High-Resolution CT Findings of Mycobacterium avium-intracellulare Complex Pulmonary Disease: Correlation with Pulmonary Function Test Results
Abstract
OBJECTIVE. The purpose of our study was to analyze the high-resolution CT findings of the nodular bronchiectatic form of Mycobacterium avium-intracellulare complex (MAC) pulmonary disease and to correlate the extent of high-resolution CT findings with pulmonary function test (PFT) results.
MATERIALS AND METHODS. From January 2005 through December 2005, we identified 47 patients (mean age, 58 ± 13 years; age range, 24–72 years; male–female ratio, 11:36) with the nodular bronchiectatic form of MAC pulmonary disease who underwent both high-resolution CT and PFTs. High-resolution CT findings were reviewed retrospectively in terms of the presence and extent of bronchiectasis, cellular or inflammatory bronchiolitis (centrilobular small nodules and tree-in-bud signs), cavity, nodule, and other findings. The extent of the abnormalities seen on high-resolution CT was scored by modifying the cystic fibrosis scoring system proposed by Helbich and coworkers. The scores were correlated with PFT results using Spearman's correlation coefficient.
RESULTS. On high-resolution CT, the three most frequently observed patterns of parenchymal abnormalities were, in decreasing order of frequency, cellular bronchiolitis (n = 47, 100%), bronchiectasis (n = 46, 98%), and consolidation (n = 27, 57%). The total CT score showed a significant correlation with the residual volume–total lung capacity (RV/TLC) ratio (r = 0.572, p < 0.001), forced expiratory volume in 1 second (FEV1) value (r = –0.426, p = 0.003), forced vital capacity (FVC) value (r = –0.360, p = 0.013), peak expiratory flow value (r = –0.352, p = 0.015), and peak expiratory flow between 25% and 75% of the forced vital capacity (FEF25–75%) (r = –0.289, p = 0.049).
CONCLUSION. CT scoring of pulmonary abnormalities correlates with measures of functional impairment in patients with MAC pulmonary disease.
Introduction
Mycobacterium avium-intracellulare complex (MAC) pulmonary infection, which has been reported to be increasing in incidence [1], is a highly complex disease in terms of its clinical presentation and management. MAC organisms are ubiquitous, and an MAC pulmonary infection may simulate clinically pulmonary tuberculosis [1]; therefore, an awareness of the initial and follow-up high-resolution CT findings and of clinical correlation is mandatory for the diagnosis and management of this disease.
The MAC pulmonary infection has been differentiated into two distinct subtypes—upper lobe cavitary disease and nodular bronchiectatic disease [1]. The results of several studies using chest CT have shown that the presence of bilateral multifocal cellular or inflammatory bronchiolitis (i.e., the presence of centrilobular small nodules and branching nodular structures, the so-called tree-in-bud sign) and of bronchiectasis distributed mainly in the right middle lobe and lingular division of the left upper lobe is indicative of the nodular bronchiectatic form of MAC pulmonary infection [2–6]. According to a prospective study [7], approximately one third of patients with high-resolution CT findings of bilateral bronchiectasis plus cellular bronchiolitis have a nontuberculous mycobacterial pulmonary infection, and in these cases, MAC is the most common cause.
The high-resolution CT findings of bilateral bronchiectasis and cellular bronchiolitis in an MAC pulmonary infection may simulate those in cystic fibrosis in which the predominant CT abnormalities are bilateral bronchiectasis, peribronchial wall thickening, mosaic perfusion, and mucous plugging [8–14]. In cystic fibrosis, a number of scoring systems have been proposed and are used for both clinical treatment and research purposes. High-resolution CT scoring systems are also a potentially useful surrogate for predicting prognosis in patients with this disease [8–14].
Although bronchiectasis and cellular bronchiolitis are the major high-resolution CT findings in the nodular bronchiectatic form of MAC pulmonary infection, to the best of our knowledge, the scoring system used for the evaluation of the extent of disease has not been the topic of a published study. Furthermore, the relationship between high-resolution CT findings and pulmonary function test (PFT) results has not been reported. Thus, the purpose of our study was to analyze the high-resolution CT findings of the nodular bronchiectatic form of MAC pulmonary disease and to correlate the extent of high-resolution CT findings with PFT results.
