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1 Department of Radiology, Teikyo University School of Medicine, Ichihara
Hospital, 3426-3, Anesaki Ichihara Chiba 299-0111, Japan.
2 Present address: Department of Diagnostic Radiology, Fujisawa City Hospital,
2-6-1, Fujisawa, Fujisawa-shi Kanagawa 251-8550, Japan.
Received June 7, 2002;
accepted after revision August 6, 2002.
Address correspondence to S. Matsuoka.
Abstract
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SUBJECTS AND METHODS. High-resolution CT was performed prospectively in 85 subjects without cardiopulmonary disease. The subjects were divided into three groups according to age: 29 subjects were 21-40 years old; 29 subjects, 41-64 years old; and 27 subjects, 65 years or older. Both bronchoarterial ratios, defined as the diameter of the bronchial lumen divided by the diameter of its accompanying artery, and the T/D ratio, defined as wall thickness (T) divided by the total diameter of the bronchus (D), were measured at the segmental and subsegmental levels of the apical and posterior basal segments. Each calculated ratio was evaluated according to age and smoking status.
RESULTS. Significant correlation was found between the bronchoarterial ratio and age (r = 0.768, p < 0.0001), with the bronchoarterial ratio increasing with age and exceeding 1 in 41% of subjects older than 65 years. No significant correlation was seen between the T/D ratio and age. No significant differences in bronchoarterial ratio and T/D ratio were seen between smokers and nonsmokers in subjects overall; but in the elderly group, the T/D ratio was significantly higher in smokers than in nonsmokers (p = 0.021).
CONCLUSION. The bronchoarterial ratio is influenced by aging. The normal bronchoarterial ratio in a substantial number of subjects older than 65 years overlaps with the ratio considered to represent bronchiectasis. Thus, when this ratio is used for the quantitative analysis of pulmonary and cardiovascular disease, the influence of age should be considered.
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In most cases, bronchiectasis is considered to be present when the internal diameter of a bronchus is greater than the diameter of the adjacent pulmonary artery—that is, when the bronchoarterial ratio is greater than 1 [13]. Although an increased bronchoarterial ratio is typical in bronchiectasis, a bronchoarterial ratio greater than 1 does not always indicate the presence of bronchiectasis. Lynch et al. [1] showed that 26% of bronchi in healthy subjects have an internal diameter greater than that of adjacent pulmonary arteries. Kim et al. [9] used high-resolution CT to examine the arterial and outer bronchial diameter ratio in patients who did not have cardiopulmonary disease and found a wide range of ratios. Factors that may affect these variations in normal bronchoarterial ratios have not been clarified.
Kim et al. [14] recently reported that the normal bronchoarterial ratio increases and bronchial wall thickness decreases with altitude; they speculated that these findings are related to hypoxic bronchodilatation and vasoconstriction. Aging and smoking cause changes in the structure of the lung, and mild hypoxia is relatively common in the elderly [15,16,17]. We hypothesized that aging and smoking might affect the bronchoarterial ratio and bronchial wall thickness.
The purpose of this study was to evaluate whether the bronchoarterial ratio and bronchial wall thickness were related to age and smoking in asymptomatic healthy subjects.
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High-Resolution CT Technique
High-resolution CT scans were obtained with a W3000AD scanner (Hitachi,
Tokyo, Japan) using a thin-section (1-mm collimation) technique, 120 kVp, 175
mA, 1-sec scanning time, and a high-spatial-frequency (bone) reconstruction
algorithm. All images were obtained without injection of contrast material and
with the subject in deep inspiration and in the supine position. In the apical
segment and the posterior basal segment, we obtained three CT sections at
10-mm intervals from 1 cm below the superior margin of the aortic arch, and an
additional three sections were obtained from 4 cm above the top of the
diaphragm, which resulted in six sections per subject. The images were viewed
at a window level of -450 H and a window width of 1500 H. The window level of
-450 H has been shown to be the best level for accurate measurement of
bronchial diameters and wall thickness
[18,
19]. A window width of 1500 H
was used because narrower width causes less than optimal visualization of
anatomic landmarks at the -450 H level
[19].
