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Published online before print June 30, 2004, 10.1148/radiol.2323031059
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(Radiology 2004;232:757-761.)
© RSNA, 2004

Thoracic Imaging

Organizing Pneumonia: Perilobular Pattern at Thin-Section CT1

Masuo Ujita, MD, Elisabetta A. Renzoni, MD, Srihari Veeraraghavan, MB, Athol U. Wells, MD and David M. Hansell, MD

1 From the Department of Radiology (M.U., D.M.H.) and Interstitial Lung Disease Unit (E.A.R., S.V., A.U.W.), Royal Brompton Hospital, Sydney St, London SW3 6NP, England. Received July 7, 2003; revision requested September 25; final revision received March 11, 2004; accepted March 24. Address correspondence to D.M.H. (e-mail: d.hansell@rbh.nthames.nhs.uk).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To describe the appearance and frequency of a perilobular pattern at thin-section computed tomography (CT) in patients with organizing pneumonia.

MATERIALS AND METHODS: Thin-section CT scans of 21 consecutive patients with cryptogenic organizing pneumonia were retrospectively reviewed. Two thoracic radiologists in consensus recorded the presence and distribution of the CT abnormalities (consolidation, ground-glass opacification, nodules, bandlike opacities, interlobular septal thickening, and findings of fibrosis), with a particular focus on the presence and predominant location of the perilobular pattern, that is, a poorly defined arcadelike or polygonal appearance.

RESULTS: The perilobular pattern was present in 12 (57%) of 21 patients, 10 of whom had five or more perilobular opacities. Other CT features were consolidation (20 patients, 95%), which was predominantly a subpleural and/or peribronchial distribution in 17 patients, and ground-glass opacification (18 patients, 86%). Bandlike opacities and interlobular septal thickening were observed in four patients and one patient, respectively. The perilobular pattern abutted the pleural surface in 10 of 12 patients and was surrounded by aerated lung parenchyma in 11 of 12 patients. There was no obvious relationship between perilobular opacities and CT findings indicative of established fibrosis.

CONCLUSION: A perilobular pattern was present in more than half of the patients, along with the expected thin-section CT features of organizing pneumonia.

© RSNA, 2004

Index terms: Computed tomography (CT), thin-section, 60.12118 • Lung, CT, 60.12118 • Pneumonia, nonspecific interstitial and fibrosis, 60.213


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Organizing pneumonia is a nonspecific pathologic pattern of response by the lung to injury, with many causes and associations, including infection, drugs, connective tissue disease, and aspiration (1,2). The diagnosis of cryptogenic organizing pneumonia is based on typical pathologic and clinicoradiologic features and the exclusion of a determinable cause or associated disorder (1–4). The main histopathologic feature of organizing pneumonia is the presence of polypoid plugs of loose fibroblastic tissue within alveoli and distal small airways that are associated with a variable degree of interstitial and alveolar infiltration with mononuclear cells and foamy macrophages (3–6). The typical radiographic appearances of organizing pneumonia are multiple, usually bilateral, foci of consolidation. Computed tomography (CT) often demonstrates a subpleural or peribronchial distribution of the consolidation (7–10).

We have observed a perilobular distribution of opacities in some patients with organizing pneumonia. The perilobular region comprises the structures bordering the secondary lobule (11–13). In this context, accumulation of organizing exudate in the perilobular alveoli, with or without interlobular septal thickening at histologic examination, contributes to the ill-defined perilobular pattern (12). Some unusual variants of the CT features of organizing pneumonia have been reported (14–18), but to our knowledge, a perilobular distribution has not been reported. Thus, the purpose of our study was to describe the appearance and frequency of the perilobular pattern at thin-section CT in patients with organizing pneumonia.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
Medical records of 32 consecutive patients with a diagnosis of cryptogenic organizing pneumonia who attended our hospital between April 1993 and June 2001 were reviewed. The medical records were collected and reviewed (E.A.R., S.V.), and relevant details were recorded (M.U.). Patients without initial CT scans available for review (n = 9) and patients with severe fibrocystic changes on CT scans due to previous granulomatous infection (n = 2) were excluded. The final study population consisted of 21 patients (17 women, four men; age range, 25–77 years; mean age, 47 years). Lung biopsy specimens were obtained at open lung biopsy in 13 cases and transbronchial lung biopsy in eight cases. In three patients, transbronchial lung biopsies were not diagnostic of organizing pneumonia, and the diagnosis was made on a clinical and radiologic basis. No patient had previous lung disease or an underlying condition such as connective tissue disease or idiopathic interstitial pneumonia at the time of diagnosis of cryptogenic organizing pneumonia or during follow-up. Our institutional ethics committee did not require its approval or informed patient consent for this retrospective study.