Materials and Methods
The institutional review board approved this retrospective study with a waiver of informed consent.
Patients and Diagnoses
For a 1-year period from January 2005 through December 2005, we identified 89 untreated new patients with MAC pulmonary infection who fulfilled the American Thoracic Society criteria for the diagnosis of nontuberculous mycobacterial disease [1]. Most patients had been referred to the outpatient-based bronchiectasis-specific clinic of our hospital. For a diagnosis of MAC pulmonary disease, sputum acid-fast bacillus (Ziehl-Neelsen method) staining and culture examinations for Mycobacteria organisms were performed at least three times in each of the 89 patients. Bronchoscopy also was performed for bronchial washing or transbronchial lung biopsy was performed in 70 of the 89 patients. In all cases, sputum examinations were performed within 0–34 days (mean, 9 days) of CT, and bronchoscopic samples were obtained within 0–24 days (mean, 7 days) of CT.
Expectorated sputum and samples obtained with bronchoscopy were examined using acid-fast bacil lus staining and then were cultured for Mycobacteria organisms using 3% Ogawa egg medium (Shinyang Chemical Co. Ltd.). Colony numbers were counted after incubation for as long as 8 weeks, and identification of nontuberculous Mycobacteria species was con firmed using a polymerase chain reaction–restriction fragment length polymorphism method based on the rpoB gene [15]. Because non tuberculous mycobacterial disease is a subacute or chronic pulmonary infection, the absence of con current bacterial infection was ensured by clinical history—that is, the absence of symptoms and signs of acute respiratory infection including purulent sputum, high fever, or sepsis.
Of the 89 patients, 70 patients were thought to have the nodular bronchiectatic form of MAC pulmonary disease on the basis of high-resolution CT findings of bilateral patchy areas of bronchiectasis and cellular or inflammatory bronchiolitis (centrilobular small nodules and tree-in-bud signs) irrespective of the presence of cavities in the upper lobes. Of these 70 patients, 47 patients (mean age, 58 ± 13 years; range, 24–72 years), in whom both high-resolution CT and pulmonary function test (PFT) results were available, were included in the study. The 47 patients included 11 men (mean age ± SD, 66 ± 14 years; age range, 43–72 years) and 36 women (mean age, 56 ± 12 years; age range, 24–78 years) (p = 0.06, Mann-Whitney U test). In these patients, PFTs were performed within 3 weeks (mean, 8 days; range, 0–21 days) of the high-resolution CT examination.
Patients complained of cough (n = 41), sputum (n = 41), fever (n = 1), and weight loss (n = 1). Of these 47 patients, two had a history of smoking (ex-smokers, with 20-pack years and 100-pack years, respectively).
CT Acquisition
CT scans were obtained using a helical technique; a 4-MDCT scanner (LightSpeed QX/i, GE Healthcare; 18 patients) and an 8-MDCT unit (LightSpeed Ultra, GE Healthcare; 29 patients) were used. IV contrast medium was not given to any of the patients. A helical CT technique (collimation of 2.5 mm, 120 kVp, 70 mA, beam width of 10 mm, and beam pitch of 1.375–1.5) was used, and all CT data were reconstructed using a high-spatial-frequency algorithm. Expiratory CT scans were not obtained. The image data were reconstructed with a 2.5-mm section thickness for transverse images and a 2.0-mm section thickness for coronal images. Scans were obtained from the lung apices to the lung bases. The scan data were displayed directly on monitors of a PACS (Path Speed or Centricity 2.0, GE Healthcare Integrated Imaging Solutions). The monitors displayed both mediastinal (window width, 400 H; window level, 20 H) and lung (window width, 1,500 H; window level, –700 H) window images.
