British Journal of Radiology 74 (2001),32-41 © 2001 The British Institute of Radiology
Visibility of small peripheral lung cancers on chest radiographs: influence of densitometric parameters, CT values and tumour type
Z-G Yang, MD1,
S Sone, MD1,
F Li, MD1,
S Takashima, MD1,
Y Maruyama, MD1,
T Honda, MD2 and
M Hasegawa, MD1
1 Departments of Radiology
2 Laboratory Medicine, Shinshu University School of Medicine, Asahi, Matsumoto, 390 8621, Japan
Correspondence: Prof. S Sone, MD, Azumi General Hospital, Ikeda, Nagano 399-8695, Japan
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Abstract
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The purpose of this study was to determine the effects of tumour density and tumour type on the visibility of small peripheral lung cancers on chest radiographs. We retrospectively evaluated the visibility of 63 small (
20 mm) peripheral lung cancers on chest radiographs. 48 (76%) were detected in our low dose CT screening for lung cancer and 15 (24%) in routine clinical examination. Analysis was based on tumour optical contrast, gradient at the tumour margin, CT values and tumour type. There were 31 (49%) visible cancers and 32 (51%) invisible cancers on chest radiographs. Visible tumours had an optical density of 0.1–0.3 OD and a gradient of 0.03–0.11 OD mm-1. The mean size of visible tumour (14.3 mm) was larger than that of invisible tumour (11.1 mm; p<0.001). The mean CT value (-140 HU) of visible tumour was higher than that of invisible tumour (-490 HU; p<0.001). The detection rates of adenocarcinomas with lepidic growth (0% for type A, 29% for type B and 68% for type C) were less than those with hilic growth (100% for types D–F). All squamous and small cell carcinomas with hilic growth were visible on chest radiographs, but the numbers of each were small. In summary, tumour type influenced the contrast, gradient, CT values and margin of the tumour. Small adenocarcinomas with a lepidic tumour growth were less well seen on chest radiographs compared with small lung cancers with hilic tumour growth.
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Introduction
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The low cure rate of lung cancer is mainly owing to delayed diagnosis based on the poor diagnostic value of the conventional chest radiograph (CXR) in detecting small lung cancers [1–3]. Several recent studies from Japan and USA have shown that low radiation dose spiral CT (low dose CT) can greatly improve the detection of lung cancer [4–6]. Diederich et al [7] reported that pulmonary nodules were reliably detected at low dose CT with 50 mA or 25 mA. In our screening trial for lung cancer by low dose CT, many small peripheral lung cancers were found among the general population, and most of these tumours were invisible on CXRs even when the films were examined retrospectively. Specifically, we noticed that the majority of adenocarcinomas that were 20 mm were difficult to recognize on CXRs, even when they were located in well penetrated lung fields and were not concealed by the mediastinum, heart, hilum, hemidiaphragm or clavicle. Further analysis suggested that tumour growth pattern as evidenced by histopathological examination was a potentially important factor that could determine tumour visibility, although these conclusions have not appeared in recent studies [1–3, 4, 8].
In the present study, we compared densitometric parameters, CT values and histopathological features of 63 small peripheral lung cancers that were visible or invisible on CXRs. The aim of the study was to determine the effects of tumour density and histopathological tumour type on the visibility of small peripheral lung cancer on CXRs and to define the relationships between optical contrast, gradient at the tumour margin, CT values and histopathological tumour type.
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Materials and methods
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Patients
The subjects in this study consisted of twogroups of patients. The first group were consecutive patients identified in our screening trial for lung cancer using low dose CT, which was performed for a general population in a rural area of Japan, and comprised 47 patients with 48 small (20 mm in diameter) peripheral lung cancers. The second group consisted of 15 consecutive clinical cases of small peripheral lung cancers measuring 20 mm treated surgically at our hospital. All tumours in the second group were detected on initial CXRs taken during routine clinical examination.
