Bronchiolitis Obliterans Organizing Pneumonia

REVIEW ARTICLE Bronchiolitis Obliterans Organizing Pneumonia

Gary R. Epler, MD

ronchiolar disorders can be divided into 2 general categories: (1) airway disorders (cel- lular bronchiolitis and obliterative bronchiolitis) and (2) parenchymal disorders (respiratory bronchiolitis–interstitial lung disease, which occurs in smokers and is treatable with smoking cessation or corticosteroid therapy, and bronchiolitis obliterans organizingB pneumonia, an inflammatory lung disease simultaneously involving the terminal bronchioles and alveoli). This article reviews the clinical findings and therapeutic management of bronchiolitis obliterans organizing pneumonia. Arch Intern Med. 2001;161:158-164

Bronchiolitis obliterans organizing pneu- The BOOP pattern might also occur as a monia (BOOP) was described in 19851 as secondary process in several clinical set- a distinct entity, with different clinical, ra- tings, such as the inflammatory-appearing diographic, and prognostic features than lesion of UIP/IPF, with Wegener granulo- the airway disorder obliterative bronchi- matosis, in the walls of lung abscesses, olitis2 and the interstitial fibrotic lung dis- around lymphoma or other neoplasms, and order usual interstitial pneumonia/ with bronchiectasis. In these patients, the idiopathic pulmonary fibrosis (UIP/IPF).3 underlying process is the primary cause of BOOP is characterized by polyploid en- symptoms and the subsequent clinical dobronchial connective tissue masses com- course. posed of myxoid fibroblastic tissue resem- The terms organizing pneumonia and bling granulation tissue filling the lumens cryptogenic organizing pneumonia are some- of terminal and respiratory bronchioles and times used for the broad category of pa- extending in a continuous fashion into al- tients with organizing pneumonia. There veolar ducts and alveoli, representing an are several reasons that the term BOOP organizing pneumonia (Figure 1).1-3 should continue to be used for the clini- Other histological features include cen- cal disorder and corresponding pathologi- tral clusters of mononuclear inflamma- cal lesion described in this review. First, tory cells possibly found in the intralumi- investigators and clinicians throughout the nal polyps (the polyps appear to float freely world recognize the clinical and patho- within a bronchiole or are focally attached logical features of this disorder, and they to the wall), chronic inflammation in the commonly use the term BOOP. Second, walls of the surrounding alveoli with re- BOOP is a histological process that in- active type II cells, increased foamy mac- volves distal airways and alveoli simulta- rophages in the alveoli, and preserved lung neously. Although various lung diseases architecture.2 represent a chronic inflammatory pro- BOOP continues to be reported cess, it is now apparent that the pro- throughout the world.4-7 Most patients have cesses differ markedly among various idiopathic BOOP, but there are several diseases, such as chronic obstructive known causes of BOOP, and several sys- pulmonary disease, asthma, and BOOP, temic disorders have BOOP as an associ- with different inflammatory cells, media- ated primary pulmonary lesion (Table). tors, inflammatory effects, and response to treatment.8 Therefore, an inflamma- From Harvard Medical School, Pulmonary and Critical Care Medicine, Brigham and tory lesion that involves only airways or Women’s Hospital, Boston, Mass. only alveoli may have different in-

