Published online before print October 26, 2005, 10.1148/radiol.2373041141
(Radiology 2005;237:1091-1096.)
© RSNA, 2005
Interlobular Septal Thickening in Idiopathic Bronchiectasis: A Thin-Section CT Study of 94 Patients1
Naomi A. Sibtain, MRCP, FRCR,
Masuo Ujita, MD,
Robert Wilson, MD, FRCP,
Athol U. Wells, MD, FRACP and
David M. Hansell, MD, FRCP, FRCR
1 From the Departments of Radiology (N.A.S., M.U., D.M.H.) and Respiratory Medicine (R.W.) and Interstitial Lung Disease Unit (A.U.W.), Royal Brompton Hospital, Sydney St, London SW3 6NP, England. Received June 30, 2004; revision requested August 19; revision received January 4, 2005; accepted February 3.
Address correspondence to D.M.H. (e-mail: d.hansell{at}rbh.nthames.nhs.uk).
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ABSTRACT
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PURPOSE: To retrospectively establish the prevalence of interlobular septal thickening at thin-section computed tomography (CT) in patients with bronchiectasis and to retrospectively examine the relationship between septal thickening and various CT features of bronchiectasis and functional parameters.
MATERIALS AND METHODS: Institutional review board approval or informed consent are not required for such a retrospective study. Thin-section CT scans of 94 patients (29 men, 65 women; age range, 18–82 years) with idiopathic bronchiectasis confirmed at thin-section CT and without any history or condition that causes bronchiectasis were assessed independently by two observers. The presence and signs of bronchiectasis, extent and distribution of septal thickening at global and lobar levels, and presence of emphysema were recorded. Univariate and multiple regression analyses were used to identify relationships between individual parameters of bronchiectasis, the extent of septal thickening, and functional indices.
RESULTS: Interlobular septal thickening was present in 56 (60%) of 94 patients with idiopathic bronchiectasis, excluding those with trivial septal thickening (34 of 94, 36%). At a lobar level, 69% (514 of 748) of lobes with bronchiectasis had septal thickening. There was strong correlation between the extent of septal thickening and the extent (r = 0.61, P < .001) and severity (r = 0.54, P < .001) of bronchiectasis. Stepwise regression analysis showed a relationship between the extent of septal thickening and the extent of bronchiectasis (P < .001). Septal thickening was not linked to functional indices of obstruction or restriction.
CONCLUSION: At thin-section CT, interlobular septal thickening is a frequent finding in patients with idiopathic bronchiectasis.
© RSNA, 2005
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INTRODUCTION
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In many diffuse lung diseases, particularly those with lymphatic or perilymphatic involvement, thickening of interlobular septa is a frequent finding at thin-section computed tomography (CT) (1,2). There is little in the histopathology literature about the state of the interstitium, and in particular the interlobular septum, in patients with bronchiectasis (3). Thickened interlobular septum is not an expected feature in most diseases of the airways, although there are theoretical reasons why thickened interlobular septa may be present in patients with bronchiectasis. We have observed thickening of interlobular septa on thin-section CT scans in several patients with bronchiectasis. Thus, the purposes of our study were to retrospectively establish the prevalence of interlobular septal thickening at thin-section CT in patients with bronchiectasis and to retrospectively examine the relationship between septal thickening and various CT features of bronchiectasis and the functional parameters.
