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Thoracic Imaging |
1 From the Departments of Radiology (T.H.H., G.H.P., P.W., C.J.H.) and Pediatrics (I.E., M.G., C.W.), University of Vienna, Waehringer Guertel 18-20, A-1090 Vienna, Austria, and the Department of Radiology, University of California, San Francisco, Calif (R.C.B.). From the 1994 RSNA scientific assembly. Received November 10, 1998; revision requested December 29; revision received March 8, 1999; accepted April 15. Supported in part by the Ludwig-Boltzmann-Institute for Radiologic Tumor Research. T.H.H. supported in part by a grant from the Max Kade Foundation. Address reprint requests to T.H.H. (e-mail: Thomas.Helbich @akhwien.ac.at).
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Abstract |
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MATERIALS AND METHODS: Pulmonary CT findings were assessed in 117 patients with cystic fibrosis, with cases classified according to three groups by age; 0–5 years, 6–16 years, and 17 years and older. Images were examined for specific abnormalities, and the severity and anatomic extent of each sign were used to generate a score. Scores in each category and the global score for each patient were correlated with pulmonary function test results, clinical status, serum immunoglobulin levels, and genotype, all obtained within 2 weeks of CT.
RESULTS: The most frequent individual CT abnormalities were bronchiectasis in 94 (80.3%), peribronchial wall thickening in 89 (76.1%), mosaic perfusion in 71 (63.9%), and mucous plugging in 56 (51.3%) patients. The percentage of patients with specific CT findings and the overall CT scores increased significantly (P < .05) with progressively increasing age groups. All CT findings and the overall CT scores correlated significantly (P < .05) with the pulmonary function test results, serum immunoglobulin levels, and clinical scores. No relationship was observed between genotype and CT scores.
CONCLUSION: Scoring of CT studies in patients with cystic fibrosis seems to offer a reliable way to monitor disease status and progression and may provide a reasonable tool to assess treatment interventions.
Index terms: Bronchi, CT, 60.1211 • Bronchiectasis, 60.26 • Children, respiratory system, 60.252 • Emphysema, pulmonary, 60.751 • Fibrosis, cystic, 60.252 • Lung, CT, 60.1211 • Lung, interstitial disease, 60.252, 60.26, 60.751, 60.756, 60.76
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Introduction |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Authors of numerous radiologic studies (16–22) have reported the diagnostic superiority of computed tomography (CT) over conventional chest radiography for the morphologic assessment of various lung diseases. Thin-section CT of the lung has been advocated for the diagnosis and follow-up of chronic lung diseases (16–21,23,24). Yet, despite the technical superiority of CT, chest radiography remains the primary imaging modality used by clinicians in the follow-up of patients with cystic fibrosis (1,2,4,12,16,17). CT typically is used as a supplemental modality when specific, fine anatomic details are necessary (16–18,24). Several investigative groups have suggested that routine CT evaluation of cystic fibrosis is potentially of great value, and CT scoring systems have been proposed (16–24). Reports on the use of CT scoring systems in patients with cystic fibrosis, however, have been limited to relatively small numbers of patients, and little attention has been focused on the influence of patient age on CT abnormalities (16,19,20,21,23).
In the current study, we evaluated an expanded CT-based scoring system in a population of 117 subjects and gave special focus to the influence of patient age. Patient scores based on specific anatomic abnormalities and overall scores based on all CT abnormalities were correlated with previously proposed nonimaging evaluation methods, including pulmonary function tests, clinical scores obtained by using the Shwachman-Kulczycki method (6), serum immunoglobulin levels, and genotype of cystic fibrosis.
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MATERIALS AND METHODS |
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Study evaluation included CT in all 117 patients, clinical examination with the Shwachman-Kulczycki scoring system (6) and immunoglobulin, or IgG, assays in 104 patients, pulmonary function test in 90 patients, and genotypic evaluation in 77 patients. All examinations of each patient were completed within 2 weeks. To assess the influence of age on disease status, patients were divided into three age groups: group 1 (age range, 0–5 years; mean age, 2.4 years ± 1.5; n = 20; seven girls, 13 boys), group 2 (age range, 6–16 years; mean age 9.4 years ± 3.1; n = 61; 31 girls, 30 boys), and group 3 (age range, 17 years and older; mean age, 22.1 years ± 4.1; n = 36; 19 women, 17 men).