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Idiopathic BOOP Rapidly progressive BOOP Focal nodular BOOP Postinfection BOOP Chlamydia, Legionella, and Mycoplasma Adenovirus, cytomegalovirus, and influenza virus Malaria and Pneumocystis Cryptococcus Drug-related BOOP Antibiotics: amphotericin B, cephalosporins, minocycline, nitrofurantoin, sulfasalazine, and sulfamethoxypyridazine Bleomycin sulfate and methotrexate Gold Amiodarone Illicit use of cocaine B L-tryptophan Phenytoin Carbamazepine Ticlopidine hydrochloride Rheumatologic or connective tissue BOOP Lupus erythematosus Rheumatoid arthritis Sjögren syndrome and Sweet syndrome Polymyositis-dermatomyositis Scleroderma–progressive systemic sclerosis Ankylosing spondylitis Polymylagia rheumatica Behçet syndrome Immunologic disorder BOOP Common variable immunodeficiency syndrome Essential mixed cryoglobulinemia Organ transplantation BOOP Bone marrow, lung, and renal Figure 1. A, Intraluminal organization and polypoid granulation tissue within a small bronchiole. Radiotherapy BOOP B, Organization and polypoid granulation tissue within small bronchioles, alveolar ducts, and alveoli. Environmental exposures The associated alveolar walls show type II cell metaplasia and mild inflammatory thickening. Courtesy Textile printing dye of Thomas V. Colby, MD, Department of Pathology, Mayo Clinic Scottsdale (Ariz) (both parts). Penicillium mold dust House fire Miscellaneous BOOP Inflammatory bowel disease flammatory components than the PATHOGENESIS OF BOOP Lymphoma and cancer BOOP lesion that involves airway T-cell chronic lymphocytic leukemia and alveoli simultaneously. Third, BOOP is an inflammatory lung dis- Human immunodeficiency virus investigations of specific treat- ease and thus is related to the inflam- infection ments for BOOP will be more matory pathway rather than the fi- Myelodysplastic syndrome Hunner interstitial cystitis strongly positive if the specific defi- brosing pathway that occurs with Chronic thydroiditis and alcoholic nition of BOOP is used for inclu- UIP/IPF. The inflammatory re- cirrhosis sion of patients rather than using the sponse associated with disorders such Seasonal syndrome with cholestasis broad definition of organizing pneu- as asthma, chronic obstructive pul- Primary biliary cirrhosis monia. This is similar to IPF, in monary disease, granulomatous dis- Coronary artery bypass graft surgery which many distinct histological diseases, and BOOP have common fea- *BOOP indicates bronchiolitis obliterans orders were included in this cat- tures of the sequential inflammatory organizing pneumonia. egory in the past, resulting in dilu- response, yet these disorders seem to tion of the actual mechanism and have differences that have not yet poor treatment results. Now that IPF been fully characterized. These dif- and UIP/IPF; in BOOP it can be com- is limited to UIP,3 the opportunity ferences are important because treat- pletely reversed by corticosteroid to fully characterize the fibrotic path- ment directed toward one type of in- therapy, but in UIP/IPF this tissue way is much greater, and antifi- flammatory response might not be participates in the remodeling and brotic treatment tailored to this fi- effective against another type.8 destruction of the interstitium.9,10 brotic pathway will be tested more There is newly formed fibro- Reasons for the response to cortico- efficiently and accurately. myxoid connective tissue in BOOP steroid in BOOP and the destruc-

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Figure 2. A, Chest radiograph of a 54-year-old man with a flulike illness, bilateral crackles, decreased vital capacity, and a decreased diffusing capacity that shows bilateral patchy infiltrates in the lower lungs. B, High-resolution chest computed tomographic scan shows areas of patchy consolidation and ground glass opacities. Courtesy of Philip Costello, MD, and Andetta R. Hunsaker, MD, Department of Radiology, Brigham and Women’s Hospital, Boston, Mass. C, Chest computed tomographic scan shows a triangular area of consolidation posteriorly.

