When tissue is the issue: A histological review of chronic lung allograft dysfunction.
biopsy
bronchiolitis obliterans (BOS)
lung (allograft) function/dysfunction
lung transplantation/pulmonology
pathology/histopathology
rejection: antibody-mediated (ABMR)
rejection: chronic
translational research/science
Journal
American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons
ISSN: 1600-6143
Titre abrégé: Am J Transplant
Pays: United States
ID NLM: 100968638
Informations de publication
Date de publication:
10 2020
10 2020
Historique:
received:
30
01
2020
revised:
03
03
2020
accepted:
05
03
2020
pubmed:
19
3
2020
medline:
22
6
2021
entrez:
19
3
2020
Statut:
ppublish
Résumé
Although chronic lung allograft dysfunction (CLAD) remains the major life-limiting factor following lung transplantation, much of its pathophysiology remains unknown. The discovery that CLAD can manifest both clinically and morphologically in vastly different ways led to the definition of distinct subtypes of CLAD. In this review, recent advances in our understanding of the pathophysiological mechanisms of the different phenotypes of CLAD will be discussed with a particular focus on tissue-based and molecular studies. An overview of the current knowledge on the mechanisms of the airway-centered bronchiolitis obliterans syndrome, as well as the airway and alveolar injuries in the restrictive allograft syndrome and also the vascular compartment in chronic antibody-mediated rejection is provided. Specific attention is also given to morphological and molecular markers for early CLAD diagnosis or histological changes associated with subsequent CLAD development. Evidence for a possible overlap between different forms of CLAD is presented and discussed. In the end, "tissue remains the (main) issue," as we are still limited in our knowledge about the actual triggers and specific mechanisms of all late forms of posttransplant graft failure, a shortcoming that needs to be addressed in order to further improve the outcome of lung transplant recipients.
Identifiants
pubmed: 32185874
doi: 10.1111/ajt.15864
pii: S1600-6135(22)22455-1
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2644-2651Informations de copyright
© 2020 The Authors. American Journal of Transplantation published by Wiley Periodicals LLC on behalf of The American Society of Transplantation and the American Society of Transplant Surgeons.
Références
Venuta F, Van Raemdonck D. History of lung transplantation. J Thorac Dis. 2017;9(12):5458-5471.
Derom FR, Barbier F, Ringoir S, et al. Ten-month survival after lung homotransplantation in man. J Thorac Cardiovasc Surg. 1971;61(6):835-846.
Epler GR, Colby TV. The spectrum of bronchiolitis obliterans. Chest. 1983;83(2):161-162.
Ralph DD, Springmeyer SC, Sullivan KM, Hackman RC, Storb R, Thomas ED. Rapidly progressive air-flow obstruction in marrow transplant recipients. Possible association between obliterative bronchiolitis and chronic graft-versus-host disease. Am Rev Respir Dis. 1984;129(4):641-644.
Burke CM, Theodore J, Dawkins KD, et al. Post-transplant obliterative bronchiolitis and other late lung sequelae in human heart-lung transplantation. Chest. 1984;86(6):824-829.
Glanville AR, Baldwin JC, Burke CM, Theodore J, Robin ED. Obliterative bronchiolitis after heart-lung transplantation: apparent arrest by augmented immunosuppression. Ann Intern Med. 1987;107(3):300-304.
Tazelaar HD, Yousem SA. The pathology of combined heart-lung transplantation: an autopsy study. Hum Pathol. 1988;19(12):1403-1416.
Kramer MR, Stoehr C, Whang JL, et al. The diagnosis of obliterative bronchiolitis after heart-lung and lung transplantation: low yield of transbronchial lung biopsy. J Heart Lung Transplant. 1993;12(4):675-681.
Cooper JD, Billingham M, Egan T, et al. A working formulation for the standardization of nomenclature and for clinical staging of chronic dysfunction in lung allografts. International Society for Heart and Lung Transplantation. J Heart Lung Transplant. 1993;12(5):713-716.
Verleden S, Vandermeulen E, Ruttens D, et al. Neutrophilic reversible allograft dysfunction (NRAD) and restrictive allograft syndrome (RAS). Semin Respir Crit Care Med. 2013;34(3):352-360.
Pakhale SS, Hadjiliadis D, Howell DN, et al. Upper lobe fibrosis: a novel manifestation of chronic allograft dysfunction in lung transplantation. J Heart Lung Transplant. 2005;24(9):1260-1268.
Konen E, Weisbrod GL, Pakhale S, Chung T, Paul NS, Hutcheon MA. Fibrosis of the upper lobes: a newly identified late-onset complication after lung transplantation? AJR Am J Roentgenol. 2003;181(6):1539-1543.
