Idiopathic Interstitial Pneumonias: High-Resolution CT and Histologic Findings1
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1 Idiopathic Interstitial Pneumonias: High-Resolution CT and Histologic Findings1 Nestor L Muller, MD, PhD #{149}Thomas V. Colby, MD Table 1 Classifications of Idiopathic Interstitial Pneumonias Liebow Classification Current Classification Usual interstitial pneumonia Usual interstitiah pneumonia Desquamative interstitial pneumonia Desquamative interstitial pneumonia Lymphocytic interstitial pneumonia Now considered a lymphoprohiferative disorder Giant cell interstitial pneumonia Now considered a pneumoconiosis Bronchiolitis with interstitial pneumonia Bronchiohitis obliterans with organizing pneumonia * Several cases described by Liebow have been reclassified as respiratory bronchiolitis and interstitial lung disease. U INTRODUCTION The idiopathic interstitial pncumonias are a heterogeneous group of inflammatory and interstitial fibrosing lesions that manifest as infiltrative lung disease. On the basis of differences in histohogic appearances, they were initially classifled by Liebow (1) into five types: usual interstitiah pneumonia (UIP), desquamative interstitial pneumonia (DIP), hymphocytic interstitial pneumonia (LIP), giant cell interstitial pneumonia (GIP), and bronchiolitis with interstitial pneumonia (BIP) (Table 1). It has since been shown that giant cell interstitial pneumonia is a pneumoconiosis, being found almost exclusively in workers exposed to cobalt, primarily in the form of hard-metal, an alloy of tungsten carbide and cobalt (2). Lymphocytic interstitial pneumonia includes cases characterized by a diffuse interstitial infiltrate of polyclonal lymphocytes and plasma cells, as well as cases of diffuse hymphoid hyperplasia in the hung. Many cases of lymphocytic interstitial pneumonia have been reclassified as lymphomas. Lymphocytic interstitial pneumonia and related entities are therefore better classified as lymphoproliferative disorders rather than included with chronic interstitiah pneumonias (3). The term bronchiolitis obliterans with interstitialpneumonia has been replaced by idiopathic bronchiolitis obliterans with organizingpneumonia (BOOP) (4); because of the air-space involvement in this entity, some have excluded it from the chronic interstitial pncumonias (5). Recently, two other forms of idiopathic interstitial pneumonia have been described: acute interstitial pneumonia (AlP) and nonspecific interstitial pneumonia and fibrosis (NIPF) (also called nonclassifiable interstitial pneumonia) (6,7). AlP corresponds closest to the entity originally described by Hamman and Rich (8,9). Although the term Hamman-Rich syndrome has frequently been used to refer to the clinicopathologic features of chronic interstitial pulmonary fibrosis (10), use ofhamman-ricb syndrome should be limited to cases ofaip (1 i). The confusion in terminology is further aggravated by the tendency to lump the various idiopathic interstitial pneumonias under the term idiopatbicpulmonaryflbrosis or cryptogenic Abbreviations: AlP acute interstitial pneumonia, BOOP = bronchiolitis obliterans with organizing pneumonia, DIP = desquamative inter. stitial pneumonia. NIPF = nonspecific interstitial pneumonia and fibrosis, UIP = usual interstitial pneumonia Index terms: Bronchiolitis obliterans, #{149}Lung, fibrosis, #{149} Lung. interstitial disease #{149} Pneumonia. with fibrosis, , #{149}Pneumonitis, desquamative interstitial, interstitial RadloGraphlcs 1997; 17: From the Department of Radiology, University of British Columbia and Vancouver Hospital and Health Sciences Center, 855 W 1 2th Aye, Vancouver, British Columbia, Canada V5Z 1M9 (N.L.M.); and the Department of Laboratory Medicine/Pathology, Mayo Clinic Scottsdale, Scottsdale, Anz (T.V.C.). From the Plenary Session, Friday Imaging symposium: Chest Radiology Update-1996, at the 1996 RSNA scientific assembly. Received February 18, 1997; revision requested March 17 and received April 2: accepted April 3. Address reprint requests to N.L.M. RSNA, U Imaging Symposium Volume 17 Number 4