tion in UIP/IPF remain unknown.11 opacities occurring at the bases are be recommend as first-line treat- There seems to be abundant capil- usually associated with a poorer ment for patients with symptomatic larization in the intra-airway fibro- prognosis; however, a study6 of and progressive disease. Patients with myxoid lesions in BOOP compared BOOP in 23 patients in Korea indi- asymptomatic mass lesions or non- with minimal vascularization in UIP/ cated recovery in all patients regard- progressive disease can be observed IPF.9 This might be because of vas- less of their radiographic findings. and treated at a later time if needed. cular growth factors in BOOP that Generally, the infiltrates gradually The dosage is generally 1 mg/kg (60 will result in normal apoptosis (natu- enlarge from their original site or mg/d) for 1 to 3 months, then 40 ral-occurring cell death) in BOOP new infiltrates appear as the clini- mg/d for 3 months, then 10 to 20 mg/d but not in UIP/IPF. Results of an ad- cal course progresses; however, mi- or every other day for a total of 1 year. ditional study10 showed that the gratory or “mobile” pulmonary in- Every-other-day scheduling can be apoptotic activity is higher in the fi- filtrates have been reported6,14,15 in successfully used for this disorder. A bromyxoid lesion of BOOP com- 10% to 25% of patients. Unilateral shorter 6-month course may be suf- pared with UIP/IPF, suggesting that BOOP also has been reported.16,17 ficient in certain situations. Total and apoptosis has an important role in The chest computed tomo- permanent recovery is seen in most the resolution process of the newly graphic scan shows findings similar patients and is somewhat depen- formed connective tissue in BOOP. to the chest radiograph, with bilat- dent on the cause or associated sys- eral areas of consolidation and ground temic disorders. Anecdotally, eryth- DIAGNOSING BOOP glass opacities, usually with a periph- romycin, inhaled triamcinolone, and eral location (Figure 2B). Costabel et cyclophosphamide have been used to Lung biopsy continues to be the pre- al15 reported that sometimes the pe- treat BOOP.19-21 Epidemiological ferred method for establishing a diag- ripheral opacities are in the form of studies of these agents have not yet nosis. The video-assisted thoraco- triangles, with the base of the tri- been performed for confirmation of scopic procedure has become the es- angle along the pleural surface and the efficacy. tablished technique. In a study12 of 49 tip of the triangle toward the medi- patients who underwent the video- astinum (Figure 2C). In a study18 RECURRENCE OF BOOP assisted thoracoscopic procedure for from England, high-resolution chest interstitial lung disease, the mean computed tomographic scans showed In patients treated for less than 1 length of the operation was 45 min- 2 types of linear opacities: the first ex- year, BOOP might recur in one third. utes, the chest tube was inserted for tends in a radial manner along the line It is a lung disorder that can be suc- 1.3 days, there were no deaths, there of the bronchi toward the pleura and cessfully treated a second and third werenoreexplorations,andnonewere the second occurs in a subpleural lo- time with the previously respon- converted to an open thoracotomy. cation with no relation to the bron- sive dosage level of prednisone.1 chi. Both types usually occur in the Relapse of BOOP may be related to RADIOGRAPHIC FINDINGS lower lobes, frequently associated the severity of the illness. In a group OF BOOP with multifocal areas of consolida- of 7 patients who had a relapse it tion, and usually completely resolve was found that the level of hypox- The typical chest radiograph shows with treatment. emia at the time of diagnosis was the bilateral patchy (alveolar) infil- most important determinant of re- trates (Figure 2A). Cavities are rare, TREATMENT OF BOOP lapse22; however, Cordier11 did not although 4 of 5 patients with a single find this relation. pulmonary nodule had cavita- Prednisone, with its potent anti- For patients who do not re- tion.13 Effusions are rare. Linear inflammatory property, continues to spond to treatment, it is important

