CHEST. A55-year-old man was initially given a diagnosis of. Postgraduate Education Corner
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1 CHEST Postgraduate Education Corner CHEST IMAGING AND PATHOLOGY FOR CLINICIANS Recurrent Fevers, Cough, and Pulmonary Opacities in a Middle-Aged Man Philippe R. Bauer, MD, PhD, FCCP ; Clive S. Zent, MD ; Marie-Christine Aubry, MD, FCCP ; and Jay H. Ryu, MD, FCCP CHEST 2010; 137( 6 ): Case Presentation A55-year-old man was initially given a diagnosis of chronic lymphocytic leukemia (CLL) in April 1994 at age 44 years. After a period of observation, he was treated for progressive disease with chlorambucil in 1996 and again in In 2003, a prognostic marker evaluation showed that his CLL cells displayed highrisk biologic factors (unmutated Ig heavy chain variable region, and expression of CD38 and z-chain-associated protein 70) for progressive disease. 1 The patient then developed cytopenia and was treated for progressive CLL in October 2003 with one cycle of high-dose dexamethasone (200 mg m 22 day days) and rituximab (375 mg m 22 week weeks) (Rituxan; Biogen Idec, Inc. and Genentech, Inc.; South San Francisco, CA ), with an improvement in his blood counts. In 2005, he was treated on a phase one clinical trial with a single subcutaneous dose of CpG 7909 (ProMune; Pfizer Inc; New York, NY) (a new class of investigational synthetic oligonucleotide agonists of Toll-like receptor 9). This resulted in a short-term decrease in his lymphocyte count. In June 2005, the patient was again treated for progressive CLL causing cytopenias with high-dose methylprednisolone (1,000 mg m 22 day21 35 days) and rituximab (375 mg m 22 week weeks). He had a good response and was in remission until April 2006, when he developed drenching night sweats, fever, dry cough, back pain, and weight loss. Physical examination and chest radiographs were unremarkable. CT scan of the chest showed moderate bilateral axillary lymphadenopathy, mild bilateral hilar, and mediastinal lymphadenopathy, along with diffuse, finely nodular opacities in both lungs ( Fig 1 ). On bronchoscopy, the right upper lobe transbronchial biopsy specimen showed focal organizing pneumonia ( Fig 2 ). Special stains on the biopsy specimen and microbial cultures of the BAL fluid were negative for microorganisms. Because of cytopenia and worsening disease, the patient was again treated with methylprednisolone and rituximab. Two days later, he had recurrence of chills, cough, backache, and muscle cramps, similar to the symptoms he had initially presented with the month before. He improved with prednisone treatment (80 mg daily initially), which was tapered off over a 3-month period. In November 2006, he had severe sinusitis, which responded to antibiotics and corticosteroids; he was subsequently started on IV Ig infusions. In August 2007 and in March 2008, he was again treated with methylprednisolone and rituximab for Manuscript received May 20, 2009 ; revision accepted January 7, Affiliations: From the Division of Pulmonary and Critical Care Medicine (Drs Bauer and Ryu), the Division of Hematology (Dr Zent), and the Division of Anatomic Pathology (Dr Aubry), Mayo Clinic, Rochester, MN. Correspondence to: Philippe R. Bauer, MD, PhD, FCCP, Division of Pulmonary and Critical Care Medicine, Mayo Clinic, 200 First Street SW, Rochester, MN 55905; bauer.philippe@mayo.edu. Reproduction of this article is prohibited without written permission from the American College of Chest Physicians ( www. chestpubs. org site misc reprints.xhtml ). DOI: chest Figure 1. Chest CT scan during the first episode showing diffuse centrilobular nodules highly suggestive of subacute hypersensitivity pneumonitis. CHEST / 137 / 6 / JUNE,
2 Figure 2. Transbronchial lung biopsy specimen during the first episode. Photomicrograph shows intraalveolar plugs of proliferating fibroblasts in a myxoid background (hematoxylin and eosin stain; original magnification 3 200). Figure 4. Chest CT scan during the second episode. Predominant pattern of randomly distributed (both centrilobular and subpleural) poorly defined nodular opacities (white arrows), more extensive than seen on the initial chest CT scan, with a noticeably different morphology and without evidence of air-space consolidation or ground glass attenuation. progressive disease with pancytopenia. One week after the second treatment, he developed