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MATERIALS AND METHODS
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Patients
The study population was drawn from patients referred to our institution between June 1994 and October 2002 for investigation of suspected bronchiectasis. Ninety-four patients (29 men, 65 women; mean age, 52 years; age range, 18–82 years) were included in the study. There was no significant difference in age between men (mean age, 49 years; range, 22–70 years) and women (mean age, 52 years; range, 18–82 years) with the Student t test. Of 94 patients, 64 were life-long nonsmokers and 30 were current or former smokers. Age at diagnosis of bronchiectasis ranged from 5 to 76 years (median age, 35 years). All patients underwent a protocol that included pulmonary function tests and were designated as having idiopathic bronchiectasis on the basis of confirmation of bronchiectasis at thin-section CT, the absence of a history of a putative cause of bronchiectasis (eg, childhood pneumonia), or an associated medical condition (including allergic bronchopulmonary aspergillosis; cystic fibrosis, known as 
1-antitrypsin deficiency; mycobacterial infections; or autoimmune disease). Determination of the idiopathic nature of bronchiectasis was made on the basis of clinical and laboratory data that failed to identify a cause for the bronchiectasis (case records examined by N.A.S.). Exclusion criteria included a known diagnosis of (a) coexisting interstitial lung disease of any cause (eg, lymphangitis carcinomatosis), (b) cardiac failure, (c) congenital lymphangiectasia, or (d) pneumothorax. The following information was extracted from case records: (a) demographic details, (b) smoking history ("ever" vs "never"), (c) age at diagnosis, and (d) previous lobectomy. Our institutional board review does not require its approval or patient informed consent for this type of study, a retrospective study of case records and CT examinations.
Imaging and Evaluation
CT scans were obtained with an electron-beam CT scanner (Imatron, San Francisco, Calif) in 87 patients and a multi–detector row CT scanner (Volume Zoom Plus 4; Siemens Medical Systems, Erlangen, Germany) in seven patients. Thin sections (1 or 1.5 mm) were acquired at full inspiration (10-mm intervals) and expiration (30-mm intervals) in the supine position in all patients. Breath holding was rehearsed with each patient before the CT examination. A high-spatial-resolution reconstruction algorithm was used, and images were viewed at appropriate window settings for the lungs (window level, –500 to –600 HU; window width, 950 to 1500 HU).
The CT images were assessed in random order by two independent observers (N.A.S. and M.U., with 5 and 7 years of experience in thoracic CT interpretation, respectively) who recorded the following features for each of six lobes (the lingula was regarded as a separate lobe): bronchiectasis, interlobular septal thickening, and emphysema. The presence and signs of bronchiectasis were determined according to established criteria (4,5), with the following features being scored: (a) extent of bronchiectasis (score of 0 = none, score of 1 = one or part of one bronchopulmonary segment involved, score of 2 = more than one bronchopulmonary segment involved, and score of 3 = generalized bronchiectasis), (b) bronchial wall thickening (score of 0 = none, score of 1 = less than one-half times the diameter of the adjacent pulmonary artery, score of 2 = one-half to one times the diameter of the adjacent pulmonary artery, and score of 3 = greater than one times the diameter of the adjacent pulmonary artery), and (c) severity of bronchial dilatation (score of 0 = none, score of 1 = less than two times the diameter of the adjacent pulmonary artery, score of 2 = two to three times the diameter of the adjacent pulmonary artery, and score of 3 = greater than three times the diameter of the adjacent pulmonary artery). The overall disposition of bronchiectasis was categorized as predominantly central, peripheral, or mixed. The distinction between central and peripheral distribution was taken as a radial point midway between the hilum and the chest wall. Signs of exudative small airways disease (tree-in-bud pattern) were recorded as present or absent for each lobe.
Interlobular septal thickening was scored according to extent as follows: score of 0, no interlobular septa visible; score of 1, fewer than five interlobular septa visible; score of 2, five or more interlobular septa or interlobular septa over less than 50% pleural surface; score of 3, interlobular septa over more than 50% pleural surface; and score of 4, profuse interlobular septa. The location of interlobular septal thickening was categorized as predominantly central, peripheral, or mixed. The presence or absence of paraseptal and centrilobular emphysema was documented for each of the six lobes and was scored according to the lobar volume occupied (centrilobular) or pleural surface involved (paraseptal) as follows: score of 0 = none, score of 1 = less than 25% lobar volume or pleural surface, and score of 2 = more than 25% lobar volume or pleural surface. The presence or absence of pleural thickening at thin-section CT was recorded in each of the upper, middle, and lower zones for the right and left hemithorax. Mediastinal lymph node enlargement defined as lymph nodes greater than 1.5 cm in short-axis diameter was also recorded. For each CT feature, a total score was generated by summing the lobar scores.