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Downloaded From: https://jamanetwork.com/ on 10/01/2021 to determine if the BOOP pattern is pathological findings indicating an fections, including Cryptococcus neo- primary or secondary. On close organizing adult respiratory dis- formans41 and Pneumocystis carinii,42 evaluation by a lung pathologist, the tress syndrome pattern with the ap- have also been reported as a cause of biopsy specimen that shows the pearance of BOOP.30 Clinically, rap- the BOOP lesion. BOOP pattern might also show the idly progressive BOOP can be Generally for these patients, typical leading edge of “fibroblastic indistinguishable from acute inter- there is initial improvement of the foci” that indicates UIP/IPF. The stitial pneumonia.31,32 Early histo- infectious pneumonia with use of ap- BOOP pattern might respond to cor- logical diagnosis of the primary propriate antimicrobial agents, but ticosteroid therapy, yet the fibrotic BOOP lesion and initiation of cor- after a few days, it becomes appar- process of UIP/IPF is the driving ticosteroid therapy might improve ent that the symptoms and radio- force of the progressively deterio- survival in these patients.29 graphic findings persist. The pneu- rating clinical course. Focal nodular BOOP was re- monia process has now become ported33 in 1989 in 5 of 16 patients organized into the BOOP lesion. TYPES OF BOOP with idiopathic BOOP. Since then it Corticosteroid treatment at this point has become a clinically important is almost always successful. Idiopathic BOOP is the most com- process, especially because it might Drug-related BOOP has been mon type.1 A flulike illness, fever, and be indistinguishable from carci- reported11,15 from use of several dif- an increased erythrocyte sedimenta- noma of the lung.13,26,34-36 Although ferent types of medications, includ- tion rate continue to be typical find- some focal nodular lesions might ing anti-inflammatory and immu- ings of this form of BOOP. Cough and progress to the typical bilateral pro- nosuppressive agents such as dyspnea are common but generally cess of idiopathic BOOP, most do bleomycin sulfate, gold, and metho- mild. Hemoptysis is uncommon, al- not, and resection results in a cure. trexate; antibiotics such as sulfa- though it has been reported in 2 pa- Multiple nodular lesions can salazine, sulfamethoxypyridazine, tients as a presenting symptom23 and also occur,34,35 and most regress cephalosporins, and amphotericin in some patients with nodules.13,24 spontaneously. Of 12 patients with B; illicit use of cocaine; and a mas- Crackles occur in two thirds of pa- multiple large nodules or masses, all sive dose of L-tryptophan. Minocy- tients. Pneumothorax has occurred had complete resolution of their cline-associated BOOP has been as a complication of BOOP in one pa- symptoms, 10 with no therapy and reported43 in a woman who was tak- tient with an effusion,25 one with a 2 after corticosteroid therapy.34 In ing this medication for acne. De- solitary nodule,26 and another with these patients, pleuritic chest pain scriptions of amiodarone-related respiratory distress.27 Results of pul- was the most common presenting BOOP continue to be reported.44 monary function studies show mildly symptom, occurring in 50%. The Phenytoin-related BOOP with rapid to moderately decreased vital capac- number of masses varied from 2 to improvement after corticosteroid ity. The flow rates are normal ex- 8 (mean, 5). The authors con- therapy has been reported.45 There cept in smokers. The diffusing ca- cluded that BOOP should be con- has been a report46 of a woman who pacity is decreased in almost all sidered when multiple large nodu- developed carbamazepine-induced patients, although generally mildly to lar lesions have chest computed lupus erythematosus and associ- moderately. The prognosis of idio- tomographic findings showing air ated BOOP, both of which re- pathic BOOP remains good, some pa- bronchograms, irregular margins, sponded to corticosteroid therapy. tients resolve without treatment, and broad pleural tags, parenchymal There has been a report47 of ticlopi- 65% to 80% of patients treated with bands, or subpleural lines. dine hydrochloride, an inhibitor of corticosteroid therapy are cured. Clinician investigators36 in New platelet aggregation, associated with Rapidly progressive BOOP can Orleans suggest that BOOP may have BOOP that resolved after with- occur in a small percentage of pa- a connection to reports of sponta- drawal of the agent. BOOP has now tients, but it is a deadly form of the neous regression of lung metasta- been added to the spectrum of pul- disease.28,29 In some of these pa- ses. They concluded that a major rea- monary lesions associated with ni- tient reports, there was an underly- son that reports of spontaneous trofurantoin.48 ing fibrotic process as the cause of regression of lung metastasis have Rheumatologic or connective the ultimate fatal course, with BOOP decreased in recent years is the in- tissue BOOP is clinically similar to as a secondary component, yet some creasing emphasis on obtaining di- the idiopathic form and has been re- patients seemed to have a primary, agnostic tissue of multiple nodular ported49-57 with all of the connec- rapidly developing BOOP, which lesions for lung metastasis, many of tive tissue diseases. BOOP repre- had a better prognosis. This form of which have proven to be BOOP. sents the patchy infiltrative lesions BOOP occurs equally in men and Postinfection BOOP can de- seen in patients with lupus erythem- women and at all ages. It can occur velop after a variety of different types atosus, rheumatoid arthritis, Sjo¨- in healthy, vigorous individuals or of infectious pneumonias,11 includ- gren syndrome, and dermatomyo- can be associated with other sys- ing those caused by bacterial agents sitis. The process often responds to temic disorders. The course can be such as Chlamydia,37 Legionella, and corticosteroid therapy, unlike the fi- rapid, with 1 to 3 days of symp- Mycoplasma pneumoniae38 and viral brotic process that may occur in toms and acute respiratory failure. agents such as parainfluenza virus16 these disorders. Patients might present with adult and adenovirus.39 Parasitic infec- There has been a report of a pa- respiratory distress syndrome, with tions such as malaria40 and fungal in- tient with BOOP associated with der-

