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Thoracic Imaging |
1 From the Department of Radiology and Center for Imaging Science (Y.J.J., K.S.L., T.S.K.), Division of Pulmonary and Critical Care Medicine, Department of Medicine (W.J.K., O.J.K.), and Department of Pathology (J.H.), Samsung Medical Center, Sungkyunkwan University School of Medicine, 50 Ilwon-Dong, Kangnam-Ku, Seoul 135–710, Korea. Received May 29, 2003; revision requested August 12; revision received September 17; accepted October 14. Supported by a grant from the Korea Health 21 R&D Project, Ministry of Health & Welfare, Republic of Korea (00-PJ1-PG1-CY03–0001). Address correspondence to K.S.L. (e-mail: melon2@samsung.co.kr).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Between April 2002 and March 2003, the thin-section chest CT findings in and histopathologic lung tissue specimens from 22 patients who fulfilled the American Thoracic Society diagnostic criteria for NTM pulmonary infection were retrospectively reviewed. The lung lesion patterns (ie, small nodules, branching centrilobular nodules [ie, tree-in-bud pattern], consolidation, cavities, bronchiectasis, and volume loss) seen at CT at the sites of transbronchial lung biopsy (n = 22) or lobectomy (n = 1) were compared with the histopathologic findings.
RESULTS: Thirteen of the 22 patients were found to have Mycobacterium abscessus pulmonary infection; seven, to have Mycobacterium avium-intracellulare complex infection; and two, to have Mycobacterium fortuitum infection. Regardless of the specific infective mycobacterial species, bilateral small nodules (in 22 [100%] lung locations), cylindric bronchiectasis (in 20 [91%] locations), and branching centrilobular nodular lesions (in 17 [77%] locations) were the most common CT findings seen at the biopsy sites. All of the transbronchial lung biopsy specimens showed a thickened bronchiolar wall and bronchiolar and peribronchiolar inflammation at histopathologic analysis. Dilated bronchioles were identified in 19 (86%) patients, and epithelioid granulomas with or without caseation were seen in seven (32%).
CONCLUSION: Regardless of the specific infective mycobacterial species, the most common thin-section CT findings of NTM pulmonary infection are bilateral small nodules, cylindric bronchiectasis, and branching centrilobular nodules. These findings correspond histopathologically to bronchiolectasis and bronchiolar and peribronchiolar inflammation with or without granuloma formation.
© RSNA, 2004
Index terms: Lung, CT, 60.12111, 60.12115, 60.12118 • Lung, diseases, 60.203, 60.2191, 60.26, 60.28 • Lung, infection, 60.203 • Mycobacteria, 60.203
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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NTM pulmonary infection develops in white middle-aged or elderly men who smoke and abuse alcohol, but it is also seen in older nonsmoking women, who, according to one report (11), represent up to 50% of all patients with NTM pulmonary infection. Because NTM organisms are ubiquitous and difficult to conclusively culture or identify, even in bronchoalveolar lavage fluid, it is difficult to prove that the radiologic patterns—the CT patterns especially—of pulmonary lesions that are suspected of being NTM pulmonary infection are caused by NTM organisms per se. Therefore, without lung biopsy specimen analysis, months to years of clinical, radiologic, and microbiologic follow-up of certain patients may be required to make a reliable diagnosis of NTM pulmonary infection (12).
Despite the increasing incidence and diagnoses of NTM infections, to the best of our knowledge, comparisons between the radiologic and histopathologic findings of this disease in immunocompetent hosts have not been described in the English-language literature. The purpose of this study was to identify and describe the thin-section CT findings of NTM pulmonary infection in immunocompetent patients and to compare these findings with histopathologic findings.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Between April 2002 and March 2003, 53 patients underwent both bronchoalveolar lavage and transbronchial lung biopsy for the diagnosis of NTM pulmonary infection. In these 53 patients, NTM pulmonary infection was suspected on the basis of a clinical history of a cough with sputum and thin-section CT findings of bilateral patchy areas of bronchiectasis and branching centrilobular nodules (ie, tree-in-bud pattern), irrespective of the presence of cavities in the upper lung lobes. Of these 53 patients, 22—five men (mean age, 56 years; age range, 29–79 years) and 17 women (mean age, 57 years; age range, 35–72 years)—proved to have NTM pulmonary infection on the basis of positive microbiologic findings (n = 15), positive histopathologic findings (n = 3), or both (n = 4) at examinations of bronchoalveolar lavage fluid or transbronchial lung biopsy specimens.