fever, dyspnea, and hypotension; he was hospitalized for bilateral pneumonia ( Fig 3 ) and treated with IV antibiotics. Chest CT scan ( Fig 4 ) showed multilobar opacities, and BAL showed no evidence of malignant cells or infection. He was discharged home on antibiotics but continued to complain of cough and dyspnea. Faint crackles were heard at the left base. Repeat chest radiograph ( Fig 5 ) and CT scan, about 2 weeks later ( Fig 6 ), showed worsening of the pulmonary opacities. On pulmonary function testing, FEV 1 was 3.68 L (81% predicted), FVC was 3.47 L (76% predicted), the FEV 1 FVC ratio was 82%, diffusing capacity to carbon monoxide was 16.4 ml min 2 1 mm Hg 2 1 (57% predicted), and oximetry showed oxygen saturation of 93% at rest and 85% with exercise on room air. The patient underwent another bronchoscopy, which again showed organizing pneumonia ( Fig 7 ) on the transbronchial biopsy sample, and no pathogens on the lung biopsy specimen or in the BAL fluid. Total cell count in the BAL fluid was ml, with 67% alveolar macrophages, 6% lymphocytes, 23% neutrophils, and 4% eosinophils. Blood cultures, urinary histoplasma antigen, and fungal serologies were negative. The patient was given oral prednisone, 80 mg daily. A repeat bone marrow study showed a hypercellular bone marrow (80%) with 60% involvement Figure 3. Chest radiograph during the second episode. Illdefined hazy increased density in both bases is more pronounced on the left side, causing partial obscuration of the left hemidiaphragm. Figure 5. Chest radiograph during the second episode with worsening symptoms, showing increase in the diffuse nodular opacities throughout both lungs Postgraduate Education Corner
3 What is the diagnosis? Figure 6. Chest CT scan during the second episode with worsening symptoms. Progression of radiologic abnormalities to include diffuse, randomly distributed lung nodules, curvilinear subpleural consolidation and or atelectasis involving the left base, and evidence of subtle increased peripheral subpleural reticular densities in the posterior right lung base, suggesting the development of mild fibrosis. by CLL. The patient s condition improved. By early May 2008 he was fully recovered. Repeat chest radiograph showed improvement, and pulmonary function results had normalized. Prednisone was tapered off over 6 weeks. A subsequent CT scan showed resolution of the pulmonary opacities. Figure 7. Transbronchial lung biopsy specimen during the second episode. Photomicrograph shows intraalveolar plugs of proliferating fibroblasts in a myxoid background, similar to the previous biopsy specimen (hematoxylin and eosin stain; original magnification 3 200). CHEST / 137 / 6 / JUNE,
4 Diagnosis: Recurrent organizing pneumonia caused by rituximab therapy Discussion Table 1 Respiratory Complications of Rituximab (Serious Pulmonary Adverse Effects) Hypersensitivity pneumonitis ARDS Interstitial pneumonitis Organizing pneumonia Pulmonary fibrosis Alveolar hemorrhage Rituximab is an anti-cd20 chimeric mouse-human monoclonal antibody that has become an important and widely used component of therapy for many B-cell lymphoid malignancies and autoimmune diseases. 2 It is being used increasingly off-label in a wide variety of nonhematologic conditions, such as rheumatologic conditions, renal disease, solid organ transplantation, neuromuscular disorders, and skin and endocrine disorders. 3 Respiratory symptoms related to rituximab use are relatively common and usually mild and of short duration. The first administration of rituximab is commonly associated with the first dose effect of uncertain cause, which can include cough, rhinitis, and dyspnea. Rarer, but often more serious, complications can occur, including organizing pneumonia 4-9 (Table 1 ). Organizing pneumonia is a histopathologic pattern of lung injury characterized by intraalveolar and intrabronchiolar fibrosis as the predominant features. 