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1
Department of Radiology, Shinshu University School of Medicine, Asahi 3-1-1,
Matsumoto, 390 8621, Japan.
2
Present address: Azumi General Hospital, Ikeda, Nagano, 399-8695, Japan.
3
Department of Laboratory Medicine, Shinshu University School of Medicine,
Asahi, Matsumoto, 390 8621, Japan.
Received September 29, 2000;
accepted after revision November 13, 2000.
Address correspondence to S. Sone.
Abstract
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MATERIALS AND METHODS. We examined high-resolution CT morphologic features of 59 small, surgically resected peripheral lung adenocarcinomas (diameter, 6-20 mm) that were detected on screening for lung cancer using low-dose helical CT. Among these adenocarcinomas, 14 (24%) were visible and 45 (76%) were invisible on conventional chest radiography. The correlation between high-resolution CT morphologic features and tumor growth patterns was analyzed.
RESULTS. Sixteen (94%) of 17 type A (Noguchi's classification) adenocarcinomas appeared as nodules of pure ground-glass attenuation (high-resolution CT type I). Ten (71%) of 14 type B tumors appeared as heterogeneous, low-attenuation nodules (type II). Seven (29%) of 24 type C tumors appeared as nodules with ground-glass attenuation in the periphery and a high-density central zone (type III), and 12 (50%) of 24 type C tumors appeared as homogeneous nodules with soft-tissue density (type IV). Among tumors with a replacement growth pattern, the size and CT values of type C tumors were larger than those of type A or type B tumors (p < 0.05), whereas the percentage of ground-glass attenuation and retained air space in type C tumors was smaller than those in type A or type B tumors (p < 0.01). All (100%) four type D tumors appeared to be homogeneous nodules with soft-tissue density (type IV).
CONCLUSION. Small peripheral lung adenocarcinomas shown on CT exhibit four high-resolution CT patterns that corresponded to the histopathologic findings of different tumor growth patterns.
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In recent years, adenocarcinoma has replaced squamous cell carcinoma as the
most frequent histologic subtype of lung cancer
[10]. Noguchi et al.
[11] classified small (
20
mm) adenocarcinoma of the lung into six types (types A—F) based on tumor
growth patterns. Aoki et al.
[12] evaluated the evolution
of peripheral lung adenocarcinoma using CT findings and histologic
classification (types A—F) in their series, which included tumors as
large as 30 mm in diameter and a few tumors smaller than 20 mm. However, the
correlation of high-resolution CT and histologic growth patterns for small
peripheral adenocarcinomas (20 mm) has not been fully evaluated.
The aim of this study was to determine the correlation between
high-resolution CT morphologic features of small peripheral lung
adenocarcinoma (20 mm) and tumor growth patterns classified by the
criteria of Noguchi et al.
[11]. In addition, we
evaluated the visibility of tumors on chest radiographs according to
high-resolution CT patterns.
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Overall, 66 adenocarcinomas were surgically identified in 63 patients,
including one tumor larger than 20 mm and 65 tumors equal to or less than 20
mm in diameter. In this study, we excluded the single patient with a tumor
larger than 20 mm and six patients in whom high-resolution CT images or
pathologic specimens were not available for review. The remaining 59
peripheral lung adenocarcinomas (20 mm) found in 56 patients were examined
in this study. Analysis of 14 small adenocarcinomas of these tumors has been
previously reported [13]. All
56 patients were asymptomatic. They included 26 men and 30 women ranging in
age from 33 to 75 years (mean age, 64.2 years). Twenty-two tumors were 10 mm
or less, 22 were 11-15 mm, and 15 were 16-20 mm in diameter. Twenty-three
tumors were located in the upper lobe, seven in the middle lobe, and 14 in the
lower lobe of the right lung, and six tumors were located in the upper lobe
and nine in the lower lobe of the left lung. Histologically, the tumors
included 49 well-differentiated adenocarcinomas, five moderately
differentiated adenocarcinomas, and five poorly differentiated
adenocarcinomas.