2 Table 2 Features of Idiopathic Interstitial Pneumonlas Typical... High-Resolution CT Features Course of Histologic Histologic Name Presentation Features Main Findings Predominant Distribution Acute interstitial i -4 wk Alveolar edema, Consolidation Middle and lower hung pneumonia hyaline membranes zones (Hamman-Rich syndrome) Desquamative mo Many macrophages Ground-glass Middle and lower lung interstitial in air spaces, attenuation, zones, subpleural in pneumonia homogeneous irregular -60% of cases appearance lines (mild) Usual interstitial 1-3 y Heterogeneous Irregular lines, Middle and lower lung pneumonia (idiopathic pattern with foci of honeycombing zones, subpleural in pulmonary fibrosis) normal lung, active -90% of cases inflammation, and end-stage fibrosis Nonspecific interstitial mo Homogeneous pattern, Ground-glass Diffuse or patchy pneumonia and interstitial infiltrate attenuation fibrosis (nonchassi- of mononuclear fiable interstitial cells pneumonia) Bronchiohitis obhiterans 1-6 mo Granulation tissue Consolidation Patchy, peribronchial with organizing polyps in alveolar or subpleurah in pneumonia (crypto- ducts and bron- -60% of cases genic organizing chioles, organizing pneumonia) pneumonia fibrosing alveolitis. This tendency is unfortunate because the various interstitial pneumonias have different clinical, radiologic, and histologic manifestations and different prognoses. HIP is primarily the form that corresponds to idiopathic pulmonary fibrosis or cryptogenic fibrosing alveolitis; a small percentage of cases of DIP make up the remainder. The aim of this review is to summarize the histologic and high-resolution CT features of the various idiopathic interstitial pneumonias (Table 2). Although idiopathic BOOP (also called cryptogenic organizing pneumonia) is mainly an air-space disease, it is included because it may have similar clinical manifestations, requires lung biopsy for definitive diagnosis, and may be confused with the other entities. U ACUTE INTERSTITIAL PNEUMONIA AlP is characterized by respiratory failure developing over days to weeks and histologic features of organizing diffuse alveolar damage in which no etiologic agent is identified (6,9). The histologic findings include alveolar edema, hyaline membrane formation, and extensive fibroblast proliferation but little mature collagen deposition (6,9) (Fig 1). The radiologic manifestations arc similar to those of adult respiratory distress syndrome and consist of progressive parenchymal consolidation that may be patchy or diffuse but tends to involve mainly the lower lung zones (1 2, i 3) (Fig 2). Primack et al (12) reviewed the highresolution CT findings in nine patients with AlP. The CT findings consisted of extensive bilateral air-space consolidation (67% of cases) and patchy (67% of cases) or diffuse (33% of cases) bilateral areas of ground-glass attenuation. A predominantly central or subpleural distribution was present in only 22% of cases. AlP has a poor prognosis, with 90% of patients dying 1-6 months after presentation (6,12). July-August 1997 Muller and Colby U RadioGraphics U 1017
