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1 Department of Radiology, Shinshu University School of Medicine, 3-1-1 Asahi,
Matsumoto 390-8621, Japan.
2 Department of Radiology, JA Azumi General Hospital, 3207-1, Ikeda, Nagano
399-8695, Japan.
Received June 3, 2002;
accepted after revision September 26, 2002.
Address correspondence to S. Takashima.
Abstract
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MATERIALS AND METHODS. We reviewed thin-section CT findings on the initial diagnostic CT (lesion size; percentages of ground-glass-opacity areas of lesion; and presence or absence of lobulation, spiculation, air bronchogram, cavity, satellite lesions, pleural tag, concave margins, polygonal shape, and peripheral subpleural lesion) in 80 pulmonary nodules (36 malignancies and 44 benign lesions) of 80 patients. We evaluated changes in size (regression, no change, or growth) on the first follow-up CT performed 42-120 days (mean, 93 days) after the initial CT.
RESULTS. The greatest accuracy (81%) with 89% sensitivity and 75% specificity for determining malignancy was attained with a combined criterion of growth of lesions or predominantly ground-glass-opacity lesions. Of all criteria that were specific to malignancy, the greatest sensitivity (50%) was achieved with a combination of growth or no change in size of lesions and predominantly ground-glass opacity and no concave margins. Of all criteria that were specific to benign lesions, the greatest sensitivity (45%) was attained with a combination of lesion regression or polygonal shape.
CONCLUSION. Follow-up CT findings were useful, and a combination of findings on initial CT and follow-up CT was optimal for differentiating benign and malignant pulmonary nodules.
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Although many articles have reported promising results for the detection of lung cancer at early stages with screening CT, few articles have discussed how to manage non-calcified solitary pulmonary nodules discovered with screening CT [1, 2, 3, 4, 5, 6]. Benign lesions grow very rapidly or very slowly, whereas malignant tumors grow at intermediate rates, depending on the histology of tumor [11, 12, 13]. Thus, radiologic follow-up is usually performed for those solitary pulmonary nodules if it is thought that the gain will outweigh the risk. In this series, we retrospectively assessed the role of the first follow-up CT for differentiation of benign and malignant lesions in indeterminate solitary pulmonary nodules detected at a population-based screening CT for lung cancer.
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Diagnostic CT was recommended for 477 individuals (3.5%), of whom 458 (96%) underwent the procedure. We compared the size of lesion on hard-copy images obtained at low-dose CT and the initial diagnostic 1-cm thick-section CT. During this trial, we used arbitrary size criteria as follows: regression was defined when lesions showed more than a 2-mm decrease in maximum or perpendicular diameters or both; growth was defined when lesions showed more than a 2-mm increase in either or both diameters; changes ranging from -2 to 2 mm were regarded as no change. Of the 458 patients, 219 (48%) were diagnosed as having benign lesions because the lesions showed regression (12%) or disappearance (69%) or had benign calcification (16%) or fat (3%) at initial diagnostic CT [7, 9].
Of the remaining 239 patients, a final diagnosis was obtained in 135 patients (lung cancer, 73; atypical adenomatous hyperplasia, nine; and benign lesions, 53 [10 by surgical resection and 43 by no interim growth for 2 years or more on follow-up diagnostic CT]). The final diagnosis was not obtained in the other 104 patients because they had insufficient follow-up intervals (<2 years) with diagnostic CT regardless of having nodules thought to be benign on diagnostic CT (n = 94), or because they were lost to follow-up or refused to have surgery (n = 10). All 94 patients with insufficient follow-up intervals had at least one follow-up diagnostic CT. Diagnostic high-resolution CT revealed solid pulmonary nodules without coarse spiculation or lobulation that showed no change in lesion size on the follow-up diagnostic CT in all 94 patients.
On the basis of the first diagnostic CT findings, we recommended biopsy procedures (transbronchial bronchoscopic aspiration, CT-guided percutaneous transthoracic biopsy, or surgical biopsy) for pulmonary nodules larger than 1 cm that showed no interim regression and that had coarse spiculation or ground-glass-opacity components. We recommended follow-up diagnostic CT for the other pulmonary nodules. The final decision as to whether nodules should undergo biopsy or follow-up diagnostic CT depended on the patient's willingness. Of the 135 patients in whom the final diagnosis was obtained, 80 patients had the first follow-up diagnostic CT within 4 months (mean interval, 93 days; range, 42-120 days) from the initial diagnostic CT because the diagnosis at the initial CT was indeterminate for those lesions. The other 55 patients were excluded from this series; 47 patients (42 with lung cancer, four with atypical adenomatous hyperplasia, and one with cryptococcoma) underwent surgical excision without follow-up diagnostic CT; eight patients with clinically benign lesions underwent repeated annual CT followed by diagnostic CT. No individuals were treated with antibiotics before the first diagnostic CT or before the first follow-up CT.
