Pulmonary Mycobacterium Avium Disease with a Solitary Pulmonary Nodule Requiring Differentiation from Recurrence of Pulmonary Adenocarcinoma
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1 CASE REPORT Pulmonary Mycobacterium Avium Disease with a Solitary Pulmonary Nodule Requiring Differentiation from Recurrence of Pulmonary Adenocarcinoma Yoshihiro KOBASHI, Kouichiro YOSHIDA, Naoyuki MIYASHITA, Yoshihito NIKI and Toshiharu MATSUSHIMA Abstract A 56-year-old man with a past history of surgical resection of a primary pulmonary adenocarcinoma in the right upper lobe was admitted to our hospital because of a rapidly increasing solitary nodule (50 mm) in the right S 5 followed on the chest computed tomography (CT) for three months. Although we suspected recurrence of the pulmonary adenocarcinoma and performed a CTguided lung biopsy, we could not make a definite diagnosis. Therefore, to rule out recurrence of the primary pulmonary adenocarcinoma completely, a partial surgical resection of the right middle lobe was performed and a caseating epitheloid granuloma with acid-fast bacilli was found. As the causative pathogen, Mycobacterium avium complex () disease should be considered in the differential diagnosis of a rapidly increasing solitary nodule through this peculiar case of pulmonary disease. (Internal Medicine 43: , 2004) Key words: pulmonary Mycobacterium avium complex () disease, pulmonary adenocarcinoma, solitary nodule Introduction Pulmonary Mycobacterium avium complex () disease has been become a disease of significant importance in Japan, comprising about 80% of pulmonary nontuberculous disease-related cases in the country (1), and there have been many reports concerning radiological findings (2 5). Although 5% of cases with pulmonary tuberculosis characterized by solitary nodules have been diagnosed as pulmonary tuberculoma (6, 7), cases of pulmonary diseases with solitary nodules are rare. In the present case, it was difficult to make a definite diagnosis and the recurrence of a past history of surgical resection of pulmonary adenocarcinoma. Finally, however, after surgical resection, we made a diagnosis of pulmonary disease with a solitary nodule by Mycobacterium avium. Case Report A 56-year-old man with a three pack-per-day smoking history was admitted to our hospital on August 20, 2003 because of an abnormal chest shadow caused by a solitary nodule with an unclear margin which had recently appeared in the right S 5.Hehad a past history of surgical resection of a primary pulmonary adenocarcinoma (20 20 mm, poorly differentiated, T2N0M0, Stage IB) in the right upper lobe on December 25, 2001 (Fig. 1). There were no abnormal findings in the right middle lobe on chest computed tomography (CT) three months before this admission (Fig. 2) or on a previous periodic chest CT during the follow-up period after surgical resection. On admission, his height was 172 cm and his weight was 64 kg. His pulse rate was 66/min and blood pressure was 136/68 mmhg. His body temperature was 36.2 C. There were no abnormal physical findings, and laboratory data on admission (Table 1) revealed mostly normal results. Only FEV1.0 % was decreased in the pulmonary function test. Purified protein derivative (PPD) was moderately positive. A chest radiograph on admission showed a solitary nodule (35 25 mm) in the right upper lung field and multiple bullae in both upper lung fields (Fig. 3). A chest CT disclosed a solitary nodule (Fig. 4). Gallium scintigraphy revealed a hot lesion corresponding to this solitary nodule, but there were From the Division of Respiratory Diseases, Department of Medicine, Kawasaki Medical School, Kurashiki Received for publication January 26, 2004; Accepted for publication May 31, 2004 Reprint requests should be addressed to Dr. Yoshihiro Kobashi, the Division of Respiratory Diseases, Department of Medicine, Kawasaki Medical School, 577 Matsushima, Kurashiki