Quantitative CT Measurements
The maximum and minimum diameters of the pulmonary artery, the luminal
diameter (L) of the bronchus, and the bronchial wall thickness
(T), magnified 1.5-1.8 times, were measured using electronic
calipers. Measurements were made by a single observer in a blinded fashion.
All measurements were made five times, and the mean values were recorded.
Images containing segmental and subsegmental bronchi with internal diameters
of 2 mm or larger seen in a cross-section of the right apical and right
posterior basal segments were selected by a consensus interpretation of two
radiologists. These sites were chosen because they are more convenient for
obtaining a tangential view of the bronchus and artery. Only the right lung
was evaluated, because no difference exists between the right and left lungs
in bronchoarterial ratio or wall thickening
[9,
14], and transmitted cardiac
motion artifacts may obscure detail in the left lower lobe
[20].
In each segment, the following ratios were calculated: bronchoarterial ratio (defined as L divided by the diameter of its accompanying arteries) and T/D ratio (defined as T divided by the total diameter of the bronchus [D], D = L + 2T). For each subject, bronchoarterial ratios and T/D ratios were obtained at each scanning level. The mean bronchoarterial ratio and T/D ratio were calculated in each individual, and the mean values of those ratios at different segments were obtained.
Obliquity was calculated by dividing the largest diameter of the bronchus and arteries by the smallest diameter. Bronchi and arteries with an obliquity greater than 1.5 were excluded from the analysis. To minimize error and optimize consistency of measurement, we used only the short-axis diameters of the bronchi and arteries for calculation of the bronchoarterial and T/D ratios.
Smoking
Subjects were divided according to their smoking habit: 40 were current or
former smokers and 45 were lifetime nonsmokers. The smoking habit of the
subjects was quantified as the number of pack-years smoked, where 1 pack-year
= 20 cigarettes daily for 1 year
[21].
Statistical Analysis
All statistical analyses were performed using StatView 5.0 software (SAS
Institute, Cary, NC). Data are expressed as mean ± standard deviation.
Linear regression analysis was used to evaluate the relationship between age
and calculated ratios. Comparison of measured ratios among the three groups
classified by age was performed using a one-way analysis of variance, with
multiple comparisons determined by the Scheffé test. Each measured
ratio in the apical segment and the posterior basal segment was compared using
the Student's t test. Comparison of measured ratios between smokers
and nonsmokers was made using the Student's t test. For all
statistical analyses, a p value of less than 0.05 was considered
significant.
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We obtained 422 T/D ratios. The mean T/D ratio for all subjects was 0.200 ± 0.015 (range, 0.171-0.227). No significant correlation was seen between the T/D ratio and age (r = 0.169, p = 0.121) (Fig. 4). The mean T/D ratio in each group was 0.203 ± 0.013 in group A, 0.199 ± 0.017 in group B, and 0.197 ± 0.014 in group C. No significant differences were found in T/D ratios among the three groups (p = 0.275) (Table 1). The T/D ratios did not show statistically significant differences between the apical segmental bronchi of the upper lobes and the posterior basal segmental bronchi of the lower lobes (p = 0.432) (Table 3).
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Table 4 shows each measured ratio in the smoking and nonsmoking groups. The mean number of pack-years smoked was significantly greater in group C than in groups A and B (p < 0.05). For all subjects, no significant difference was found in bronchoarterial ratios between smokers and nonsmokers (p = 0.791). The mean T/D ratio in smokers was 0.203 ± 0.014 versus 0.197 ± 0.015 in nonsmokers. Despite the lack of statistical significance (p = 0.114), the T/D ratio tended to be higher in smokers. In each group classified by age, no significant difference was noted in the mean bronchoarterial ratio between smokers and nonsmokers. Similarly, the mean T/D ratio did not show a significant difference between smokers and nonsmokers in group A versus group B. Conversely, in group C, the mean T/D ratio was 0.205 ± 0.012 in smokers and 0.191 ± 0.014 in nonsmokers. Smokers had a significantly greater T/D ratio than nonsmokers in this elderly group (p = 0.021).