CT Evaluation
Scanning was performed with either a TCT 900S (Toshiba, Tokyo, Japan) or Tomoscan SR 7000 (Philips, Best, The Netherlands) CT unit. CT studies consisted of scans of 2-mm-thick (Toshiba unit) or 1.5-mm-thick (Philips unit) sections at 10-mm intervals, extending from the lung apices to below the costophrenic angles and obtained with the use of a 350-mm field of view and a 512 x 512 reconstruction matrix. Examinations were performed at 137 kV and 250 mA (Toshiba unit) or 140 kV and 175 mA (Philips unit) with a 1-second scanning time. Images were reconstructed with a high-spatial- frequency algorithm and with window settings appropriate for assessment of pulmonary parenchyma (level, -450 and -700 HU; width, 1,500 and 1,000 HU). Scans at the level of the hilus were additionally reconstructed with window settings suitable for evaluation of the mediastinum (level, 35 HU; width, 400 HU). Six images were transferred to each 14 x 17-inch film hard copy.
CT images were acquired at suspended end-inspiratory volume in older children who could cooperate. In children unable to cooperate with breathing, images were obtained during quiet breathing. Scans were obtained with the patient in the supine position, and additional scans were obtained with the patient in the prone position when the reversibility of dependent areas of increased attenuation were assessed.
Morphologic Analysis of CT Studies
Two radiologists (T.H.H., G.H.P.) together reviewed the studies in random order and arrived at a consensus opinion. Both radiologists were blinded to the results of the clinical scores (Shwachman-Kulczycki scoring system), the immunoglobulin assay results, the pulmonary function test results, and the genotype. The radiologists determined the grade and the anatomic distribution of each morphologic sign listed in Table 1. The morphologic changes were scored with respect to severity and extent by using a modification of the system proposed by Bhalla and co-workers (19). As in the Bhalla scoring system, the severity and extent of bronchiectasis, peribronchial wall thickening, mucous plugging, sacculations, bullae, emphysema, and collapse or consolidation were evaluated.
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Pulmonary Function Tests
Pulmonary function tests included forced vital capacity, forced expiratory volume in the first second, and maximum expiratory flow at 50% and 25% of vital capacity. Changes were recorded in the form of a maximum expiratory flow volume curve according to standards of the American Thoracic Society (32). Thoracic gas volume and specific airway resistance were obtained by means of body plethysmography (Master Lab, Jäger, Germany) as described previously (33). Total lung capacity was calculated by adding residual volume and inspiratory vital capacity. The best of three efforts was used for calculations. Results were expressed as percentages of predicted values based on accepted reference standards (34).
Clinical and Laboratory Evaluations
Clinical status was scored by two pediatric pulmonologists (I.E., M.G.) in consensus by using a modified Shwachman-Kulczycki technique (6). This quantitative system determines the clinical severity of cystic fibrosis by scoring three parameters: general activity, physical examination of the thorax, and nutrition status. Each of these domains is scored from 5 (severely impaired) to 25 (normal), which results in a total score ranging from 25 (severe) to 75 (normal).
Serum immunoglobulin levels were determined by means of an automated nephelometric technique described by Ritchie et al (10). The predicted normal values based on age for each subject were obtained from standard tables (35).
Chromosomes were screened for the presence of a specific gene mutation, 
F508 (deletion of three base pairs at position 508, with loss of phenylalanine from the resultant protein production) (3). The mutations were analyzed by means of heteroduplex analysis (26) or polymerase chain reaction with allele-specific primes (27).
Statistical Analysis
Statistical analysis was performed with the SAS statistical software package (version 6.10; SAS Institute, Cary, NC). Results are expressed as the mean plus or minus SD. Means were compared by using one-way analysis of variance and the Duncan multiple range test for testing pairwise differences between groups (36). Comparisons of proportions were made with the 
2 test or the 2 test for trends; when small numbers invalidated the 2 approximation, the Fisher exact test was used (36). Multivariate analysis of variance was performed to evaluate the influence of the severity and extent of morphologic findings on the overall CT score in all three age groups. Furthermore, the partial correlation coefficient between the effects of the aging process on the severity and extent of lung CT abnormalities was calculated (36). A P value of less than .05 was regarded as statistically significant. Spearman rank correlation was performed to calculate the correlation between radiologic findings, pulmonary function test results, clinical scores, and serum immunoglobulin levels (36).
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RESULTS |
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In group 2 (6–16 years of age), 80% of the patients had bronchiectasis: 38% mild, 21% moderate, and 21% severe. Most of the bronchiectasis affected multiple bronchopulmonary segments—one to five in 12%, six to nine in 34%, and more than nine in 34%—and was evident up to the fifth generation bronchi in 54% and sixth generation bronchi in 16% of patients. Peribronchial wall thickening, usually mild, was seen in 77% of patients. Mosaic perfusion was observed in 60% of patients. Mucous plugging was present in 53% of patients but tended to be sparse and involve only a few segments. Lung collapse was demonstrated in 30% and emphysema in 14% of patients. All other findings were seen in less than 10% of patients. The overall CT score was 7.9 ± 4.9.
