Chest Radiographic Findings of Missed Lung Cancers

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1 Chin J Radiol 2004; 29: Chest Radiographic Findings of Missed Lung Cancers GIGIN LIN SHEUNG-FAT KO YUN-CHUNG CHEUNG KEE-MIN YEOW SHU-HANG NG First Division of Diagnostic Radiology, Linkou Chang Gung Memorial Hospital School of Medical Technology, Chang Gung University To assess the failure of detection of lung cancer at chest radiography. From 2002 to 2003, we collected 37 cases of lung cancer that were initially undetected but were diagnosed retrospectively at chest radiography. Of these 37 cases, 17 were adenocarcinoma, 15 were squamous cell carcinoma and the other 5 were non-small cell carcinoma. Size, locations, and patterns of the missed tumors as well as the superimposed structures at chest radiography were reviewed. Lung cancers were missed at chest radiography in 37 of 685 (5.3%) patients, of whom 28 (76%) were men and 9 (24%) were women. The median patient age was 71 years. The mean diameter of the missed cancers was 2.1cm. Most of the missed cancers (81%) were centrally located. In respects of lobar distribution of the missed lesions, 46% of the lesion was in the upper lobe, 38% in the lower lobe and 16% in the middle lobe. The majority of the missed cancers presented either as a nodular, ill-defined, or hypodense lesion. In all our 37 cases, the lesions were obscured at least in part by the superimposed structures, particularly the ribs and pulmonary vessels. Well recognition of the characteristics of missed lung cancer may help in the way of tumor detection. Key words: Diagnosis radiology, observer performance; Lung neoplasms, diagnosis; Thorax, radiology Reprint requests to: Dr. Shu-Hang Ng Department of Diagnostic Radiology, Chang Gung Memorial Hospital. No. 5, Fu Hsing Street, Kwei-Shan, Taoyuan 333, Taiwan, R.O.C. Lung cancer, one of the most insidious and aggressive neoplasms, is the most frequent fatal malignancy in Taiwan [1]. Statistics notwithstanding, it is a potentially curable disease if the cancer can be diagnosed at the early stage [2]. Upon the current medical practice, chest radiograph is still the primary imaging modality in the detection of lung cancer. However, not every lung cancer can be identified at chest radiograph at the first sight. According to the literatures, the reported rates of missed lung cancer varied from 12% to 90%, depending on study designs [3-8]. Some were designed to measure the miss rate of solitary pulmonary nodules rather than lung cancer, while other studies were planned to investigate different parameters influencing failure to detect small pulmonary lesions or to detect early lung cancer in high-risk patients. Such study in Taiwan has not been reported. The purpose of our study is to assess the failure of lung cancer detection at Chest posteroanterior (PA) radiographs in order to increase the detection rate of radiologists to the missed lung cancers. MATERIALS AND METHODS Our data were based on 685 consecutive patients with lung cancer diagnosed at our institution from July 2002 to July Missed lung cancer on chest radiographs was defined as follows: (a) evidences of pulmonary opacity that had not been described in the initial radiographic report but were confirmed by two board-certified radiologists at retrospective review of computer tomography (CT) of chest, (b) such opacity was subsequently proved to be lung cancers within 12 months interval, either by bronchoscopic lavage cytology, CT-guided biopsy, or open lung biopsy. The imaging parameters and screen-film system used in this study for chest radiographs were as follows: Philips radiography unit, kvp, 10:1 grid, a 180-cm focus-to film distance, Fuji film HB- GB, reading on view-box.