CT screening group
Between May 1996 and December 1998 we conducted a population-based mass screening trial for lung cancer using a low dose CT scanner (model CT W950SR; Hitachi Medical, Tokyo, Japan). Details of the trial have been described previously [5, 9]. In brief, scanning parameters were set at 10 mm collimation, 10 mm s-1 table speed, 120 kVp, 50 mA (in 1996) or 25 mA (in 1997 and 1998), and 2 s per rotation of the X-ray tube. The reconstruction interval of the CT image was 10 mm using a standard reconstruction algorithm with 180° linear interpolation. We interpreted CT images on two high resolution cathode ray tube (CRT) monitors (2300x1700 lines). Each CT examination was first read by one of five radiologists, three with more than 10 years experience and two with more than 5 years experience in this field, to evaluate the presence or absence of any abnormality and to clarify tentatively the abnormality into one of five categories. One radiologist, a specialist in thoracic radiology, re-evaluated the CT images of the abnormality. When any abnormality in the lung was suggestive of a probable or possible lung cancer, we performed further diagnostic work-ups, including chest radiography and diagnostic CT (including thin section CT) scan.
In this trial we identified 70 patients with 71 surgically confirmed lung cancers 20 mm in diameter. Among these, 48 lung cancers in 47 patients were located in well penetrated lung fields on CXRs. These fields were not concealed by the mediastinum, heart, hilum, hemidiaphragm or clavicle when the location of tumour shown on CT images was used as reference. These cases comprised the subjects of the present study. The remaining 23 patients were excluded from further analysis: five patients did not undergo work-up examinations at our hospital and thin section CT images were not available for review; and 18 patients had tumours concealed by the mediastinum, heart, hilum or hemidiaphragm (n=15) or by the clavicle (n=3), and were not visible on CXRs, regardless of tumour density and histopathological tumour type.
Clinical group
To compare the image features of small lung cancers detected in the CT screening trial with those cancers detected in clinical work, we studied 15 small peripheral lung cancers located in well penetrated lung fields on CXRs. All of these cases were detected on initial CXRs taken during routine clinical examination, and were diagnosed and treated at our hospital within the period of the CT screening trial (May 1996 to December 1998).
Final study group
The present series included 62 patients with 63 small peripheral lung cancers of 20 mm in diameter. It consisted of 29 males and 33 females, ranging in age from 33–76 years (mean 65.6 years). The size of each of the lung cancers was 10 mm in diameter (n=22), 11–15 mm (n=27) and 16–20 mm (n=14). 20 tumours were located in the upper lobe, 9 in the middle lobe and 12 in the lower lobe of the right lung, while 11 tumours were located in the upper lobe and 11 in the lower lobe of the left lung. Histological diagnosis waswell differentiated adenocarcinoma (n=50), moderately differentiated adenocarcinoma (n=7), poorly differentiated adenocarcinoma (n=2), squamous cell carcinoma (SCC) (n=3) and small cell lung carcinoma (SCLC) (n=1).
Chest radiography and thin section CT techniques
Chest radiography and CT examinations (including thin section CT) were performed in all patients. Standard posteroanterior (14x17 inch) and lateral (14x14 inch) CXRs were obtained with a radiographic system (KXO 80G Toshiba Co., Tokyo, Japan). The technical parameters for chest radiography were: 135 kVp, 14:1 grid ratio and 180 cm focus-to-film distance, with a compensatory filter to provide an adequate film blackening in mediastinal and diaphragmatic areas. A rare earth film–screen combination (screen, XGS; film, ES-G; Konica, Tokyo, Japan) of a standard system speed (speed 250) and contrast was employed. Non-enhanced CT (including thin section CT) for all patients was performed with a state-of-the-art CT scanner (HiSpeed Advantage, GE Medical Systems, Milwaukee, WI). Non-enhanced CT scans were taken from the lung apex to the base at end inspiration, with technical parameters of 120 kVp, 200 mA, 1 s scanning time, 10 mm collimation, 10 mm s-1 table speed and 32 cm field of view. Additional thin section CT scans were taken through the nodule, with technical scan parameters of 120 kVp, 200 mA, 1 mm collimation, 1 mm s-1 table speed, 1 s per rotation, pitch 1, reconstruction interval of 0.5 mm by employing a bone algorithm, and field of view of 20 cm.