CT Imaging and Evaluation
CT examination was performed by using a fast electron-beam scanner (C-100; Imatron, San Francisco, Calif) with a scan acquisition time of 200 msec. CT scans were obtained at end inspiration with 1.5-mm collimation at 10-mm intervals in the supine position and were reconstructed with a high-spatial-resolution reconstruction algorithm. The CT scans were viewed at window settings optimized for the lung parenchyma (width, 1500 HU; level, –500 HU). The interval between the CT examination and lung biopsy was less than 1 month in nine patients, 1–3 months in nine patients, and between 6 and 8 months in three patients.

CT observations were made in consensus by two thoracic radiologists (M.U. and D.M.H., 6 and 16 years of experience in thoracic CT, respectively). The CT scans were assessed for the presence and distribution of the following recognized features of organizing pneumonia (7,9,15): areas of airspace consolidation, ground-glass opacification, nodules, bandlike opacities, interlobular septal thickening, and findings of fibrosis. The presence of bandlike opacities, seen as either linear opacities extending in a radial manner along the line of a bronchus toward the pleura, intimately related to bronchi, or linear opacities occurring in a peripheral location bearing no relationship to the bronchi, was recorded (14). Findings taken to indicate fibrosis included a reticular pattern with associated distortion (ie, displacement of bronchi, vessels, or fissures; and loss of the lobular architecture of the lung), honeycombing, and traction bronchiectasis or bronchiolectasis (19). The anatomic distribution of each finding was recorded as subpleural, if abnormalities were mainly in contact with the visceral pleura; peribronchial, if lesions occurred along the bronchovascular bundle; or random, if no particular anatomic distribution was observed. For craniocaudal distribution, the upper lung zone was defined as the region above the tracheal carina; middle zone, as the region between the carina and inferior pulmonary veins; and lower zone, as the region below the inferior pulmonary veins.

A perilobular pattern was defined as curvilinear opacities that were of greater thickness and, more important, were less sharply defined than those encountered in thickened interlobular septa, with an arcadelike or polygonal appearances (Fig 1) (12). The presence of the perilobular pattern was graded in the three lung zones with the following three-point scale: score 1, single perilobular opacity; score 2, two to four perilobular opacities; and score 3, more than four perilobular opacities. The observers also assessed the predominant location of the perilobular opacities, that is, whether they abutted the pleura and whether they were surrounded by normal lung or were contiguous with consolidation.



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  		Figure 1. Transverse thin-section CT scan at the level of dome of the right hemidiaphragm in a 50-year-old woman with cryptogenic organizing pneumonia shows poorly defined arcadelike and polygonal opacities (perilobular pattern) in the left lower lobe in both subpleural and central regions of the lung. The opacities resemble thickened interlobular septa.

 

   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Twenty (95%) of 21 patients had airspace consolidation at CT, with no particular craniocaudal distribution but with predominantly subpleural and/or peribronchial distribution in 17 patients (Table 1). Consolidation was not observed in isolation in any patient: ground-glass opacification, which was present in a random distribution, was observed in 18 (86%) patients (Table 1). Nodules and bandlike opacities were present in a random distribution in five and four patients, respectively (Table 1). Bandlike opacities (either radial or peripheral) occurred predominantly in the middle and lower zones in the longitudinal planes and were always accompanied by consolidation or ground- glass opacification. Unequivocal interlobular septal thickening was seen in only one patient (Fig 2). Five (24%) patients had CT signs indicating fibrosis, predominantly in the middle and lower zones: two patients had peribronchial fibrotic changes, and three patients had fibrosis distributed randomly (Table 1).


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  		TABLE 1. CT Findings and Distribution in 21 Patients with Cryptogenic Organizing Pneumonia

 


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  		Figure 2. Transverse thin-section CT scan through upper lobes in a 49-year-old woman with cryptogenic organizing pneumonia. Few abnormally thickened interlobular septa (arrowheads) are seen anteriorly in both upper lobes. These linear opacities are thinner and more sharply demarcated than perilobular opacities in Figures 1 and 3.

