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Original Report |
1
Department of Radiology, Vancouver Hospital & Health Sciences Centre,
University of British Columbia, 855 W. 12th Ave., Vancouver, B.C., V5Z 1M9
Canada.
2
Department of Radiology, Lucile Salter Packard Children's Hospital, Stanford
University, 725 Welch Rd., Palo Alto, CA 94304.
3
Department of Radiology, Royal Brompton National Heart and Lung Hospital,
Sydney St., London, SW3 6NP England.
Received June 11, 1999;
accepted after revision September 29, 1999.
Address correspondence to N. L. Müller.
Abstract
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CONCLUSION. The cardinal CT features of bronchopulmonary dysplasia survivors include multifocal areas of reduced lung attenuation and perfusion, bronchial wall thickening, and decreased bronchus-to—pulmonary artery diameter ratios.
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We reviewed the CT appearances of adult survivors of bronchopulmonary dysplasia.
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Ten control subjects participated in the study (five women, five men; age range, 18-30 years; mean age, 26 years). All control subjects were healthy nonsmokers without any known history of lung disease. In particular, the control subjects had no known history of asthma or recurrent chest infection. Six control subjects were prospectively recruited as part of another study. Informed consent was obtained from these six subjects. CT for the remaining subjects was performed as part of an evaluation for spontaneous pneumothorax (n = 2) or suspected metastatic disease (n = 2). All control subjects were retrospectively selected to match the bronchopulmonary dysplasia patients in terms of age and sex.
CT Protocol
CT was performed on an electron beam Imatron C-100 scanner (Imatron, San
Francisco, CA) (n = 10) or a GE 9800 scanner (General Electric
Medical Systems, Milwaukee, WI) (n = 5). In the patients with
bronchopulmonary dysplasia, 1- to 1.5-mm collimation sections were obtained at
three levels: the aortic arch, the tracheal carina, and the level of the
inferior pulmonary veins. In the 10 control subjects, 1- to 1.5-mm collimation
sections were obtained at 10-mm intervals. Images were obtained with window
settings appropriate for viewing the lungs (window width, 800-1500 H; window
level, -850 to -600 H). CT scans were independently interpreted by two
radiologists. Interobserver agreement was determined using the kappa
statistic.
CT scans were analyzed in random order at a lobar level (the lingula was considered a separate lobe) for the presence and extent of areas of reduced lung attenuation, bronchial wall thickening and dilatation, bullae, and linear opacities. The presence and extent of associated findings such as architectural distortion, nodules, and pleural effusion were also assessed. Areas of reduced lung attenuation were categorized according to the involvement of a small focal area corresponding to less than three adjacent secondary pulmonary lobules; the involvement of an area greater than three adjacent secondary pulmonary lobules but less than a pulmonary segment; or the involvement of an area equal to or greater than a pulmonary segment. The diagnosis of bronchial wall thickening was based on subjective assessment. Bullae were defined as round focal air spaces of 1 cm or more in diameter, demarcated by a thin wall.
The external diameters of the bronchus and the accompanying pulmonary artery were measured using manual Vernier calipers (Scienceware, Pequannock, NJ) on an image magnified by a factor of 5. At least four sets of measurements were obtained in each patient. The external diameters of the bronchus and pulmonary artery were measured only when they were perpendicular to the cross-sectional plane of the CT image. Location of the measurement site was determined by consensus. The actual measurement were made by one radiologist. The short axes of the bronchus and the accompanying pulmonary artery were measured and individual bronchus-to—pulmonary artery diameter ratios were determined. For each patient, a range of bronchoarterial diameter ratios and a mean ratio were determined for all bronchi and pulmonary arteries that were measured in both lungs.
Pulmonary Function Tests
Pulmonary function tests were performed within 1 day of the CT examination
in all five patients with bronchopulmonary dysplasia. Results were expressed
as a percentage of values predicted from the patient's age, sex, height, and
weight. The following characteristics were recorded: forced vital capacity,
forced expiratory volume in 1 sec, total lung capacity, residual volume, ratio
of residual volume to total lung capacity, and maximum expiratory flow rate at
50% of vital capacity. Indexes of gas transfer (corrected for hemoglobin
concentration) were obtained using the carbon monoxide single-breath
technique.
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Extensive bilateral areas of reduced lung attenuation were present in all five patients with bronchopulmonary dysplasia (Fig. 1A,1B). These areas were always associated with a decrease in the size and number of vessels. In all patients, the total lung involvement with areas of reduced lung attenuation was larger than a pulmonary segment. Focal areas of low attenuation (involving fewer than three adjacent secondary pulmonary lobules) were observed in six of 10 control subjects.
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Bronchial wall thickening was observed in all patients with bronchopulmonary dysplasia (Fig. 2A,2B). Thickening was bilateral in all patients and either diffuse (n = 4) or primarily involved the lower zones (n = 1). A total of 42 bronchoarterial diameter ratios were measured in the 10 control subjects, and 23 bronchoarterial diameter ratios were measured in the five patients with bronchopulmonary dysplasia. The mean bronchusto—pulmonary artery diameter ratio was 0.91 ± 0.08 (range, 0.85-1.1) in healthy subjects and 0.45 ± 0.04 (range, 0.38-0.49; p < 0.001) in patients with bronchopulmonary dysplasia.