2 KOBASHI et al Figure 2. A chest CT three months before this admission, showing no abnormal findings in the right middle lobe. Figure 1. A chest radiograph on December 25, 2001, showing a solitary nodular shadow in the right upper lobe. The final diagnosis was primary pulmonary adenocarcinoma (20 20 mm, poorly differentiated, T2N0M0, Stage IB). no other hot lesions. The histological finding of a CT-guided lung biopsy showed a partially epitheloid granuloma without caseating necrosis, but with no acid-fast bacilli on day 7 after admission. Subsequently, we were unable to make a definite diagnosis. Therefore, we finally surgically removed the solitary nodule on day 20 because adhesion of the pleura was severe. This nodule originated from the right middle lobe (S 5 )and was mm in size. Macroscopically, it was whiteyellow in color and had become completely necrotic inside. Histologically, it was found to be a so-called tuberculous granuloma consisting of epitheloid cells and Langhans giant cells with caseating necrosis (Fig. 5), and acid-fast bacilli were positive in this tissue. Thereafter, antituberculous drugs (isoniazid (INH), rifampicin (RFP), and ethambutol (EB)) were administered until it could be determined by polymerase chain reaction (PCR) whether the solitary nodule was associated with Mycobacterium tuberculosus or suspected pulmonary tuberculoma. Afterwards, because the PCR examination of Mycobacterium tuberculosis was negative, we made a diagnosis of pulmonary disease and changed treatment to RFP, EB, clarithromycin (CAM), and streptomycin (SM). Figure 3. A chest radiograph on admission, showing a solitary nodule (35 25 mm) in the right upper lung field and multiple bullae in both upper lung fields. However, drug eruptions and eosinophilia were observed three days after the initiation of this combined therapy. Finally, a drug lymphocyte stimulation test (DLST) was positive for SM alone and we continued combined therapy 856
3 Pulmonary Disease with a Solitary Nodule Table 1. Laboratory Data on Admission Peripheral blood RBC / l Hb 13.6 g/dl Ht 40.0% WBC 3,920/ l Seg 62% Eo 3% Baso 2% Mono 5% Lym 28% Plt / l ESR 13 mm/h Blood chemistry TP 6.9 g/dl BS 101 mg/dl Bil (T) 0.8 mg/dl ALP 179 IU/l Cho 175 mg/dl -GTP 13 IU/l LDH 143 IU/l Alb 4.1 g/dl Glb 2.8 g/dl ChE 353 IU/l GPT 10 IU/l GOT 10 IU/l Crn 0.78 mg/dl UN 20 mg/dl UA 3.7 mg/dl Amy 91 IU/l CRP 0.04 mg/dl Na 141 meq/l K 3.9 meq/l Cl 105 meq/l Ca 9.2 mg/dl Serology AFP CEA CA19-9 SLX CYFRA NSE ProGRP Canditec 2 Aspergillus antigen Aspergillus antibody 4.1 ng/ml 2.4 ng/ml 5.1 U/ml 21.4 U/ml 1.0 ng/ml 5.6 ng/ml 23.5 pg/ml Cryptococcus antigen -D-glucan <6.0 pg/ml Arterial blood gas analysis (room air) ph PaO mmhg PaCO mmhg BE +0.2 Pulmonary function test %VC (VC) 123.3% (4.55 l) FEV1.0% (FEV1.0) 69.3% (3.16 l) %DLCO 80.7% PPD Sputum Bacteria Normal flora Tbc Smear, Culture Cytology Class II with RFP, EB, and CAM. Microbiologically, acid-fast bacilli were detected in tissue culture and sputum specimens and Mycobacterium avium was identified by the DNA-DNA hybridization (DDH) method. The patient experienced no relapse during the follow-up period as an outpatient. Discussion Regarding radiological findings for pulmonary disease, Albelda et al noted that alveolar infiltration, and nodular, cavitary lesions were characteristic (8). Otherwise, Tanaka et al reported that the transitional pattern of pulmonary disease was initially characterized by subpleural multiple small nodules and secondary bronchial wall thickening and dilatation (9). However, this patient s radiological findings did not fall into any classification from type 1 to type 7 of pulmonary disease by Tanaka et al (9). Therefore, this patient who suffered from pulmonary disease was thought to be a rare case showing a solitary nodular shadow. Eight cases have been previously reported in Japan (10 15) (Table 2). In 1991, Gribetz et al reported that 12 of their 20 cases (60%) showing a solitary nodular shadow and demonstrating acid-fast bacilli from a resected specimen were pulmonary disease and noted a close relationship between and solitary pulmonary nodules in Western countries (16) (Table 3). Arai et al in a study of the microbiological findings of resected specimens in 32 cases diagnosed as pulmonary tuberculosis histologically by surgical resection, noted that the detection rate of acid-fast bacilli was within 52% (17). Therefore, many cases which have been thought to be pulmonary tuberculoma histologically might be pulmonary disease. We studied the clinical findings in 21 cases of pulmonary disease with solitary nodules mentioned in all previous reports in both Japan and Western countries. Subsequently, the mean age was 63.6 years old, with 9 being male and 12 female. The isolated strains identified in six cases were all Mycobacterium avium. The original locations were the upper lobe in seven cases, the middle or lingular lobe (18) and from those of the secondary infectious type dominant in the 857