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Downloaded From: https://jamanetwork.com/ on 10/01/2021 matomyositis that was resistant to Radiotherapy BOOP has be- with cholestasis.76 It has been re- corticosteroid therapy; with initia- come an important clinical disorder ported in patients with human tion of cyclophosphamide therapy, in patients receiving radiotherapy to immunodeficiency virus infec- there was improvement of pulmo- the breast.65-68 Symptoms might oc- tion,77 with one report during preg- nary and cutaneous findings.52 cur 1 to 12 months after completion nancy.78 Inflammatory bowel disease– BOOP can also occur in patients with of radiotherapy. Symptoms might be related BOOP has been described79 as ankylosing spondylitis,53 polymyal- minimal, but most patients have fe- an important treatable disorder in gia rheumatica,54,55 and Behc¸et dis- ver, nonproductive cough, and mild these patients. The BOOP lesion ease56 and might be the first mani- shortness of breath. The chest radio- might be associated with lym- festation of a connective disorder.57 graph shows peripheral patchy or al- phoma, and an atypical course of Immunologic disease BOOP veolar infiltrates, often outside the ra- what is thought to be idiopathic has been reported with common diation field.66 One study68 indicated BOOP may indicate a neoplastic pro- variable immunodeficiency syn- that all 11 patients studied had spon- cess such as a lymphoma.80 Recur- drome58 and essential mixed taneous migration of infiltrates from rent BOOP responsive to predni- cryoglobulinemia.59 the irradiated lung to the contralat- sone treatment has been reported in Bone marrow transplantation eral nonirradiated lung with no nodu- T-cell leukemia.81,82 BOOP has also BOOP has been described in patients lar or reticular lesions. There can be been reported in primary biliary cir- who underwent allogeneic marrow a dramatic improvement with corti- rhosis83 and after coronary artery by- transplantation. There has also been costeroid therapy, but relapses may pass graft surgery.84 a report of BOOP in a patient who occur.66,67 Some investigators66,68 have received a syngeneic bone marrow suggested that radiotherapy may CONCLUSIONS transplant from his twin brother.60 “prime” the development of BOOP. There is an additional report of a pa- Bronchoalveolar lavage studies of The busy clinician will see patients tient who developed ulcerative coli- these patients indicate an increase in with a febrile illness and patchy in- tis and BOOP 7 months after receiv- lymphocytes, mast cells, CD3 cells, filtrates who have not responded to ing a bone marrow transplant from his and CD8 cells and a decrease in CD4 antibiotic drug therapy. The pa- brother.61 It was not clear whether the cells and the CD4-CD8 ratio68; how- tient might have BOOP. Sometimes BOOP was associated with the ulcer- ever, the underlying mechanism re- this disorder is treated in the hos- ative colitis or from another cause, mains unknown. pital, but it is generally managed on such as a cytomegalovirus infection. Environment-related BOOP an ambulatory basis. Typical idio- Too few reports have been published continues to be reported rarely. In pathic BOOP is characterized by a to determine whether BOOP in these 1992, textile printing dye–related flulike illness, bilateral crackles, and patients is an incidental finding or rep- BOOP was described in 22 textile air- patchy infiltrates and can be cured resents a complication of bone mar- brush workers.69 Six died initially. in 65% to 80% of patients with pred- row transplantation. Follow-up of some of the workers in- nisone therapy. BOOP has become Lung transplantation BOOP has dicated gradual improvement over an important consideration in the di- been reported62,63 in 10% to 28% of time.70 It has been suggested69 that agnosis of focal nodular lesions. lung transplant recipients. The le- the cause was related to the spray- Postinfectious pneumonia BOOP re- sion generally occurs 1 to 10 months ing of a respirable aerosol into the mains a treatable process. BOOP oc- after transplantation and is usually distal airways and alveoli; how- curs in virtually all of the connec- associated with the acute rejection ever, the reactive chemical agent and tive tissue disorders and generally reaction. The process is reversible for mechanism remain unclear. It is also responds to corticosteroid therapy. most of these patients, especially if not known whether the organizing It is an important treatable inflam- the underlying acute rejection is pneumonia was a de novo process matory lung disease. successfully treated. The BOOP le- or resulted from the late organiza- sion may occur before the onset of tion of pulmonary edema.69 Penicil- Accepted for publication August 15, obliterative bronchiolitis,62 and lium mold dust–related BOOP has 2000. whether this is a risk factor for lung been described71 in a patient who de- Corresponding author and re- transplantation obliterative bron- veloped BOOP after inhalation of prints: Gary R. Epler, MD, Pulmo- chiolitis has not been established, powdery dust of a growth of Peni- nary and Critical Care Medicine, but it is prudent to treat the BOOP cillium janthinellum mold on the top Brigham and Women’s Hospital, 75 reactions aggressively in these pa- of a discarded orange juice con- Francis St, Boston, MA 02115 (e- tients. Cytomegalovirus pneumonia– tainer. Smoke inhalation BOOP has mail: [email protected]). associated BOOP has also been de- been reported72 in a patient who was scribed63 in lung transplant in a house fire and had erythema no- recipients and is generally respon- dosum. REFERENCES sive to corticosteroid therapy. Miscellaneous BOOP contin- Renal transplantation BOOP has ues to be reported, eg, in association 1. Epler GR, Colby TV, McLoud TC, Carrington CB, been described64 in 1 patient 12 weeks with myelodysplastic syndrome,73 Gaensler EA. Bronchiolitis obliterans organizing 74 pneumonia. N Engl J Med. 1985;312:152-158. after transplantation. A rapid recov- Hunner interstitial cystitis, chronic 2. Colby TV. Bronchiolitis. Am J Clin Pathol. 1998; 75 75 ery occurred after an increase of the thyroiditis, alcoholic cirrhosis, 109:101-109. daily dose of methylprednisolone. and, in England, seasonal syndrome 3. American Thoracic Society and European Respi-

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