High-Resolution CT and Chest Radiography Techniques
CT (including high-resolution CT) was performed on a state-of-the-art CT
scanner (HiSpeed Advantage; General Electric Medical Systems, Milwaukee, WI).
Unenhanced CT scans were performed from the lung apices to the bases during
breath-holding at mid inspiration. The technical parameters were 120 kVp, 200
mA, 1-sec scanning time, 10-mm collimation, and 32-cm field of view. An
additional 1-mm collimation was made through the entire nodule with scan
parameters of 120 kVp, 200 mA, 1 mm/sec table speed, a rotation speed of 1
sec, and a pitch of 1. High-resolution CT images were reconstructed at 0.5-mm
intervals with a high-spatial-frequency algorithm (bone algorithm). Images
were hard-copied using the lung (level, -700 H; width, 1000 H) and mediastinal
(level, 35 H; width, 250 H) window settings. We also used another window
setting (level, -550 H; width, 1500 H) to adequately reveal the internal
structures of the nodule, particularly of homogeneous nodules with soft-tissue
density.
The CT values of each tumor were measured inside the region of the interest, which was defined on the cathode-ray tube monitor by manual tracing just along the interior edge of the tumor. CT values of type III tumors were measured separately for the ground-glass attenuation and the central high-density zone; two areas of entire tumor or ground-glass attenuation were defined by manual tracing using a light pen. We calculated the percentage of the tumor area occupied by ground-glass attenuation.
Standard chest radiographs (14 x 17 or 14 x 14 inches [35.5 x 43.2 or 35.5 x 35.5 cm]) were obtained with a KXO 8OG unit (Toshiba, Tokyo, Japan). The exposure settings were 135 kVp, 14:1 grid ratio, and 180-cm focus-film distance, with a compensatory filter to provide adequate film blackening in the mediastinal and diaphragmatic areas. A rare earth film-screen combination of a standard system speed (speed 250) and a standard contrast was used.
Review of Images
Two radiologists who were unaware of the pathologic diagnosis independently
reviewed all contiguous high-resolution CT scans of the entire nodule on
hard-copy images and recorded morphologic characteristics of the nodules,
including their location, size, margin, and internal structure, and the
presence or absence of convergence toward the tumor of surrounding pulmonary
vessels. The observers independently classified each case of 59 cancers into
one of four high-resolution CT morphologic patterns on the basis of the
density distribution and visibility of vessels in the tumor. These nodule
patterns were pure ground-glass attenuation, heterogeneous low attenuation,
ground-glass attenuation in the periphery and a high-density central zone, and
homogeneous soft-tissue density. Discrepancies in interpretation between
radiologists were resolved by consensus.
To evaluate the visibility of the tumor on the basis of high-resolution CT patterns, two radiologists independently examined 59 tumors on chest radiographs that were placed on a standard viewbox in a darkened room. Observers were asked to detect and locate nodular opacities in the lung parenchyma using four levels of confidence: level 1, no nodule present; level 2, nodule present with 50% certainty; level 3, nodule probably present; and level 4, nodule certainly present. Discrepancies in interpretation between the observers were resolved by a third radiologist. When a lung field was given a confidence level rating of 2, 3, or 4 (indicating the presence of a nodule) that was in agreement with the CT finding of tumor, the interpretation was designated true-positive (visible tumor). When a confidence level of 1 was assigned to a lung field without a cancerous nodule but a tumor was identified on CT images, the interpretation was designated false-negative (invisible tumor) [9].
Histopathologic Study
All surgical specimens were fixed in the inflated state by the
transbronchial injection of formalin liquid and were sectioned transversely at
approximately 10-mm intervals in nearly the same transverse plane as the CT
scan. All sections were stained with H and E and the elastica—van Gieson
stain and were then examined by light microscopy. The following parameters
were examined in each tumor: tumor margin, tumor growth type, alveolar
collapse, interstitial components, elastic fibers, and histologic cell type.