Pulmonary Function Tests
Pulmonary function tests were performed within 4 weeks of the CT examination in 81 of 94 patients. The functional parameters recorded were forced expiratory volume in 1 second (FEV1), forced vital capacity (FVC), FEV1/FVC ratio, total lung capacity (TLC), residual volume (RV), RV/TLC ratio, carbon monoxide transfer factor, and carbon monoxide transfer coefficient; these were expressed as percentages of values predicted for the patient's age, sex, and height (6). Spirometric volumes were measured with a rolling seal spirometer (P. K. Morgan, Kent, England). Lung volumes were measured by using a constant-volume body plethysmograph (Masterlab Equipment, E. Jaeger, Market Harborough, England). Indices of gas transfer were measured by using a carbon monoxide single-breath technique; gas transfer results were adjusted for hemoglobin level (model B, P. K. Morgan; and 6200 Autobox DL, Sensormedics, Yorba Linda, Calif).
Statistical Analysis
Interobserver variation for the scoring of individual CT features was assessed by using the weighted 
statistic. values were defined as follows: value of less than or equal to 0.2, poor agreement; 0.21–0.40, fair agreement; 0.41–0.60, moderate agreement; 0.61–0.80, good agreement; and 0.81–1.00, very good agreement (7). Spearman rank correlation analysis was used to evaluate univariate correlations between (a) the extent of central and peripheral interlobular septal thickening and the remaining CT features scored, (b) the extent of interlobular septal thickening and lung function indices, and (c) the peripheral and central interlobular septal thickening. Stepwise regression analysis was used to (a) determine the relationship between each of the individual parameters of bronchiectasis and the extent of emphysema versus the extent of interlobular septal thickening, with the extent of total, central, and peripheral interlobular septal thickening as dependent variables in separate models, and (b) identify the functional effects of CT features, with FEV1, RV/TLC ratio, FEV1/FVC ratio, and carbon monoxide transfer factor evaluated as dependent variables in separate models. A P value < .05 was considered to indicate a significant difference. For the aforementioned univariate and multiple regression analyses, CT scores of the two observers were summed.
Further analyses were performed at a lobar level to assess the prevalence of interlobular septal thickening per se and the extensive interlobular septal thickening in lobes with bronchiectasis. Lobar interlobular septal thickening scores were graded as follows: score of 0 = none, score of 1 = trivial, and score of 2 or more = extensive. Comparisons of proportions were made by using the 
2 test. In analysis of these lobar findings, the observations of the two observers were used as separate observations. The range of interlobular septal thickening scores per patient over the population sampled was also evaluated by calculating the total summed interlobular septal thickening score for each patient and using the following grading system: score of 0 = absent, score of 1–6 = trivial, and score of 13 and greater = extensive.
Statistical analyses were performed by using STATA software (version 4; STATA Computing Resource Center, Santa Monica, Calif).
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RESULTS
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Interobserver agreement was very good for the scoring of centrilobular emphysema (weighted = 0.81); good for the extent of bronchiectasis (weighted = 0.70), severity of bronchiectasis (weighted = 0.76), tree-in-bud sign (weighted = 0.80), extent of interlobular septal thickening (weighted = 0.75), peripheral interlobular septal thickening (weighted = 0.62), and paraseptal emphysema (weighted = 0.63); and moderate for bronchial wall thickness (weighted = 0.49) and central interlobular septal thickening (weighted = 0.44).