2 316 Missed lung cancers on CXR The size of each lesion was defined as the maximal diameter that was measured in millimeter on the initial radiograph, and the magnification effect on radiograph was corrected by correlation with the tracheal luminal diameter on CT. The location of each lesion was marked on a representative chest PA scheme. The lobar locations were determined with chest CT, and the left lingula was labeled as the middle lobe region. Each missed lesion on chest PA was also categorized as hilar (level of a main or lobar bronchus, including the origin of a segmental bronchus), juxtahilar (adjacent to the hilum and /or at the level of a segmental bronchus, including the origin of a subsegmental bronchus) or peripheral (any site distal to juxtahilar). The radiologic manifestations were categorized as (a) nodule or mass, (b) atelectatic pneumonitis, (c) hilar enlargement. The superimposed structures obscuring the lesions were recorded as well. The attenuation of the opacity was assessed subjectively with a three-point scale (low, moderate, and high). Moderate attenuation of opacity was defined as softtissue density comparable to that of the retro-cardial region, while low and high attenuation corresponded to those densities below and above respectively. The margins of these lesions were categorized into welldefined, partially well-defined, and ill-defined. RESULTS In our review, 37 of 685 lung cancer patients (5.3%) met these criteria. The clinical and pathological data are listed in Table 1. Twenty-eight missed lung cancers (76%) occurred in men and 9 (24%) occurred in women. Age of the patients ranged from 37 to 87 years, with the mean age of years ± (SD) and the median age of 71 years. The mean diameter of the 37 missed lung cancers on the initial chest radiographs was 2.1cm ± 0.9 (SD) (median, 2.0cm; range, cm). Nine (24%) of the 37 missed lung cancers had diameter greater than 3.0cm (4 of these lesions occurred in upper lobe, 4 in middle lobe and 1 in lower lobe), whereas 7 (19%) lesions were less than 1.2cm in diameter (3 in upper lobe and 4 in lower lobe). No obvious size differences occurred in lesions among various locations or lobes. Of these 37 cases, 17 were adenocarcinoma, 15 were squamous cell carcinoma and the other 5 were non-small cell carcinoma. At the time of tissue proof obtaining, 16 cases were at Stage I, 5 were at Stage II, and 16 were at stage III, according to the American Joint Committee on Cancer Cancer Staging Manual, sixth edition. Table 1. Clinical and Pathological Data of 37 missed lung cancers at chest radiograph Characteristics Data (%) Age (years) Range Mean ± SD ± Median 71 Sex Male 28 (76) Female 9 (24) Pathology Adenocarcinoma 17 (46) Squamous cell carcinoma 15 (40) Non-small cell carcinoma 5 (14) Table 2. Radiologic findings of 37 missed lung cancers at chest radiograph Characteristics Data (%) Size (cm) Range Mean ± SD 2.1 ± 0.9 Median 2.0 Lobar distributions Upper lobe 17 (46) Middle lobe (lingula) 6 (16) Lower lobe 14(38) Locations Hilar 17 (46) Juxtahilar 13 (35) Peripheral 7 (19) Margin Well-defined 1 (3) Partially well-defined 9 (24) Ill-defined 27 (73) Attenuation Low 23 (62) Intermediate 13 (35) High 1 (3) Patterns Nodule 25 (68) Obstructive pneumonitis 10 (27) Hilar enlargement 17 (46) Overlying structures Rib 33 (89) Pulmonary vessels 14 (38) Scapula 6 (16) Heart 5 (14) Mediastinum 4 (11) The distributions and the radiographic findings of our missed lung cancers are shown in Table 2. The lesions distributed rather evenly between the left lung and the right lung. Of these 37 lesions, 17 lesions (46%) occurred in the upper lobe, 6 (16%) in the middle lobe or lingula lobe, and 14 (38%) in the lower lobe. Lesions were predominantly centrally located, with 17 (46%) of cases occurring in the hilar region and 13 (35%) in the juxtahilar region. Only 7 (19%) cases occurred in peripheral region. All the missed lesions are marked on the representative chest radi-

3 Missed lung cancers on CXR 317 ograph scheme (Fig. 1). Regarding the radiographic features, most of the lesions were ill-defined (73%), hypodense (62%), or nodular (68%). None of our cases demonstrated pleural effusion. All the 37 missed lesions were more or less obscured by the overlying anatomic structures on chest radiograph, of which 33 lesions (89%) was obscured by ribs, 14 (38%) by pulmonary vessels, 6 (16%) by scapula, 5 (14%) by heart, 4 (11%) by mediastinum, 4 (11%) by clavicle and 1 (3%) by aortic arch. DISCUSSION Figure 1. All 37 missed lung cancers were marked on a representative chest P-A scheme. Here we could observe those lesions locating in clusters at some particular areas, such as the hila (1), retrocardia (2), and lung fields underlying the clavicle (3) and the medial (4) and inferior edge (5) of the scapula. In our series, missed lung cancers predominantly occurred in old patients with the mean age of 68. However, a rather wide range of affected age (37 to 87 years) was also noted. This age distribution showed no significant difference with that in the lung cancer reg- 2a 2b 2c Figure 2. A 53 year-old male patient had lung cancer in the left upper lobe at the hilar region, presenting as 2.5 cm-diameter mass with atelectasis that was missed at the initial chest radiograph a. This lesion (arrow) was superimposed by the adjacent rib and pulmonary vessel, and aortic arch b. Chest CT revealed the lesion (arrow) 2 months later c. Bronchoscopic lavage cytology yielded squamous cell carcinoma.