3 (. #{149},.:_#{149} : &.,: :.:; -_ ,,....,.,...,$J.,,,. :...:.::. : #{182}.#{149}, S,.#{149}.,..4,.. a 3 I - 5, :---,. :,#{232} %*,,. -,. S ;:,,.- : 1. Figures 1, 2. (1) AlP. Photomicrograph (hematoxylin-eosin stain) shows a uniformly widened and edematous interstitium without significant fibrosis. Residual hyahine membranes line the alveolar ducts (straight arrows). 2. There is prominent type II cell proliferation, which indicates early repair (curved arrows). The appearance is nonspecific and histologically represents acute and organizing diffuse alveolar damage. (2) AlP in an 83-year-old woman. High-resolution CT scan (1.5-mm collimation) demonstrates extensive bilateral areas of consolidation. The consolidation is most severe in the dependent hung regions. Also noted are areas of ground-ghass attenuation, particularly in the right middle lobe and hingula. U DESQUAMAT1VE INTERSTITIAL PNEUMONIA DIP is characterized histologically by large numbers of macrophages within the air spaces, mild fibrosis, and relative histologic uniformity from field to field (4, 14) (Fig 3). The disease is rare: A review of all patients who underwent highresolution CT and received a biopsy-proved diagnosis over an 8-year period at four major institutions in North America and Europe identified only 22 cases (1 5). Several cases initially classifled by Carrington et al (16) as DIP have been shown to represent respiratory bronchiolitis and interstitial lung disease (17). At presentation, patients with DIP are typically years of age and have a month history of dry cough and slowly progressive shortness of breath (16). The predominant high-resolution CT findings in DIP are bilateral areas of ground-glass attenuation that involve mainly the middle and lower lung zones (15). A predominantly subplcural distribution is seen in approximately 60% of cases (1 5) (Fig 4). Irregular lines of attenuation suggestive of fibrosis are seen in approximately 50% of cases, and honeycombing is seen in 30%. The fibrosis is mild, involving mainly the subphcural regions and lung bases (15). Although traction bronchiectasis may be seen in the areas of fibrosis (1 3), it is not a prominent feature (15). DIP has a relatively good prognosis, with 60%-80% of patients responding to corticosteroids (16,18). The 5-year mortality rate is only 5% (16). U USUAL INTERSTITIAL PNEUMONIA UIP is characterized histologically by a variegated pattern with foci of normal lung, interstitiah cellular infiltrates, and zones of active fibrosis and end-stage fibrosis (4,5, 16) (Fig 5). At presentation, most patients arc years of age and have a 1-3-year history of nonproductive cough and slowly progressive shortness of breath (16, 19). UIP accounts for approximately 90% of cases clinically diagnosed as idiopathic pulmonary fibrosis or cryptogenic fibrosing ahvcolitis. Although the term usual interstitial pneumonia is often used synonymously with idiopathicpulmonaryflbrosis, the pattern of UIP may also be seen in other conditions, such as collagen vascular diseases and drug reactions. The characteristic high-resolution CT findings in UIP are irregular linear areas of increased attenuation and honeycombing invoiving predominantly the basal and subpleural lung regions (20,21) (Fig 6). This pattern and distribution allow a specific diagnosis with CT in the majority of cases (22,23). Lack of sub U Imaging Symposium Volume 17 Number 4
4 3. 4. Figures 3, 4. (3) DIP. Scanning power micrograph (hematoxylin-eosin stain) shows uniform filling of air spaces by macrophages (arrows). The uniformity of the process is in distinct contrast to the variegation seen in UIP. (4) DIP in a 53-year-old man. High-resolution CT scan (1.5-mm collimation) shows extensive bilateral areas of ground-glass attenuation. These can be best appreciated in contrast with the air in the trachea and bronchi (black bronchus sign). There is evidence of mild fibrosis in the form of irregular linear areas of increased attenuation in the subpleurai lung regions (arrows) Figures 5, 6. (5) UIP. Photomicrograph (hematoxyhin-eosin stain) of a whole-mount section shows histologic variegation with zones of dense fibrosis and microscopic honeycombing (arrows), whereas elsewhere there is preservation of alveolar structure. At the junction of the fibrotic zones and the normal hung, there are foci of active fibroblastic proliferation (representing the active component of the disease), which are not apparent at this