 
The perilobular pattern was observed in 12 (57%) of 21 patients. As summarized in Table 2, it occurred in all lung zones, with a predominance in middle and lower zones. In ten of 12 patients, the perilobular pattern was extensive (five or more perilobular opacities) and abutted the pleural surface (Fig 3). The perilobular opacities were mainly surrounded by aerated lung parenchyma in 11 patients (Fig 4) and were contiguous with consolidation in one patient (Fig 5). Perilobular opacities were invariably accompanied by consolidation (12 of 12) and/or ground-glass opacification (11 of 12) in the same lung zones. In three of five patients with findings indicative of an established fibrosis, a relatively extensive perilobular pattern coexisted with fibrosis in the same lung zones (scores of 2 and 3 for all three zones) (Fig 6); however, no perilobular pattern was observed in the remaining two patients.


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  		TABLE 2. Extent of Perilobular Pattern and Zonal Distribution in 12 Patients

 


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  		Figure 3. Transverse thin-section CT scan at the level of lung base in a 51-year-old woman with cryptogenic organizing pneumonia. Perilobular opacities (arrows) are seen abutting the pleural surface in the left lower lobe. There is extensive airspace consolidation posteriorly in the right lower lobe.

 


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  		Figure 4. Transverse thin-section CT scan through lower lobes in a 44-year-old man with cryptogenic organizing pneumonia. The perilobular opacities (arrows) in right lower lobe are centrally located and surrounded by aerated lung parenchyma.

 


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  		Figure 5. Transverse thin-section CT scan at the level of lung base in a 61-year-old man with cryptogenic organizing pneumonia. Perilobular opacity (arrow) not immediately obvious is located adjacent to a focus of airspace consolidation in the left lower lobe. There are few bandlike opacities (arrowheads) in the right lower lobe.

 


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  		Figure 6. Transverse thin-section CT scan through lower lobes in a 37-year-old woman with cryptogenic organizing pneumonia. There is perilobular opacity (arrowhead) and dilatation and distortion of airways (arrow) indicating presence of interstitial fibrosis.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
REFERENCES
 
Since the description of a cryptogenic organizing pneumonia in 1983 by Davison et al (3) and the subsequent report on bronchiolitis obliterans organizing pneumonia by Epler et al (4), there have been several reports about the imaging features of organizing pneumonia. The characteristic radiographic appearance is patchy, nonsegmental, unilateral or bilateral areas of airspace consolidation. Less frequent findings include irregular linear or reticulonodular opacities (3,4,20–22).

The CT findings mirror the radiographic appearances and comprise airspace consolidation, which is present in more than 80% of cases, associated with ground-glass opacification in between 33% and 100% of cases (8–10,23). Consolidation predominantly involves subpleural and/or peribronchial distribution, whereas ground-glass opacification is distributed in a random fashion (9,10). In our study group, the prevalence of these cardinal features of organizing pneumonia was similar to that in previously reported series.

In addition to these common features, some unusual CT findings in patients with organizing pneumonia have been described (14–18). Murphy et al (14) reported two types of linear opacities that occur in isolation or in combination with other CT abnormalities. One of these opacities extended in a radial manner along the line of a bronchus toward the pleura and was intimately related to bronchi. The other was seen in a subpleural location and bore no relationship to the bronchi. The first linear opacity was referred to as "parenchymal bands" in the study by Akira et al (15) or as "axial interstitial thickening" by Preidler et al (23). It has been suggested that these lines represent involvement of the more proximal airways, with peribronchial inflammation and focal areas of linear atelectasis (14). The second type of linear opacity was observed in three of 43 patients with cryptogenic organizing pneumonia in the study by Lee et al (9) and in two of 12 patients in the study by Bouchardy et al (24). In our series, we did not make the distinction between these two linear opacities when scoring the CT scans, and we included both in the term bandlike opacities. We documented their presence in only four of 21 patients.

Another unusual CT feature encountered in organizing pneumonia are crescentic or ring-shaped opacities surrounding areas of ground-glass opacification, first reported by Voloudaki et al (16). Zompatori et al (17) fancifully named this appearance the atoll sign. More recently, Kim et al (18) recorded this sign in 19% of patients with cryptogenic organizing pneumonia and referred to it as the reversed halo sign. Histopathologically, the central areas of ground-glass opacification correspond to alveolar septal inflammation and cellular debris within airspaces, whereas the ring-shaped or crescentic periphery, approximately 10 mm in thickness, corresponds mainly to organizing pneumonia within alveolar ducts (16).