4 318 Missed lung cancers on CXR 3b 3a Figure 3. A 70 year-old male patient had lung cancer in the peripheral portion of the right lower lobe, presenting as a 0.5cm-diameter solitary pulmonary nodule that was missed at chest radiograph a. This lesion (arrow) was superimposed by the adjacent rib and the right scapula b. Follow up chest CT demonstrated the lesion (arrow) 2 weeks later c. Open lung biopsy yielded adenocarcinoma. 3c istration data in Taiwan [1]. These implied that lung cancer could be missed in various age groups of adult patients. In the series reported by Austin et al. [9], missed lung cancers occurred in disproportionately greater numbers in women with the male to female ratio of 1:2. They claimed that the radiologists might have had a lower suspicion for lung cancer in women during interpretation of chest radiography. Our study showed a different result with male to female ratio of 3:1, which was comparable to the sex distribution of the lung cancer population in Taiwan [1]. Thus, our study showed no sex bias in the failure of detecting lung cancer at chest radiograph, probably due to increasing awareness of radiologists for the growing patient number of lung cancer in women in recent years. None of our missed lung cancers was small cell carcinoma. Small cell carcinoma generally grows rapidly and has high metastatic potential. They typically present as a large hilar or juxtahilar mass with obvious mediastinal widening. Such conspicuous radiographic presentation facilitates the radiologist to identify them. Mean diameter of missed lung cancer was 2.1 cm at chest radiographs in our study, which was similar with from those in the series of Shah et al. [10] but was larger than that in the study of Austin et al. (mean diameter, 1.6cm ± 0.8) [9]. Quekel et al. [3] reported that centrally located missed lesions were larger than those peripheral lesions. In our study, however, we could not find significant size differences among lesion groups in different locations. There are three major kinds of error of radiologic detection of pulmonary nodules: search (failing to look at the abnormality), recognition (not identifying the abnormality), and decision-making (deciding to ignore the abnormality) [11]. The leading cause of detection errors is failures of recognition, followed by errors of search and errors of decision-making [12, 13]. Since our lesions located in cluster on representative chest PA scheme, whether any anatomical factors would increase difficulty in searching or recognition should be assessed. A striking preference of missed lesions for the

5 Missed lung cancers on CXR 319 4a 4b 4c upper lobes, ranging from 72% to 81%, had been reported [5, 6]. In this study, slight upper lobe preference of missed lesions (46%) was observed, which was comparable to the upper lobe to the lower lobe ratio of lung cancer for the birth-year cohort reported by Melamed et al. [14]. Thus, it seemed that lung cancers may not prone to be missed in the upper lobe in Taiwan nowadays [1]. The increased awareness of our radiologists in the upper lobe may be due to the increased recognition of preference of missed cancers in the upper lobe from previous reports [5, 6, 9, 10, 15] or the high prevalence of pulmonary tuberculosis in Taiwan. Most missed lung cancers (81%) in our study were centrally located, predominantly locating at the hilar and juxtahilar regions. Such results were in agreement with the screening program of Muhm et al. [6], which showed 65% of the missed lung cancers locating at the hilum, but were contradistinctive to Figure 4. A 61 year-old male had a 2.0 cm-diameter lung nodule in the left lower lobe at the juxtahilar region a. This lesion (arrow) was obscured by the heart and the rib b. This lesion (arrow) was shown in the follow up chest CT c. CT-guide biopsy yielded squamous cell carcinoma. those reports [2, 9, 10] which showed predominant peripheral distribution. The plausible explanation is that the centrally located lesions might be easily obscured by overlying the pulmonary vessels, heart or mediastinum. We believe that wide variability of the hilar anatomy hampers detection of subtle hilar lesions. Therefore, meticulously evaluating the hilar position, tracing the pulmonary vasculature continuity, and identifying any abnormal hilar density are mandatory to increase the detection rate. We also propose that our patient group, in comparison with those in the west countries, might generally have a lower soft tissue density in the chest wall, making the peripheral lesions easier to be detected. Regarding the radiologic patterns, we found that the lesions presenting as a nodular mass were more frequently be missed than those as hilar enlargement or obstructive pneumonitis. Almost all our missed lesions had intermediate to low density (97%), or were

