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Bronchiolitis Obliterans Organizing Pneumonia
Gary R. Epler, MD
Arch Intern Med. 2001;161:158-164.
ABSTRACT
Bronchiolar disorders can be divided into 2 general categories: (1)
airway disorders (cellular 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 organizing 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.
INTRODUCTION
Bronchiolitis obliterans organizing pneumonia (BOOP) was described in
19851 as a distinct entity, with different
clinical, radiographic, and prognostic features than the airway disorder obliterative
bronchiolitis2 and the interstitial fibrotic
lung disorder usual interstitial pneumonia/idiopathic pulmonary fibrosis (UIP/IPF).3 BOOP is characterized by polyploid endobronchial connective
tissue masses composed of myxoid fibroblastic tissue resembling granulation
tissue filling the lumens of terminal and respiratory bronchioles and extending
in a continuous fashion into alveolar ducts and alveoli, representing an organizing
pneumonia (Figure 1).1, 2, 3
Other histological features include central clusters of mononuclear inflammatory
cells possibly found in the intraluminal polyps (the polyps appear to float
freely within a bronchiole or are focally attached to the wall), chronic inflammation
in the walls of the surrounding alveoli with reactive type II cells, increased
foamy macrophages in the alveoli, and preserved lung architecture.2
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Figure 1. A, Intraluminal organization and
polypoid granulation tissue within a small bronchiole. B, Organization and
polypoid granulation tissue within small bronchioles, alveolar ducts, and
alveoli. The associated alveolar walls show type II cell metaplasia and mild
inflammatory thickening. Courtesy of Thomas V. Colby, MD, Department of Pathology,
Mayo Clinic Scottsdale (Ariz) (both parts).
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BOOP continues to be reported throughout the world.4, 5, 6, 7
Most patients have idiopathic BOOP, but there are several known causes of
BOOP, and several systemic disorders have BOOP as an associated primary pulmonary
lesion (Table 1). The BOOP pattern
might also occur as a secondary process in several clinical settings, such
as the inflammatory-appearing lesion of UIP/IPF, with Wegener granulomatosis,
in the walls of lung abscesses, around lymphoma or other neoplasms, and with
bronchiectasis. In these patients, the underlying process is the primary cause
of symptoms and the subsequent clinical course.
The terms organizing pneumonia and cryptogenic organizing pneumonia are sometimes used for the broad category
of patients with organizing pneumonia. There are several reasons that the
term BOOP should continue to be used for the clinical
disorder and corresponding pathological lesion described in this review. First,
investigators and clinicians throughout the world recognize the clinical and
pathological features of this disorder, and they commonly use the term BOOP.
Second, BOOP is a histological process that involves distal airways and alveoli
simultaneously. Although various lung diseases represent a chronic inflammatory
process, it is now apparent that the processes differ markedly among various
diseases, such as chronic obstructive pulmonary disease, asthma, and BOOP,
with different inflammatory cells, mediators, inflammatory effects, and response
to treatment.8 Therefore, an inflammatory lesion
that involves only airways or only alveoli may have different inflammatory
components than the BOOP lesion that involves airway and alveoli simultaneously.
Third, investigations of specific treatments for BOOP will be more strongly
positive if the specific definition of BOOP is used for inclusion of patients
rather than using the broad definition of organizing pneumonia. This is similar
to IPF, in which many distinct histological disorders were included in this
category in the past, resulting in dilution of the actual mechanism and poor
treatment results. Now that IPF is limited to UIP,3
the opportunity to fully characterize the fibrotic pathway is much greater,
and antifibrotic treatment tailored to this fibrotic pathway will be tested
more efficiently and accurately.