Correlations
There were strong correlations between the extent of interlobular septal thickening and the extent and severity of bronchiectasis (Figs 1 –3), and a moderately strong correlation was found with bronchial wall thickness (Fig 4) (Table). There was a weak correlation between interlobular septal thickening and a tree-in-bud sign, and this correlation was stronger with central than with peripheral interlobular septal thickening (Fig 5).
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Figure 1. Transverse thin-section CT image of upper lobes in a patient with idiopathic bronchiectasis in both upper lobes (score of 2 for the extent of bronchiectasis) accompanied by abnormally thickened interlobular septa (score of 3 for the extent of septal thickening) in the peripheral (arrows) and central (white arrowheads) lung. There is no interlobular septal thickening adjacent to the tree-in-bud pattern (black arrowheads) in the periphery of the left upper lobe.
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Figure 2. Transverse thin-section CT image of the right upper lobe shows mild idiopathic bronchiectasis with bronchial wall thickening and mildly thickened interlobular septa anteriorly (arrows).
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Figure 3. Transverse thin-section CT image of idiopathic bronchiectasis in a 68-year-old woman shows mild thin-walled bronchiectasis in the left upper lobe and sparse smooth thickening of interlobular septa (arrowheads).
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Figure 4. Transverse thin-section CT image of the right lower lobe of idiopathic bronchiectasis shows dilatation and thickening of the bronchi with generalized thickened interlobular septa (arrows) in the adjacent lung.
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Univariate Spearman Correlations between CT Scores and Extent of Peripheral, Central, and Overall Septal Thickening
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Figure 5. Transverse thin-section CT image of the left lower lobe shows idiopathic bronchiectasis and a tree-in-bud pattern with scanty thickened interlobular septa located centrally in the left lower lobe but no obvious relationship between interlobular septal thickening (arrowheads) and the peripheral tree-in-bud pattern (arrows).
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Examination of the stepwise regression model showed that there was a relationship between the extent of interlobular septal thickening and the extent of bronchiectasis (P < .001). There was a much weaker relationship between the extent of interlobular septal thickening and the extent of emphysema (P = .02). Given this latter relationship, a subanalysis of patients, excluding those with CT evidence of emphysema (n = 28), was performed and revealed that the extent of bronchiectasis was the sole determinant of the extent of interlobular septal thickening.
In 81 patients undergoing concurrent pulmonary function tests, there were weak relationships between the extent of interlobular septal thickening and both FEV1 (r = –0.30, P < .01) and RV/TLC ratio (r = 0.30, P < .01). However, with stepwise regression analysis, increasing bronchial wall thickness was the sole morphologic feature associated with decreasing FEV1 (P < .001) and increasing RV/TLC values (P < .001). After adjusting for bronchial wall thickness, no other CT feature, including the extent of interlobular septal thickening, was linked to FEV1 or RV/TLC ratio. In addition, interlobular septal thickening was not linked to the lung function evidence of restriction (as judged with FEV1/FVC ratio) or carbon monoxide diffusing capacity with either univariate or multiple regression analysis.
A strong correlation was found between central and peripheral interlobular septal thickening (r = 0.60, P < .001). At multivariate analysis, an increase in peripheral septal thickening was independently linked to more extensive bronchiectasis (P < .001) and more severe bronchial wall thickening (P = .001). An increase in central interlobular septal thickening was also, albeit less strongly, independently linked to more extensive bronchiectasis (P = .042) and more severe bronchial wall thickening (P = .027). However, there was also a relationship with increasing extent of centrilobular emphysema (P = .041).
Lobar Observations
Of the total of 1128 potential lobar observations, 12 were lobectomies and seven were collapsed lobes; thus, analysis was performed on the 1090 lobar observations. Bronchiectasis was identified at CT in 748 lobes and of those cases, 514 (68.7%) had interlobular septal thickening. In the lobes without bronchiectasis (n = 342), 68 (19.9%) had interlobular septal thickening (P < .001 with 2 test). The frequency of severe interlobular septal thickening was 28.9% (216 of 748) in the lobes with bronchiectasis. In the lobes without bronchiectasis, the frequency of severe interlobular septal thickening was 2.1% (seven of 342) (P < .005 with 2 test).