On the basis of the tumor growth patterns described by Noguchi et al.
[11], 59 small adenocarcinomas
were independently classified by three pathologists as localized
bronchioloalveolar carcinoma (type A, n = 17), localized
bronchioloalveolar carcinoma with foci of collapse of alveolar structure (type
B, n = 14), localized bronchioloalveolar carcinoma with foci of
active fibroblastic proliferation (type C, n = 24), poorly
differentiated adenocarcinoma (type D, n = 4), tubular adenocarcinoma
(type E, n = 0), or papillary adenocarcinoma with compressive and
destructive growth (type F, n = 0). Discrepancies in interpretation
among the pathologists were resolved by consensus.
To correlate the CT value of the tumor and retained air space in the tumor, we measured the area of retained air space in the central and peripheral zones of the tumors on a representative microscopic field of each H and E—stained section (magnification factor, 4) using a digital planimeter (Planix 7; Tamaya, Tokyo, Japan). In addition, we evaluated the amount and framework of elastic fibers on elastica van Gieson—stained sections and graded the amount of fibers as follows: grade 1, normal; grade 2, one to a few layers of thick wavy elastic fibers; and grade 3, crowded or multiple layers of thick wavy (tortuous) elastic fibers. We also classified the framework of the elastic fibers as being the preserved or the disrupted form.
Radiologic—Histopathologic Correlation
High-resolution CT morphologic features of the tumor based on the internal
density distribution were correlated with the tumor growth patterns based on
histopathologic findings.
Statistical Analysis
One-way analysis of variance followed by the Bonferroni method of multiple
comparisons was used to compare the mean size, CT values, percentage of
ground-glass attenuation, and percentage of retained air space in different
tumor growth patterns. The correlation between CT values and retained air
space was examined using Pearson's correlation. A p value of less
than 0.05 was considered statistically significant. Statistical analyses were
performed using Statistical Package for the Social Sciences software, version
6.1 (SPSS, Chicago, IL).
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High-Resolution CT Characteristics of Lung Tumors
Eighteen (31%) of 59 adenocarcinomas appeared as nodules of pure
ground-glass attenuation (type I) (Fig.
1A,1B,1C,1D).
The tumor margin was round or slightly lobulated, with spicules in three
tumors, a pleural tag in four, and an air bronchiologram in five. The tumor
size ranged from 6 to 18 mm (mean, 10.7 mm) in diameter. The averaged CT value
of the 18 tumors was -590 H.
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Fifteen (25%) of 59 tumors appeared as heterogeneous low-attenuation nodules (type II) (Fig. 2A,2B,2C,2D,2E). Spicules were noted in 13 tumors, a pleural tag in five, and an air bronchiologram in 10. Tumor size ranged from 6 to 18 mm (mean, 11.3 mm) in diameter. The average CT value of the 15 tumors was -360 H.
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Ten (17%) of 59 tumors appeared as nodules with ground-glass attenuation in the periphery and a central high-density zone (type III). Six (60%) of the 10 tumors showed convergence of bronchovascular structures from the surrounding lung parenchyma (Fig. 3A,3B,3C,3D,3E). The tumor margin was lobulated, with spicules in seven tumors, a pleural tag in four, and an air bronchiologram in nine. Tumor size ranged from 10 to 19 mm (mean, 15.2 mm) in diameter. The average CT value of the 10 tumors was -440 H, with -610 H for the ground-glass attenuation in peripheral zone and -150 H for the high density in the central zone.
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Sixteen (27%) of 59 tumors appeared as homogeneous nodules of soft-tissue density (type IV) (Fig. 4A,4B,4C,4D). The tumor margin was lobulated, with spicules in 15 tumors, a pleural tag in seven, and an air bronchiologram in seven. Tumor size ranged from 8 to 20 mm (mean, 14.5 mm) in diameter. The average CT value of the 16 tumors was 10 H.