CT Scoring System
We developed a CT scoring system of nontuberculous mycobacterial disease (Table 1) in which the extent of lung involvement was recorded and calculated. Various kinds of scoring systems have been reported [8–14]; our scoring system was created by modifying the previously used scoring system proposed by Helbich and coworkers [9, 10]. A total maximum score of 42 was allocated for evaluating the overall extent of a lung lesion. Scores were given by considering the lobar volume decrease and the presence, severity, and extent of bronchiectasis, cellular or inflammatory bronchiolitis, cavity, nodules, consolidation, bullae, emphysema, and mosaic perfusion in both lungs.
| Score | |||||
|---|---|---|---|---|---|
| CT Finding (Maximum No. of Points) | 0 | 1 | 2 | 3 | Subtotal |
| Bronchiectasis (12 points) | |||||
| Severity | Absent | Mild (bronchus diameter > adjacent vessel diameter) | Moderate (bronchus diameter = 2-3× vessel diameter) | Severe (bronchus diameter > 3× vessel diameter) | |
| Extent | Absent | 1-5 segments | 6-9 segments | > 9 segments | |
| Bronchial wall thickening | Absent | Mild (wall thickness = adjacent vessel diameter) | Moderate (vessel diameter < wall thickness < 2× vessel diameter) | Severe (wall thickness ≥ 2× vessel diameter) | |
| Mucus plugging | Absent | 1-5 segments | 6-9 segments | > 9 segments | |
| Bronchiolitis (6 points) | |||||
| Severity | Absent | Mild (identifiable; peripheral lung < 2 cm from pleura) | Moderate (definite; involvement > 2 cm from pleura) | Severe (extensive; extending to central lung) | |
| Extent | Absent | 1-5 segments | 6-9 segments | > 9 segments | |
| Cavity (6 points) | |||||
| Severity | Absent | Mild (diameter < 3 cm) | Moderate (3 cm < diameter < 5 cm) | Severe (diameter ≥ 5 cm) | |
| Extent | Absent | 1-3 in number | 4-5 in number | > 5 in number | |
| Nodules (10-30 mm in diameter) (3 points) | Absent | 1-5 segments | 6-9 segments | > 9 segments | |
| Consolidation, lobular, segmental, or peribronchial (3 points) | Absent | < 3 segments | 3-5 segments | > 5 segments | |
| Bullae (3 points) | Absent | Unilateral (< 4 in number) | Bilateral (< 4 in number) | Bilateral (≥ 4 in number) | |
| Emphysema (3 points) | Absent | 1-5 segments | > 5 segments | NA | |
| Mosaic perfusion (3 points) | Absent | 1-5 segments | > 5 segments | NA | |
| Lobar volume decrease (3 points) | Absent | 1 lobe | 2 lobes | ≥ 3 lobes | |
| Total CT score (add subtotals)a | |||||
Two independent chest radiologists with 2 and 18 years' experience interpreting chest CT, respectively, evaluated retrospectively the chest CT scans and completed scoring sheets. When there were discrepancies in their readings, final decisions were reached by consensus. The observers were unaware of the PFT results. Six lung lobes in each patient, with the lingual division of the left upper lobe being considered a separate lobe, were assessed for the presence of lung parenchymal abnormalities. Each lung lobe was evaluated for the presence and extent of the lung abnormalities mentioned earlier. The laterality (i.e., unilateral or bilateral) and the locations of the lung lesions were also analyzed. A total of 282 lung lobes in 47 patients (six lobes per patient) with MAC infection was evaluated for the presence of lung lesions.
Bronchiectasis was defined to be present when the diameter of the bronchial lumen was greater than that of the adjacent pulmonary artery without tapering of bronchial lumen diameter (Fig. 1A, 1B). Because bronchial wall thickening and mucus plugging are frequently accompanied by bronchiectasis, those findings were considered under the subcategory of bronchiectasis. Bronchial wall thickness was estimated by measuring the ratio of the thickness of the airway wall to the outer diameter of the corresponding bronchus. Mucus plugging was regarded as present when a broad linear or branching attenuation lesion was observed in a proximal airway (lobar, segmental, or subsegmental bronchus) and was associated with airway dilatation.
Bronchiolitis, the cellular or inflammatory type, was defined as the presence of centrilob ular small nodules (< 10 mm in diameter) and branching nodular structures (i.e., tree-in-bud signs) on high-resolution CT scans (Fig. 2A, 2B, 2C). Dif ferent from Helbich and colleagues [9, 10], we did not consider tree-in-bud signs (most of which indicated cellular or inflammatory bronchiolitis) as mucus plug ging; thus, these signs were not included in scoring mucus plugging.