PATHOGENESIS OF BOOP
BOOP is an inflammatory lung disease and thus is related to the inflammatory
pathway rather than the fibrosing pathway that occurs with UIP/IPF. The inflammatory
response associated with disorders such as asthma, chronic obstructive pulmonary
disease, granulomatous diseases, and BOOP have common features of the sequential
inflammatory response, yet these disorders seem to have differences that have
not yet been fully characterized. These differences are important because
treatment directed toward one type of inflammatory response might not be effective
against another type.8
There is newly formed fibromyxoid connective tissue in BOOP and UIP/IPF;
in BOOP it can be completely reversed by corticosteroid therapy, but in UIP/IPF
this tissue participates in the remodeling and destruction of the interstitium.9, 10 Reasons for the response to corticosteroid
in BOOP and the destruction in UIP/IPF remain unknown.11
There seems to be abundant capillarization in the intra-airway fibromyxoid
lesions in BOOP compared with minimal vascularization in UIP/IPF.9 This might be because of vascular growth factors in
BOOP that will result in normal apoptosis (natural-occurring cell death) in
BOOP but not in UIP/IPF. Results of an additional study10
showed that the apoptotic activity is higher in the fibromyxoid lesion of
BOOP compared with UIP/IPF, suggesting that apoptosis has an important role
in the resolution process of the newly formed connective tissue in BOOP.
DIAGNOSING BOOP
Lung biopsy continues to be the preferred method for establishing a
diagnosis. The video-assisted thoracoscopic procedure has become the established
technique. In a study12 of 49 patients who
underwent the video-assisted thoracoscopic procedure for interstitial lung
disease, the mean length of the operation was 45 minutes, the chest tube was
inserted for 1.3 days, there were no deaths, there were no reexplorations,
and none were converted to an open thoracotomy.
RADIOGRAPHIC FINDINGS OF BOOP
The typical chest radiograph shows bilateral patchy (alveolar) infiltrates
(Figure 2A). Cavities are rare,
although 4 of 5 patients with a single pulmonary nodule had cavitation.13 Effusions are rare. Linear opacities occurring at
the bases are usually associated with a poorer prognosis; however, a study6 of BOOP in 23 patients in Korea indicated recovery
in all patients regardless of their radiographic findings. Generally, the
infiltrates gradually enlarge from their original site or new infiltrates
appear as the clinical course progresses; however, migratory or "mobile" pulmonary
infiltrates have been reported6, 14, 15
in 10% to 25% of patients. Unilateral BOOP also has been reported.16, 17
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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.
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The chest computed tomographic scan shows findings similar to the chest
radiograph, with bilateral areas of consolidation and ground glass opacities,
usually with a peripheral location (Figure
2 B). Costabel et al15 reported that
sometimes the peripheral opacities are in the form of triangles, with the
base of the triangle along the pleural surface and the tip of the triangle
toward the mediastinum (Figure 2
C). In a study18 from England, high-resolution
chest computed tomographic scans showed 2 types of linear opacities: the first
extends in a radial manner along the line of the bronchi toward the pleura
and the second occurs in a subpleural location with no relation to the bronchi.
Both types usually occur in the lower lobes, frequently associated with multifocal
areas of consolidation, and usually completely resolve with treatment.
TREATMENT OF BOOP
Prednisone, with its potent anti-inflammatory property, continues to
be recommend as first-line treatment for patients with symptomatic and progressive
disease. Patients with asymptomatic mass lesions or nonprogressive disease
can be observed and treated at a later time if needed. The dosage is generally
1 mg/kg (60 mg/d) for 1 to 3 months, then 40 mg/d for 3 months, then 10 to
20 mg/d or every other day for a total of 1 year. Every-other-day scheduling
can be successfully used for this disorder. A shorter 6-month course may be
sufficient in certain situations. Total and permanent recovery is seen in
most patients and is somewhat dependent on the cause or associated systemic
disorders. Anecdotally, erythromycin, inhaled triamcinolone, and cyclophosphamide
have been used to treat BOOP.19, 20, 21
Epidemiological studies of these agents have not yet been performed for confirmation
of efficacy.