We selected those 80 patients with 80 indeterminate solitary pulmonary nodules for the study to assess the role of the first follow-up CT for differentiation between benign and malignant lesions. We treated atypical adenomatous hyperplasia as malignancy in our series. This retrospective study consisted of 36 malignancies and 44 benign lesions in 80 patients, including 43 men and 37 women with a mean age of 65 years (range, 40-80 years). Of the 44 benign lesions, 35 were diagnosed as benign because of no interim growth on repeated high-resolution CT performed more than 2 years after the first high-resolution CT. Pathologic diagnosis through surgical resection was obtained for all 36 malignant tumors and the remaining nine benign lesions (Table 1).
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Diagnostic CT was performed on a HiSpeed Advantage CT scanner (General Electric Medical Systems, Milwaukee, WI). First, conventional CT scans were obtained through the chest with contiguous 10-mm-thick sections during breath-holding at mid inspiration. The technical parameters were 120 kVp, 200 mA, 1-sec scanning time, 10-mm collimation, a 30-cm field of view, and a 512 x 512 matrix (pixel size, 0.6 mm). An additional 1-mm collimation sequence was performed through the lesion with scanning 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, with a 20-cm field of view and a 512 x 512 matrix (pixel size, 0.4 mm). The images were photographed using a window level of -550 H and a window width of 1500 H for lung window settings and a level of 35 H and width of 250 H for mediastinal window settings.
Without knowledge of histologic diagnoses, two radiologists independently evaluated the findings on the initial high-resolution CT such as presence or absence of lobulation, coarse spiculation, air bronchogram, cavity, satellite lesions, pleural tag, concave margins, polygonal shape, and peripheral subpleural lesion. Next, the changes in size (regression, no change, or growth) were assessed by comparing one half of the sum of the maximum and perpendicular diameters of the lesion (i.e., the mean diameter) in the transverse section of the initial and first follow-up high-resolution CT images (Fig. 1). The measurement was made in a transverse section in which the greatest diameter of the lesion was included. The perpendicular diameter of the lesion was defined as the sum of line segments drawn perpendicular to the maximum transverse diameter that reached the edges of the nodule that were furthest from the line segment corresponding to the maximum transverse diameter. In this study, we did not assess longitudinal diameters, because scanning of entire lesions with thin-section CT was incomplete in some patients with pulmonary nodules larger than 1.5 cm.
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On high-resolution CT, regression was defined when lesions showed a decrease of 0.5 mm (0.3 mm in mean diameter) or more in the maximum or perpendicular diameter or both; growth was defined when lesions showed an increase of 0.5 mm or more in the maximum or perpendicular diameter or both. This threshold (0.5 mm) for changes in size was adopted because this value exceeded one pixel size (0.4 mm) of high-resolution CT and the value was a minimal unit of the mechanical calipers used for measurement. Satellite lesions were defined as one or more distinctly separate nodular areas of high attenuation located in the same subsegment as the dominant lesion. Concave margins were defined when a part of the lesion surface except the portions in contact with the pleura showed concave or straightened configuration. Polygonal shape was defined when the entire lesion surface was surrounded by concave margins only. Interobserver agreement for the 10 high-resolution CT findings was measured using the kappa statistic. When interpretations differed, a third radiologist reviewed the cases, and a majority opinion became the final decision.
The same two radiologists independently measured the maximum transverse diameter of the lesion (lesion size) and the percentage of ground-glass-opacity areas in the entire lesion as reported in the literature [14]. A predominantly solid lesion was defined as a lesion of ground-glass opacity of less than 50%, whereas a predominantly ground-glass-opacity lesion was defined as a lesion of ground-glass opacity greater than or equal to 50%. All assessments of CT images were performed on hard-copy images. Measurements were made using mechanical calipers in 0.5-mm increments. Intraclass correlation was used to assess interobserver agreement in the measurement of lesion size and the percentage of areas of ground-glass opacity [15]. The averaged values of the measurement of lesion size, the percentage of ground-glass opacity, and the increase in mean diameter obtained by the two observers were used for analysis in this study. As shown in Figure 1, the volume doubling times were calculated using the method described by Schwartz [16].
