Focal Organizing Pneumonia on Surgical Lung Biopsy* Causes, Clinicoradiologic Features, and Outcomes

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1 CHEST Focal Organizing Pneumonia on Surgical Lung Biopsy* Causes, Clinicoradiologic Features, and Outcomes Fabien Maldonado, MD; Craig E. Daniels, MD; Elizabeth A. Hoffman, MD; Eunhee S. Yi, MD; and Jay H. Ryu, MD, FCCP Original Research ORGANIZING PNEUMONIA Background: Organizing pneumonia (OP) is a histologic pattern that is morphologically distinctive but nonspecific and can be seen in diverse clinical settings. Focal OP has been described as a discrete form of OP, but relatively little is known regarding this clinicopathologic entity. Methods: We sought to clarify the clinicoradiologic presentation, underlying causes, and outcomes associated with focal OP by retrospectively reviewing 26 consecutive cases diagnosed by surgical lung biopsy over an 8-year period from January 1, 1997, to December 31, Results: All patients presented with an unifocal opacity detected on chest radiography (20 patients) or CT scans (6 patients). At the time of presentation, 10 patients (38%) had symptoms, including cough, shortness of breath, or chest pain; 16 patients were asymptomatic. Contrast-enhancement CT scanning or positron emission tomography (PET) scan was performed in 11 patients, and the results were positive in all. Surgical procedures included wedge resection in 21 patients (81%), segmentectomy in 3 patients (11%), and lobectomy in 2 patients (8%). Three case of focal OP (12%) were related to infections, but the remaining cases were cryptogenic. Follow-up over a median interval of 11 months (range, 1 to 71 months) yielded no recurrence of OP. Conclusions: The radiologic features of focal OP are often indistinguishable from those of lung cancer, and include positivity on contrast-enhancement CT scan and PET scan. Most cases of focal OP are cryptogenic, and infection is identified in a minority of cases. Surgical resection alone appears to suffice in the management of cryptogenic focal OP. (CHEST 2007; 132: ) Key words: cryptogenic organizing pneumonia; interstitial lung disease; organizing pneumonia; pulmonary nodule Abbreviations: COP cryptogenic organizing pneumonia; OP organizing pneumonia; PET positron emission tomography Organizing pneumonia (OP) is a histopathologic pattern that is characterized by polypoid intraluminal plugs of proliferating fibroblasts and myofibroblasts within alveolar ducts and airspaces with varying degrees of bronchiolar involvement. 1 5 Although the histologic lesion of OP is morphologically distinctive, it is clinically nonspecific and represents a reparative reaction that may be seen in a variety of clinical contexts. OP may occur in association with infections, connective tissue diseases, inhalational injury, hypersensitivity pneumonitis, drug reactions, radiation-induced lung injury, or aspiration. 1 5 OP occurring in the absence of an identifiable cause or underlying disease is recognized as a clinicopathologic syndrome (ie, cryptogenic OP [COP]), which usually presents with patchy bilateral alveolar infiltrates. 6 8 Focal OP has been described as a discrete form of OP and presents as an isolated focal lesion on chest imaging. 6,9 13 However, relatively little is known regarding the potential causes and clinical implications of this lesion. In this study, we sought to clarify the clinicoradiologic presentation, underlying causes, and outcomes associated with CHEST / 132 / 5/ NOVEMBER,

2 focal OP by retrospectively reviewing a consecutive series of patients in whom focal OP had been diagnosed by surgical lung biopsy. Materials and Methods Patients with OP diagnosed by surgical lung biopsy at the Mayo Clinic in Rochester, MN, from January 1, 1997, to December 31, 2004, were identified by a computer-assisted search of medical records. There were 203 patients whose surgical lung biopsy specimens demonstrated OP; 26 patients (13%) presented with a unifocal lesion on chest imaging and were included in the study group. This study was approved by the Institutional Review Board of the Mayo Foundation. Histopathology Surgical lung biopsy slides were retrieved and reviewed by two pathologists (E.A.F. and J.E.Y.) without knowledge of clinical or radiologic data. The histopathologic diagnosis of OP was made by consensus using criteria outlined in the American-European consensus statement on idiopathic interstitial pneumonias. 