Image interpretation
The CXRs of 62 patients with 63 small lung cancers, together with the CXRs of 58 control patients who had demonstrated no lung lesion on CT images were evaluated independently by two chest radiologists (Z-GY, FL) who were not told of the presence or absence of any lesion on CXRs. Interpretation was conducted while the radiograph was placed on a standard view box in a dim lit room, without controlling the viewing distance. Observers were asked to detect and to locate nodular opacities in the lung parenchyma, using four confidence levels: (1) no lesion present; (2) nodule present with 50% certainty; (3) nodule probably present; and (4) nodule certainly present. Discrepancies in interpretation between observers were resolved by a third radiologist (SS). When a radiologist rated a lung field at a confidence level of 2, 3 or 4 to indicate nodule presence, and this was evidenced by CT finding of tumour, the interpretation was classified as true-positive (visible tumour). With a confidence level rating of 1 (a lung field without a cancerous nodule), but a tumour visible on CT images, the interpretation was designated as false-negative (invisible tumour). Regarding the border of visible tumour on CXRs, we considered it as distinct when the tumour contour could be convincingly identified, and as indistinct when it was difficult to recognize a continuous boundary between the tumour and the surrounding lung.
Measured parameters
31 visible tumours on the posteroanterior CXRs were scanned using a densitometer (Sakura PDM5, Konica, Tokyo, Japan) set at an aperture size of 1.25 mmx0.125 mm and a scanning speed of 0.25 mm s-1. The contrast of the nodule (the difference in optical density of the tumour and that of the surrounding lung parenchyma) and the density gradient across the tumour border (the rate of change of density as a function of distance through which the density changes at the nodule margin) were computed according to the method described by Revesz et al [10, 11].
For 63 tumours including visible and invisible tumours, tumour size was determined by averaging the long and short axes measured at the largest tumour diameter level, using a window width of 1000 HU and a window level of -700 HU on thin section CT images. The mean CT value of tumour shown on the thin section CT images was measured inside the region of interest (ROI) determined on the CRT by manual tracing using a light pen just along the interior edge of the tumour. The CT value of the surrounding lung parenchyma, excluding juxtatumoral pulmonary emphysema seen in one patient, was also measured using ROIs of the same size as described above. The difference in CT values (
CT) between the tumour and its surrounding lung parenchyma was then calculated.
Histopathological examination
All surgical specimens were fixed at an inflated state by transbronchial infusion of formalin. Surgical specimens were sectioned transversely at 1.0–1.5 cm distances in almost the same transverse plane as the CT scan, and stained with hematoxylin-eosin (H&E) or elastic van Gieson stain. A representative slice with the largest tumour diameter was selected for macroscopic and microscopic examination of the tumour. For each case of 63 cancers, two pathologists independently evaluated histopathological tumour type. Discrepancies in interpretation between the pathologists were resolved by consensus. Adenocarcinomas (n=59) were classified into six types according to Noguchi's classification [12]: Type A, tumour growth of the alveolar lining; type B, alveolar lining tumour growth with scattered fibrotic foci due to alveolar collapse; type C, alveolar lining tumour growth with foci of active fibroblastic proliferation; and type D–F, solid tumour growth, which showed frequent expansive tumour growth; type D indicates poorly differentiated adenocarcinoma, E, tubular adenocarcinoma, and F, papillary adenocarcinoma with compressive and destructive growth. Types A, B and C were lepidic tumour growth; whereas types D, E, F, and SCC and SCLC were hilic (solid) tumour growth [12, 13].