magnification. (6) UIP in a 7i-year-old man. High-resolution CT scan (1.5-mm collimation) shows the variegated pattern and the predominantly subpheurah distribution of UIP. The abnormalities consist of irregular linear areas of increased attenuation, focal areas of honeycombing (arrows), and focal areas of ground-glass attenuation. Note the relative sparing of the most anterior aspects of the lungs. pleural honeycombing at CT or hung biopsy should suggest an alternative diagnosis. Areas of ground-glass attenuation are also frequently noted and most commonly reflect potentially treatable active inflammation (24-26). UIP has a poor prognosis, with only 10%- 1 5% of patients responding to corticosteroid therapy and 50% of patients dying within 5 years of diagnosis (16). July-August 1997 MilDer and Colby U RadioGraphics U 1019
5 7. 8. Figures 7, 8. (7) NIPF. Scanning power micrograph (hematoxylin-eosin stain) shows diffuse mild thickening of alveolar septa (arrows) without honeycombing or significant air-space accumulation of macrophages. The uniformity of the process and the absence of honeycombing allow differentiation of NIPF (which has a better prognosis) from UIP. (8) NIPF in a 44-year-old man. High-resolution CT scan (1.5-mm collimation) shows extensive bilateral areas of ground-glass attenuation. Consolidation is present in the dependent hung regions. There is no evidence of fibrosis. Note the homogeneous pattern of abnormalities, similar to that seen in DIP. Although patients with DIP and mild fibrosis almost always respond to corticosteroid therapy, only a small percentage of patients with UIP and a comparable extent of fibrosis respond to treatment (16). This distinction is important when evaluating the value of high-resolution CT in determining the likelihood of response to corticosteroids in patients with idiopathic pulmonary fibrosis. Recently, Hartman et al (18) compared the outcomes when areas of groundglass attenuation were seen at high-resolution CT in patients with UIP or DIP. The study included 1 2 patients with biopsy-proved UIP and 1 1 patients with biopsy-proved DIP who underwent high-resolution CT before and several months after treatment with corticosteroids. In nine of 1 2 (75%) patients with UIP, the areas of ground-glass attenuation increased in extent or progressed to fibrosis despite treatment; however, only two of 1 1 (18%) patients with DIP showed progression of disease, the remaining patients having responded to treatment (18). U NONSPECIFIC INTERSTITIAL PNEU- MONIA AND FIBROSIS NIPF (also called nonclassifiable interstitial pneumonia) is essentially a diagnosis of cxclusion, representing cases of idiopathic interstitial pneumonia that cannot be classified into one of the above categories. NIPF is characterized by varying proportions of interstitial inflammation and fibrosis that arc temporally uniform (ic, of similar age, either recent and active or old and relatively quiescent) within each case (7) (Fig 7). It includes cases with cellular interstitial pneumonia and relatively little fibrosis, cases with cellular interstitial pneumonia and a significant amount of admixed fibrosis, and a relatively small proportion of cases with predominant fibrosis. The average age at presentation is 46 years (7). At presentation, patients have a 1- week to 5-year (average, 8 months) history of nonproductive cough and progressive shortness of breath (7). The high-resolution CT findings in a study of seven patients have been reported (27). The predominant CT manifestations were patchy or diffuse areas of ground-glass attenuation (Fig 8). Associated areas of consolidation were present in the lower lung zones in 71% of cases. Irregular lines were present at CT in two patients (29%) and, like the areas of ground-glass attenuation, had a patchy and random distribution with no zonal predominance. Honeycombing was not seen in any patient. NIPF has a relatively good prognosis, with most patients responding to corticosteroid treatment (7,27). Approximately 10% of patients die of progressive lung disease. No deaths 1020 U Imaging Symposium Volume 17 Number 4