10 There are intraluminal plugs of loose connective tissue characterized by fibroblasts embedded in a myxoid matrix. It may be idiopathic (cryptogenic organizing pneumonia) or secondary to infections, drugs, connective tissue disorders, or radiation therapy. The clinical correlates include fever, fatigue, weight loss, cough, dyspnea, pleuritic chest pain, crackles, and fluctuating opacities on serial chest radiographs. In cases of drug-induced organizing pneumonia, there may be intervening periods of normal chest radiograph despite continued exposure to the drug. The typical CT image pattern consists of migratory peripheral parenchymal consolidations with air bronchogram with or without surrounding ground-glass opacities. Less frequent CT image patterns include single or multiple focal nodules or masses, parenchymal consolidations with peribronchovascular distribution, atoll sign, nodular lesions, linear and bandlike opacities, perilobular pattern, and progressive fibrotic pattern. 11 BAL often reveals increased lymphocytes and sometimes neutrophils and or eosinophils in patients with organizing pneumonia, and is most useful in excluding infectious causes. Transbronchial biopsies usually do not provide a sufficient sample and an open or video-assisted thoracoscopic lung biopsy is recommended to confirm the diagnosis of organizing pneumonia. When the diagnosis of drug-induced organizing pneumonia is suspected, discontinuation of the offending drug and administration of corticosteroid therapy usually lead to prompt improvement. When the diagnosis is not recognized, relapses are common and lobar consolidation may develop, requiring a more prolonged and intense course of corticosteroid therapy. Organizing pneumonia has been reported after rituximab therapy for non-hodgkin s lymphoma, 12 rheumatoid arthritis, and Castleman disease. 13 Organizing pneumonia rarely has been reported during the course of untreated CLL, 14, 15 following chlorambucil treatment, 16 or after treatment with rituximab and fludarabine. 17 Several cases of interstitial pneumonitis, usually diagnosed on clinical and radiologic findings, have been described following rituximab treatment of CLL. 18 The case presented here involves a middle-aged man with CLL treated with five cycles of rituximab and corticosteroids. The third and fifth cycles were associated with organizing pneumonia, but the three other cycles appeared to be well tolerated. All cultures remained negative and the temporal course appeared to be consistent with drug-induced lung disease because other causes seemed rather unlikely to explain the recurrent episodes of organizing pneumonia. It is possible that the first episode of organizing pneumonia may have represented an incidental finding associated with his CLL, although this association is extremely rare. In a study of nine patients with CLL and pulmonary opacities, the lung biopsy specimen showed a dense lymphocytic infiltrate that followed bronchovascular bundles consistent with leukemic involvement in eight cases, whereas in one, organizing pneumonia was the main lesion and CLL was an incidental finding. 14 This could explain why the subsequent (fourth) cycle of rituximab was apparently well tolerated in our patient. However, that episode may also have been a delayed manifestation of drug-induced organizing pneumonia. In a series of 19 patients, organizing pneumonia occurred, on average, 2 months after the first rituximab infusion and 2 weeks after the last rituximab and corticosteroid administration. 7 However, organizing pneumonia 4 to 5 months after rituximab administration has been reported 13 because the medication has a prolonged half-life. The second episode of organizing pneumonia in this patient falls within the realm of a described drug-induced pulmonary event. 10 There was a close temporal association between exposure to 1468 Postgraduate Education Corner
5 the drug and the development of pulmonary opacities. The histopathologic features were consistent with drug-induced organizing pneumonia, and other possible causes such as other drugs, infection, or pulmonary involvement by CLL were reasonably excluded. Drug reexposure produced worsening of symptoms, whereas drug withdrawal in association with corticosteroid therapy led to rapid resolution of symptoms, pulmonary function abnormalities, and radiographic opacities. The mechanisms underlying the organizing pneumonia reaction to rituximab therapy remain unclear. Activation of complement, B-lymphocyte cytolysis, and tumor necrosis factor- a release occur rapidly following rituximab infusion. 