Characteristic Radiographic Features of Pulmonary Carcinoma Associated with Large Bulla

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1 Characteristic Radiographic Features of Pulmonary Carcinoma Associated with Large Bulla Masayoshi Tsutsui, M.D., Yasuo Araki, M.D., Takayuki Shirakusa, M.D., and Sadamitsu Inutsuka, M.D. ABSTRACT Primary lung cancer closely associated with a large bulla was investigated in an attempt to elucidate radiographic features of the tumor. On the basis of findings in 7 of our patients plus data on another 25 patients in the Japanese literature, we propose three major patterns of neoplasm development: nodular opacity within or adjacent to the bulla, partial or diffuse thickening of the bulla wall, and secondary signs of the bulla (changed diameter, fluid retention, and pneumothorax). As the incidence of occurrence of a pulmonary carcinoma in association with bullous disease is high, these radiographic findings will aid in early detection of a malignant lesion. The close association between pulmonary bullous disease and primary lung cancer has been emphasized [l-41. Nevertheless, the majority of patients with both diseases receive treatment when the tumor is at an advanced stage, and hence the prognosis is poor. One possible reason for this is that it is too late to accurately diagnose a concomitant cancer. Although there are a few well-documented case reports of the specific radiographic features in individual patients, there is little documentation concerning the general radiographic features suggestive of a carcinoma. We directed attention to the characteristic radiographic appearance of the neoplasm arising in a large bulla or in adjacent lung parenchyma, and report our findings here. Material and Methods A review of the records and radiographs of 443 patients with histologically proven primary lung cancer seen in the Second Department of Surgery, Fukuoka University, from 1978 through 1987, revealed a concomitant large pulmonary bulla in 11. Hence, the incidence of bulla in association with lung cancer was 2.5%. Large bullae on a routine chest roentgenogram have been defined [l]. In brief, the term large bulla means a bulla detected as an area of radiolucency greater than the area contained within the inner circle of the first rib, where either a hairline marking the perimeter of the area or signs of compression of adjacent lung were noted. In 7 of the 11 patients, the neoplasm arose in a bulla or adjoined a From the Second Department of Surgery, School of Medicine, Fukuoka University, Fukuoka, Japan. Accepted for publication Aug 5, Address reprint requests to Dr. Tsutsui, Second Department of Surgery, School of Medicine, Fukuoka University, 45-1, 7-chome Nanakuma, Jonan-ku, Fukuoka , Japan. bulla; in the remaining 4, there was no close spatial relationship. Only the former 7 patients were included in the present study. The cases of an additional 25 patients reported in the Japanese literature* since 1968 were reviewed. Accordingly, a total of 32 patients form the basis of this report, and the roentgenograms were carefully analyzed to obtain specific details of the tumor. As a control group, we used 30 of our own patients without cancer who underwent surgcal intervention for a large bulla during the same ten-year period. Results The radiographic findings related to the tumor were classified into three major patterns: (1) nodular opacity, (2) thickening of the bulla wall, and (3) secondary signs of bulla. A nodular opacity was divided into two types based on the location of the tumor center. One was the nodular opacity situated mainly within a bulla cavity. This lesion was attached to the bulla wall at its base, and demonstrated a well-circumscribed and somewhat lobulated inner surface. The shadow occasionally resembled a fungous ball. The second type was the nodular opacity located principally in the pulmonary parenchyma adjacent to the bulla (Fig 1). This lesion usually displayed the familiar roentgenographic features of cancer except for the region adjoining the bulla. The tumor was sometimes identifiable as a partial or diffuse thickening of the bulla wall. Though we found no representative example of a partial thickness, 1 of our patients had a very small nodular shadow in the bulla line rather than a partial thickening (Fig 2). The nodule exhibited few of the well-known radiographic characteristics of cancer. A diffusely thickened wall often displayed an irregularity of the inner surface and even the so-called mural nodule (Fig 3). Secondary signs of the bulla included enlargement or shrinkage of the diameter of the bulla, straightening of the hairline arcuate shadow (Fig 4), fluid retention (Fig 5), and pneumothorax. The findings are summarized in the Table, which compares the two groups of patients. There were twelve adenocarcinomas, nine squamous cell carcinomas, four large cell carcinomas, and one adenosquamous carcinoma; for the other 6 patients, radiographs were not available. There was no clear relationship between the histological tumor type and the roentgenographic findings. *The full bibliography of the sixteen references in Japanese can be obtained from Dr. Tsutsui. 679 Ann Thorac Surg 46: , Dec Copyright by The Society of Thoracic Surgeons