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Histopathologic Findings
Type I histologic specimens showed tumor cells lining the alveolar walls
and replacing the preexisting alveolar epithelium (lepidic growth), whereas
the small vessels within the nodule were surrounded by aerated alveoli
(Fig. 1C). The average retained
air space area in the tumor was approximately 50% of the tumor area. The
framework of elastic fibers was a preserved form with the amount classified as
grade 1 or 2 (Table 1). This
type was seen in 18 well-differentiated adenocarcinomas.
Type II histologic specimens showed tumor cells lining the moderately thickened alveolar walls and accompanied by scattered foci of collapsed alveoli (Fig. 2C). The collapsed alveoli showed a prominent distribution in the vicinity of the vessels in the tumor. Small airways in the tumor showed retraction bronchiolectasis. The average retained air space area in the tumor was approximately 32% of the tumor area. Elastic fibers in the preserved framework in the area of the collapsed alveoli were crowded; the pattern was classified as grade 3 (Fig. 2D and Table 1). This type was seen in 15 well-differentiated adenocarcinomas.
Type III histologic specimens showed collapsed or collagenous alveoli, crowded pulmonary vessels, disrupted elastic fibers, and a variable amount of anthracotic foci in the central zone of the tumor (Figs. 3C and 3D). The average area of the retained air space was approximately 6% of the central zone. Tumor cells in the alveolar lining were noted in the peripheral zone of the tumor. Furthermore, deformation of the alveoli was also noted, which was probably caused by the contraction process of central desmoplastic response (Fig. 3C). The average area of the retained air space was approximately 51% of the peripheral zone of the tumor area, with the amount of elastic fibers in the alveolar walls classified as grade 2 (Table 1). This type was seen in 10 well-differentiated adenocarcinomas.
Type IV histologic specimens showed a solid mass with distinct margins. Tumor cells were scattered within the tumor, with accompanying stromal invasion (Fig. 4C). Little retained air space was seen within the tumor. The framework of elastic fibers was the disrupted form with scattered distribution and with the amount classified as grade 1, 2, or 3 (Table 1). This type was seen in six well-differentiated adenocarcinomas and in all five moderately differentiated and all five poorly differentiated adenocarcinomas.
High-Resolution CT-Histopathologic Correlation
The pure ground-glass attenuation of type I corresponded to the growth of
tumor cells in the alveolar lining. The small vessels in the tumor, visible on
high-resolution CT images, were surrounded by aerated alveoli (Figs.
1B and
1C).
The heterogeneous low attenuation of type II nodules was the result of the combined effect of uneven tumor cell growth, thickened alveolar walls, and scattered foci of collapsed alveoli that were caused by increased elastic fibers (Fig. 2D). Small vessels in the tumor, invisible on high-resolution CT images, were probably silhouetted by the surrounding collapsed alveoli (Figs. 2B and 2C).
The high-density central zone of type III was attributed to the combined effect of collapsed alveoli, fibroblast proliferation, increased amount of elastic fibers, and central fibrosis with a variable degree of anthracosis. The contraction process (desmoplastic response) in the tumor probably caused the irregularly shaped high-density central zone and the convergence of bronchovascular structures from the surrounding lung parenchyma. The ground-glass attenuation in the peripheral zone corresponded to the growth of tumor cells in the alveolar lining (Figs. 3B and 3C).
The homogeneous soft-tissue density of type IV corresponded to solid tumor growth, with little retained air space (Figs. 4B and 4C).
Correlation Between High-Resolution CT Patterns and Subtypes of Small
Adenocarcinoma
Sixteen (94%) of 17 type A (Noguchi's classification
[11]) adenocarcinomas were
classified as nodules having pure ground-glass attenuation (high-resolution CT
type I). Ten (71%) of 14 type B tumors appeared as heterogeneous
low-attenuation nodules (type II). Seven (29%) of 24 type C tumors appeared as
nodules with ground-glass attenuation in the periphery and a high-density
central zone (type III), and 12 (50%) of 24 type C tumors appeared as
homogeneous nodules of soft-tissue density (type IV). All (100%) of four type
D tumors were type IV.