Sato M, Waddell TK, Wagnetz U, et al. Restrictive allograft syndrome (RAS): a novel form of chronic lung allograft dysfunction. J Heart Lung Transplant. 2011;30(7):735-742.
Ofek E, Sato M, Saito T, et al. Restrictive allograft syndrome post lung transplantation is characterized by pleuroparenchymal fibroelastosis. Mod Pathol. 2013;26(3):350-356.
Glanville AR, Verleden GM, Todd JL, et al. Chronic lung allograft dysfunction: definition and update of restrictive allograft syndrome-A consensus report from the Pulmonary Council of the ISHLT. J Heart Lung Transplant. 2019;38(5):483-492.
Verleden GM, Glanville AR, Lease ED, et al. Chronic lung allograft dysfunction: definition, diagnostic criteria, and approaches to treatment-A consensus report from the Pulmonary Council of the ISHLT. J Heart Lung Transplant. 2019;38(5):493-503.
Levine DJ, Glanville AR, Aboyoun C, et al. Antibody-mediated rejection of the lung: a consensus report of the International Society for Heart and Lung Transplantation. J Heart Lung Transplant. 2016;35(4):397-406.
Verleden SE, Vasilescu DM, Willems S, et al. The site and nature of airway obstruction after lung transplantation. Am J Respir Crit Care Med. 2014;189(3):292-300.
Colombat M, Holifanjaniaina S, Hirschi S, Mal H, Stern M. Histologic reconstruction of bronchiolar lesions in lung transplant patients with bronchiolitis obliterans syndrome. Am J Surg Pathol. 2014;38(8):1157-1158.
Swatek AM, Lynch TJ, Crooke AK, et al. Depletion of Airway submucosal glands and TP63+KRT5+ basal cells in obliterative bronchiolitis. Am J Respir Crit Care Med. 2018;197(8):1045-1057.
Kuehnel M, Maegel L, Vogel-Claussen J, Robertus JL, Jonigk D. Airway remodelling in the transplanted lung. Cell Tissue Res. 2017;367(3):663-675.
Todd JL, Wang X, Sugimoto S, et al. Hyaluronan contributes to bronchiolitis obliterans syndrome and stimulates lung allograft rejection through activation of innate immunity. Am J Respir Crit Care Med. 2014;189(5):556-566.
Todd JL, Kelly FL, Nagler A, et al. Amphiregulin contributes to airway remodeling in chronic allograft dysfunction after lung transplantation. Am J Transplant. 2020;20(3):825-833.
Borthwick LA, Suwara MI, Carnell SC, et al. Pseudomonas aeruginosa induced airway epithelial injury drives fibroblast activation: a mechanism in chronic lung allograft dysfunction. Am J Transplant. 2016;16(6):1751-1765.
LaPar DJ, Burdick MD, Emaminia A, et al. Circulating fibrocytes correlate with bronchiolitis obliterans syndrome development after lung transplantation: a novel clinical biomarker. Ann Thorac Surg. 2011;92(2):470-477.
Nicolls MR, Hsu JL, Jiang X. Microvascular injury after lung transplantation. Curr Opin Organ Transplant. 2016;21(3):279-284.
Jonigk D, Rath B, Borchert P, et al. Comparative analysis of morphological and molecular motifs in bronchiolitis obliterans and alveolar fibroelastosis after lung and stem cell transplantation. J Pathol Clin Res. 2017;3(1):17-28.
Jonigk D, Izykowski N, Rische J, et al. Molecular profiling in lung biopsies of human pulmonary allografts to predict chronic lung allograft dysfunction. Am J Pathol. 2015;185(12):3178-3188.
Halloran PF, Venner JM, Madill-Thomsen KS, et al. Review: the transcripts associated with organ allograft rejection. Am J Transplant. 2018;18(4):785-795.
Halloran KM, Parkes MD, Chang J, et al. Molecular assessment of rejection and injury in lung transplant biopsies. J Heart Lung Transplant. 2019;38(5):504-513.
Halloran K, Parkes MD, Timofte IL, et al. Molecular phenotyping of rejection-related changes in mucosal biopsies from lung transplants. Am J Transplant. 2019;20(4):954-966.
Montero MA, de Gracia J, Culebras Amigo M, et al. The role of transbronchial cryobiopsy in lung transplantation. Histopathology. 2018;73(4):593-600.
Meignin V, Thivolet-Bejui F, Kambouchner M, et al. Lung histopathology of non-infectious pulmonary complications after allogeneic haematopoietic stem cell transplantation. Histopathology. 2018;73(5):832-842.
Paraskeva M, McLean C, Ellis S, et al. Acute fibrinoid organizing pneumonia after lung transplantation. Am J Respir Crit Care Med. 2013;187(12):1360-1368.