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Physiologic changes in respiratory function associated with aging are well known. Arterial oxygen pressure decreases with age, and mild hypoxia is relatively common in the elderly [15,16,17]. Herold et al. [22] and Wetzel et al. [23] showed that hypoxia induces pulmonary vasoconstriction and bronchial dilatation in animal experiments. Furthermore, Kim et al. [14] found that nine (53%) of 17 normal subjects living at an altitude of 1600 m had at least one bronchus equal to or larger than the adjacent pulmonary artery, as compared with two (12.5%) of 16 individuals living at sea level. In their study, the mean bronchoarterial ratio was 0.76 at an altitude of 1600 m, which was similar to the value in elderly asymptomatic subjects in our study. Therefore, a possible reason for the increase in the bronchoarterial ratio with aging is related to hypoxic bronchodilatation and vasoconstriction.
With aging, morphologic changes of the lung occur that include increased alveolar duct air; decreased complexity of the alveolar surface or surface-to-volume ratio; loss of alveolar wall tissue, elastic tissue, and bronchiolar muscle; and increased frequency of emphysema [24]. Radiographically, the relation between aging and morphologic changes of the lung has also been investigated. Lee et al. [25] reported that the frequency of air trapping on high-resolution CT of the lung increases with age, and its severity increases with age. Air trapping is induced from occlusion or narrowing of the airway. Lee et al. suggested that occlusion or a luminal narrowing of the airway related to aging might occur at the lobular bronchiole level. Meanwhile, Hansell et al. [26] showed a clear relationship between the extent of bronchiectasis and the attenuation values on CT scans, which suggests that involvement of the small airways is an integral part of bronchiectasis. Although the relationship of the involvement of the small airways to the development of bronchodilatation has not yet been clearly established, these reports provide some support for a relationship between bronchodilatation and age. That relationship might be another possible reason for the increases in the bronchoarterial ratio that occur with age.
Wojtowicz [6] used chest tomography to investigate the relationship between the diameter of the pulmonary artery and that of the bronchus lumen in healthy subjects. Wojtowicz concluded that the bronchoarterial ratio is independent of age. Although Wojtowicz divided the subjects into four groups according to age, unfortunately one group consisted of all subjects older than 40 years. Therefore, the failure to find a correlation between the bronchoarterial ratio and aging might be due to insufficient evaluation for the elderly subjects. In our study, the bronchoarterial ratio exceeded 1 in 41% of healthy subjects older than 65 years. Bronchiectasis is usually considered to be present when the bronchoarterial ratio is greater than 1; therefore, the normal bronchoarterial ratio in a substantial number of subjects older than 65 years overlaps with the ratio considered to represent bronchiectasis.
Most previous reports using high-resolution CT [4, 14] and histologic assessments [7] to measure the bronchoarterial ratio did not show a significant difference between sites in the lung. In our study, bronchoarterial ratios did not show statistically significant differences between the apical segment and the posterior basal segment. Conversely, Kim et al. [9] evaluated the normal values of the arterial—bronchial ratio, defined as the outer diameter of the artery divided by the outer diameter of its accompanying bronchus, and found statistically significant differences between segments and lobes. Choe et al. [10] also reported that the arterial—bronchial ratio was slightly different in each lobe in healthy controls. The interpretation of these findings is difficult because of discrepancies among the reports, but the discrepancies might be related to regional differences in pulmonary circulation affected by gravity and changes in body position. When an individual is in a supine position, increased blood flow to the dependent lung leads to a decrease in the bronchoarterial ratio [8]. However, measurements of the pulmonary arteries and bronchi are best carried out in a cross-sectional area. Pulmonary arteries and bronchi in more anterior or posterior positions tend to lie in the oblique plane, and their accurate evaluation is difficult. Hence, it is possible that the selection of bronchi and pulmonary arteries used for measurements in these studies accounted for the discrepancies in the findings.