3 Table 1 Demographic and Clinical Features of 26 Patients With Focal OP* Characteristics Values Age, yr Median 66 Range Sex Male 15 (58) Female 11 (42) Smoking history Never 6 (23) Ever 13 (50) Current 7 (27) Symptoms Asymptomatic 16 (62) Cough 6 (23) Shortness of breath 2 (8) Chest pain 2 (8) Hemoptysis 1 (4) Fever 1 (4) Weight loss 1 (4) *Values are given as No. (%), unless otherwise indicated. Clinical, Laboratory, and Radiologic Findings Data extracted from the medical records included the demographics, clinical presentation, physical findings, laboratory results, radiologic findings, diagnosis, treatment, and clinical course. Presenting signs and symptoms were recorded from the first encounter at the Mayo Clinic that led to a diagnosis of OP. The cause of OP was assigned by a consensus of three of the authors (F.M., C.E.D., and J.H.R.) based on the review of all available clinical, laboratory, radiologic, and biopsy data. One of the patients included in this study (with a case of cytomegalovirus pneumonia with OP) has been previously reported. 14 Results Demographics and Clinical Presentation The median age of the patients was 66 years (range, 36 to 86 years); 11 patients (42%) were women (Table 1). Seven patients were current smokers (27%). No other relevant exposure was elicited except for one patient who worked as a welder. Ten patients (38%) had symptoms, as listed on Table 1; the remaining 16 patients (62%) were asymptomatic. *From the Division of Pulmonary and Critical Care Medicine (Drs. Maldonado, Daniels, and Ryu), and the Department of Laboratory Medicine and Pathology (Drs. Hoffman and Yi), Mayo Clinic, Rochester, MN. The authors have reported to the ACCP that no significant conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article. Manuscript received May 10, 2007; revision accepted July 7, Reproduction of this article is prohibited without written permission from the American College of Chest Physicians ( org/misc/reprints.shtml). Correspondence to: Jay H. Ryu, MD, FCCP, Division of Pulmonary and Critical Care Medicine, Desk East 18, Mayo Clinic, 200 First St SW, Rochester, MN 55905; ryu.jay@mayo.edu DOI: /chest Twenty patients (77%) had no relevant findings on physical examination; the remaining 6 patients were noted to have bibasilar crackles or wheezes, which were probably not related to focal OP. Six patients (23%) had a history of malignancy, including one patient with previous lung cancer resection. Two of these patients had an active malignancy; one patient with a mediastinal germ cell tumor was being treated with combination chemotherapy, and another patient with metastatic prostate cancer was being treated with leuprolide therapy. Three patients had COPD, and another patient had bronchiectasis. Two patients were immunocompromised, including the patient with germ cell tumor and a patient who had undergone heart transplantation 1 year before. Screening laboratory results including CBC count and chemistry tests were unremarkable in all cases. Pulmonary Function Studies Preoperative pulmonary function studies were obtained in 16 patients and included spirometry in all 16 patients and single-breath diffusing capacity for carbon monoxide in 12 patients. Spirometry results were normal in seven patients (44%). In eight patients, including three patients in whom COPD had previously been diagnosed, spirometry revealed an obstructive defect with an FEV 1 that ranged from 25 to 77% predicted. The remaining patient had a mild restrictive defect. The single-breath diffusing capacity for carbon monoxide was normal in seven patients (58%) and reduced in five patients with values that ranged from 37 to 67% predicted Original Research