19 Cytokine release and or tumor lysis syndrome have been implicated in ARDS and diffuse alveolar damage induced by rituximab infusion. Immune-mediated mechanisms in organizing pneumonia are supported by a high CD4 lymphocyte count in BAL fluid, a positive drug lymphocyte stimulation test for rituximab (the lymphocyte transformation test for a drug measures the proliferation of T cells in vitro and is suggestive of a previous sensitization to that drug), 20 a rapid response to corticosteroid therapy, and recurrence after rechallenge with the offending drug. Of interest, the time frame between rituximab infusion and the occurrence of organizing pneumonia seems to have shortened with repeated drug exposures in our patient. Conclusion In conclusion, we presented a middle-aged man with CLL who experienced recurrent episodes of pulmonary opacities on exposure to rituximab therapy, with organizing pneumonia on lung biopsy specimen, who improved with corticosteroid therapy and withholding of rituximab therapy. Other potential causes of organizing pneumonia were excluded. Although rituximab-related pulmonary events are extremely rare in CLL, this case underlines the need for awareness of this possibility. Acknowledgments Financial nonfinancial disclosures: The authors have reported to CHEST the following conflicts of interest: Dr Zent received research funding from Genentech, Inc. The remaining authors have reported that no potential conflicts of interest exist with any companies organizations whose products or services may be discussed in this article. References 1. Zent CS, Call TG, Hogan WJ, Shanafelt TD, Kay NE. Update on risk-stratified management for chronic lymphocytic leukemia. Leuk Lymphoma ;47(9): Zent CS, Call TG, Shanafelt TD, et al. Early treatment of high-risk chronic lymphocytic leukemia with alemtuzumab and rituximab. Cancer ;113 (8 ): McDonald V, Leandro M. Rituximab in non-haematological disorders of adults and its mode of action. Br J Haematol ;146 (3 ): Tonelli AR, Lottenberg R, Allan RW, Sriram PS. Rituximabinduced hypersensitivity pneumonitis. Respiration ;78 (2 ): Saito B, Nakamaki T, Adachi D, Suzuki J, Tomoyasu S. Acute respiratory distress syndrome during the third infusion of rituximab in a patient with follicular lymphoma. Int J Hematol ;80 (2 ): Burton C, Kaczmarski R, Jan-Mohamed R. Interstitial pneumonitis related to rituximab therapy. N Engl J Med ;348 (26 ): Lioté H. Organizing pneumonia associated with rituximab: Challenges raised by establishing causality. Joint Bone Spine ;75 (3 ): Leon RJ, Gonsalvo A, Salas R, Hidalgo NC. Rituximabinduced acute pulmonary fibrosis. Mayo Clin Proc ;79 (7 ): Alexandrescu DT, Dutcher JP, O Boyle K, Albulak M, Oiseth S, Wiernik PH. Fatal intra-alveolar hemorrhage after rituximab in a patient with non-hodgkin lymphoma. Leuk Lymphoma ;45 (11 ): Camus P, Fanton A, Bonniaud P, Camus C, Foucher P. Interstitial lung disease induced by drugs and radiation. Respiration ;71 (4 ): Polverosi R, Maffesanti M, Dalpiaz G. Organizing pneumonia: typical and atypical HRCT patterns. Radiol Med (Torino) ;111 (2 ): Macartney C, Burke E, Elborn S, et al. Bronchiolitis obliterans organizing pneumonia in a patient with non-hodgkin s lymphoma following R-CHOP and pegylated filgrastim. Leuk Lymphoma ;46 (10 ): Soubrier M, Jeannin G, Kemeny JL, et al. Organizing pneumonia after rituximab therapy: two cases. Joint Bone Spine ;75 (3 ): Rollins SD, Colby TV. Lung biopsy in chronic lymphocytic leukemia. Arch Pathol Lab Med ;112 (6 ): Vaiman E, Odeh M, Attias D, Ben-Arie Y, Oliven A. T-cell chronic lymphocytic leukaemia with pulmonary involvement and relapsing BOOP. Eur Respir J ;14 (2 ): Kalambokis G, Stefanou D, Arkoumani E, Tsianos E. Bronchiolitis obliterans organizing pneumonia following chlorambucil treatment for chronic lymphocytic leukemia. Eur J Haematol ;73 (2 ): Byrd JC, Peterson BL, Morrison VA, et al. Randomized phase 2 study of fludarabine with concurrent versus sequential treatment with rituximab in symptomatic, untreated patients with B-cell chronic lymphocytic leukemia: results from Cancer and Leukemia Group B 9712 (CALGB 9712). Blood ; 101 (1 ): Wagner SA, Mehta AC, Laber DA. Rituximab-induced interstitial lung disease. Am J Hematol ;82 (10 ): Bienvenu J, Chvetzoff R, Salles G, et al ; Groupe d Etude des Lymphomes de l Adulte. Tumor necrosis factor alpha release is a major biological event associated with rituximab treatment. Hematol J ;2 (6 ): Hiraga J, Kondoh Y, Taniguchi H, Kinoshita T, Naoe T. A case of interstitial pneumonia induced by rituximab therapy. Int J Hematol ;81 (2 ): CHEST / 137 / 6 / JUNE,
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