We compared all high-resolution CT findings between benign and malignant lesions. We assessed diagnostic statistics for one or every combination of statistically significant high-resolution CT features with and without features at the first follow-up CT and proposed an optimal criterion for benign or malignant lesions. Unpaired t tests were used to compare lesion size. Fisher's exact tests were used to compare the prevalence of high-resolution CT findings. A p value of less than 0.05 was considered statistically significant. All statistical calculations were performed with Statistical Package for the Social Sciences software (SPSS, Chicago, IL).
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As shown in Table 2, a statistically significant difference between benign and malignant lesions was seen for lesion size (p = 0.014), predominantly ground-glass opacity (p < 0.001), air bronchogram (p = 0.003), concave margins (p = 0.041), and polygonal shape (p = 0.002). The prevalence of these significant CT features in each lesion category is listed in Table 1. The prevalence of concave margins and of polygonal shape was significantly greater in benign lesions than in malignant lesions. On the basis of the analysis of high-resolution CT images, concave margins were demarcated by the interlobular septa (80% of 30 lesions) or intralobular bronchioles or arteries (20%). However, this CT feature was difficult to verify in pathologic studies. Lesion size and the prevalence of predominantly ground-glass opacity and air bronchogram were significantly greater in malignant lesions than in benign lesions.
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Of 36 malignancies, 20 lesions (56%) showed growth and the other 16 lesions (44%) remained the same size (Table 1 and Figs. 2A, 2B and 3A, 3B). Of 44 benign lesions, regression was found in 12 lesions (27%), no change in size in 30 lesions (68%), and growth in two lesions (5%) (Figs. 4A, 4B, 5A, 5B, 6A, 6B). The proportion of the changes in lesion size was statistically significant (p < 0.001) between benign and malignant lesions. The increase in mean diameter (±SD) was 0.9 ± 1.0 mm (range, 0.3-3.5 mm) for 20 malignant lesions, 2 mm for inflammatory pseudotumor, and 4 mm for organizing pneumonia. The volume doubling time was 508 ± 335 days (range, 79-1435 days) for 20 malignant lesions, 215 days for inflammatory pseudotumor, and 35 days for organizing pneumonia. On the basis of the tumor histologic type, the volume doubling time was 988 ± 470 days for atypical adenomatous hyperplasia (n = 3), 567 ± 168 days for bronchioloalveolar carcinoma (n = 8), 384 ± 212 days for adenocarcinoma with bronchioloalveolar carcinoma components (n = 6), and 122 ± 68 days for squamous cell carcinoma (n = 3).
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Diagnostic Statistics for Determining Malignancy
Diagnostic statistics for determining malignant lesions are listed in
Table 3. Of the various
thresholds for lesion size, a threshold larger than or equal to 11 mm showed
the greatest accuracy, 66% (53/80). When we used a single CT feature at
initial high-resolution CT, the greatest accuracy, 73% (58/80), was obtained
with predominantly ground-glass opacity; the greatest specificity, 86%
(38/44), was attained with air bronchogram; the greatest sensitivity, 100%
(36/36), was achieved with no polygonal shape. When we used a combination of
two or more high-resolution CT findings, improved accuracy of 76% (61/80) was
obtained with a combined criterion of predominantly ground-glass opacity or a
lesion size larger than or equal to 11 mm or a combined criterion of
predominantly ground-glass opacity or air bronchogram or a combined criterion
of predominantly ground-glass opacity and no polygonal lesion. Specificity
rose to 100% (44/44) with a combined criterion of predominantly ground-glass
opacity and air bronchogram and no concave margin, but the sensitivity of that
combination was 28% (10/36).
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Using the follow-up CT findings, we found that our estimation of the growth of lesions achieved 78% accuracy (62/80) and 95% specificity (42/44). Our estimation of the growth or no change in the size of lesions showed 100% sensitivity (36/36). With the combinations of the initial and follow-up CT findings, the greatest accuracy, 81% (65/80), was attained with a combination of the growth of lesions or predominantly ground-glass opacity; of all criteria that were specific to malignant lesions, the greatest sensitivity, 50% (18/36), was achieved with a combined criterion of the growth or no change in the size of lesions and predominantly ground-glass opacity and no concave margin.
Diagnostic Statistics for Determining Benign Lesions
Diagnostic statistics for determining benign lesions, focusing on the CT
features specific to benign lesions, are listed in
Table 4. When we used a single
feature at initial high-resolution CT, 100% specificity (36/36) was attained
with polygonal shape, but its sensitivity was 23% (10/44;
Fig. 7). Combined criteria did
not improve the diagnostic statistics of the single CT features. With the
follow-up CT findings, regression of lesion showed 100% specificity (36/36)
and 27% sensitivity (12/44). With the combinations of the initial and
follow-up CT findings, a combination of lesion regression or polygonal shape
raised the sensitivity to 45% (20/44), retaining the 100% specificity
(36/36).