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A few localized linear opacities were observed in three of the five patients with bronchopulmonary dysplasia (Fig. 1A,1B), and multiple bullae were observed in two. When bullae were present, they were equally profuse in the upper and lower lobes.
The observers were in complete agreement for the interpretation of areas of
reduced lung attenuation, bullae, and linear opacities in patients with
bronchopulmonary dysplasia. The observers were in moderate agreement for the
interpretation of bronchial wall thickening (
= 0.59).
Pulmonary function tests revealed air trapping (increased residual volume to total lung capacity ratio) in all patients with bronchopulmonary dysplasia (range of residual volume to total lung capacity ratios, 120-200% of predicted value) (Table 1). Hyperinflation was present in two patients (total lung capacity, 135% and 139% of predicted value); the other three patients had normal total lung capacity (96%, 96%, and 116% of predicted value). Four patients had evidence of air-flow obstruction as revealed by a reduction of maximal expiratory flow at 50% of vital capacity to 26%, 29%, 42%, and 43% of predicted value; in the remaining patient, the maximal expiratory flow at 50% of vital capacity was normal (83% of predicted value). In all patients, the singlebreath carbon monoxide diffusing capacity was normal (range, 107-153% of predicted value).
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Limited information is available on the CT appearances of survivors of bronchopulmonary dysplasia [7]. Oppenheim et al. [7] reviewed the CT findings of 23 infants and children (age range, 2 months-13 years; mean age, 4 years) with bronchopulmonary dysplasia. Common CT findings included multifocal hyperlucent areas (observed in 86% of patients), linear opacities (observed in 95% of patients), and triangular subpleural opacities (observed in all patients). Bronchiectasis and bullae were not observed. In four patients with chest radiographs with normal findings, CT scans with abnormal findings were also obtained.
In our study, multifocal areas of reduced lung attenuation were the main findings on CT and were present in all five patients with bronchopulmonary dysplasia. In all instances, the areas of reduced lung attenuation involved areas larger than a pulmonary segment compared with the less extensive areas (less than three adjacent pulmonary lobules) observed in healthy control subjects.
Typical histologic features of bronchopulmonary dysplasia include marked airway changes and the involvement of the lung parenchyma and pulmonary arterioles [9]. Alveolar septal fibrosis is the hallmark of parenchymal injury in bronchopulmonary dysplasia with alternating areas of underexpansion and regions of hyperinflation and emphysema [9]. Lesions are often unevenly distributed throughout the lung. On the basis of these histopathologic findings, it has been postulated that the multifocal areas of reduced lung attenuation on CT might reflect obstructive emphysema caused by small airways destruction with altered ventilation [7].
Husain et al. [10] recently compared the autopsy findings of 22 children with bronchopulmonary dysplasia with those of 15 agematched control subjects. The researchers found that there was partial to complete arrest in acinar development in all bronchopulmonary dysplasia patients after birth. It is conceivable that the decreased bronchial diameter seen in the current study and the arrested acinar development shown by Husain et al. may contribute to the areas of decreased attenuation noted on high-resolution CT.
In the adult patients with bronchopulmonary dysplasia, the bronchoarterial diameter ratios were all less than 0.5, compared with ratios of 0.85-1.1 for healthy control subjects. At the levels chosen for bronchoarterial diameter ratios, the pulmonary artery diameters in bronchopulmonary dysplasia patients were no larger than those measured in the control subjects. Therefore, the decreased bronchoarterial diameter ratios reflect decreased bronchial diameters rather than increased pulmonary artery diameters. These CT findings are not surprising given the typical histologic airway changes observed in bronchopulmonary dysplasia: marked squamous metaplasia of large and small airways, peribronchial and peribronchiolar fibrosis, obliterating fibroproliferative bronchiolitis, and prominent hypertrophy of peribronchiolar smooth muscle [9].
In our study, pulmonary function abnormalities consisted of airway obstruction and air-trapping. Airway obstruction, present in 80% (4/5) of our patients, was manifested by decreases in forced expiratory volume in 1 sec and maximum expiratory flow velocity at 50% of vital capacity. Air-trapping was observed in all patients with bronchopulmonary dysplasia. Northway et al. [4] found similar patterns of pulmonary dysfunction in 68% of adolescents and young adults with bronchopulmonary dysplasia in infancy, consisting of airway obstruction, airway hyperactivity, and air-trapping. These researchers postulated that the reduction of airway growth during the rapid postnatal phase of lung growth might contribute to a disproportionate undergrowth of the luminal diameter of the airways and result in a persistent increase in airway resistance.
In summary, we reviewed the CT scans of five adult survivors of bronchopulmonary dysplasia. The cardinal signs of this disease included a mixed pattern of multifocal areas of reduced lung attenuation, bronchial wall thickening, and inverse bronchopulmonary artery diameter ratios.
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