2 Fig 1. Chest roentgenograms of a 59-year-old man reveal (A) a large bulla of the left upper lobe in 1977, and (B) in October, 1983, an obvious nodular opacity adjoining the bulla. (C) Tomogram obtained concomitantly in The extensive, ill-defined mass clearly demonstrates malignant features, and slightly bulges upward into the bulla. Fig 2. Chest roentgenograms of a 56-year-old man show (A) large, air-containing cystic spaces in the right lung in 1985, and (B) on August 27, 1987, a small nodular opacity (arrow), 0.8 cm in maximum diameter, contiguous to one of the bulla lines. The opacity is hardly visible and does not display any of the familiar features of malignancy. (C) Computed tornogram made four days later. The nodule (arrow) is more clearly visible. 680

3 Fig 3. Chest laminagrams of a 58-year-old man show (A) a sizable thin-walled cystic lesion of the right lower lobe in 1982, and (B) four years later, a marked shrinkage in the diameter of the lesion and a diffuse thickening of the wall. Note the mural nodule (arrow). (C) Computed tomogram made at that same time. Both the diffuse thickening and the mural nodule (arrow) are clearer. Fig 4. Chest roentgenograms of a 59-year-old man reveal (A) bullous disease of the right lung in 1978, and (B) in May, 1986, considerable changes. The bulla line is straightened, substantially decreasing the size of the bulla. A nodular opacity is obvious in the hilar aspect of the bulla wall. The horizontal hairline previously noticeable in the right middle field is absent. (C) Laminagram made at the same time. The nodule reveals radiographic features of cancer. 681

4 ~ ~~~~~~ 682 The Annals of Thoracic Surgery Vol46 No 6 December 1988 Fig 5. Chest roentgenograms of a 52-year-old man show (A) bullous disease of the right upper lobe in 1984, and (B) in September, 1986, several changes. The fluid level in the bulla is apparent, and an area of infiltration is present in adjacent lung tissue. (C) Laminagram after drainage of the fluid. Diffuse thickening and a mural nodule (arrow) of the bulla wall are visible. Incidence of Radiographic Findings Suggestive of Malignant Growth in Patients with Large Bulla and with or without Cancera Bulla and Bulla Cancerb Alone Radiographic Findings (N = 26) (N = 30) Nodular opacity Within bulla 9 (34.6) l(3.3) In adjacent lung parenchyma 8 (30.8) 0 Thickening of bulla wall Partial 0 2 (6.7) Diffuse 6 (23.1) 5 (16.7) Secondary signs of bulla Enlarged size 2 (7.7) 6 (20) Shrunken size 3 (11.5) 0 Straightened line 1 (3.8) 0 Fluid retention 3 (11.5) l(3.3) Pneumothorax 1 (3.8) 7 (23.3) "Numbers in parentheses are percentages. bradiographs were not available for 6 patients. Comment When a nodular opacity is seen in a close spatial relationship with a large bulla, a malignant lesion is suspected. Except for one unique case, no patient in the control group showed evidence of a nodular opacity. In the sole exception, a small, well-demarcated round nodular shadow was suspended in the cavity. This nodule proved to be a hamartoma. The nodular shadow within a bulla usually displays a relatively smooth inner surface. Hence in this patient, there probably was no pulmonary parenchyma to be invaded. To differentiate the nodular opacity of a tumor located principally within a bulla from a mycetoma, chest roentgenograms have to be made with the patient in different positions. A fungous ball is generally freely movable, while a tumor growth is not. A large bulla commonly possesses a smooth wall of minimal thickness, probably a result of compressed lung tissue. Since we found no typical example of a cancer appearing as a partial thickening of the bulla wall, it is conceivable that only a partial thickening would suggest a stage of neoplastic growth too early for clear detection on routine roentgenograms. While it is difficult to describe a specific radiographic picture of this type, there are rare instances when a cancer in the bulla is seen at thoracotomy or in the pathological study [l, 5, 61. A diffuse thickening resulting from inflammatory reactions of the adjacent lung tissue was detected in-