The presence of other abnormalities was also recorded including the following: cavities; nodules, 10–30 mm in diameter; lobular con solidation of 10–20 mm in diameter with a polygonal shape, peribronchial consolidation, or segmental consolidation; bulla; emphysema; mosaic perfusion; and lobar volume reduction. Because cavities were frequently accompanied by bronchiectasis and bronchiolitis in MAC pulmonary disease [7], the severity and extent of bronchiectasis and bronchiolitis were also counted. Bullae and emphysema were defined according to the Fleischner Society's glossary of terms [16]. Mosaic perfusion was defined as one or more areas of decreased lung attenuation with oligemic pulmonary vessels. Because we did not have expiratory CT data, mosaic perfusion was regarded as present and was differentiated from emphysema when the areas in question showed lower attenuation than the surrounding normal lung parenchyma but their attenuation was > –950 H [17].
Pulmonary Function Tests
Forced spirometry and plethysmography were performed with pulmonary function units. In all patients, pulmonary function was evaluated within 3 weeks of the time of the CT examinations. The functional indexes measured were forced vital capacity (FVC), forced expiratory volume in 1 second (FEV1), FEV1/FVC, peak expiratory flow (PEF), peak expira tory flow between 25% and 75% of the FVC (FEF25–75%), residual volume (RV), total lung capacity (TLC), and RV/TLC. These values were expressed as a percentage of the predicted value for patient age, sex, and height [18, 19].
CT–Pulmonary Function Test Comparisons
The scores of the high-resolution CT extent of disease were compared with the PFT results. The mean score of the two observers for each pattern and the total extent of each lung abnormality were recorded and compared with each component of the PFT results.
Statistical Analyses
For statistical analyses, the commercially available statistics package program (SPSS version 11.0, SPSS) was used. Values are expressed as mean ± SDs in the text. Interobserver agreement for the extent of each pattern and total amount of lung abnormalities was calculated using Spearman's correlation coefficient. The analysis of the correlation between the scores of high-resolution CT for disease extent and the PFT results were also determined using Spearman's correlation coefficient. A p value of less than 0.05 was considered statistically significant.
Results
CT Findings
The most common of the high-resolution CT findings for MAC pulmonary disease was bronchiolitis (n = 47, 100%) (Fig. 2A, 2B, 2C), followed by bronchiectasis (n = 46, 98%) (Fig. 1A, 1B), consolidation (n = 27, 57%), nodule (n = 19, 40%), cavity (n = 17, 36%), lobar volume decrease (n = 17, 36%), emphysema (n = 15, 32%), mosaic perfusion (n = 6, 13%), and bullae (n = 5, 11%). The patterns of the parenchymal findings, frequency, and laterality and the locations of the lung lesions are summarized in Table 2.
| Laterality of MAC Involvement (No. of Patients) | Location of MAC Infection (No. of Lobes) | |||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Right Lobe | Left Lobe | |||||||||
| CT Pattern | No. (%) of Patients | Unilateral | Bilateral | Upper | Middle | Lower | Upper | Lingular Segment | Lower | Total (n = 282) |
| Bronchiolitis | 47 (100) | 5 | 42 | 35 | 39 | 32 | 30 | 33 | 38 | 207 |
| Bronchiectasis | 46 (98) | 5 | 41 | 33 | 39 | 21 | 17 | 33 | 30 | 173 |
| Consolidation | 27 (57) | 13 | 14 | 15 | 14 | 8 | 5 | 9 | 8 | 59 |
| Nodules | 19 (40) | 8 | 11 | 11 | 3 | 8 | 4 | 3 | 14 | 43 |
| Cavity | 17 (36) | 13 | 4 | 8 | 2 | 5 | 6 | 1 | 7 | 29 |
| Lobar volume decrease | 17 (36) | 15 | 2 | 1 | 13 | 2 | 0 | 2 | 2 | 20 |
| Emphysema | 15 (32) | 6 | 9 | 5 | 7 | 8 | 5 | 8 | 12 | 45 |
| Mosaic perfusion | 6 (13) | 1 | 5 | 3 | 4 | 2 | 2 | 2 | 5 | 18 |
| Bullae | 5 (11) | 2 | 3 | 4 | 1 | 2 | 2 | 0 | 2 | 11 |
Note—MAC = Mycobacterium avium-intracellulare complex.