RECURRENCE OF BOOP
In patients treated for less than 1 year, BOOP might recur in one third.
It is a lung disorder that can be successfully treated a second and third
time with the previously responsive dosage level of prednisone.1
Relapse of BOOP may be related to the severity of the illness. In a group
of 7 patients who had a relapse it was found that the level of hypoxemia at
the time of diagnosis was the most important determinant of relapse22; however, Cordier11
did not find this relation.
For patients who do not respond to treatment, it is important to determine
if the BOOP pattern is primary or secondary. On close evaluation by a lung
pathologist, the biopsy specimen that shows the BOOP pattern might also show
the typical leading edge of "fibroblastic foci" that indicates UIP/IPF. The
BOOP pattern might respond to corticosteroid therapy, yet the fibrotic process
of UIP/IPF is the driving force of the progressively deteriorating clinical
course.
TYPES OF BOOP
Idiopathic BOOP is the most common type.1
A flulike illness, fever, and an increased erythrocyte sedimentation rate
continue to be typical findings of this form of BOOP. Cough and dyspnea are
common but generally mild. Hemoptysis is uncommon, although it has been reported
in 2 patients as a presenting symptom23 and
in some patients with nodules.13, 24
Crackles occur in two thirds of patients. Pneumothorax has occurred as a complication
of BOOP in one patient with an effusion,25
one with a solitary nodule,26 and another with
respiratory distress.27 Results of pulmonary
function studies show mildly to moderately decreased vital capacity. The flow
rates are normal except in smokers. The diffusing capacity is decreased in
almost all patients, although generally mildly to moderately. The prognosis
of idiopathic BOOP remains good, some patients resolve without treatment,
and 65% to 80% of patients treated with corticosteroid therapy are cured.
Rapidly progressive BOOP can occur in a small percentage of patients,
but it is a deadly form of the disease.28, 29
In some of these patient reports, there was an underlying fibrotic process
as the cause of the ultimate fatal course, with BOOP as a secondary component,
yet some patients seemed to have a primary, rapidly developing BOOP, which
had a better prognosis. This form of BOOP occurs equally in men and women
and at all ages. It can occur in healthy, vigorous individuals or can be associated
with other systemic disorders. The course can be rapid, with 1 to 3 days of
symptoms and acute respiratory failure. Patients might present with adult
respiratory distress syndrome, with pathological findings indicating an organizing
adult respiratory distress syndrome pattern with the appearance of BOOP.30 Clinically, rapidly progressive BOOP can be indistinguishable
from acute interstitial pneumonia.31, 32
Early histological diagnosis of the primary BOOP lesion and initiation of
corticosteroid therapy might improve survival in these patients.29
Focal nodular BOOP was reported33 in
1989 in 5 of 16 patients with idiopathic BOOP. Since then it has become a
clinically important process, especially because it might be indistinguishable
from carcinoma of the lung.13, 26, 34, 35, 36
Although some focal nodular lesions might progress to the typical bilateral
process of idiopathic BOOP, most do not, and resection results in a cure.
Multiple nodular lesions can also occur,34, 35
and most regress spontaneously. Of 12 patients with multiple large nodules
or masses, all had complete resolution of their symptoms, 10 with no therapy
and 2 after corticosteroid therapy.34 In these
patients, pleuritic chest pain was the most common presenting symptom, occurring
in 50%. The number of masses varied from 2 to 8 (mean, 5). The authors concluded
that BOOP should be considered when multiple large nodular lesions have chest
computed tomographic findings showing air bronchograms, irregular margins,
broad pleural tags, parenchymal bands, or subpleural lines.
Clinician investigators36 in New Orleans
suggest that BOOP may have a connection to reports of spontaneous regression
of lung metastases. They concluded that a major reason that reports of spontaneous
regression of lung metastasis have decreased in recent years is the increasing
emphasis on obtaining diagnostic tissue of multiple nodular lesions for lung
metastasis, many of which have proven to be BOOP.
