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Restrictive Allograft Syndrome Post Lung Transplantation Is Modern Pathology (2013) 26, 350–356 350 & 2013 USCAP, Inc All rights reserved 0893-3952/13 $32.00 Restrictive allograft syndrome post lung transplantation is characterized by pleuroparenchymal fibroelastosis Efrat Ofek1,2, Masaaki Sato3,4, Tomohito Saito4, Ute Wagnetz5, Heidi C Roberts6, Cecilia Chaparro4, Thomas K Waddell4, Lianne G Singer4, Michael A Hutcheon4, Shaf Keshavjee4 and David M Hwang1,2,4 1Laboratory Medicine Program, University Health Network, Toronto, ON, Canada; 2Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON, Canada; 3Department of Thoracic Surgery, Kyoto University Hospital, Kyoto, Japan; 4The Toronto Lung Transplant Program, University Health Network, University of Toronto, Toronto, ON, Canada; 5Department of Radiology, GZO Spital Wetzikon, Wetzikon, Switzerland and 6Department of Medical Imaging, University Health Network, Toronto, ON, Canada We previously described restrictive allograft syndrome as a form of chronic lung allograft dysfunction, demonstrating restrictive pulmonary function decline. However, the histopathological correlates of restrictive allograft syndrome have yet to be satisfactorily described. We hypothesized that pulmonary pleuroparenchymal fibroelastosis, as has recently been described in bone marrow transplant recipients, may also be present in the lungs of patients with restrictive allograft syndrome. Retrospective review of 493 patients who underwent lung transplantation between 1 January 1996 and 30 June 2009, was conducted. Out of 47 patients with clinical features of restrictive allograft syndrome, 16 had wedge biopsy, re-transplant lung explant, or autopsy lung specimens available for review. All lungs showed varying degrees of pleural fibrosis. Fifteen of 16 showed parenchymal fibroelastosis, characterized by hypocellular collagen deposition with preservation and thickening of the underlying alveolar septal elastic network. The fibroelastosis was predominantly subpleural in distribution, with some cases also showing centrilobular and paraseptal distribution. A sharp demarcation was often seen between areas of fibroelastosis and unaffected lung parenchyma, with fibroblastic foci often present at this interface. Concurrent features of obliterative bronchiolitis were present in 14 cases. Another common finding was the presence of diffuse alveolar damage (13 cases), usually in specimens obtained o1 year after clinical onset of restrictive allograft syndrome. The single specimen in which fibroelastosis was not identified was obtained before the clinical onset of chronic lung allograft dysfunction, and showed features of diffuse alveolar damage. In conclusion, pleuroparenchymal fibroelastosis is a major histopathologic correlate of restrictive allograft syndrome, and was often found concurrently with diffuse alveolar damage. Our findings support a temporal sequence of diffuse alveolar damage followed by the development of pleuroparenchymal fibroelastosis in the histopathologic evolution of restrictive allograft syndrome. Modern Pathology (2013) 26, 350–356; doi:10.1038/modpathol.2012.171; published online 28 September 2012 Keywords: interstitial lung disease; lung allograft rejection; lung transplantation; pleuroparenchymal fibroelastosis; pulmonary fibrosis Increasing evidence suggests that chronic lung allograft dysfunction. Although bronchiolitis oblit- allograft dysfunction following lung transplantation erans syndrome, characterized clinically by irrever- is a heterogeneous condition that includes bronch- sible obstructive deficits in pulmonary function iolitis obliterans syndrome as well as other types of tests,1–4 remains the major cause of late mortality, we recently described a distinct form of chronic lung allograft dysfunction demonstrating restrictive Correspondence: Dr DM Hwang, MD, PhD, FRCPC, Department of pulmonary function decline, which we designated Pathology, Toronto General Hospital, Room 11E423, 200 Elizabeth restrictive allograft syndrome,5 and which accounts Street, Toronto, ON, Canada M5G 2C4. for 25–35% of chronic lung allograft dysfunc- E-mail: [email protected] 5,6 Received 3 July 2012; revised 13 August 2012; accepted 13 August tion. Radiologically, a significant proportion of 2012; published online 28 September 2012 these patients demonstrated an unusual pattern of www.modernpathology.org Transplant-related pleuroparenchymal fibroelastosis E Ofek et al 351 interstitial fibrosis, often upper lobe-predominant, dysfunction, which was defined as an irreversible associated with traction bronchiectasis in computed decline in forced expiratory volume (1 s) to o80%. tomography scans. Although initial review of In total, 16 specimens (5 wedge biopsies, 4 lungs restrictive allograft syndrome cases