The range of interlobular septal thickening scores for each individual is depicted in Figure 6. This reveals that although in a large minority interlobular septal thickening was absent (four of 94, 4.3%) or trivial (34 of 94, 36%), extensive interlobular septal thickening was present in nearly one-third of cases (26 of 94, 28%). Furthermore, lobar analysis revealed that bronchiectasis was present in 216 (97%) of 223 lobes with extensive interlobular septal thickening.
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DISCUSSION
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We found that interlobular septal thickening is a frequent thin-section CT finding in patients with idiopathic bronchiectasis, occurring in approximately 60% of cases. To our knowledge, no previous studies have reported this association.
Anatomically, the secondary pulmonary lobule is marginated by connective tissue septa within which lie pulmonary veins and lymphatics. The pixel size in standard thin-section CT scanners exceeds normal septal thickness (0.1 mm), and thus interlobular septa are only occasionally identified in healthy individuals (8). We categorized the lobar interlobular septal thickening scores as absent, trivial, and extensive. Lobar analysis revealed that while interlobular septal thickening was present in nearly 70% of bronchiectatic lobes, it was also present in 20% of lobes without bronchiectasis. However, in lobes without bronchiectasis, the extent of interlobular septal thickening was scored as trivial in the majority; only 2% showed severe interlobular septal thickening.
Although weak correlations were observed between the extent of interlobular septal thickening and indices of airflow obstruction, these relationships were not present at multiple regression analysis. As in previous studies (9,10), increasing bronchial wall thickness was the sole morphologic feature associated with airflow limitation at multiple regression analysis (9,10): After adjustment for bronchial wall thickness, no other CT feature (including interlobular septal thickening) was linked to pulmonary function markers of obstruction or restriction.
The study consisted exclusively of patients with idiopathic bronchiectasis to avoid confounding variables. In particular, patients with a lymphatic component to their disease, such as yellow nail syndrome or congenital lymphangiectasia, were deliberately excluded. Nevertheless, there were some limitations to our study. First, the majority of CT studies were performed by using 1.5-mm collimation and detector geometry designed for high temporal rather spatial resolution, which raises the possibility that the detection of interlobular septal thickening was compromised. However, these factors would, if anything, have resulted in underestimation of the extent of interlobular septal thickening. Second, the lack of literature about a precise and reproducible definition of abnormal interlobular septal thickening creates some difficulties in the interpretation of our data. Webb et al (11) compared thin-section CT findings and pathologic sections of normal lungs obtained at autopsy and found that an average of 10 septa were present per lung in individuals without known pulmonary disease. This equates with an average score of 6, which would be classified as trivial septal thickening according to our study criteria. However, Bergin et al (12) highlighted that components of the secondary pulmonary lobule are more easily depicted on CT scans of lung specimens compared with in vivo 1.5-mm-thick CT sections of a normal human subject, probably owing to the absence of breathing motion and radiation scatter from chest wall structures.
Although thin-section CT findings of normal individuals were not included in the present study, the frequency of interlobular septal thickening classified as greater than trivial in our patients with idiopathic bronchiectasis was 60%; this proportion is in striking contrast to the findings of a study of healthy individuals by Remy-Jardin et al (8), which showed that septal lines were observed with a frequency of only 7%. Despite the fact that the CT features assessed in our study were defined in descriptive terms and therefore subject to interobserver variability, the consistently high level of interobserver agreement for the extent of interlobular septal thickening and the extent and severity of bronchiectasis suggests that our observations are robust.