Of the various patterns of lung abnormalities, bronchiolitis and bronchiectasis were the two most extensive patterns of abnormality. Bronchiolitis was bilateral in 42 (89%) of the 47 patients with the abnormality and involved 207 lobes (73%) among a total of 282 lobes. Bronchiectasis was bilateral in 41 (89%) of 46 patients with the abnormality and involved 173 lobes (61%) among a total of 282 lobes.
Interobserver agreement for the extent of each pattern of abnormalities was good and statistically significant. The r values for the agreement on the extent of bronchiectasis, bronchiolitis, consolidation, and total lung abnormality were 0.665, 0.440, 0.369, and 0.786, respectively (p < 0.001, p = 0.002, p = 0.011, and p < 0.001, respectively; Spearman's correlation).
High-Resolution CT–Pulmonary Function Test Correlations
The relationship of CT scores and PFT results is shown in Table 3. The total CT score showed a significant correlation with RV/TLC (r = 0.572, p < 0.001), FEV1 (r = –0.426, p = 0.003), FVC (r = –0.360, p = 0.013), PEF (r = –0.352, p = 0.015), and FEF25–75% (r = –0.289, p = 0.049). The extent of bronchiolitis showed a positive correlation with RV/TLC (r = 0.508, p = 0.001) and a negative correlation with PEF (%) (r = –0.369, p = 0.011) and FVC (r = –0.295, p = 0.044). The extent of bronchiectasis showed a positive correlation with RV/TLC (r = 0.600, p < 0.001) and a negative correlation with FEV1 (r = –0.373, p = 0.010), FVC (r = –0.372, p = 0.011), and PEF (r = –0.316, p = 0.031) (Figs. 3A, 3B and 4A, 4B). The extent of consolidation showed a positive correlation with RV/TLC (r = 0.364, p = 0.025) and a negative correlation with PEF (r = –0.324, p = 0.026). The extent of bullae, mosaic perfusion, and lobar volume decrease did not show any significant correlation with any individual index of pulmonary function (Table 3).
| FVC | FEV1 | FEF25-75% | PEF | RV/TLC | ||||||
|---|---|---|---|---|---|---|---|---|---|---|
| CT Patterns | r | p | r | p | r | p | r | p | r | p |
| Bronchiolitis | -0.295 | 0.044 | -0.227 | 0.125 | -0.081 | 0.586 | -0.369 | 0.011 | 0.508 | 0.001 |
| Bronchiectasis | -0.372 | 0.011 | -0.373 | 0.010 | -0.207 | 0.163 | -0.316 | 0.031 | 0.600 | <0.001 |
| Consolidation | -0.262 | 0.075 | -0.041 | 0.783 | 0.088 | 0.557 | -0.324 | 0.026 | 0.364 | 0.025 |
| Nodules | -0.398 | 0.006 | -0.350 | 0.016 | -0.289 | 0.049 | -0.374 | 0.010 | 0.457 | 0.004 |
| Cavity | -0.486 | 0.001 | -0.442 | 0.002 | -0.190 | 0.202 | -0.314 | 0.031 | 0.388 | 0.016 |
| Emphysema | 0.034 | 0.822 | -0.446 | 0.002 | -0.513 | <0.001 | -0.206 | 0.165 | 0.066 | 0.692 |
| Total CT score | -0.360 | 0.013 | -0.426 | 0.003 | -0.289 | 0.049 | -0.352 | 0.015 | 0.572 | <0.001 |
Note—Data presented in boldface show positive correlation between CT score and pulmonary function test results. FVC = forced vital capacity, FEV1 = forced expiratory volume in 1 second, FEF25-75% = peak expiratory flow between 25% and 75% of forced vital capacity, PEF = peak expiratory flow, RV = residual volume, TLC = total lung capacity.
Discussion
To the best of our knowledge, using CT to score the extent of lung involvement in MAC pulmonary disease has not been attempted in a previous study. In this study, we modified the cystic fibrosis scoring system [9, 10] to estimate the extent of lung involvement of MAC pulmonary disease because the high-resolution CT scoring system in cystic fibrosis is reproducible and shows a good correlation with PFT results [8–14]. Furthermore, the nodular bronchiectatic form of MAC pulmonary disease manifests similar high-resolution CT findings, with cellular or inflammatory bronchiolitis and bronchiectasis being the predominant findings in MAC pulmonary disease just as in cystic fibrosis [2–7, 20].