6 Figures 9, 10. (9) BOOP. Photomicrograph (hematoxylin-cosin stain) shows edematous rounded polyps of connective tissue within air spaces (arrows). The adjacent air spaces are atelectatic and appear somewhat pinker. Away from the foci of organization (ie, at the periphery of the illustration), residual normal alveolar structure is apparent. When the edematous connective tissue involves the bronchioles, the term bronchiolitis obliterans (with intraluminal polyps) has been used, whereas similar tissue extending into alveolar ducts and more distal hung parenchyma has been termed organizing pneumonia. The presence of both entities is termed bronchiolitis obliterans with organizingpneurnonia; the organizing pneumonia component is illustrated here. (10) BOOP in an 81-year-old woman. High-resolution CT scan (1.0-mm collimation) shows bilateral areas of consolidation in a patchy distribution. The consolidation has a predominantly subpheural distribution, particularly in the right lung, and a peribronchial distribution in the left upper lobe. occurred in patients whose biopsy specimens showed pure inflammation and no fibrosis (7). It is important to distinguish NIPF from UIP because the latter has a poor prognosis. U IDIOPATHIC BOOP Idiopathic BOOP (also called cryptogenic organizing pneumonia) is characterized histologically by granulation tissue pohyps in the lumina of alveolar ducts and bronchioles in association with a variable degree of interstitial and airspace infiltration by mononuclear cells and foamy macrophages (28,29) (Fig 9). At presentation, most patients have a 1-6-month history of low-grade fever, dry cough, and progressive shortness of breath (19,30). The characteristic high-resolution CT fmdings are bilateral areas of consolidation, which have a predominantly subpleural or peribronchiah distribution in approximately 50%-60% of cases (3 1,32) (Fig 10). The consolidation tends to involve all lung zones. Less common findings include areas of ground-glass attenuation, small ifi-dcfmed nodules, and irregular linear areas of increased attenuation (31,32). BOOP has a relatively good prognosis, with most patients showing complete resolution of the abnormalities after corticosteroid treatment (28,30). Approximately 30% of patients have persistent abnormalities, and 10% die of progressive or recurrent disease (30). U CONCLUSIONS High-resolution CT allows confident diagnosis of UIP in most cases. The remaining idiopathic interstitial pneumonias have nonspecific CT fmdings. The prognosis is best in patients with active inflammation (ground-glass attenuation at high-resolution CT) and relatively little fibrosis (reticulation or honcycombing at high-resolution CT) but is worse in AlP and UIP regardless of the CT findings. July-August 1997 Muller and Colby U RadioGraphics U 1021
7 U REFERENCES 1. Liebow AA. New concepts and entities in pulmonary disease. Monogr Pathol 1968; 8: Ohori NP, Sciurba FC, Owens GR, et al. Giant cell interstitial pneumonia and hard-metal pneumoconiosis: a clinicopathologic study of four cases and review of the literature. Am J SurgPathol 1989; 13: Gibbs AR, Seal RME. Primary lymphoproli.ferative conditions of the lung. Thorax 1978; 33: Colby TV, Carrington CB. Interstitial hung disease. In: Thurlbeck WM, Churg AM, eds. Pathology of the hung. 2nd ed. New York, NY: Thieme Medical, 1995; Churg A, Katzenstein ALA, eds. The hung: current concepts. Baltimore, Md: Williams & Wilkins, Katzenstein ALA, Myers JL, Mazur MT. Acute interstitial pneumonia: a chinicopathologic, ultrastructural, and cell kinetic study. Am J Surg Pathol 1986; 10: Katzenstein ALA, Fiorelhi RF. Nonspecific interstitial pneumonia/fibrosis. Am J