The perilobular pattern we describe differs from the aforementioned opacities in both the CT appearance and in the presumed pathologic distribution. The perilobular pattern consists of bowed or polygonal opacities with poorly defined margins bordering the interlobular septa. We observed this feature in just over half of the patients with cryptogenic organizing pneumonia. The perilobular region, a term coined by Murata et al, includes not only the bordering structures of the secondary lobule such as the pleura, interlobular septa, and pulmonary vein, but also the larger bronchovascular structures, paraseptal interstitium, paraseptal alveoli, and subpleural interstitium (11–13). In this context, a variety of diseases affecting mainly alveoli can involve the perilobular region and, in so doing, mimic abnormalities of the septal structures at thin-section CT (12). Therefore, organizing pneumonia, which is characterized by buds of granulation tissue in the distal airspaces, may manifest as apparent septal thickening, contributing to a coarse reticular pattern, even though it is not associated histologically with thickening of the interlobular septa (12,13).

In some CT studies of cryptogenic organizing pneumonia, authors have described thickening of the interlobular septa, which was usually associated with areas of consolidation, nodules, and masses (7,10,15,23). The reported frequency of interlobular septal thickening in organizing pneumonia is between 20% and 40% of cases (7,10,23), whereas we found it in only one of 21 patients. However, it is a matter of speculation as to the true frequency of interlobular septal thickening in organizing pneumonia, given the potential similarity of these appearances. Scrutiny of some of the illustrations in some previous articles (7,14) reveals a perilobular pattern, even though it was not specifically described as such.

Most patients with cryptogenic organizing pneumonia have an exquisite response to steroid therapy, but as many as 15% of patients have progressive disease (20,25). Cohen et al (26) described a subset of patients with organizing pneumonia who presented with a fulminant course, leading to death or chronic severe fibrosis and marked impairment of lung function. Autopsy revealed that the histologic pattern was that of alveolar septal inflammation and severe fibrotic honeycombing. In a histopathologic study of 19 patients with cryptogenic organizing pneumonia, the authors reported that the presence of background remodeling of the pulmonary parenchyma (scarring and/or interstitial fibrosis) was a predictor of an unfavorable outcome (25). In a study by Cordier et al (20), the authors defined a separate group of patients whose radiographs showed diffuse interstitial opacities. In this subgroup, three of seven patients did not improve with steroid therapy, and two died of progressive pulmonary disease (20).

Bouchardy et al (24) observed reticular interstitial infiltrates on CT scans in three of 12 patients, which pathologically demonstrated the presence of interstitial thickening and fibrosis in addition to the features of organizing pneumonia. In a recent study (27) of 26 patients with organizing pneumonia, the authors stated that reticular opacities on CT scans at presentation were associated with persistent or progressive disease. In our study, findings indicative of fibrosis were observed in five of 21 patients, three of whom showed relatively extensive perilobular patterns, whereas the remaining two did not exhibit a perilobular pattern. Since reticular opacities demonstrated in the Lee et al study (27) differ from the perilobular pattern we describe, and because of the small number of patients who had fibrosis and perilobular pattern in our series, the importance of the perilobular pattern as a prognostic factor is yet to be determined.

There are some caveats to our retrospective study. From a diagnostic point of view, we do not know how specific is the perilobular pattern in organizing pneumonia, because we did not examine the prevalence of a perilobular pattern in similar diseases, such as infectious pneumonia, chronic eosinophilic pneumonia, lymphoproliferative disorders, and bronchioloalveolar carcinoma (2,8,18). Furthermore, we did not have exact histologic correlation with the perilobular pattern, although this would, in practice, be difficult to obtain because lung biopsy usually targets the more densely consolidated abnormal lung. Furthermore, the relatively small volume of tissue sampled would make the chance inclusion of perilobular involvement unlikely.

In summary, a perilobular pattern is frequently observed in patients with organizing pneumonia. It appears as poorly defined, bowed or polygonal opacities and is predominantly subpleural and surrounded by aerated lung. Among the already described variations of the CT features of organizing pneumonia, it is useful to be aware of the perilobular pattern, which may be helpful in the differential diagnosis.


   FOOTNOTES
 
Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, D.M.H.; study concepts and design, M.U., D.M.H.; literature research, M.U.; clinical studies, E.A.R., S.V.; data acquisition, M.U., E.A.R., S.V.; data analysis/interpretation, M.U., D.M.H., A.U.W.; statistical analysis, A.U.W.; manuscript preparation, M.U.; manuscript definition of intellectual content, M.U., D.M.H.; manuscript editing, revision/review, and final version approval, M.U., D.M.H., A.U.W.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 

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