Microbiologic findings were regarded as positive for NTM infection when cultures of the bronchoalveolar lavage fluid or transbronchial biopsy specimen were positive for NTM organisms. Histopathologic findings were regarded as positive when the biopsy specimen showed epithelioid granuloma with or without caseous necrosis. All patients with these positive findings also fulfilled the 1997 American Thoracic Society criteria for the diagnosis of NTM disease (12). According to the American Thoracic Society criteria, a patient whose chest radiograph or thin-section chest CT scan findings suggest mycobacterial infection and who presents with compatible symptoms and signs should receive a diagnosis of an NTM pulmonary disease when the patient’s fluid and tissue specimens meet the following microbiologic and/or histopathologic criteria: three positive sputum cultures with negative acid-fast bacilli smears or two positive sputum cultures with at least one positive acid-fast bacilli smear; one positive bronchial washing with 2 to 4+ growth of mycobacteria; and/or a biopsy specimen positive for mycobacteria.
Four of the 22 patients had a history of smoking: three current smokers and one ex-smoker. The 22 patients had undergone both helical thin-section CT and bronchoscopy. In 17 of the 22 patients, bronchoscopy was performed within 7 days after the CT examination by one pulmonologist (W.J.K.) with 6 years of experience; overall, it was performed within a mean of 10.4 days of CT (range; 0–79 days). At bronchoscopy, all tracheobronchial trees (in their entirety) at the orifice of the subsegmental bronchi were inspected. Then, for bronchoalveolar lavage, 50 mL of sterilized saline was injected via a bronchoscope wedged into the segmental or subsegmental bronchus of the most heavily involved lobe, as determined at thin-section CT. Transbronchial lung biopsy was performed after bronchoalveolar lavage at the bronchoscopic examination. The specimens were evaluated histopathologically and microbiologically. Among the 22 patients, one patient, who had a Mycobacterium avium-intracellulare complex pulmonary infection, underwent lobectomy for treatment of the disease.
CT Scan Acquisition and Review
CT scans were acquired by using a GE LightSpeed QX/i scanner (GE Medical Systems, Milwaukee, Wis) without intravenous injection of contrast medium. All CT data were reconstructed by using a high-spatial-frequency algorithm. Helical volumetric scans of the thorax were obtained by using multi–detector row CT with 120 kVp, 70 mA, 2.5-mm collimation, a pitch of 6, and a reconstruction interval of 2 mm. The data obtained were reconstructed with a 2.5-mm section thickness for the transverse scans and with a 1.2–2.0-mm section thickness for the coronal scans. The scan data were displayed directly on four monitors (with 1,536 x 2,048 image matrices, 8-bit viewable gray scale, and 60-ft-lambert luminescence) of a picture archiving and communication system, or PACS (Pathspeed; GE Medical Systems Integrated Imaging Solutions, Mt Prospect, Ill). Both mediastinal (window width, 400 HU; window level, 20 HU) and lung (window width, 1,500 HU; window level, –700 HU) window scans could be viewed.
The thin-section CT scans were retrospectively reviewed by two independent chest radiologists (K.S.L., T.S.K.) who had 13 and 7 years of experience, respectively. These radiologists had no knowledge of the histopathologic results or any clinical information except that the patients had NTM pulmonary infections. Final conclusions regarding the CT scan findings were reached by consensus.
A total of 132 lung locations in the 22 patients were evaluated for the presence of lung lesions and other abnormal findings. Six locations in each patient were evaluated: right upper lobe, right middle lobe, right lower lobe, left upper lobe, lingular segment, and left lower lobe. Each location was evaluated at CT for the presence or absence of well-defined small (ie, <10 mm in diameter) nodules, branching centrilobular nodules (ie, tree-in-bud pattern), nodules 10–30 mm in diameter, lobular consolidation (ie, with polygonal shape and 10–25 mm in diameter), subsegmental or segmental consolidation, cavities, bronchiectasis, and volume loss. When a cavity was present, the longest diameter of the cavity was recorded. On the basis of morphologic features, bronchiectasis was classified as cylindric, varicose, or cystic. The presence of mediastinal or hilar lymph node enlargement and of pleural effusion or thickening also was recorded.
