubling time, 124 days). CT scan obtained 374 days after initial CT scan shows that nodule is larger (13 x 9 mm) and still solid. Pleural tag and vascular convergence also developed.

Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
Noguchi et al. [10] proposed a simple histologic subclassification of lung adenocarcinomas based on tumor growth patterns. Types A, B, and C are adenocarcinomas showing a growth pattern that involves replacement of alveolar lining cells. Types A and B show no lymph node metastasis and have an excellent outcome after surgical resection. Significant differences in the lymph node metastasis and 5-year survival rate are noted between tumors of type A or B and tumors of type C with foci of active fibroblastic proliferation; type C is considered to be a more advanced stage of types A and B. Types D, E, and F are nonreplacement types of adenocarcinomas with a less favorable prognosis [10].

In this study, we used this histologic classification because it shows a good correlation with the prognosis and is well suited for the comparison of CT findings. Although Noguchi et al. [10] limited their materials to tumors smaller than 2 cm, we included tumors as large as 3 cm in diameter because we found few tumors smaller than 2 cm. For our purpose of observing the growth and changes of the tumors on CT, we considered our criteria to be adequate.

High-resolution CT findings of bronchioloalveolar carcinoma that corresponded to types A, B, and C in our study have been described [15, 17,18,19]. Zwirewich et al. [15] showed a pathologic correlation with a variety of edges and internal characteristics of bronchioloalveolar carcinoma seen on CT. They reported that hazy attenuation at the periphery of a bronchioloalveolar carcinoma nodule corresponds to a lepidic growth pattern with a relative lack of acinar filling and that a compact cellular growth pattern reveals higher attenuation. In our study, ground-glass opacity, accounting for the growth pattern involving replacement of alveolar lining cells, was also recognized in many tumors. All tumors of types A and B, except for one goblet cell type, showed a nodule with ground-glass opacity occupying more than half the area in each lesion. Fifteen of the 21 tumors with type C also showed partial ground-glass opacity, but many of these areas of ground-glass opacity were smaller than those in types A and B. The area of ground-glass opacity may partially reflect the biologic behavior of bronchioloalveolar carcinoma. Kuriyama et al. [20] observed an air bronchogram or bronchiologram in 72% of the peripheral small adenocarcinomas and suggested that these features help differentiate adenocarcinomas from benign lesions. In our study, air bronchograms were seen in 59% of types A, B, and C, but only in 14% of types D, E, and F.

A focal area of ground-glass opacity can be seen in various disorders [21]. Jang et al. [19] reported four patients with bronchioloalveolar carcinoma that appeared as localized ground-glass opacity and mixed areas of ground-glass opacity and consolidation on thin-section CT. They suggested the appearance of focal areas of ground-glass opacity on CT is an early sign of bronchioloalveolar carcinoma because the areas of ground-glass opacity were small and a focal area of ground-glass opacity changed into mixed areas with consolidation on serial CT in one patient. In our patients who had previously undergone CT, the areas of ground-glass opacity increased gradually and were maintained as pure ground-glass opacity during the interval in type A, but the solid component in ground-glass opacity in types B and C increased during the interval. These changes observed in our patients suggest a progression from types A or B to the invasive type C.

Most peripheral adenocarcinomas form characteristic central fibrosis, and this is currently considered a desmoplastic reaction to the tumor. Eto et al. [22] analyzed the elastic fibers in the adenocarcinomas and concluded that the elastic framework of the stroma is preserved in the early development of the tumor but is disrupted as the tumors grow, indicating stromal invasion. The development of areas of solid attenuation replacing previous areas of ground-glass opacity in our cases of type C probably corresponds to this histologic change. One type C tumor showed a solid attenuation on the initial CT when the tumor was only 1 cm in diameter. All type A and B tumors had a tumor doubling time of more than 1 year, but tumors of type C ranged from 42 to 1346 days. These findings suggest that type C tumors have miscellaneous growth patterns and that stromal invasion may occur even when the tumor is small.

Types D, E, and F showed a nonreplacement growth pattern and were small advanced adenocarcinomas with a less favorable prognosis [10]. Histologically, type D tumors mostly show solid features with minor papillary and tubular growth patterns. Type E is considered to originate from or be related to bronchial glands and consists of acinar, tubular, and cribriform structures. Type F shows papillary growth but does not grow by replacing the alveolar lining cells. Macroscopically, type D, E, and F tumors show a clear boundary between the cancer and the noncancerous parenchyma. All seven tumors with types D, E, and F showed mostly solid attenuation on CT, and the tumor doubling times were less than 1 year in six of the seven tumors. These types are clearly different both histologically and on CT and radiography from types A, B, and C, which have a slow and stepwise progression.

Small lung nodules are found more frequently with the recent advances of diagnostic techniques, including CT, and treatment of the small nodules has become an important issue. The use of video-assisted endoscopic thoracosurgery [23] and limited resection for lung cancer with a favorable prognosis are under examination [24,25,26,27,28]. Our study was limited because the number of patients studied was small and previous CT findings were available for only about one third of the patients; however, peripheral adenocarcinomas of the lung seem to show a good correlation between the tumor growth and the radiographic appearances on CT.

We conclude that two main types of peripheral adenocarcinoma of the lung exist. One starts as a localized ground-glass opacity on CT with slow growth and the other starts as a solid attenuation with rapid growth. Radical surgery may not be necessary for a small lung adenocarcinoma that appears as a localized ground-glass opacity on CT, but further studies are necessary to determine the best surgical approach for peripheral adenocarcinoma of the lung.

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