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The prevalence of predominantly ground-glass opacity was significantly greater in malignant lesions than in benign lesions in this study. As documented in the literature, most localized bronchioloalveolar carcinomas and all atypical adenomatous hyperplasia lesions showed a predominantly ground-glass-opacity pattern on high-resolution CT, squamous cell carcinoma exhibited a predominantly solid pattern, and adenocarcinoma with bronchioloalveolar carcinoma components showed a predominantly ground-glass-opacity or solid pattern [10, 19, 20]. Nodular fibrosis and clinically benign lesions were the only benign entities that exhibited predominantly ground-glass opacity in this series, but the proportion of these lesions that showed a predominantly ground-glass-opacity pattern was only 20% of all benign lesions. As has been reported by other authors [21, 22, 23, 24], organizing pneumonia, inflammatory pseudotumor, intrapulmonary lymph nodes, and sclerosing hemangioma exhibited a predominantly solid pattern in this series. Thus, the high proportion (67%) of bronchioloalveolar carcinomas and atypical adenomatous hyperplasia lesions among the malignant tumors and the high proportion of predominantly solid benign lesions may explain why a predominance of ground-glass opacity was a significant factor for lesion malignancy in our study.
Air bronchogram was also a significant factor for malignancy in our study. Air bronchograms are caused by patent bronchi or bronchioles in the nodule and are seen when the tumor proliferates along the alveolar walls without disrupting the lung architecture [25]. Another malignant counterpart that produces this CT finding is malignant lymphoma, but other malignant conditions rarely exhibit air bronchograms [26]. This CT feature was detected only in adenocarcinoma and atypical adenomatous hyperplasia in our study. As documented in prior series [21, 23], organizing pneumonia and inflammatory pseudotumor also showed air bronchograms in our study.
Concave margin was a significant factor for benign lesions in our study. However, localized bronchioloalveolar carcinomas, adenocarcinomas with bronchioloalveolar carcinoma components, and atypical adenomatous hyperplasia lesions often showed this CT feature, and the lesions abutted mostly on the interlobular septa. When seen in neoplasms, concave margins may suggest a lepidic growth pattern; therefore, tumor spread may be hindered by the interlobular septa or intralobular bronchioles or arteries.
Polygonal shape was specific to benign lesions in our study. All malignant nodules had at least one or more sides bulging toward the normal lung parenchyma. As verified in the pathologic studies in a case of nodular fibrosis, the polygonal shape may represent advanced scar tissue as a result of inflammatory processes. Therefore, the possibility of malignancy may be substantially low.
In a 1962 study in which the doubling time of lesions was calculated using serial chest radiography, all solitary pulmonary nodules for which the doubling time was 7 days or less or 460 days or more were benign [11]. Steele and Buell [13] reported that doubling times of primary lung cancers ranged from 30 to 490 days and that adenocarcinomas grew more slowly than did squamous cell or undifferentiated carcinomas. In our study, the doubling time ranged from 79 to 1435 days (mean, 508 days) for malignant lesions, and the doubling times of two surgically resected benign lesions (215 days and 35 days) over-lapped with those of malignant lesions. On the basis of the tumor histology, the longest mean doubling time (988 days) was seen for atypical adenomatous hyperplasia, followed by bronchioloalveolar carcinoma (567 days), adenocarcinoma with bronchioloalveolar carcinoma components (384 days), and squamous cell carcinoma (122 days).
These results for lung cancer were compatible with those in the series of Hasegawa et al. [27], who assessed doubling times using CT. We found many tumors with doubling times exceeding 490 days that would have been categorized as benign lesions in the past. These cancers consisted of bronchioloalveolar carcinoma and some proportion of adenocarcinoma with bronchioloalveolar carcinoma components, which showed predominantly ground-glass lesions on CT and were invisible on chest radiography. Thus, we think that the literature lacks information about doubling times in slowly growing cancers, because all these authors evaluated the doubling times on chest radiography [11, 13, 28].