In our study, the total extent of lung involvement in MAC pulmonary disease showed significant correlation with RV/TLC, FEV1, FVC, PEF, and FEF25–75%. These results suggest that the extent of lung involvement in MAC disease is significantly correlated with both restrictive and obstructive functional indexes. The extent of bronchiectasis was associated with derangement of FVC, FEV1, and PEF and an increased amount of RV, whereas the extent of cellular bronchiolitis was associated with derangement of FVC and PEF and an increased amount of RV.
The severity of pulmonary function abnormalities in airway obstruction is mainly based on FEV1. The degree of hyperinflation, which can be measured by RV/TLC, also parallels the severity of airway obstruction [21–23]. In our study, indexes of bronchiectasis, nodules, cavity, emphysema, and the total CT score showed a significant correlation with FEV1 derangement, and indexes of bronchiolitis, bronchiectasis, consolidation, nodules, cavity, and the total CT score showed a significant correlation with an increased amount of RV.
Because the findings of our study suggest that the high-resolution CT scoring of lung lesions has a significant correlation with the functional derangement in MAC pulmonary disease, high-resolution CT scoring will be useful for predicting functional deterioration in patients with MAC pulmonary disease. In addition, using this scoring system, one can objectively measure treatment response and assess the progression of the disease with or without treatment. Moreover, because the main CT findings of MAC pulmonary disease are irreversible changes of bronchiectasis, scoring lung involvement in patients with MAC pulmonary disease may enable one to predict the amount of irreversible lung damage, just as in patients with cystic fibrosis [8–14].
One may argue that PFTs rather than CT should be used as a follow-up study device once a significant correlation between CT scores and PFT results has been established. However, according to a study dealing with patients with cystic fibrosis [10], CT seems to have advantages over PFT results and clinical scoring systems in depicting pulmonary changes over time. Therefore, high-resolution CT, especially using a low-dose technique, may be more appropriate than PFTs for follow-up evaluation of patients with MAC pulmonary disease.
Our study has several limitations. First, in our study, the mean age of the 47 patients was 58 years, with the mean age of the 36 women being 56 years and that of the 11 men, 66 years. Thus, a mean age of 58 for our series seems to be rather young compared with those of other studies [3, 5, 6]. This may suggest a selection bias. Second, in our study, we characterized mild disease (score of 1) as occurring in up to five segments in many of the categories, which may be a rather generous use of the term “mild.” A 4-point scoring system (e.g., score of 1 as involvement of 1–3 segments; score of 2, 4–6 segments; score of 3, 7–9 segments; and score of 4, ≥ 10 segments) might be more powerful in scoring lung involvement of MAC pulmonary disease. Third, we did not obtain an expiratory CT study for the evaluation of mosaic perfusion areas. With expiratory CT, we could have assessed exactly the extent of airflow obstruction and air trapping (obstructive indexes of PFT) [24]. Last, two patients who were ex-smokers were included in our study population; in these patients, smoking might have caused morphologic abnormalities of the lungs independent of the parenchymal changes caused by MAC infection and made an additional alteration to the functional abnormalities.
In conclusion, we attempted to score the extent of lung involvement in MAC pulmonary disease by modifying the cystic fibrosis scoring system [9, 10]. Using this modified scoring system, we identified that the total CT score shows a significant correlation with FVC, FEV1, FEF25–75%, PEF, and RV/TLC. Therefore, CT scoring of pulmonary abnormalities using a modified cystic fibrosis scoring system shows a correlation with measures of functional deterioration and thus allows one to estimate the functional impairment in patients with MAC pulmonary disease. However, this is a preliminary study to show that our scoring system correlates with PFT results. Further studies, such as studies of the relationship between changes in serial high-resolution CT findings using our proposed scoring system and PFT changes, life-quality measurement, or mortality, need to be performed.
Footnotes
Address correspondence to K. S. Lee ([email protected]).
This study was supported by the SRC/ERC Program of MOST/KOSEF (R11-2002-103).
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Submitted: December 5, 2007
Accepted: May 1, 2008
First published: November 23, 2012
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