Statistical analysis
Data analysis was performed with the SPSS analysis program (SPSS Inc., Chicago, IL). The pooled-variance t-test was used to compare the mean values of size and CT values between visible and invisible tumours, or between the CT screening group and the clinical group, as well as the mean values of contrast and gradient between tumours with distinct and indistinct borders on CXRs. One-way analysis of variance followed by Bonferroni method of multiple comparisons was used to compare the mean values of the size, contrast, gradient and CT values among different tumour types. 
2 test of association was used to assess the significance of difference in proportion between the CT screening group and the clinical group. A statistically significant difference was considered to be present when the p-value was less than 0.05.
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Results
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We examined 63 small peripheral lung cancers located in well penetrated lung fields on CXRs. 31 (49%) were visible and 32 (51%) were invisible on CXRs. Examples of these tumours are illustrated in Figures 1–3
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Figure 1. 67-year-old male smoker with squamous cell carcinoma (16 mmx16 mm) in the apical segment of the right lower lobe, with hilic growth pattern. (a) Low dose CT shows a small nodule (arrow). (b) High resolution CT shows a homogeneous solid tissue density nodule (arrow). (c) Histopathological examination of the tumour shows hilic (solid) tumour growth (H&E stain; original magnificationx1.25). (d) Close-up view of the posteroanterior chest radiograph shows the lung nodule (arrow). (e) Optical densitometric measurement of visible tumour on the chest radiograph. The contrast and gradient values are 0.21 OD and 0.11 OD mm-1, respectively, which corresponds to the histopathological findings of hilic tumour growth.
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Figure 2. 56-year-old male smoker with a well differentiated type A adenocarcinoma (11 mmx12 mm) in the apical segment of the right lower lobe, with lepidic growth pattern. (a) Low dose CT shows a small faint lesion (arrow). (b) High resolution CT shows a ground-glass attenuation nodule through which the small vessels are visible (arrow). (c) Histopathological examination shows alveolar lining tumour growth without alveolar collapse (H&E stain; original magnificationx1.25). (d) Close-up view of the posteroanterior chest radiograph shows no evidence of the nodule in the middle zone of the right lung field.
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Figure 3. 33-year-old male non-smoker with a well differentiated type B adenocarcinoma (8 mmx9 mm) in the apical segment of the left lower lobe, with lepidic growth pattern. (a) Low dose CT shows a small, faint lesion (arrow). (b) High resolution CT shows a heterogeneous, low attenuation nodule (arrow). (c) Histopathological examination shows alveolar lining tumour growth with scattered foci of alveolar collapse (H&E stain; original magnificationx1.25). (d) Close-up view of the posteroanterior chest radiograph shows no evidence of the nodule in the middle zone of the left lung field.
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Visibility of tumours on CXRs based on tumour size, contrast, gradient, CT values and position
Table 1 shows the factors that influenced visibility of tumours on CXRs. The size of visible tumours was larger than that of invisible tumours; the minimum tumour size detected on CXRs was 9 mm. In general, tumours 10 mm in diameter were difficult to detect on CXRs, with a detection rate of only 18% (4/22). In contrast, the detection rate of tumours >10 mm was 66% (27/41) (Figure 4; p<0.001). Visible tumours had anoptical density of 0.10–0.30 OD and a gradientof 0.03–0.11 OD mm-1. The mean CT value of visible tumours was higher than that ofinvisible tumours. Furthermore, CT between the tumour and surrounding lung parenchyma was greater forvisible tumours than invisible tumours. Tumours 400 HU CT were difficult to detect on CXRs, with a detection rate of 8% (2/24), whereas tumours >400 HU CT had an improved detection rate of 74% (29/39) (Figure 4; p<0.001).
The detection rate of tumours on CXRs was 40% (8/20) for the upper lobe, 56% (5/9) for the middle lobe and 58% (7/12) for the lower lobe ofthe right lung; and 36% (4/11) for the upper lobe and 64% (7/11) for the lower lobe of the left lung.