Postinfection BOOP can develop after a variety of different types of
infectious pneumonias,11 including those caused
by bacterial agents such as Chlamydia,37 Legionella, and Mycoplasma pneumoniae38 and viral agents such as parainfluenza
virus16 and adenovirus.39
Parasitic infections such as malaria40 and
fungal infections, including Cryptococcus neoformans41 and Pneumocystis carinii,42 have also been reported as a cause of the BOOP lesion.
Generally for these patients, there is initial improvement of the infectious
pneumonia with use of appropriate antimicrobial agents, but after a few days,
it becomes apparent that the symptoms and radiographic findings persist. The
pneumonia process has now become organized into the BOOP lesion. Corticosteroid
treatment at this point is almost always successful.
Drug-related BOOP has been reported11, 15
from use of several different types of medications, including anti-inflammatory
and immunosuppressive agents such as bleomycin sulfate, gold, and methotrexate;
antibiotics such as sulfasalazine, sulfamethoxypyridazine, cephalosporins,
and amphotericin B; illicit use of cocaine; and a massive dose of L-tryptophan.
Minocycline-associated BOOP has been reported43
in a woman who was taking this medication for acne. Descriptions of amiodarone-related
BOOP continue to be reported.44 Phenytoin-related
BOOP with rapid improvement after corticosteroid therapy has been reported.45 There has been a report46
of a woman who developed carbamazepine-induced lupus erythematosus and associated
BOOP, both of which responded to corticosteroid therapy. There has been a
report47 of ticlopidine hydrochloride, an inhibitor
of platelet aggregation, associated with BOOP that resolved after withdrawal
of the agent. BOOP has now been added to the spectrum of pulmonary lesions
associated with nitrofurantoin.48
Rheumatologic or connective tissue BOOP is clinically similar to the
idiopathic form and has been reported49, 50, 51, 52, 53, 54, 55, 56, 57
with all of the connective tissue diseases. BOOP represents the patchy infiltrative
lesions seen in patients with lupus erythematosus, rheumatoid arthritis, Sjögren
syndrome, and dermatomyositis. The process often responds to corticosteroid
therapy, unlike the fibrotic process that may occur in these disorders.
There has been a report of a patient with BOOP associated with dermatomyositis
that was resistant to corticosteroid therapy; with initiation of cyclophosphamide
therapy, there was improvement of pulmonary and cutaneous findings.52 BOOP can also occur in patients with ankylosing spondylitis,53 polymyalgia rheumatica,54, 55
and Behçet disease56 and might be the
first manifestation of a connective disorder.57
Immunologic disease BOOP has been reported with common variable immunodeficiency
syndrome58 and essential mixed cryoglobulinemia.59
Bone marrow transplantation BOOP has been described in patients who
underwent allogeneic marrow transplantation. There has also been a report
of BOOP in a patient who received a syngeneic bone marrow transplant from
his twin brother.60 There is an additional
report of a patient who developed ulcerative colitis and BOOP 7 months after
receiving a bone marrow transplant from his brother.61
It was not clear whether the BOOP was associated with the ulcerative colitis
or from another cause, such as a cytomegalovirus infection. Too few reports
have been published to determine whether BOOP in these patients is an incidental
finding or represents a complication of bone marrow transplantation.
Lung transplantation BOOP has been reported62, 63
in 10% to 28% of lung transplant recipients. The lesion generally occurs 1
to 10 months after transplantation and is usually associated with the acute
rejection reaction. The process is reversible for most of these patients,
especially if the underlying acute rejection is successfully treated. The
BOOP lesion may occur before the onset of obliterative bronchiolitis,62 and whether this is a risk factor for lung transplantation
obliterative bronchiolitis has not been established, but it is prudent to
treat the BOOP reactions aggressively in these patients. Cytomegalovirus pneumonia–associated
BOOP has also been described63 in lung transplant
recipients and is generally responsive to corticosteroid therapy.