4 KOBASHI et al Figure 4. A chest CT on admission, showing a solitary nodule (50 mm) in the right S 5 and no satellite lesions around this nodule. Figure 5. Microscopic finding of the resected solitary nodule indicated a caseating epitheloid granuloma consisting of epitheloid cells, and Langhans giant cells and acid-fast bacilli were positive in this tissue (HE staining, 100). Table 2. Clinical Features of Solitary Pulmonary Nodule due to Mycobacterium Avium Intracellulare Complex Reported in Japan Case Age, Sex Cultured organism Location Size (mm) Diagnostic examination Treatment (Interval) Follow-up Our case 72, M 75, F 75, M 73, F 55, M 56, M 79, F 72, M 56, M Rt. S 8 Rt. S 4 Rt. S 9 Lt. S 5 Lt. S 1+2 Lt. S 8 Rt. S 10 Rt. S 1 Rt. S Bronchoscopy Transcutaneous lung biopsy Bronchoscopy Open lung biopsy Lobectomy Open lung biopsy resection Open lung biopsy VATS VATS resection INH+RFP+EB (1 year) RFP+EB+OFLX+CAM () INH+RFP+EB () 10 years 8 months 10 months 3 months 2 months : Not done, : Mycobacterium avium intracellulare complex, : Mycobacterium avium, VATS: Video-assisted thoracoscopic surgery. upper lobe (19). No apparent tendency was recognized and it was difficult to determine the causative pathogens from the original location. The size of the solitary nodules ranged from 15 to 50 mm, with the present case showing the maximum size and a comparatively accelerated increase because a newly solitary nodular shadow appeared in the right middle lobe on this admission despite the absence of any abnormal findings on chest CT three months before this admission (Figs. 2 and 3). As for diagnostic procedures, three cases reported in Japan were diagnosed by bronchoscopic examination or percutaneous lung biopsy and the other cases were diagnosed from surgical tissue specimens. Although the treatment for pulmonary disease consisted of only antituberculous drugs in 12 of the 21 cases, there were no recurrent cases. Initially, a recurrence of pulmonary adenocarcinoma was suspected because the patient had a past history of surgical resection of pulmonary adenocarcinoma with no clinical symptoms or negative inflammatory findings for the differential diagnosis. However, as the solitary nodule rapidly increased in size on chest CT during a three-month period and the specimen from a CT-guided lung biopsy was histologically determined to be an epitheloid granuloma, we also considered such chronic inflammatory diseases as tuberculosis or mycosis after his admission to our hospital. Although the present case was thought to be of the tuberculous resembling type because it was of the secondary infectious type and was characterized by a large nodule, no cavitary lesion had 858
5 Pulmonary Disease with a Solitary Nodule Table 3. Clinical Features of Solitary Pulmonary Nodule due to Mycobacterium Avium Intracellulare Complex Reported by Gribetz et al Case Age, Sex Cultured organism Location PPD No. acid-fast bacilli seen on smear Treatment (Interval) Follow-up , F 50, M 62, F 66, F 67, F 50, F 71, F 75, F 73, M 32, M 64, M 49, F LUL RUL RM L RUL RUL LUL LLL LLL (+) (+) Negative Few Numerous Numerous Negative Negative Numerous Lingulectomy Lobectomy Lovectomy INH+EB (1 yr) INH+EB (6 mo) INH+EB (1 yr) INH+EB (2 mo) INH+EB (2 mo) INH+RFP (1 yr) None INH+EB (1 yr) INH+EB (1 mo) 5yr 5yr 3yr 18 mo 2yr 1yr 14 mo 5mo : Mycobacterium avium intracellulare complex, : Not done, PPD: Purified protein derivative, INH: isoniazid, RFP: rifampicin, EB: ethambutol, LUL: upper love of the left lung, RUL: upper love of the right lung, : lower love of the right lung, RML: middle love of the right lung, LLL: lower lobe of the left lung. formed. Instead, we found a solid tumor with caseating necrosis and a surrounding epitheloid granuloma, which in a final histological finding was considered to possibly be a socalled tuberculous nodule. Tsukamura proposed that because pulmonary disease is characterized by a thin-walled cavitary lesion on chest radiographs, there should be marked caseating necrosis and fibrosis histologically (19). From the histological findings, we could not determine why the solitary nodule was rapidly increasing from the histological