Visibility of tumours on CXRs based on histopathological tumour type
Table 2 summarizes the visibility of 63 tumours according to histopathological type. 31 visible tumours consisted of 27 adenocarcinomas (4 of type B, 17 of type C, 6 of type D–F), 3 SCCs (Figure 1
) and 1 SCLC. On the other hand, 32 invisible tumours consisted of type A (Figure 2), type B (Figure 3) and type C adenocarcinoma. Specifically, types D–F adenocarcinoma, SCC and SCLC were the most easily detectable on CXRs, while type A was the least detectable.
Size, contrast, gradient and CT values of tumours based on histopathological tumour type
Table 3 summarizes the size, contrast, gradient and CT values of tumours according to histopathological type. The size of type A tumours was lower than type B, type C, type D–F, and SCC/SCLC (Bonferroni method of multiple comparisons, p=0.039, p<0.001, p<0.013 and p<0.015, respectively; Table 3). The contrast of type B tumours was lower than type C, type D–F, and SCC/SCLC (Bonferroni method of multiple comparisons, p=0.005, p=0.017 and p=0.017, respectively; Table 3). Analysis of the gradient of tumours based on their histopathological type showed a lower gradient for type B tumours relative to type D–F, and SCC/SCLC (Bonferroni method of multiple comparisons, p=0.013 and p=0.013, respectively; Table 3).
Regarding CT values of tumours based on their histopathological type, CT values of type A or type B tumours were lower than type C, type D–F, and SCC/SCLC, and values of type C tumours were lower than type D–F, and SCC/SCLC. Analysis of the CT of tumours based on their histopathological type showed a smaller CT for type A or type B tumours relative to type C, type D–F, and SCC/SCLC, and a smaller CT for type C tumours relative to type D–F, and SCC/SCLC (Table 3).
Border of 31 visible tumours on CXRs
The entire margin of 9 of 31 tumours was indistinct; that of 18 was partially indistinct and partially distinct; and the entire margin was distinct in 4. The mean contrast (0.21 OD) and gradient (0.08 OD mm-1) of tumours with a distinct border were higher than those (0.14 OD, 0.05 OD mm-1) of tumours with an indistinct border (p<0.001).
Characteristics of tumours detected in CT screening group vs clinical group
We also compared the characteristics of tumours detected in the CT screening group and the clinical group (Table 4). The mean CT values of tumours in the CT screening group were lower than those of the tumours in the clinical group, while the mean CT of tumours in the CT screening group was smaller than that of tumours in the clinical group. Furthermore, tumours with lepidic growth were detected more often in the CT screening group than the clinical group (Table 4).
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Discussion
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Perception of the pulmonary lesion is influenced by various factors, including the observer, lesion characteristics, and film or technical parameters. The focus of this study was to determine the effects of nodule characteristics, particularly tumour density and tumour type, on the visibility of small peripheral lung cancer on CXRs.
Our results showed that the minimum optical contrast of small visible tumours on CXRs was at least 0.1 OD. This is consistent with previous studies [14], but is different from the minimum contrast of 0.03 OD that has been cited as a threshold density for a nodule placed on a homogeneous background to be detected by a naked eye [15]. This phenomenon may be explained by the presence of complex surrounding anatomical structures, such as pulmonary vessels and/or ribs, even if the nodule is located in a well penetrated lung field on the CXR, as described previously [14, 16]. However, to our knowledge, our report is the first to describe measurement of contrast and gradient of visible tumours, as well as corresponding CT values, and compares these values with those of invisible tumours, and with histopathological tumour type.