Another possible confounder is the potential overcalling of interlobular septa in areas of emphysema due to increased conspicuity of the septa by adjacent parenchymal destruction (13). Indeed, we found a link between centrilobular emphysema and central interlobular septal thickening. It is known that a degree of interstitial fibrosis may frequently accompany centrilobular emphysema (14). Tonelli et al (15) reported this thin-section CT observation and presumed that in the majority of cases, the fibrosis in cigarette smokers is too mild to be detected at CT. In our study, a subanalysis of patients, excluding those with emphysema, helped confirm that the extent of bronchiectasis was the sole determinant of the extent of interlobular septal thickening.
It is known that interlobular septa are not well developed and defined uniformly throughout the lung, and that the centrally located lobules are less well marginated than those in the periphery (11,16). As a result, peripheral septa are more easily visualized in the normal state. Thus, the demonstration of central interlobular septal thickening is more likely to indicate a pathologic process. Analysis of central and peripheral septal thickening as separate variables in the current study demonstrated that the extent of peripheral interlobular septal thickening was strongly linked to the extent of bronchiectasis, while central interlobular septal thickening was more strongly linked to the severity of bronchiectasis.
It can be speculated that other factors have influenced our observations of central and peripheral interlobular septal thickening; for example, paraseptal emphysema might result in the peripheral septa becoming more visually apparent. However, given that there was a very strong correlation between central and peripheral interlobular septal thickening, it is difficult to argue that either is confounded by spurious factors. Thus, the extent of bronchiectasis was found to be the cardinal determinant of total interlobular septal thickening, with separate links to both central and peripheral interlobular septal thickening, although the link to peripheral interlobular septal thickening was much stronger.
A chronic inflammatory cell infiltrate and lymphoid aggregates with germinal centers are present in the submucosa of a bronchiectatic airway at microscopic examination, and inflammation occurs to varying degrees (17). Given the anatomic continuum between the peribronchial interstitium and interlobular septa, there may be infiltration of the septa by inflammatory cells or lymphatic congestion within the septa due to increased lymphatic flow or lymphatic obstruction. Either process could result in interlobular septal thickening. Impaired lymphatic drainage may theoretically be the precursor to idiopathic bronchiectasis; it is considered to be the cause of bronchiectasis in yellow nail syndrome owing to its effect of increasing susceptibility to infection (18).
It is noteworthy that although only 4% of patients had no interlobular septal thickening, 20% of lobes without bronchiectasis had interlobular septal thickening. Thus the interlobular septa may not only be thickened as a result of the serving airways being bronchiectatic but also as a result of the presence of dilated bronchi elsewhere in the lung, and increased lymphatic flow may occur across lobes owing to a complex anastomotic lymphatic network. It is also known that inflammatory lesions are present in bronchi that appear normal at bronchography (19), and these lesions may be responsible for the sometime progressive course of bronchiectasis following resection of bronchiectatic segments or lobes. Therefore, although there may be no imaging features of bronchiectasis, inflammation may still be present at a pathologic level. The chronicity and irreversibility of the disease may also be important contributors in allowing interlobular septal thickening to develop.
In conclusion, we have shown that interlobular septal thickening is a frequent feature of thin-section CT in patients with idiopathic bronchiectasis, and the extent of bronchiectasis is the cardinal determinant of interlobular septal thickening.
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FOOTNOTES
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Abbreviations: FEV1 = forced expiratory volume in 1 second • FVC = forced vital capacity • RV = residual volume • TLC = total lung capacity
Authors stated no financial relationship to disclose.
Author contributions: Guarantor of integrity of entire study, D.M.H.; study concepts and design, D.M.H., A.U.W.; literature research, N.A.S.; clinical studies, M.U.; data acquisition, N.A.S., R.W.; data analysis/interpretation, A.U.W., N.A.S., D.M.H.; statistical analysis, A.U.W.; manuscript preparation, N.A.S., M.U.; manuscript definition of intellectual content, N.A.S., D.M.H.; manuscript editing, M.U., D.M.H.; manuscript revision/review, D.M.H., A.U.W., M.U., R.W.; manuscript final version approval, D.M.H.
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ABSTRACT
INTRODUCTION