Awadh et al. [5] reported a mean T/D ratio in normal control subjects of 0.21, which is similar to the mean ratio of 0.20 in our study. The T/D ratio showed no significant correlation with aging. However, Kim et al. [14] reported that bronchial wall thickness in healthy subjects living at an altitude of 1600 m was thinner than in subjects living at sea level; this finding was presumed to be the result of bronchial dilatation. The bronchoarterial ratio in our elderly subjects resembles the ratio in subjects who were living at high altitudes in the report of Kim et al. If hypoxia alone causes the decrease in bronchial wall thickness, the T/D ratio should decrease with aging even in our results. Nevertheless, we could not statistically recognize the thinning of the bronchial wall with aging. This discrepancy might be partially the result of different methodology. Kim et al. measured the dimension of bronchial wall thickness directly without standardization of airway size. Although precise definitions of bronchial wall thickness have been proposed by several investigators, generally accepted criteria for determining abnormal bronchial wall thickness have yet to be established.
Cigarette smoking is the major risk factor for the development of chronic obstructive pulmonary disease. The concept that the site responsible for this airflow limitation in smokers is the peripheral airway is well established [27]. In addition, the large airways are also affected by an inflammatory process in smokers [28, 29]. Recently, high-resolution CT analyses of airway dimensions in smokers were reported [29,30,31], and abnormal bronchial wall thickening was observed with a significantly greater frequency in smokers than in nonsmokers. However, in our study, bronchial wall thickening in smokers was found only in the group of elderly subjects; results in the overall subject group showed no statistically significant difference in bronchial wall thickness between smokers and nonsmokers. The discrepancy between our data and that of previous reports may be the result of subject selection. Previous investigators included subjects with respiratory symptoms, whereas none of our subjects had respiratory symptoms.
Nakano et al. [29] evaluated airway wall dimensions in the cartilaginous airways of smokers. Those authors found that airway wall thickness was greater as the forced expiratory volume in 1 sec (percentage of predicted) decreased, and their data suggested that the airway wall is thicker in smokers who have more severe airflow obstruction. Although we did not perform pulmonary function tests, our subjects had no clinical pulmonary symptoms; at least, no subject with severe airway obstruction was included in our study. Nevertheless, we cannot explain why the bronchial wall was thicker in smokers than in nonsmokers only in the elderly group. The smokers in the group of the elderly subjects had a significantly higher smoking index. However, previous studies have shown that the smoking index is not related to the morphometric measures of airway dimensions [29, 32]. Alternatively, the findings of bronchial wall thickness in the elderly smoker might be related to the synergistic effect between aging and smoking.
Undoubtedly, most of our older subjects had spent many years in an industrial environment, and it was hard to differentiate between the influence of age and the influence of atmospheric pollution. Souza et al. [33] evaluated the potential association between long-term exposure to air pollution and histopathologic evidence of damage to the lung. They found inflammation and bronchial wall thickness with high pollution exposure were quite strong even after controlling for individual differences in age, sex, and level of cigarette smoking. Although several hypotheses can be suggested to explain our results, further investigation is necessary.
Our study has several limitations. We did not perform pulmonary function tests on our subjects. Although pulmonary function declines with age, individual variability cannot be disregarded. The possibility that some subjects did not have age-appropriate pulmonary function cannot be excluded. In addition, our criteria for choosing asymptomatic subjects may not have been strict enough. For example, a subject may have had a history of pulmonary disease, such as an infectious disease, that was not reported.
In conclusion, our results indicate that the bronchoarterial ratio increases with age. Although the bronchoarterial ratio has previously been proposed as a useful parameter for evaluating pulmonary and cardiovascular disease, the influence of aging should be considered. In the meantime, the morphometric changes associated with aging are not clearly seen on measurements of bronchial wall thickness. However, in elderly smokers bronchial wall thickening is found even in the absence of respiratory symptoms.
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