Our data showed that the contrast of tumour nodules correlated with tumour growth pattern. Tumour growth of peripheral lung cancer has traditionally been divided into two patterns, lepidic growth and hilic growth. Lepidic growth is basically alveolar lining tumour cell growth, which maintains more or less air-filled alveolae in the tumour; while hilic growth is characteristically a solid tumour growth, which frequently enlarges, displacing the surrounding lung parenchyma [13]. Lepidic tumour growth pattern, frequently seen in adenocarcinoma, is often associated with a variable degree of alveolar aeration within the tumour, yielding a low density lesion and subsequently resulting in a low detection rate. On the other hand, hilic tumour growth pattern is associated with growth of solid nodules with little air spaces, subsequently resulting in higher contrast and a higher detection rate. In the present study, we classified adenocarcinoma according to Noguchi's classification into types A, B, C, D, E and F. Type A–C adenocarcinomas represent tumours with a lepidic growth pattern, while type D–F adenocarcinomas exhibit a hilic growth pattern [12, 13]. The retained aeration within lepidic tumours results in a faint opacity (ground-glass attenuation) nodule, and thus low contrast and a very low detection rate on CXRs. Type D–F adenocarcinomas are hilic tumours and characteristically appear as homogeneous solid, soft tissue attenuation nodules; all such tumours were detected on CXRs when located in well penetrated lung field. Our results indicated that the gradient was also influenced by tumour type. For example, type B adenocarcinomas, which showed the least degree of alveolar lining, had vague borders and lowest gradient (mean gradient 0.04 OD mm-1), whereas type D–F adenocarcinomas, which exhibited a hilic growth pattern, had distinct borders and a high gradient (mean gradient, 0.08 OD mm-1). This factor may result in a poor detection rate for low density tumours.
It is well known that tumour size is an important determinant of visibility of nodular lesions. Previous studies have shown that approximately 50% of lesions (mostly simulated nodules) of 8–10 mm in diameter were visible on CXRs [3, 16]. In our study, the detection rate of small lung cancers measuring 10 mm in diameter was only 18%, while the detection rate of those measuring 11–20 mm was 66%. The inconsistent results between our study and those of previous reports could be owing to different morphological features of the tumours in terms of density and border of the nodule. The simulated nodule that frequently showed well marginated and dense characteristics was different from the small peripheral lung cancer; the majority of the latter were often of inhomogeneous density and had an indistinct border.
According to a previous report, position of the tumour was one of the factors influencing visibility of the lesion, the upper lobe being the leading site for missed lung cancer [1]. In this study, we found a preference of the upper lobe of the right lung for lung cancer, with lower detection rates than the lower or middle lobes, indicating that the position of the tumour in the well penetrated lung field also influenced visibility of the tumour on CXRs.
In general, tumour size, contrast and gradient directly influenced the visibility of the tumour. Small lung cancers become visible on CXRs when their contrast exceeds the cut-off value of 0.10 OD. Furthermore, histopathological tumour types influenced the contrast, gradient, CT values and margin of the tumour, and their visibility varied on CXRs. Based on these findings, we propose that small tumours of the alveolar lining growth type are difficult to detect on CXRs owing to their low contrast and gradient.
This study showed that tumours detected in the CT screening group had lower CT values and smaller CT compared with tumours detected in the clinical group, and the majority of the former were invisible on CXRs. These differences were attributable to the fact that low dose CT could demonstrate small-sized, low density adenocarcinoma with lepidic growth, particularly type A adenocarcinoma, which was difficult to detect on CXRs taken during routine clinical examination or chest radiography screening for lung cancer.
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Acknowledgments
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The authors are indebted to Dr Takeshi Yamanda and Dr Masayuki Haniuda, from the Department of Surgery, and Dr Keishi Kubo, from the Department of Internal Medicine, for their collaboration in the present study. We also thank Kazuhisa Hanamura, BS, and Kazuhiro Asakura, EE, from the Telecommunications Advancement Organization of Japan Matsumoto Research Center for their technical support.
Received for publication July 7, 2000.
Accepted for publication August 31, 2000.
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Top
Abstract
Introduction
, Invisible tumour in CT screening group; 
, visible tumour in CT screening group; 
, invisible tumour in clinical group; •, visible tumour in clinical group.