Tumor Characteristics According to Subtypes of Small
Adenocarcinoma
The size of type A or type B was smaller than that of type C (p
< 0.001 and p = 0.046, respectively), supporting the opinion of
Noguchi et al. [11] that
"type C appeared as an advanced stage of type A and type B,"
whereas the CT values of types A and B were lower than those of types C and D
(all, p < 0.001), indicating a progressive increase in density as
the tumor changed from type A, B, or C to type D. Furthermore, the
ground-glass attenuation of the tumor area for type A or type B was larger
than that for type C or type D (all, p < 0.001), and the
ground-glass attenuation of tumor area of type C was larger than that of type
D (p < 0.05, Table
3).
Analysis of the retained air space of tumors based on their histologic subtype showed larger retained air space for type A or type B than for type C or type D, and for type C than for type D (Table 3).
The tumor density showed a negative correlation with the retained air space in the tumor (r = -0.87, p < 0.001) (Fig. 5).
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Visibility of Tumors on Chest Radiographs According to
High-Resolution CT Pattern
Fourteen visible tumors on chest radiographs consisted of three type II
(Fig. 2E), three type III, and
eight type IV. On the other hand, 45 tumors that were invisible on chest
radiographs comprised nodules of all four high-resolution CT patterns (Figs.
1D,
3E, and
4D). Specifically, type IV was
the most easily detectable on chest radiographs, and type I was the least
detectable (Table 4).
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The results of our study further confirmed our original hypothesis that
high-resolution CT features of small peripheral lung adenocarcinoma correlate
well with histopathologic patterns
[13]. In addition, we found a
good correlation between CT patterns and tumor growth patterns described by
Noguchi et al. [11]. In 1995,
Noguchi et al. classified small peripheral adenocarcinomas of the lung (20
mm) into six types (A—F) on the basis of tumor growth patterns. Types A,
B, and C represented alveolar lining (i.e., lepidic) tumor growth (replacement
tumor growth), and types D, E, and F were nonreplacement, solid (i.e., hilic)
tumor growth [14]. Our study
of the correlation between high-resolution CT patterns and histopathologic
subtypes indicated that type A appeared as nodules of pure ground-glass
attenuation (type I). Most type B lesions appeared as heterogeneous
low-attenuation nodules (type II), but some appeared as nodules with
ground-glass attenuation in the periphery and a high-density central zone
(type III). Type C lesions appeared as either type III or homogeneous nodules
of soft-tissue density (type IV), and type D appeared as type IV.
The desmoplastic response (central scar tissue) is important in adenocarcinoma of the lung because it is often associated with a poor prognosis [23,24,25]. In this study, 17% of small adenocarcinomas showed a central scar. Furthermore, tissue contraction, which is usually associated with desmoplastic response in the central zone of a tumor, appeared to cause an irregularly shaped high-density central zone and convergence of bronchovascular structures from the surrounding lung parenchyma toward the tumor.
Noguchi et al. [11] reported that types A and B showed no lymph node metastasis and had an excellent prognosis (5-year survival rate, 100%). Conversely, type C was occasionally associated with lymph node metastasis and a poor prognosis. The prognosis of nonreplacement-type adenocarcinoma (types D—F) was worse than that of replacement-type adenocarcinoma. Comparison of our data with those of Noguchi et al. indicates that types I and II, mainly seen in types A and B, respectively, may indicate a favorable prognosis; whereas type III, mainly seen in type C, may indicate a poor prognosis. Furthermore, type IV, which usually corresponds to part of type C and type D, may be associated with the poorest prognosis.