5 683 Tsutsui et al: Lung Cancer and Large Bulla cidentally in a large bulla. Although the number of patients with a diffusely thickened wall was similar between the two groups, differentiation between a malignant and a benign thickening on radiographs was not difficult. The former generally shows irregularity of the thickness accompanying even a mural nodule, while the latter has a smooth inner surface and a homogeneous opacity obviously; hence it is probably not a cancer. A diffuse thickening due to cancer seems to occur either in the tumor growing along the bulla wall or in the tumor developing multifocally in the wall [7]. Neoplastic growth is more likely to be present if the patient has no clinical evidence of inflammation or if there is no improvement with the usual drug therapy. Of the 5 patients with no cancer but with a diffuse thickening, only 1 had a marked irregularity of the thickness and a mural nodule with fluid retention. Inflammatory processes were involved here. A very slow increase in the diameter of the bulla is common. Therefore, the number of patients with gradual enlargement of the size of the lesion might be larger if previous chest roentgenograms had been available for all patients in both groups. A rapid increase or decrease in the shape of the bulla was an ominous sign. Those with cancer displayed each change within a short period, whereas those without cancer showed neither a rapid increase nor a decrease in the diameter of the lesion. Such changes might be caused by obstruction of air passage routes, that is, enlargement is due to a checkvalve effect and shrinkage is due to absorption of the air in the cavity. Fluid retention is also the result of occlusion of the air passages. Straightening of the bulla line is due to traction of the wall. A large bulla complicates the situation but seldom spontaneously ruptures, thereby producing pneumothorax, but a pneumothorax is occasionally caused by an undetected cancer [8, 91. The large number of patients with pneumothorax in the control group may be related to the fact that the patients who were candidates for surgical intervention were seen and treated in our department. In general, few patients had secondary signs. However, the numbers might be greater if minimal changes in the bulla could be investigated by comparing current and previous chest roentgenograms. Tumor in the advanced stage was seen in 58.3% of the patients in our study. Presumably, the correct diagnosis of cancer was not readily made, despite the evidence of change in the bulla on the radiographs [5]. One reason may be that the neoplasm developing in a bulla or in adjacent lung tissue shows no conventional roentgenographic features of cancer until it has reached considerable size. Older patients with bullous lung disease should be given a thorough workup when first seen to exclude a possible early occult cancer [l-4,8]. When the tumor is obscure on the usual chest roentgenograms, a computed tomographic scan will provide useful information on the possible existence of a neoplasm. We recommend resection of a large bulla in patients older than 50 years whenever feasible. The highest incidence of coexisting cancer and bulla (51.6%) was found in patients in the sixth decade of life. In 45.5% of the patients, the neoplasm could not be diagnosed using cytological or histological methods. In addition, a large bulla can interfere with respiratory function, and excision can bring functional improvement [lo, 111. However, even when a resection is done, roentgenograms of the chest should be made each year. In conclusion, a possible occult cancer can be present in patients with pulmonary bullous disease. Nodular opacity, thickening of the bulla wall, and secondary signs of the bulla are highly suggestive of a tumor. We thank Dr. M. Ohara for pertinent advice. References 1. Stoloff IL, Kanofsky P, Magdner L: The risk of lung cancer in males with bullous disease of the lung. Arch Environ Health 22163, Korol E: The correlation of carcinoma and congenital cystic emphysema of the lungs: report of ten cases. Dis Chest 23:403, Goldstein MJ, Snider GL, Liberson M, Poske RM: Bronchogenic carcinoma and giant bullous disease. Am Rev Respir Dis 97:1062, Aronberg DJ, Sage1 SS, LeFrak S, et al: Lung carcinoma associated with bullous lung disease in young men. AJR , Peabody JW Jr, Katz S, Davis EW: Bronchial carcinoma arising in a lung cyst. AJR , Miyata Y, Ishihara T, Omiya T, et al: A case of bilateral giant emphysematous bullae with lung cancer. Kyobu Geka 34:392, 1981 (in Japanese) 7. Prichard MG, Brown PJE, Sterrett GF: Bronchioloalveolar carcinoma arising in long-standing lung cysts. Thorax 39: 545, Scannell JG: "Bleb" carcinoma of the lung. J Thorac Cardiovasc Surg 80:904, Maassen W, Greschuchna D Bronchiallcarzinom bei grossbullosen Lungenerkrankungen. Prax Klin Pneumol , Potgieter PD, Benatar SR, Hewitson RP, Ferguson AD: Surgical treatment of bullous lung disease. Thorax 36:885, Laros CD, Gelissen HJ, Bergstein PGM, et al: Bullectomy for giant bullae in emphysema. J Thorac Cardiovasc Surg 91:63, 1986