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Organizing Pneumonia: a Kaleidoscope of Concepts and Morphologies

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Organizing Pneumonia: a Kaleidoscope of Concepts and Morphologies Eur Radiol (2011) 21:2244–2254 DOI 10.1007/s00330-011-2191-6 CHEST Organizing pneumonia: a kaleidoscope of concepts and morphologies Benjamin J. Roberton & David M. Hansell Received: 17 January 2011 /Revised: 13 April 2011 /Accepted: 6 May 2011 /Published online: 10 July 2011 # European Society of Radiology 2011 Abstract The basic histopathological pattern of organizing What is organizing pneumonia? pneumonia (OP) is well recognized, but the contexts in which it is encountered continue to increase. In parallel with an & A histopathological pattern characterised by whorls of appreciation of new causes and associations of OP, an myofibroblasts and inflammatory cells in a connective understanding of OP in the spectrum of lung injury and repair tissue matrix within the distal airspaces. has evolved. There is an increasing array of HRCT manifes- & A non-specific response to lung injury associated with tations of OP, some of which have only recently been described. infection, drugs, inflammatory, and other conditions. (see This article concentrates on new concepts surrounding OP and Table 1). highlights newly described imaging patterns. & As a primary clinical entity, it is termed cryptogenic OP. Keywords Organizing pneumonia . Cryptogenic organizing pneumonia . Bronchiolitis obliterans organizing History, terminology and classification pneumonia . BOOP Early references to OP can be found in the late nineteenth century literature [1], but the first detailed histopathological Introduction descriptions come from the early twentieth century [2]. These were largely based on autopsy studies performed on Organizing pneumonia (OP) can be considered as one stage patients with non-resolving bacterial pneumonia, before the of a non-specific response to lung injury and is character- advent of antimicrobial therapy [3, 4]. It was established ized by inflammatory cells and a connective tissue matrix early on that OP occurred as a result of infection, but during within the distal airspaces. The histopathological entity of the course of the twentieth century OP began to be OP is encountered in many conditions, including infection, recognized in such varied conditions as interstitial diseases drug reaction and connective tissue diseases. OP also [5], drug toxicity [6] and connective tissue disorders [7]. occurs as an idiopathic and well-characterized clinicopath- Reports of OP with no known cause or association ological disorder, cryptogenic organizing pneumonia appeared in 1983, when Davidson coined the term (COP). The CT signs of OP are many and varied and the cryptogenic organizing pneumonia [8]. Two years later, classic and more recently reported imaging patterns of OP Epler et al. described the same entity, which they named are reviewed, in addition, practical diagnostic issues for the bronchiolitis obliterans organizing pneumonia (BOOP)[9]. radiologist are emphasized. These two names for the same condition resulted in much confusion [10]. The term BOOP emphasized the histolog- : ical airspace predominance, but the semantic similarity to B. J. Roberton D. M. Hansell (*) obliterative bronchiolitis (bronchiolitis obliterans), an unre- Department of Radiology, Royal Brompton Hospital, lated condition, muddied the waters [11, 12]. Sydney Street, London SW36NP, UK The disorder had become firmly established as a distinct e-mail: [email protected] clinicopathological entity by the 1990s, and at that time it Eur Radiol (2011) 21:2244–2254 2245 Table 1 Causes and associations of secondary organizing pneumonia the alveolar ducts and surrounding alveoli), consisting of buds Cause/association: Example: of granulation tissue, whorls of fibroblasts and myofibroblasts in a connective matrix (Masson bodies [17]) (Fig. 1). These Drugs: buds may extend from one alveolus to the next through the Antibiotics nitrofurantoin narrow pores of Kohn (butterfly pattern). Alveoli may also Antiepileptics carbamazepine contain foamy macrophages and there is often mild Antiarrythmics amiodarone interstitial inflammation of the surrounding lung [16, 18]. Immuno-modulatory interferon In its purest form, background features of diffuse alveolar Infections: damage or fibrosis are absent. However, these components Bacteria Streptococci areincreasinglyrecognizedinspecificsituationsorvariant Viruses Influenza forms of organizing pneumonia, which are discussed later. Parasites Plasmodium vivax The initial trigger leading to intra-alveolar OP is a degree Fungi Cryptococci of alveolar epithelial injury, causing the death of pneumo- Inflammatory: cytes and the formation of gaps in the basal lamina. Crucial Connective tissue diseases poly/dermatomyositis to the development of OP