findings. Although such possibilities as an immune response of the host, a difference in infectious site, such as the alveolar region or the peripheral airway, or organic factors exist, the reason for the nodule s rapid increase is still unknown. Regarding treatment, we initially diagnosed this case of pulmonary disease with a solitary nodule in the lung field as a pulmonary tuberculoma based on the histological diagnosis and started combined therapy with antituberculous drugs. However, since the clinical effectiveness of chemotherapy using antituberculous drugs is presently poor (20, 21), surgical resection; e.g., video-assisted thoracoscopic surgery (VATS), should be recommended for the treatment of pulmonary tuberculosis but also pulmonary disease should be considered when a rapidly increasing solitary nodule is detected, as in this peculiar case, the nodule should be examined histologically and a culture examination of acidfast bacilli should be made to obtain identification. References 1) Sakatani M. Nontuberculous mycobacteriosos (NTM) in Japanepidemiologic and clinical study. Kekkaku 69: , 1994 (in 2) Moore EH. Atypical mycobacterial infection in the lung: CT appearance. Radiology 187: , ) Prinack SL, Logan PM, Hartman TE, et al. Pulmonary tuberculosis and mycobacterium avium-intracellulare: a comparison of CT findings. Radiology 194: , ) Lynch DA, Simone PM, Fox MA. CT features of pulmonary Mycobacterium avium complex infection. J Comput Assist Tomogr 19: , ) Hartman TE, Swensen SJ, Williams DE, et al. Mycobacterium aviumintracellulare complex: evaluation with CT. Radiology 187: 23 26, ) Woodring JH, Vandiviere HM, Fried AM, et al. Update: the radiographic features of pulmonary tuberculosis. Am J Roentogenol 146: , ) Miller WT, MacGregor RR. Tuberculosis: frequency of unusual radiographic findings. Am J Roentogenol 1: , ) Albelda SM, Kern JA, Marinelli DL, Miller WT. Expanding spectrum of pulmonary disease caused by nontuberculous mycobacteria. Radiology 157: , ) Tanaka E, Amitani R, Kuze F. Clinical features of the patients with secondary infection of Mycobacterium avium complex. Kekkaku 68: 57 61, 1993 (in 10) Yamazaki Y, Matsumoto H, Ogasa T, et al. A case of pulmonary Mycobacterium avium infection with a rapid-growing solitary node. Nippon Kokyuki Gakkaisi 39: , 2001 (in Japanese, Abstract in English). 11) Shimamoto H, Fujii S, Yamauchi M, et al. A case of Mycobacterium avium complex disease presenting a solitary nodule on chest radiograph. Nippon Kyoubu Rinshou 59: 62 65, 2000 (in Japanese, Abstract in English). 12) Yokomura Y, Yasuda K, Sato M, et al. A case of solitary pulmonary nodule caused by Mycobacterium avium. Kansenshogaku zasshi 72: , 1998 (in 13) Matsumoto H, Tsuji T, Takahashi T, et al. A case of Mycobacterium avium complex disease presenting a solitary pulmonary nodule. Nippon Kyoubu Rinshou 55: , 1996 (in 14) Suzuki K, Hashimoto T, Tanaka E, et al. A case of Mycobacterium avium disease presenting as a solitary pulmonary nodule and resected under a suspicion of lung cancer. Kekkaku 70: 25 29, 1995 (in 15) Murata Y, Kusajima K, Ooishi H, et al. Two cases of complex infection presenting as a solitary pulmonary nodule. Nippon Kokyuki Gakkaisi 31: , 1993 (in Japanese, Abstract in English). 859
6 KOBASHI et al 16) Gribetz AR, Damsker B, Bottone EJ, et al. Solitary pulmonary nodules due to nontubercuolous mycobacterial infection. Am J Med 70: 39 43, ) Arai T, Hirata M, Kimura S, et al. Analysis of pulmonary tuberculomas diagnosed by exploratory excision. Kekkaku 61: 1 7, 1986 (in 18) Ueda E. Clinical features of the patients with primary infection of Mycobacterium avium complex. Kekkaku 68: 51 56, 1993 (in 19) Tsukamura M. Characterized of X-ray feature of lung disease due to Mycobacterium avium-mycobacterium intracellulare complex. Kekkaku 56: 23 33, 1082 (in 20) Tanaka E, Kimoto T, Tsuyuguchi K, et al. Effect of clarithromycin regimen for Mycobacterium avium complex pulmonary disease. Am J Respir Crit Care Med 160: , ) Kobashi Y, Matsushima T. The effect of combined therapy according to the guidelines for the treatment of Mycobacterium avium complex pulmonary disease. Intern Med 42: , ) Shiraishi Y, Fukushima K, Komatsu H, et al. Early pulmonary resection for localized Mycobacterium avium complex disease. Ann Thorac Surg 66: ,
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