Renal transplantation BOOP has been described64
in 1 patient 12 weeks after transplantation. A rapid recovery occurred after
an increase of the daily dose of methylprednisolone.
Radiotherapy BOOP has become an important clinical disorder in patients
receiving radiotherapy to the breast.65, 66, 67, 68
Symptoms might occur 1 to 12 months after completion of radiotherapy. Symptoms
might be minimal, but most patients have fever, nonproductive cough, and mild
shortness of breath. The chest radiograph shows peripheral patchy or alveolar
infiltrates, often outside the radiation field.66
One study68 indicated that all 11 patients
studied had spontaneous migration of infiltrates from the irradiated lung
to the contralateral nonirradiated lung with no nodular or reticular lesions.
There can be a dramatic improvement with corticosteroid therapy, but relapses
may occur.66, 67 Some investigators66, 68 have suggested that radiotherapy
may "prime" the development of BOOP. Bronchoalveolar lavage studies of these
patients indicate an increase in lymphocytes, mast cells, CD3 cells, and CD8
cells and a decrease in CD4 cells and the CD4-CD8 ratio68;
however, the underlying mechanism remains unknown.
Environment-related BOOP continues to be reported rarely. In 1992, textile
printing dye–related BOOP was described in 22 textile airbrush workers.69 Six died initially. Follow-up of some of the workers
indicated gradual improvement over time.70
It has been suggested69 that the cause was
related to the spraying of a respirable aerosol into the distal airways and
alveoli; however, the reactive chemical agent and mechanism remain unclear.
It is also not known whether the organizing pneumonia was a de novo process
or resulted from the late organization of pulmonary edema.69 Penicillium mold dust–related BOOP has been described71 in a patient who developed BOOP after inhalation
of powdery dust of a growth of Penicillium janthinellum mold on the top of a discarded orange juice container. Smoke inhalation
BOOP has been reported72 in a patient who was
in a house fire and had erythema nodosum.
Miscellaneous BOOP continues to be reported, eg, in association with
myelodysplastic syndrome,73 Hunner interstitial
cystitis,74 chronic thyroiditis,75
alcoholic cirrhosis,75 and, in England, seasonal
syndrome with cholestasis.76 It has been reported
in patients with human immunodeficiency virus infection,77
with one report during pregnancy.78 Inflammatory
bowel disease–related BOOP has been described79
as an important treatable disorder in these patients. The BOOP lesion might
be associated with lymphoma, and an atypical course of what is thought to
be idiopathic BOOP may indicate a neoplastic process such as a lymphoma.80 Recurrent BOOP responsive to prednisone treatment
has been reported in T-cell leukemia.81, 82
BOOP has also been reported in primary biliary cirrhosis83
and after coronary artery bypass graft surgery.84
CONCLUSIONS
The busy clinician will see patients with a febrile illness and patchy
infiltrates who have not responded to antibiotic drug therapy. The patient
might have BOOP. Sometimes this disorder is treated in the hospital, but it
is generally managed on an ambulatory basis. Typical idiopathic BOOP is characterized
by a flulike illness, bilateral crackles, and patchy infiltrates and can be
cured in 65% to 80% of patients with prednisone therapy. BOOP has become an
important consideration in the diagnosis of focal nodular lesions. Postinfectious
pneumonia BOOP remains a treatable process. BOOP occurs in virtually all of
the connective tissue disorders and generally responds to corticosteroid therapy.
It is an important treatable inflammatory lung disease.
AUTHOR INFORMATION
Accepted for publication August 15, 2000.
From Harvard Medical School, Pulmonary and Critical Care Medicine,
Brigham and Women's Hospital, Boston, Mass.
Corresponding author and reprints: Gary R. Epler, MD, Pulmonary and
Critical Care Medicine, Brigham and Women's Hospital, 75 Francis St, Boston,
MA 02115 (e-mail: gepler{at}mediaone.net).
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