Histopathologic and Microbiologic Evaluations and CT-Histopathologic Comparisons
For the microbiologic studies, bronchoalveolar lavage fluid and transbronchial lung biopsy specimens were examined with Ziehl-Neelsen stain and cultured.The culture specimens were inoculated into Lowenstein-Jensen solid media, and the number of colonies was counted for up to 8 weeks after inoculation.
To provide a histopathologic basis for the CT findings, one lung pathologist (J.H.) with 9 years of experience who had no knowledge of the thin-section CT findings or any clinical information examined all available histopathologic specimens, including those obtained at transbronchial lung biopsy (n = 22) and lobectomy (n = 1), with routine light microscopy by using hematoxylin-eosin stain and acid-fast bacilli stain to detect mycobacteria. One chest radiologist (Y.J.J.) with 2 years of experience and the pathologist (J.H.) who evaluated the histopathologic specimens compared the patterns of the lung lesions (ie, nodule smaller than 10 mm in diameter, nodule 10–30 mm, lobular consolidation, subsegmental or segmental consolidation, branching centrilobular nodules [ie, tree-in-bud pattern], cavities, bronchiectasis, and volume loss) seen at CT at the site of transbronchial lung biopsy or lobectomy with the microscopic structures seen in the histopathologic specimens. The radiologist did not take part in the reading of the CT images and was not blinded to the histopathologic or clinical information.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The patterns of the lesions at the sites of transbronchial lung biopsy are summarized in Table 3. Regardless of the specific infective mycobacterial species, bilateral small nodules (seen at all 22 biopsy locations), cylindric bronchiectasis (seen at 20 locations), and branching centrilobular nodules (ie, tree-in-bud pattern; seen at 17 locations) were the most common findings, followed by varicose bronchiectasis (seen at nine locations), cystic bronchiectasis (seen at eight locations), cavities (seen at six locations), lobar volume loss (seen at six locations), well-defined nodules larger than 10 mm in diameter (seen at five locations), lobular consolidation (seen at three locations), and subsegmental or segmental consolidation (seen at three locations) (Figs 1, 2).
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The lobectomy specimen obtained in one patient showed large peribronchial caseating granulomas and extensive peribronchial infiltration of lymphocytes surrounding a dilated bronchus or a bronchiole (Fig 1). Some solid caseous materials also were seen within the bronchioles. These histopathologic findings correlated well with the thin-section CT findings. The small nodules and branching centrilobular nodules (ie, tree-in-bud pattern) seen at thin-section CT represented NTM granulomas and caseous materials within the terminal or respiratory bronchioles. The nodules larger than 10 mm in diameter and the lobular consolidation corresponded to areas of centrally located caseating granulomas, marginal nonspecific inflammation, and coalescent lymphocytic infiltrates completely replacing the normal alveoli. The wall of cavitary lesions within the lobectomy specimen consisted of caseous materials, epithelioid cells with multinucleated giant cells, granulation tissue, and a fibrous capsule.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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However, because some patients with true pulmonary infections produce minimal amounts of sputum, it may be difficult to differentiate NTM pulmonary infection from other diseases such as chronic obstructive pulmonary disease and bronchiectasis, which may cause symptoms and signs similar to those of NTM pulmonary infection. In such circumstances, bronchoscopy may be useful in obtaining the material needed for mycobacterial culture and to acquire histologic evidence of granulomatous infection (7). However, even with bronchoscopy, the diagnosis may be elusive (13,14). In our study, which initially involved 53 patients who had CT findings that were suggestive of NTM pulmonary infection, including bilateral patchy areas of bronchiectasis and branching centrilobular nodules (ie, the tree-in-bud pattern), only 22 patients ultimately received a diagnosis of NTM pulmonary infection based on findings at histopathologic and/or microbiologic examinations performed by using bronchoscopy.