In group three (17 years and older), all patients had bronchiectasis: 8% mild, 31% moderate, and 61% severe. Of these patients, 80% showed involvement in more than 50% of bronchopulmonary segments. Bronchiectasis was evident up to the fifth generation bronchi in 33% and sixth generation bronchi in 61% of patients. Peribronchial wall thickening was observed in 94% of patients. Mosaic perfusion was seen in 70% of patients and involved multiple bronchopulmonary segments. Mucous plugging was present in 72%. Emphysema was demonstrated in 62%, sacculations or abscesses were demonstrated in 42%, lung collapse was demonstrated in 39%, and bullae were demonstrated in 33% of patients. The overall CT score was 14.1 ± 4.8.
A statistically significant score increase (P < .05) was observed for all CT abnormalities between each of the three age groups. These trends were further shown by the strong correlation between the age of the patient and the severity and extent of morphologic CT changes (r = 0.81 and r = 0.74, respectively; P = .001). The overall CT score was influenced more by the extent than by the severity of the morphologic findings. The stronger influence of the extent of the CT abnormalities was statistically significant for the primary effect (P < .001, F = 34.84, df = 2) and for the interactions (P < .001, F = 10.1, df = 2) in all three age groups.
Clinical and Functional Characteristics
Results of pulmonary function tests, clinical scanning, immunoglobulin assays, and genotype determination are summarized in Table 4. Pulmonary function test results confirmed a general pattern of obstructive lung disease with decreased expiratory volumes and flow rates and increased residual volumes in all patients. In general, pulmonary function tests could not demonstrate significant changes between groups 1 and 2. The overall Shwachman-Kulczycki clinical score was 61.7 ± 8.8. Of note, this clinical scoring system failed to indicate any progression between groups 1 and 2, with both age groups having almost the same mean score of 63. For both the pulmonary function tests and the Shwachman-Kulczycki scores, a statistically significant (P < .05) increase was observed for patients 17 years and older (group 3). The immunoglobulin levels were in a normal range in patients in groups 1 and 2 but were slightly elevated in group 3. The differences of the immunoglobulin levels between each group were statistically significant (P < .05). The genotypes were similar among all three age groups (P = .67).
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DISCUSSION |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Earlier CT studies (16,19–21) in patients with cystic fibrosis were performed primarily to demonstrate the spectrum of abnormalities visible at CT or to develop CT scoring systems. Limitations of earlier studies (16,19–21) include the use of selected and relatively small patient populations and the lack of clinical correlations. Consequently, clinicians at most cystic fibrosis centers have chosen not to incorporate CT in the routine treatment of their patients (16,17). Our study differs from previous efforts in that we have included a larger patient population, divided patients into age groups to assess the CT changes over time, and compared CT findings with pulmonary function test results, clinical scores, immunoglobulin levels, and chromosomal genotypes. The age range of all three study groups was deliberate because each group reflects different periods of life and treatment standards in patients with cystic fibrosis.
The most frequent morphologic CT abnormalities in our study were bronchiectasis (80%), peribronchial wall thickening (76%), mosaic perfusion (64%), and mucous plugging (51%). Attention should be directed to their presence, severity, and extent. These most common morphologic CT abnormalities increased in extent and severity with increasing patient age and correlated significantly with worsening of nonmorphologic parameters of pulmonary status. The continuous advance of these CT signs with the duration of the disease can been explained on the basis of recurrent pulmonary infections and chronic inflammation (1–3,17,23,37). Thus, prolonged mucous plugging of airways has been linked to progressive bronchial damage, with resultant bronchial wall thickening and bronchiectasis (1–3,17,23,37).
Early detection of mosaic perfusion, a CT finding added to our expanded scoring system, is important because early treatment can reduce its severity (23, 24,29–31). Mosaic perfusion is one of the first signs of small airway disease and is related to regional constrictive bronchiolitis, a common feature of cystic fibrosis, although mosaic perfusion can also be a sign of pulmonary embolism, both acute and chronic (24,28–31). The frequent CT observation (64%) in our patients and the age-related increase reflect the importance of the incorporation of this finding into our CT scoring system. The relatively high occurrence of mosaic perfusion in the youngest patient population (50%) is expected and explained by the relatively increased airway compliance and hence early airway closure of the younger patient, even in normal lung (24,29,30). Conversely, increased disruption of airways, as well as increased severity and extent of bronchiectasis and peribronchial wall thickening, might explain the lack of prevalence of mosaic perfusion in older patients (group 2, 60%; group 3, 70%) (24,29,30).