Elastic fibers form the basic microstructure of the lung interstitium. We found a variable framework pattern of elastic fibers in each of the four high-resolution CT patterns. Types I and II had a preserved framework of elastic fibers, whereas types III and IV often exhibited a disrupted framework of elastic fibers. Eto et al. [25] considered tumors with preserved elastotic framework of the stroma to be in situ peripheral lung adenocarcinomas. As the tumor grew, the elastotic framework tended to be disrupted, which was associated with a high recurrence rate. On the basis of the study by Eto et al., types I and II, with a preserved framework of elastic fibers, may be associated with a favorable prognosis, whereas types III and IV, with a disrupted framework of elastic fibers, may suggest a poor prognosis.
Ground-glass opacity, which is defined as hazy increased attenuation of the lung with bronchial and vascular structures in the lesion seen on CT scans, could represent inflammatory to malignant entities [26]. Jang et al. [15] considered focal areas of ground-glass attenuation on thin-section CT to be an early sign of localized bronchioloalveolar carcinoma. Furthermore, Kuriyama et al. [16] reported that the percentage of ground-glass opacity on CT could help differentiate small localized bronchioloalveolar carcinoma (types A and B) from small adenocarcinoma with (type C) or without (types D—F) a replacement growth pattern. In our study, the percentage of ground-glass attenuation was higher in type A (92%) and type B (52%) than in type C (20%) or type D (0%), indicating ground-glass attenuation was also useful in differentiating subtypes of small adenocarcinomas.
In this study, we compared tumor size, CT values, and retained air space according to subtypes of small adenocarcinomas. The diameters and CT values of type C tumors were larger than those of type A or type B, which lend support to the theory that type C appears to be an advanced stage of types A and B [11]. The retained air space of tumor decreased from type A to types B, C, and D in decreasing order because of increased tumor tissue component and thickening of the alveolar septa. Tumor CT values inversely correlated with retained air space in the tumor. The variable degree of alveolar aeration within a tumor with replacement growth yielded low density, which can explain why CT-detected small adenocarcinomas had surprisingly low (negative) CT values. In contrast, nonreplacement tumor growth, showing the solid tumor growth with little air space, yielded higher density.
Kuriyama et al. [27] reported that the presence of an air bronchogram or air bronchiologram in a lung nodule was a useful finding for differentiating adenocarcinoma from benign lesions. They showed that 72% of small peripheral adenocarcinomas had an air bronchogram, compared with only one (5%) of 20 benign nodules. In our study, air bronchograms were noted in 31 (56%) of 55 tumors of types A—C, but in none of type D, indicating that the air bronchogram appears predominantly in tumors with a replacement growth pattern.
As shown in our study, the visibility of various high-resolution CT patterns varied on chest radiographs. Nodules of ground-glass attenuation could not be detected. Histopathologically, small adenocarcinomas with types A and B tumors appeared as low-density nodules and were difficult to detect on chest radiographs, whereas the density of type D tumors was that of a homogeneous nodule of soft-tissue density, and these tumors were easier to identify. Almost half (53%) of adenocarcinomas in our study were types A and B, which was a greater percentage than in previous two studies (17% and 34%) [12, 16]. This difference is likely a result of the high proportion of small low-density adenocarcinomas, invisible on chest radiographs but visualized on low-dose helical CT, that were included in our series.
In conclusion, we showed that high-resolution CT morphologic features of CT-detected small peripheral lung adenocarcinomas are of four patterns that correlate well with histologic findings of different tumor growth patterns.
Acknowledgments
We thank Takeshi Yamanda from the Department of Surgery and Keishi Kubo
from the Department of Internal Medicine for their collaboration in our study.
We also thank Kazuhisa Hanamura and Kazuhiro Asakura from the
Telecommunications Advancement Organization of Japan Matsumoto Research Center
for their technical support.
This study was performed as a research program at the Matsumoto Research Center of the Transmission Advancement Organization of Japan (from 1996 to 1999).
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= type A adenocarcinoma, 
= type B
adenocarcinoma, 
= type C adenocarcinoma, and 
= type D
adenocarcinoma using the classification of Noguchi et al.
[