6 320 Missed lung cancers on CXR ill-defined (97%). The detection probability is closely related to the unsharpness of the pulmonary lesion, and Kundel et al [11] have shown that detection rate fell from 90% in sharply bordered to 30% in illdefined bordered lesions. Austin et al [9] found that 95% of the missed lesions were ill-defined. Those lesions with such radiologic patterns may be difficult to be recognized through viewing on the view-box, so experienced radiologists used to lift the film or strengthen the penetrative light to enhance the lesion contrast. There were different opinions about the role of lateral chest radiography for lung cancer. In the study of Tala [16], lateral chest radiograph was decisive in 20% of the lung cancer patients. Some authors [5, 7, 9] stated that 3 to 4% of lung cancers could only be detected on lateral chest radiograph. However, Forrest and Sagel [17] reported that all their lung cancers were visible on chest PA radiographs. In our study, most missed lung cancers located in the central lung, which posed diagnostic difficulties on lateral radiograph. Regarding the role of CT in lung cancer detection, low-dose spiral CT had been suggested as a better screening modality than plain radiography to detect early lung cancer in patients with risk factors [18]. However, not all of the uncalcified pulmonary nodules noted on CT presenting lung cancer, and a significant portion of cases may due to benign processes, particularly in tuberculosis epidemic areas such as Taiwan. Therefore, large scale studies are needed to validate the cost-effectiveness of spiral CT in screening lung cancer in Taiwan. CONCLUSION The rate of missed lung cancer in chest radiography was 5.3%. The average size of the missed lung cancers on chest radiography was 2.1 cm and independent of the location. Most of them were centrally located, ill-defined, of intermediate to low density, or superimposed by the ribs or pulmonary vessels. Upon daily chest radiograph interpretation, special attention should be paid to avoid missing such lesions. REFERENCE 1. Lu KT, Chang DB. Lung cancer in Taiwan. The establishment of data bank for domestic medicine and its application in health policy. Formosan medical association. htm 2. Johnston MR. Curable lung cancer: how to find it and treat it. Postgrad Med 1997; 101: 3 on line 3. Quekel LGBA, Kessels AGH, Goei R, van Engelshoven JMA. Miss rate of lung cancer on the chest radiograph in clinical practice. Chest 1999; 115: Turkington PM, Kennan N, Greenstone MA. Misinterpretation of he chest x-ray as a factor in the delayed diagnosis of lung cancer. Postgrad Med J 2002; 78: Heelan RT, Flehinger BJ, Melamed MR, et al. Nonsmall cell lung cancer: result of the New York screnning program. Radiology 1984; 151: Muhm JR, Miller WE, Fontana RS, Sanderson DR, Uhlenhopp MA. Lung cancer detected during a screening program using four-month chest radiographs. Radiology 1983; 148: Forrest JV, Friedman PJ. Radiologic errors in patients with lung cancer. West J Med 1981; 134: Stitik FP, Tockman MS. Radiographic screening in the early detection of lung cancer. Radiolo Clin North Am 1978; 16: Austin JHM, Romney BM, Goldsmith LS. Missed bronchogenic carcinoma: radiologic findings in 27 patients with a potentially resectable lesion evident in retrospect. Radiology 1992; 182: Shah PK, Austin JHM, White CS, et al. Missed nonsmall cell lung cancer: radiographic findings of potentially resectable lesions evident only in retrospect. Radiology 2003; 226: Kundel HL, Nodine CF, Krupinski EA. Searching for lung nodules: visul dwell indicates locations of falsepositive and false-negative decision. Invest Radiol 1989; 24: Turkington PM, Kennan N, Greenstone MA. Misinterpretation of the chest x ray as a factor in the delayed diagnosis of lung cancer. Postgrad Med J 2002; 78: Berbaum KS, Franken EA Jr, Dorfman DD, Caldwell RT, Krupinski EA. Role of faulty decision making in the satisfaction of search effect in chest radiography. Acad Radiol 2000; 7: Melamed MR, Flehinger BJ, Zaman MB, et al. Screening for early lung cancer: results of the Memorial Sloan-Kettering study in New York. Chest 1984; 86: Sobue T, Masaki M, Misawa J, Suzuki A. CT-detection stage I lung cancer: how curable is it and is there overdiagnosis. Presented at the International Conference on Screening for Lung Cancer, Weill Medical College,Cornell University, New York, NY, October 1-3, Tala E. Carcinoma of the lung: a retrospective study with special reference to pre-diagnosis period and roentgenographic signs. Acta Radiol Diagn (Stockh) 1967; 268 (suppl): Forrest JV, Sagel SS. The lateral radiograph for early diagnosis of lung cancer. Radiology 1979; 131: Kaneko M, Eguchi K, Ohmatsu H, et al. Peripheral lung cancer: screening with low-dose spiral CT versus radiography. Radiology 1996; 201:

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