In the youngest patient population (group 1), six patients younger than 3.5 years were unable to cooperate with breathing. Thus, mosaic perfusion could be confused with normal lung or air trapping, depending on the lung volume during each CT scan. In all these patients, however, CT scans were obtained during quiet breathing to minimize this problem. On the other hand, none of these patients had pulmonary abnormalities at CT (0 score). Thus, there is a high probability that these patients had no signs of mosaic perfusion.
Clinicians are in favor of using nonmorphologic parameters in the evaluation and follow-up of patients with cystic fibrosis (1–5,12). A comparison of those parameters with our proposed CT scoring system seems, therefore, to be appropriate. The overall CT score increased significantly with the duration of the disease and correlated significantly with increasing abnormality of pulmonary functions test results, decrease of clinical scores, and changes in immunoglobulin levels. Our expanded CT score, therefore, seems to predict accurately the clinical severity of the disease. The less strong correlation of each individual CT finding with the nonmorphologic parameters, on the other hand, emphasizes the importance of such a global CT scoring system. Thus, the evaluation and evolution of pulmonary changes in patients with cystic fibrosis should no longer be confined to a small number of CT findings (20,21).
Pulmonary function testing showed no significant difference between groups 1 and 2, whereas CT demonstrated such differences. Thus, the proposed CT scoring system seems to represent airway disease more accurately. CT signs associated with hyperinflation (eg, emphysema, mosaic perfusion, bullae) correlated poorly with the functional parameters. Thus, further studies should include gas transfer measurements, such as diffusing capacity of lung for carbon monoxide, or DLCO, and adjusted for alveolar volume, or KCO, as they most strongly relate to the signs of hyperinflation at CT (31).
The Shwachman-Kulczycki score determines the clinical severity of cystic fibrosis by means of three parameters: general activity, physical examination of the thorax, and nutrition status (7). Similar to findings in a previous study (4), the Shwachman-Kulczycki score decreased significantly with patient age and correlated significantly with our proposed CT scoring system. The lack of a stronger correlation might be explained on the basis of the parameters of the Shwachman-Kulczycki score, which do not accurately reflect the pulmonary status.
Similar to the changes in the CT morphologic abnormalities, immunoglobulin G levels represent pulmonary progression in patients with cystic fibrosis (13). Thus, patients with hypogammaglobulinemia G have milder lung disease and a better prognosis than patients with normal or elevated immunoglobulin G levels (13). On the basis of the strong correlation of the immunoglobulin G levels and the overall CT score obtained in our study, both the immunoglobulin G levels and the CT scores may be used as predictors of the progression of the disease.
As a final result of the comparison of the clinical and the CT data, homozygous patients with cystic fibrosis did not differ from heterozygous patients in their CT findings. Thus, in agreement with previous studies (14,15), for none of the genotypes studied can predictions be made about the severity and extent of pulmonary disease.
Chest radiographs are essential in the evaluation of the pulmonary status in patients with cystic fibrosis; thus, their exclusion in our study may be seen as a limitation. Authors of previous studies (16–22), however, have recognized a superiority of CT over conventional chest radiography in patients with cystic fibrosis. Further comparative studies are necessary to confirm the use, advantages, and costs of CT over standard chest radiography in assessing clinical progression and response to therapy. The subjectivity of the scoring assignments in our patients may be seen as another limitation. On the other hand, it would be impossible to conceal the age completely when dealing with both adults and pediatric age groups because the age of the patient correlates with the scan appearance to a great extent.
Enlarged lymph nodes and central pulmonary vessels may indicate severity of disease in cystic fibrosis and are identified much better on CT scans than on chest radiographs (2). We did not choose to evaluate their presence, which may be another limitation. For this purpose, especially if follow-up studies are planned, helical CT of the thorax is more appropriate because CT studies with 10-mm intervals cannot accurately reflect the status of lymph nodes and central pulmonary vessels.
Recent advances in the therapy of cystic fibrosis have improved the survival rate (1–5). Minimization of radiation exposure should be considered, as these patients may have numerous CT and radiologic procedures for the long term follow-up of lung disease. Thus, low-dose CT techniques may be useful to minimize radiation dose by at least 40%–50% (38,39). These techniques demonstrated the same pulmonary parenchymal resolution as the high-dose techniques (38).
The proposed expanded CT scoring system provides a sensitive and useful method of monitoring disease status and progression in patients with cystic fibrosis. It seems that CT may be more sensitive than the previously proposed nonmorphologic parameters. Thus, the CT scoring system could be reasonably incorporated into the routine follow-up evaluation of this patient population. Before CT can be advocated as a useful follow-up modality, however, its effect on clinical management and patient outcome should be proved. In addition, the optimal time window for follow-up studies should be determined.
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Acknowledgments |
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Footnotes |
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