is leakage of plasma proteins Vasculitis Wegener’s granulomatosis (including clotting factors) into the airspaces [18]. Malignancy lung cancer The process of organization then takes over, both the Transplantation bone marrow coagulation and fibrinolytic cascades are activated in the Interstitial lung disease UIP airspaces; the coagulation cascade predominates causing Miscellaneous lung injury radiotherapy fibrin deposition. The first stage of organization of the exudate involves the formation of fibrinoid inflammatory cell clusters (lymphocytes, neutrophils and some eosinophils). In the was more frequently referred to (certainly in North second stage, inflammatory cells are less numerous, fibro- America) as BOOP, which was also the preferred term at blasts migrate through gaps in the basal lamina then proliferate the first international congress on organizing pneumonia in and undergo phenotypic modification to become myofibro- 1992 [13, 14]. In 1998, Katzenstein and Myers’ landmark blasts, and an extracellular reticulin framework is laid down. paper on the clinical relevance of the pathologic classifica- Mature fibrotic buds characterize the final stage; inflammatory tion of idiopathic pulmonary fibrosis, the term BOOP was cells are increasingly scarce, concentric rings of myofibro- used; however, the condition was not included in their blasts alternate with layers of collagen (predominantly type classification of interstitial disorders owing to its intra- III), fibronectin and proteoglycans [18]. luminal rather than interstitial distribution and radiographic Cordier has proposed an interesting analogy for orga- appearance of air space consolidation [15]. These issues nizing pneumonia by comparing it to the granulation tissue were further explored in 2002, when a working group of skin wounds, another example of a reversible fibro- sponsored by the American Thoracic Society and the inflammatory process [18]. OP lesions share a few European Respiratory Society settled on the term COP for characteristics with granulation tissue which may shed light the clinical entity [16]. They also included the condition in on the reversible nature of the lesion; these include their classification of idiopathic interstitial pneumonias because a) it may be confused with other interstitial disorders, b) the histopathological features include an element of interstitial inflammation and c) in some cases interstitial fibrosis is an obvious component (see later). The term COP remains preferred to BOOP as it conveys the characteristics of the condition and avoids confusion with airway-centered diseases; the trend towards the use of COP is reflected in its proportionately greater use over recent years, although the now abandoned term BOOP is still surprisingly frequently used in the literature. Histopathology Fig. 1 Histopathology of organizing pneumonia. A surgical lung biopsy specimen stained with haematoxylin and eosin shows a Masson body (arrow); organized granulation tissue within the alveolar At a histopathological level, OP is characterized by intra- space, consisting of myofibroblasts and inflammatory cells within a luminal plugs of inflammatory debris (predominantly within connective tissue matrix 2246 Eur Radiol (2011) 21:2244–2254 prominent capillarization of the intra-alveolar buds [19] and mortality or long-term functional morbidity [18, 28]. The a predominance of type III collagen, which occurs in a reported relapse rate ranges from 13% to 58% [28, 29], loose matrix and is relatively susceptible to degradation (as likely due to the heterogeneity of the groups studied. opposed to irreversible type I collagen which is encoun- Treatment for at least 6 months is usually advised [9, 24], tered in fibrotic lung disease such as UIP) [18, 20–22]. but Cordier has proposed low dose and short duration of treatment, with informed patients accepting a higher relapse rate whilst avoiding steroid side effects [18]. Overall, the Histopathogenesis of organizing pneumonia: prognosis is good, however, a proportion of patients will progress to fibrosis, respiratory failure and death [18]; this & Alveolar epithelial injury leads to pneumocyte cell challenging subgroup is discussed later. death forming gaps in the basal lamina. Plasma proteins One study has suggested that there is no obvious (including clotting factors) and inflammatory cells leak difference between cryptogenic and secondary OP in terms into the airspace. (Leakage) of symptomatology, physical signs, laboratory and pulmo- & Activation of coagulation cascade leading to fibrin nary function tests, radiologic or pathologic findings [29]. deposition. (Coagulation) However, the authors also reported that secondary OP leads & Organization into intra alveolar fibro-inflammatory to more respiratory related deaths than COP and has a buds involving whorls of myofibroblasts in
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