It has been reported that the radiologic appearances of NTM pulmonary infection are not influenced by specific mycobacterial species (15). We found this to be true in the present study: Regardless of the specific mycobacterial species that caused the infection, bilateral small nodules, cylindric bronchiectasis, and branching centrilobular nodules were the most common thin-section CT findings seen. Cavities were relatively uncommon.
NTM pulmonary infection in immunocompetent hosts has two distinct radiologic manifestations: an upper lobe cavitary form and a nodular bronchiectatic form (3,12,13). The characteristic radiologic findings of the upper lobe cavitary form are heterogeneous nodular and cavitary opacities that are indistinguishable from those seen with postprimary pulmonary tuberculosis, but this form of NTM pulmonary infection usually has a more indolent course. Patients with the cavitary form are typically elderly men with underlying chronic lung disease—usually chronic obstructive pulmonary disease.
The nodular bronchiectatic form of NTM pulmonary infection usually occurs in middle-aged women without underlying lung disease. The radiologic features of the nodular bronchiectatic form are bronchiectasis and branching centrilobular nodules (ie, tree-in-bud pattern), which are most severe in the lingular segment and in the right middle lobe. However, in our study, the cylindric bronchiectasis and branching centrilobular nodules were bilateral and extensive and showed no specific lobar predominance.
The nodular bronchiectatic form of NTM pulmonary infection has often been referred to as airway colonization, in which the real underlying condition is bronchiectasis. The results of several previous investigations (4–6) have supported this concept of colonization—that is, the isolation of the organism from the respiratory tract without evidence of tissue invasion. The results of more recent studies involving the use of thin-section CT with or without serial examination, however, indicate that patients with the nodular bronchiectatic form of NTM infection have the specific radiologic features of parenchymal disease—specifically, bronchiectasis and branching centrilobular nodules—which progress over time (10,16–19). In addition, transbronchial lung biopsy specimens show granulomatous inflammation, which suggests lung tissue invasion by the organism involved (7–9). Therefore, the term colonization may be inappropriate. Our study results demonstrate that the characteristic histopathologic findings seen in the transbronchial lung biopsy specimens of patients with NTM pulmonary disease are bronchiolectasis and bronchiolar and peribronchiolar inflammation with or without granuloma formation.
The lobectomy specimen showed large peribronchial caseating granulomas and extensive peribronchial infiltration of lymphocytes surrounding a dilated bronchus or a bronchiole. Some solid caseous materials within the respiratory bronchioles also were observed. These characteristic histopathologic findings of NTM pulmonary infection suggest that bronchiectasis and bronchiolitis are caused by NTM infection.
When we compared the CT and histopathologic findings, the branching centrilobular nodules seen on thin-section CT scans corresponded histopathologically to NTM granulomas and caseous materials within the terminal or respiratory bronchioles. These caseating granulomas, which comprised epithelioid macrophages and giant cells, are typical of NTM pulmonary infection in immunocompetent hosts and are no different from the caseating granulomas seen with postprimary pulmonary tuberculosis (7–9,20,21). The nodules larger than 10 mm in diameter and the lobular consolidation corresponded histopathologically to areas of centrally located caseating granulomas, marginal nonspecific inflammation, and coalescent lymphocytic infiltrates completely replacing normal alveoli. The wall of cavitary lesions seen at CT consisted histopathologically of caseous materials, epithelioid cells with multinucleated giant cells, granulation tissue, and a fibrous capsule.
According to the results of one CT study (10), existing bronchiectasis progresses in extent and new areas of bronchiectasis are formed over time. These findings suggest that bronchiectasis not only may predispose individuals to NTM pulmonary infection, but it also may be caused by NTM pulmonary infection. However, recognition of the pathogenicity of these microorganisms is limited in the clinical setting owing to the difficulty in isolating the responsible organism from sputum specimens and the frequent coexistence of pathogens other than NTM species, especially in patients with the nodular bronchiectatic form of NTM pulmonary infection.
A published report revealed that because of the high rate of false-negative sputum cultures in patients with the nodular bronchiectatic form of NTM infection, 45% of patients required bronchoscopy or lung biopsy for the diagnosis of active NTM infection (14). The lack of specificity of the signs, symptoms, and radiologic findings of these infections makes it important to consider obtaining a biopsy specimen and, more important, to obtain adequate amounts of lavage material for mycobacterial culturing.