3 Figure 1. CT scan of the chest in a 59-year-old ex-smoker with focal OP. A cm opacity (arrow) with spiculated margins is present in the left lower lobe. Radiologic Findings Focal lung lesion was initially detected by chest radiography in 20 patients (77%) and by CT scan in 6 patients (23%). The lesion was located in the right lung in 10 patients (38%) and in the left lung in 16 patients (62%); 15 lesions (58%) were in the upper lobes including 1 in the lingula and 11 (42%) in the lower lobes. None of the patients had intrathoracic lymphadenopathy. The median diameter of the lesion was 1.9 cm (range, 0.6 to 6.75 cm). The margin of the lesion was smooth in 10 patients (38%) and irregular or spiculated in 16 patients (62%) [Fig 1]. These lesions had the appearance of a nodule, mass, or focal consolidation; two were associated with air bronchograms (8%). Cavitation was present in one lesion that proved to be associated with cytomegalovirus infection. IV contrast enhancement study was performed in seven patients and was positive in all (enhancement of 15 Hounsfield units 15 ); six of these lesions were cryptogenic, and the remaining case was associated with bronchiectasis and Pseudomonas infection. Positron-emission tomography (PET) with fluorodeoxyglucose 18 F was performed in four patients, and hypermetabolic activity of the focal lung lesion was demonstrated in all; all four cases were cryptogenic. Figure 2. OP forming a well-demarcated nodule. Alveolar spaces are filled with fibromyxoid plugs. Interstitial thickening with chronic inflammatory cells and type 2 pneumocyte hyperplasia are also evident. In the upper left corner, adjacent normal lung parenchyma is visible (hematoxylin-eosin, original 100). Bronchoscopy Bronchoscopy was performed in 12 patients (46%); in 6 of these patients, bronchoscopy was performed in the operating room immediately prior to surgery to assess for endobronchial disease. The six remaining patients underwent diagnostic bronchoscopy prior to surgical consultation and included bronchoscopic lung biopsy in four patients. Bronchoscopy was nondiagnostic in all of these patients with no histologic evidence of OP obtained. Surgical Lung Biopsy In all 26 cases, malignancy was clinically suspected and was the reason for surgical resection, which was performed by thoracotomy in 16 patients (62%) and video-assisted thoracoscopic surgery in 10 patients (38%). Surgical resection consisted of wedge resection in 21 patients (81%), segmentectomy in 3 patients (12%), and lobectomy in 2 patients (8%). All resected lung specimens demonstrated features of OP (Fig 2). The presence of prominent lymphoid infiltrates was associated with OP in three cases that included two cryptogenic cases and one patient with cytomegalovirus infection. In two other cases, features of diffuse alveolar damage were seen. Multinucleated giant cells and a nonspecific scar were associated with OP in one case each. Surgical lung biopsy yielded specific clues to the underlying cause for OP in 3 cases (12%). These included one patient each with focal bacterial pneumonia (Pseudomonas aeruginosa recovered from lung biopsy specimen), focal lung abscess (patient had been receiving empiric antibiotic therapy, and microbial cultures yielded no pathogens), and cytomegalovirus pneumonia in an immunocompetent host. These were the only positive results (P aeruginosa and cytomegalovirus) in 21 surgical lung biopsy specimens that were submitted for microbiological studies. Postoperative complications were noted in five patients (19%) and included nosocomial pneumonias in two patients, respiratory distress with myocardial CHEST / 132 / 5/ NOVEMBER,

4 infarction in one patient, and persistent air leak with prolonged hospital stay in two patients. There were no deaths directly attributable to the surgical procedure. Causes of Focal OP An infectious cause was diagnosed in three patients based on the results of the surgical lung biopsy and microbial cultures performed with these specimens, as already discussed. No cause was identified in the remaining 23 patients (88%) [ie, cryptogenic]. However, four of these patients had symptoms suggestive of a respiratory tract infection in the weeks preceding the surgical lung biopsy. Treatment and Follow-up After surgical resection, two patients received antimicrobial therapy. These included the patient with P aeruginosa and the patient with a lung abscess. No other treatment (eg, corticosteroids) was provided to the remaining 24 patients (92%). Radiologic follow-up was obtained for 25 patients with a median follow-up period of 14 months (range, 1 to 71 months). One patient had a recurrence of a focal pulmonary lesion contralateral to the location of the focal OP lesion (cryptogenic) that had been resected 2 months