confirmed the explanted for retransplantation, 7 autopsies) from 16 presence of interstitial fibrosis,5 the histopatho- patients with restrictive allograft syndrome were logical correlates of restrictive allograft syndrome available for review. Specimens were processed have yet to be satisfactorily described. according to routine surgical pathology protocols. Idiopathic pleuroparenchymal fibroelastosis was Hematoxylin and eosin-stained sections were first proposed as a novel, distinct clinicopathologi- reviewed for all cases, with elastic trichrome or cal entity in 2004 by Frankel et al,7 to describe cases Movat stains for representative tissue blocks in of upper lobe-predominant pleural and subpleural selected cases. The cases were assessed for fibrosis with a clinical presentation suggestive of a histopathological findings by two pathologists with chronic idiopathic interstitial pneumonia. Several pulmonary expertise (EO and DMH), including: cases and small series with similar radiologic and degree of pleuroparenchymal fibroelastosis (0, pathologic features have also been reported.8–14 none; 1, 40–10% of area; 2, 410–25%; 3, 425– Radiologically, idiopathic pleuroparenchymal 50%; 4, 450%) and distribution (subpleural, para- fibroelastosis has been characterized by pleural septal, centrilobular or parenchymal) of pleuro- thickening associated with underlying parenchy- parenchymal fibroelastosis; presence of bronchio- mal reticular abnormalities, architectural distortion litis obliterans within and/or outside the areas of and traction bronchiectasis in a mostly upper lobe- pleuroparenchymal fibroelastosis; histological predominant distribution.7,10,11 Histologically, idio- features at the interface between pleuroparen- pathic pleuroparenchymal fibroelastosis is chara- chymal fibroelastosis and uninvolved lung cterized by pronounced visceral pleural fibrosis parenchyma (whether this margin was abrupt or associated with subpleural, ‘intra-alveolar’ fibrotic not, presence of fibroblastic foci); presence of changes characterized by an admixture of elastic honeycomb changes or other distinct histopatho- and fibrous tissue (fibroelastosis). logical patterns of chronic interstitial pneumonia; In a recent report, von der Thusen et al15 presence of diffuse alveolar damage; and presence of described four cases of pulmonary disease follow- vascular changes. ing allogeneic bone marrow transplantation that The latest computed tomography scans before the presented with pneumothoraces and were found to pathology specimen for these patients were ob- demonstrate histopathologic features of pleuro- tained. Images were acquired on different scanners parenchymal fibroelastosis. Histologically, chronic ranging from 4- to 64-row detectors. All studies were graft-vs-host-disease may present with a variety of blindly evaluated by two chest radiologists (UW and patterns in the lung, including bronchiolitis HCR) as previously described.5 obliterans.16,17 In view of the fact that patients with chronic graft-vs-host-disease often demonstrate bronchiolitis obliterans that is reminiscent of that Results seen in lung transplant recipients with chronic lung allograft dysfunction, we hypothesized that pleur- Clinical and demographic characteristics of the 16 oparenchymal fibroelastosis might represent an patients for whom pathology material was available important histopathologic correlate of post-lung for review are summarized in Table 1. Computed transplant restrictive allograft syndrome. We report tomography scans were previously reviewed and here evidence that pleuroparenchymal fibroelastosis scored as part of our initial study of restrictive is indeed a major histopathologic correlate of allograft syndrome.5 These showed interstitial restrictive allograft syndrome. opacity/reticulation in all cases, with 13 showing reticulation in the upper lung zones, 12 in the middle lung zones and 14 in the lower lung zones. Materials and methods Upper lobe predominance was seen in eight patients. Traction bronchiectasis was reported in This study was approved by the Research Ethics 13 patients, with bronchial dilatation and bronchial Board of University Health Network. Patients with thickening reported in two patients each. Mosaic restrictive allograft syndrome were identified as attenuation was seen in two and air trapping in four. previously described,5 by retrospective review of Honeycombing was reported in three patients and 493 patients who underwent bilateral lung (n ¼ 478) architectural distortion in eight. or heart-lung (n ¼ 15) transplantation in the Toronto All pathology specimens reviewed showed vary- Lung Transplant Program between 1 January 1996 ing degrees of pleural fibrosis (Table 2). Fifteen of 16 and 30 June 2009. specimens showed areas of pleuroparenchymal
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