Our study had several drawbacks. First, a one-to-one comparison between the CT and histopathologic findings was performed only in one patient. Because transbronchial biopsy specimens were obtained in most patients, an exact comparison was not feasible. Second, we included patients who had findings of bronchiolitis and bronchiolectasis without epithelioid granuloma at histopathologic examination. Only seven patients had histopathologic findings of typical epithelioid granuloma. Biopsy specimens obtained at transbronchial lung biopsy allowed us to evaluate mainly the bronchioles or the peribronchiolar lesions. However, the patients in whom these specimens were obtained received a diagnosis of NTM infection because they had already fulfilled the American Thoracic Society criteria for the diagnosis of NTM disease (ie, positive sputum or bronchoalveolar lavage fluid culture). Although the American Thoracic Society criteria for NTM disease that are based solely on histopathologic findings include granulomatous inflammation (12), this histopathologic criterion cannot be met by all patients.
Third, our study might have involved some selection bias. We included only those patients who fulfilled the American Thoracic Society criteria for NTM pulmonary infection on the basis of histopathologic or microbiologic evidence of NTM pulmonary infection at bronchoscopy. Patients who had the typical thin-section CT findings of NTM pulmonary infection—specifically, bilateral small nodules, cylindric bronchiectasis, and branching centrilobular nodules (ie, tree-in-bud pattern)—but a limited number of positive microbiologic findings were excluded. These patients might have received a diagnosis of NTM infection if repeat sputum smears had been obtained or bronchoscopy had been performed.
Fourth, in this CT-histopathologic correlation study, M abscessus pulmonary infection was the most frequent; M avium-intracellullare complex and M fortuitum infections followed. In the English-language literature, however, M avium-intracellullare complex and Mycobacterium kansasii are reported as the organisms most frequently involved in NTM pulmonary infection. About 50% of patients with M avium-intracellullare complex pulmonary infection and about 90% of patients with M kansasii infection, both including immunocompetent and immunocompromised patients, present with findings of the upper lobe cavitary form of NTM infection (3,12,13). However, patients with M abscessus infection usually present with findings of the nodular bronchiectatic form (22).
Because we selectively included patients with the nodular bronchiectatic form of NTM infection, more patients with M abscessus infection were included. In addition, in this endemic area of Korea, M abscessus is the second most frequently seen organism in NTM pulmonary infection. (M avium-intracellullare complex is the most frequently seen.) Furthermore, because M abscessus pulmonary infection is refractory to medical therapy, we might have performed more aggressive diagnostic examinations of tissue invasion with bronchoscopy in the cases of M abscessus infection. Therefore, more patients with M abscessus infection were selectively included in this study.
In conclusion, regardless of the specific infective mycobacterial species, the common thin-section CT findings of NTM pulmonary infection are bilateral small nodules, cylindric bronchiectasis, and branching centrilobular nodules (ie, tree-in-bud pattern). Moreover, these CT findings correspond to the histopathologic findings of bronchiolectasis and bronchiolar and peribronchiolar inflammation with or without granuloma formation. The histopathologic findings seen in NTM pulmonary infection are the same as those seen in patients with Mycobacterium tuberculosis infection. The results of the comparison between thin-section CT findings and histopathologic findings suggest the presence of true infection with lung tissue invasion in NTM pulmonary disease rather than colonization or contamination.
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, K.S.L.; study concepts, K.S.L., W.J.K.; study design, K.S.L., Y.J.J., W.J.K.; literature research, Y.J.J., K.S.L., W.J.K.; clinical studies, W.J.K., O.J.K.; data acquisition, Y.J.J., W.J.K., O.J.K.; data analysis/interpretation, Y.J.J., K.S.L., W.J.K., T.S.K.; statistical analysis, Y.J.J., W.J.K.; manuscript preparation and editing, Y.J.J., K.S.L.; manuscript definition of intellectual content, Y.J.J., K.S.L., W.J.K.; manuscript revision/review and final version approval, all authors
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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