before. This new lesion was diagnosed to be Haemophilus influenzae pneumonia and resolved after antimicrobial therapy. Seven patients (27%) died 9 to 64 months after undergoing surgical resection of focal OP. The causes of death included cancer in four patients, end-stage COPD in one patient, chronic rejection of heart transplant in one patient, and unknown in the remaining patient (91 years old). Discussion OP is a nonspecific histopathologic lesion and can be associated with various clinical contexts and radiologic patterns. In this study, we focused on OP presenting as a unifocal lesion on chest imaging (ie, focal OP), which accounted for 13% of cases of OP diagnosed from surgical lung biopsy specimens at our institution over an 8-year period. Other studies 6,16,17 have reported similar rates of focal OP among their case series of OP. The majority of our patients with focal OP were asymptomatic, which is similar to the study by Lohr and colleagues. 6 On the contrary, other authors 11,17 have noted symptoms to be present in more than one half of their patients with focal OP. All of our patients underwent surgical resection of their lung lesion for suspicion of lung cancer similar to the circumstances described in previous reports. 6,9 13,18 The majority of our patients had a smoking history and were middle-aged or older. The radiologic appearance included nodule, mass, or focal consolidation. Not uncommonly, these lesions had an irregular or spiculated margin. The suspicion of lung cancer was heightened by positive results on a contrast-enhancement CT scan and PET scanning; all 11 patients undergoing these imaging studies had abnormal results. Yang and colleagues 11 previously reported a positive finding of focal OP on a contrastenhancement CT scan. Melloni and colleagues 18 recently described tracer uptake on a PET scan occurring in three cases of localized OP similar to the positive PET scan results seen in four of our patients. There are multiple potential causes for the histopathologic lesion of OP. In our patients with focal OP, we were able to identify a cause in only three patients (12%), all of whom had infection diagnosed on surgical lung biopsy specimens. Similarly, other authors 6,16,17 have reported the majority of their cases of focal OP to be cryptogenic. Four of our patients classified as having focal COP described symptoms suggestive of a respiratory tract infection in the weeks preceding their surgical resection. Some of the cases of focal COP probably represent resolving or incompletely resolved community-acquired pneumonia. 13,17,19 One of our patients was treated with a combination chemotherapy regimen that included bleomycin. Bleomycin therapy has been associated with several forms of lung injury including OP, which usually presents as multiple nodules or infiltrates. 20 Our patient had a unifocal lung lesion that was resected and proved to be OP with no other lung lesions or recurrence thereafter. It seemed unlikely that bleomycin therapy was the cause for this patient s focal OP. In a recently published study, Melloni et al 18 described 21 patients with localized OP, which included patients with single focal lesions as well as multiple and bilateral radiologic lesions. Most of the patients in their study were men and had COPD, while 57% had a history of recurrent lung infections, leading these authors to conclude that localized OP is more frequent in male smokers with COPD. In contrast, our patients with focal OP, as currently defined (ie, OP associated with an isolated focal lesion on chest imaging), did not demonstrate a preponderance of male smokers with COPD. We found no evidence for the recurrence of OP or the need for corticosteroid therapy after surgical resection, while 29% of patients in the study by Melloni et al 18 required corticosteroid therapy, particularly those with bilateral lesions. Previous studies 7,8 have 1582 Original Research