Sato M, Hwang DM, Ohmori-Matsuda K, et al. Revisiting the pathologic finding of diffuse alveolar damage after lung transplantation. J Heart Lung Transplant. 2012;31(4):354-363.
Vandermeulen E, Lammertyn E, Verleden SE, et al. Immunological diversity in phenotypes of chronic lung allograft dysfunction: a comprehensive immunohistochemical analysis. Transpl Int. 2017;30(2):134-143.
Watanabe T, Martinu T, Chruscinski A, et al. A B cell-dependent pathway drives chronic lung allograft rejection after ischemia-reperfusion injury in mice. Am J Transplant. 2019;19(12):3377-3389.
Koutsokera A, Royer PJ, Antonietti JP, et al. Development of a multivariate prediction model for early-onset bronchiolitis obliterans syndrome and restrictive allograft syndrome in lung transplantation. Front Med (Lausanne). 2017;4:109.
Verleden SE, Vanaudenaerde BM, Emonds M-P, et al. Donor-specific and -nonspecific HLA antibodies and outcome post lung transplantation. Eur Respir J. 2017;50(5):1701248.
Montero MA, Osadolor T, Khiroya R, et al. Restrictive allograft syndrome and idiopathic pleuroparenchymal fibroelastosis: do they really have the same histology? Histopathology. 2017;70(7):1107-1113.
Verleden SE, Vasilescu DM, McDonough JE, et al. Linking clinical phenotypes of chronic lung allograft dysfunction to changes in lung structure. Eur Respir J. 2015;46(5):1430-1439.
Sacreas A, Yang JYC, Vanaudenaerde BM, et al. The common rejection module in chronic rejection post lung transplantation. PLoS ONE. 2018;13(10):e0205107.
Calabrese F, Hirschi S, Neil D, et al. Alveolar septal widening as an “alert” signal to look into lung antibody-mediated rejection: a multicenter pilot study. Transplantation. 2019;103(11):2440-2447.
Wallace WD, Li N, Andersen CB, et al. Banff study of pathologic changes in lung allograft biopsy specimens with donor-specific antibodies. J Heart Lung Transplant. 2016;35(1):40-48.
Roux A, Levine DJ, Zeevi A, et al. Banff Lung Report: current knowledge and future research perspectives for diagnosis and treatment of pulmonary antibody-mediated rejection (AMR). Am J Transplant. 2019;19(1):21-31.
Roden AC, Maleszewski JJ, Yi ES, et al. Reproducibility of Complement 4d deposition by immunofluorescence and immunohistochemistry in lung allograft biopsies. J Heart Lung Transplant. 2014;33(12):1223-1232.
Ngo C, Danel C, Duong-Quy SY, et al. C4d detection and histological patterns in the diagnosis of antibody-mediated rejection after lung transplantation: a single-centre study. Histopathology. 2019;74(7):988-996.
Aguilar PR, Carpenter D, Ritter J, et al. The role of C4d deposition in the diagnosis of antibody-mediated rejection after lung transplantation. Am J Transplant. 2018;18(4):936-944.
Haas M. An updated Banff schema for diagnosis of antibody-mediated rejection in renal allografts. Curr Opin Organ Transplant. 2014;19(3):315-322.
Orandi BJ, Alachkar N, Kraus ES, et al. Presentation and outcomes of C4d-negative antibody-mediated rejection after kidney transplantation. Am J Transplant. 2016;16(1):213-220.
Thomas KA, Valenzuela NM, Reed EF. The perfect storm: HLA antibodies, complement, FcγRs, and endothelium in transplant rejection. Trends Mol Med. 2015;21(5):319-329.
Valenzuela NM, Reed EF. Antibody-mediated rejection across solid organ transplants: manifestations, mechanisms, and therapies. J Clin Invest. 2017;127(7):2492-2504.
Roux A, Bendib Le Lan I, Holifanjaniaina S, et al. Antibody-mediated rejection in lung transplantation: clinical outcomes and donor-specific antibody characteristics. Am J Transplant. 2016;16(4):1216-1228.
Sacreas A, Taupin J-L, Emonds M-P, et al. Intragraft donor-specific anti-HLA antibodies in phenotypes of chronic lung allograft dysfunction. Eur Respir J. 2019;54(5):1900847.
Visentin J, Chartier A, Massara L, et al. Lung intragraft donor-specific antibodies as a risk factor for graft loss. J Heart Lung Transplant. 2016;35(12):1418-1426.
Benden C, Haughton M, Leonard S, Huber LC. Therapy options for chronic lung allograft dysfunction-bronchiolitis obliterans syndrome following first-line immunosuppressive strategies: a systematic review. J Heart Lung Transplant. 2017;36(9):921-933.