Surg Pathol 1994; 18: Hamman L, Rich AR. Acute diffuse interstitiah fibrosis of the lungs. Bull Johns Hopkins Hosp 1944; 74: Olson J, Colby TV, Elliott CG. Hamman-Rich syndrome revisited. Mayo Clin Proc 1990; 65: Crystal RG, Bitterman PB, Rennard SI, Hance AJ, Keogh BA. Interstitial lung diseases of unknown cause: disorders characterized by chronic inflammation of the lower respiratory tract (first of two parts). N Engl J Med 1984; 3 10: Askin FB. Acute interstitial pneumonia: histopathologic patterns of acute lung injury and the Hamman-Rich syndrome revisited. Radiohogy 1993; 188: Primack SL, Hartman TE, Ikezoe J, Akira M, Sakatani M, Muller NL. Acute interstitial pneumonia: radiographic and CT findings in nine patients. Radiology 1993; 188: McAdams HP, Rosado-de-Christenson ML, Wehunt WD, Fishback NF. The alphabet soup revisited: the chronic interstitial pneumonias in the 1990s. RadioGraphics 1996; 16: Liebow AA, Steer A, BilhingsleyJG. Desquamative interstitial pneumonia. Am J Med 1965; 38: Hartman TE, Primack SL, Swensen SJ, Hansell D, McGuinness G, Muller NL. Desquamative interstitial pneumonia: thin-section CT findings in 22 patients. Radiology 1993; 187: Carrington CB, Gaensler EA, Coutu RE, Fitz- Gerald MX, Gupta RG. Natural history and treated course of usual and desquamative interstitial pneumonia. N EnglJ Med 1978; 298: Yousem SA, Colby TV, Gaensler PA. Respiratory bronchiohitis-associated interstitial lung disease and its relationship to desquamative interstitial pneumonia. Mayo Chin Proc 1989; 64: Hartman TE, Primack SL, Kang EY, et ah. Disease progression in usual interstitial pneumonia compared with desquamative interstitial pneumonia: assessment with serial CT. Chest 1996; 110: MUller NL, Guerry-Force ML, Staples CA, et al. Differential diagnosis of bronchiolitis obliterans with organizing pneumonia and usual interstitial pneumonia: clinical, functional, and radiologic findings. Radiology 1987; 162: Muller NL, Miller RR, Webb WR, Evans KG, Ostrow DN. Fibrosing ahveolitis: CT-pathologic correlation. Radiology 1986; 160: Staples CA, Muller NL, Vedal S, Abboud R, Ostrow D, Miller R. Usual interstitial pneumonia: correlation of CT with clinical, functional, and radiologic findings. Radiology 1987; 162: Mathieson JR, Mayo JR, Staples CA, MUller NL. Chronic diffuse infiltrative hung disease: comparison of diagnostic accuracy of CT and chest radiography. Radiology 1989; 171 : Primack SL, Hartman TE, Hansell DM, Muller NL. End-stage lung disease: CT findings in 61 patients. Radiology 1993; 189: Muller NL, Staples CA, Miller RR, Vedal S, Thurhbeck WM, Ostrow DN. Disease activity in idiopathic pulmonary fibrosis: CT and pathologic correlation. Radiology 1987; 165: Leung AN, Miller RR, Muller NL. Parenchymal opacification in chronic infiltrative hung diseases: CT-pathologic correlation. Radiology 1993; 188: Remy-Jardin M, Giraud F, Remy J, Coppin MC, Gosselin B, Duhamel A. Importance of groundglass attenuation in chronic diffuse infiltrative hung disease: pathologic-ct correlation. Radiology 1993; 189: Park JS, Lee KS, Kim JS, et al. Nonspecific interstitial pneumonia with fibrosis: radiographic and CT findings in seven patients. Radiology 1995; 195: Epler GR, Colby TV, McLoud TC, Carrington CB, Gaensier EA. Bronchiolitis obliterans organizing pneumonia. N Engi J Med 1985; 312: Davison AG, Heard BE, McAllister WAC, Turncr-Warwick M. Cryptogenic organizing pneumonitis. QJ Med 1983; 52: King TE Jr, Mortenson RL. Cryptogenic organizing pneumonitis: the North American experience. Chest 1992; 102(supph):9S- 1 3S Muller NL, Staples CA, Miller RR. Bronchiohitis obliterans organizing pneumonia: CT features in 14 patients. AJR 1990; 154: Lee KS, Kuilnig P, Hartman TE, Muller NL. Cryptogenic organizing pneumonia: CT findings in 43 patients. AJR 1994; 162: U Imaging Symposium Volume 17 Number 4
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