5 suggested that nonfocal forms of COP require corticosteroid therapy for a period of several months, and early withdrawal of corticosteroids is frequently met with the recurrence of OP. These observations cumulatively suggest that OP presenting as an isolated focal lesion may be different in clinical behavior and pathogenesis compared to OP presenting with multiple or bilateral infiltrates. Our study has several limitations. This was a retrospective study, and our cases were identified entirely by surgical biopsy results. There were likely other cases of focal OP that did not come to diagnosis by surgical lung biopsy because the suspicion of malignancy was low, such as younger patients or those with more benign appearance on radiologic imaging. These aspects likely introduced a selection bias. In addition, we chose not to include cases of OP diagnosed in bronchoscopic or transthoracic needle biopsy specimens, since the lesion of OP is nonspecific and the true underlying nature of the pulmonary lesion (eg, adjacent malignancy) may be missed due to unrepresentative sampling by these methods. 1,2 In summary, focal OP is a discrete form of OP that is associated with a unifocal lesion on radiologic imaging and can commonly mimic lung cancer including positivity on contrast-enhanced CT scans or PET scans. The majority of cases of focal OP is cryptogenic, and infection is identified in a minority of cases. However, some cases of cryptogenic focal OP may represent resolving or incompletely resolved pneumonia. Focal OP does not recur after surgical resection and does not require corticosteroid therapy that is commonly employed in cases of nonfocal COP. Although the histopathologic appearance may be similar, additional research will likely reveal that there are important differences in the pathogenesis of focal vs nonfocal COP. References 1 Myers JL, Colby TV. Pathological manifestations of bronchiolitis, constrictive bronchiolitis, cryptogenic organizing pneumonia, and diffuse panbronchiolitis. Clin Chest Med 1993; 14: Colby TV. Bronchiolitis: pathologic considerations. Am J Clin Pathol 1998; 109: American Thoracic Society, European Respiratory Society. American Thoracic Society/European Respiratory Society International Multidisciplinary Consensus Classification of the Idiopathic Interstitial Pneumonias: this joint statement of the American Thoracic Society (ATS), and the European Respiratory Society (ERS) was adopted by the ATS board of directors, June 2001 and by the ERS Executive Committee, June Am J Respir Crit Care Med 2002; 165: Ryu JH, Myers JL, Swensen SJ. State of the art: bronchiolar disorders. Am J Respir Crit Care Med 2003; 168: Cordier JF. Organising pneumonia. Thorax 2000; 55: Lohr RH, Boland BJ, Douglas WW, et al. Organizing pneumonia: features and prognosis of cryptogenic, secondary, and focal variants. Arch Intern Med 1997; 157: Lazor R, Vandevenne A, Pelletier A, et al. Cryptogenic organizing pneumonia: characteristics of relapses in a series of 48 patients. Am J Respir Crit Care Med 2000; 162: Cordier J-F. Cryptogenic organizing pneumonia. Eur Respir J 2006; 28: Chen SW, Price J. Focal organizing pneumonia mimicking small peripheral lung adenocarcinoma on CT scans. Australas Radiol 1998; 42: Kohno N, Ikezoe J, Johkoh T, et al. Focal organizing pneumonia: CT appearance. Radiology 1993; 189: Yang PS, Lee KS, Han J, et al. Focal organizing pneumonia: CT and pathologic findings. J Korean Med Sci 2001; 16: Oikonomou A, Hansell DM. Organizing pneumonia: the many morphological faces. Eur Radiol 2002; 12: Watanabe K, Harada T, Yoshida M, et al. Organizing pneumonia presenting as a solitary nodular shadow on a chest radiograph. Respiration 2003; 70: Karakelides H, Aubry MC, Ryu JH. Cytomegalovirus pneumonia mimicking lung cancer in an immunocompetent host. Mayo Clin Proc 2003; 78: Swensen SJ, Viggiano RW, Midthun DE, et al. Lung nodule enhancement at CT: multicenter study. Radiology 2000; 214: Oymak FS, Demirbas HM, Mavili E, et al. Bronchiolitis obliterans organizing pneumonia: clinical and roentgenological features in 26 cases. Respiration 2005; 72: Cordier J-F, Loire R, Brune J. Idiopathic bronchiolitis obliterans organizing pneumonia: definition of characteristic clinical profiles in a series of 16 patients. Chest 1989; 96: Melloni G, Cremonia G, Bandiera A, et al. Localized organizing pneumonia: report of 21 cases. Ann Thorac Surg 2007; 83: Sulavik SB. The concept of organizing pneumonia. Chest 1989; 96: Santrach PJ, Askin FB, Wells RJ, et al. Nodular form of bleomycin-related pulmonary injury in patients with osteogenic sarcoma. Cancer 1989; 64: CHEST / 132 / 5/ NOVEMBER,

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