Yankelevitz et al. [29] reported that follow-up thin-section CT obtained less than 169 days after initial CT revealed tumor growth in all nine patients with adenocarcinomas. However, most tumors in that study had a doubling time of less than 100 days. In our series, lesion growth was detected in only 56% of 36 malignant lesions (60% of atypical adenomatous hyperplasias, 42% of bronchioloalveolar carcinomas, 75% of adenocarcinomas with bronchioloalveolar carcinoma components, and 75% of squamous cell carcinomas) for a mean period of 93 days. The growth of malignant lesions was subtle, and the changes in mean diameter were only 0.9 mm (range, 0.3-3.5 mm) in our study.
In our series, we used a threshold of 0.3 mm in mean diameter for minimal lesion growth because we took the resolution of the CT scanner into consideration. The extent of lesion growth in a given time depends on the initial size and the doubling time of the lesion. Theoretically, a 10-mm spherical lesion that grows in mean diameter by 0.3 mm in 90 days has a doubling time of 842 days. We can diagnose lesion growth with CT for the same period of time if the same lesion has a doubling time of less than 842 days. However, we cannot diagnose the lesion growth with CT for the same period of time if the lesion has a doubling time of longer than 842 days. Shorter doubling times are required for the CT detection of growth in the same time in a lesion smaller than 10 mm. Tumor doubling times vary widely among individual tumors of the same histologic category [12, 27, 28]. The intervals between the serial CT scans varied in this study. Approximately 40% of malignant lesions were smaller than 10 mm and approximately 80% of malignant lesions were equal to or smaller than 15 mm in this series. Thus, a high proportion of small tumors with long doubling times and limited resolution of CT images may be the main reasons for the low detection rate of CT for the growth of malignant lesions. Computer-aided volumetric analysis may be useful for assessing the growth of lesions [30].
Our study revealed that the initial CT findings were limited for determining benign or malignant lesions and that the addition of follow-up CT findings improved diagnostic accuracy. Lesion growth did not necessarily indicate malignancy, because organizing pneumonia and inflammatory pseudotumor showed growth. However, lesion regression was specific to benign lesions. Of all criteria that were specific to malignant lesions, the greatest sensitivity, 50%, was achieved with a combined criterion of growth or no change in lesion size and predominantly ground-glass opacity and no concave margin. With this criterion, we could correctly assign surgical resection to 18 (50%) of the 36 cases with malignant tumors. A combined criterion of lesion regression or polygonal shape was specific to benign lesions and had an optimal sensitivity of 45%. Using this criterion, we could avoid unnecessary further diagnostic procedures in 20 (45%) of the 44 patients with benign lesions. Thus, on the whole, proper treatment planning was used in 38 (48%) of the 80 patients with our CT criteria applied retrospectively. We think that our CT criteria should be clinically applicable because our interobserver agreement was high.
Our study has limitations. First, this study was biased toward a high proportion of localized bronchioloalveolar carcinomas among malignant tumors. Therefore, our CT criteria may be valid only for a similar cohort but not for a high-risk group. Second, this study had a bias toward focusing on nodules that had no imaging findings specific to benign lesions on diagnostic CT. Thus, our CT criteria can be used only for indeterminate pulmonary nodules. Third, our CT criteria were limited, and 52% of lesions remained indeterminate on the basis of our criteria.
CT-guided transthoracic aspiration or needle biopsy is recommended for the diagnosis of indeterminate pulmonary nodules that are invisible on fluoroscopy [31, 32, 33]. Sensitivity for diagnosis of lung cancer ranges from 90% to 99% and specificity, from 96% to 100%. However, many authors have reported that the diagnostic sensitivity of CT-guided transthoracic aspiration or needle biopsy sharply decreases for small nodules [34, 35]. Li et al. [34] reported that sensitivity (72%) for nodules smaller than or equal to 1.5 cm was significantly (p < 0.05) worse than that (94%) for larger nodules. Recently, thoracoscopic excisional biopsy has been used for the diagnosis of small peripheral pulmonary nodules, and high values, reaching 100%, for both sensitivity and specificity are reported [35, 36]. Therefore, we recommend thoracoscopic excisional biopsy for predominantly ground-glass-opacity lesions with no concave margins that show no regression on the first follow-up CT, because this combination of CT findings invariably indicated malignancy in our series. Further diagnostic procedures should be avoided for polygonal lesions or lesions that show regression on the follow-up CT, because this combination of CT features always indicated benign lesions in this study. Further follow-up CT examinations may be justified for lesions that remain indeterminate on the first follow-up CT.
In conclusion, the addition of follow-up CT findings to the initial CT findings improved the diagnostic accuracy of the initial CT findings for determining benign or malignant pulmonary nodules, and the combined criteria were helpful in managing the cases with indeterminate pulmonary nodules detected at population-based CT screening for lung cancer.
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