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Published in: Insights into Imaging 1/2020

01-12-2020 | Computed Tomography | Educational Review

Imaging indications and findings in evaluation of lung transplant graft dysfunction and rejection

Authors: Mnahi Bin Saeedan, Sanjay Mukhopadhyay, C. Randall Lane, Rahul D. Renapurkar

Published in: Insights into Imaging | Issue 1/2020

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Abstract

Lung transplantation is a treatment option in end-stage lung disease. Complications can develop along a continuum in the immediate or longer post-transplant period, including surgical and technical complications, primary graft dysfunction, rejection, infections, post-transplant lymphoproliferative disorder, and recurrence of the primary disease. These complications have overlapping clinical and imaging features and often co-exist. Time of onset after transplant is helpful in narrowing the differential diagnosis. In the early post transplantation period, imaging findings are non-specific and need to be interpreted in the context of the clinical picture and other investigations. In contrast, imaging plays a key role in diagnosing and monitoring patients with chronic lung allograft dysfunction. The goal of this article is to review primary graft dysfunction, acute rejection, and chronic rejection with emphasis on the role of imaging, pathology findings, and differential diagnosis.
Literature
1.
go back to reference Chambers DC, Cherikh WS, Goldfarb SB et al (2018) The International Thoracic Organ Transplant Registry of the International Society for Heart and Lung Transplantation: thirty-fifth adult lung and heart-lung transplant report-2018; Focus theme: Multiorgan Transplantation. J Heart Lung Transplant 37(10):1169–1183PubMedCrossRef Chambers DC, Cherikh WS, Goldfarb SB et al (2018) The International Thoracic Organ Transplant Registry of the International Society for Heart and Lung Transplantation: thirty-fifth adult lung and heart-lung transplant report-2018; Focus theme: Multiorgan Transplantation. J Heart Lung Transplant 37(10):1169–1183PubMedCrossRef
2.
go back to reference Krishnam MS, Suh RD, Tomasian A et al (2007) Postoperative complications of lung transplantation: radiologic findings along a time continuum. Radiographics 27(4):957–974PubMedCrossRef Krishnam MS, Suh RD, Tomasian A et al (2007) Postoperative complications of lung transplantation: radiologic findings along a time continuum. Radiographics 27(4):957–974PubMedCrossRef
3.
4.
go back to reference Ahmad S, Shlobin OA, Nathan SD (2011) Pulmonary complications of lung transplantation. Chest 139(2):402–411PubMedCrossRef Ahmad S, Shlobin OA, Nathan SD (2011) Pulmonary complications of lung transplantation. Chest 139(2):402–411PubMedCrossRef
5.
go back to reference Levine DJ, Glanville AR, Aboyoun C et al (2016) Antibody-mediated rejection of the lung: a consensus report of the International Society for Heart and Lung Transplantation. J Heart Lung Transplant 35(4):397–406PubMedCrossRef Levine DJ, Glanville AR, Aboyoun C et al (2016) Antibody-mediated rejection of the lung: a consensus report of the International Society for Heart and Lung Transplantation. J Heart Lung Transplant 35(4):397–406PubMedCrossRef
6.
go back to reference Frost AE, Jammal CT, Cagle PT (1996) Hyperacute rejection following lung transplantation. Chest 110(2):559–562PubMedCrossRef Frost AE, Jammal CT, Cagle PT (1996) Hyperacute rejection following lung transplantation. Chest 110(2):559–562PubMedCrossRef
7.
go back to reference Choi JK, Kearns J, Palevsky HI et al (1999) Hyperacute rejection of a pulmonary allograft. Immediate clinical and pathologic findings. Am J Respir Crit Care Med 160(3):1015–1018PubMedCrossRef Choi JK, Kearns J, Palevsky HI et al (1999) Hyperacute rejection of a pulmonary allograft. Immediate clinical and pathologic findings. Am J Respir Crit Care Med 160(3):1015–1018PubMedCrossRef
8.
go back to reference Bittner HB, Dunitz J, Hertz M, Bolman MR 3rd, Park SJ (2001) Hyperacute rejection in single lung transplantation--case report of successful management by means of plasmapheresis and antithymocyte globulin treatment. Transplantation 71(5):649–651PubMedCrossRef Bittner HB, Dunitz J, Hertz M, Bolman MR 3rd, Park SJ (2001) Hyperacute rejection in single lung transplantation--case report of successful management by means of plasmapheresis and antithymocyte globulin treatment. Transplantation 71(5):649–651PubMedCrossRef
9.
go back to reference Masson E, Stern M, Chabod J et al (2007) Hyperacute rejection after lung transplantation caused by undetected low-titer anti-HLA antibodies. J Heart Lung Transplant 26(6):642–645PubMedCrossRef Masson E, Stern M, Chabod J et al (2007) Hyperacute rejection after lung transplantation caused by undetected low-titer anti-HLA antibodies. J Heart Lung Transplant 26(6):642–645PubMedCrossRef
10.
go back to reference Snell GI, Yusen RD, Weill D et al (2017) Report of the ISHLT Working Group on Primary Lung Graft Dysfunction, part I: Definition and grading-A 2016 Consensus Group statement of the International Society for Heart and Lung Transplantation. J Heart Lung Transplant 36(10):1097–1103 Snell GI, Yusen RD, Weill D et al (2017) Report of the ISHLT Working Group on Primary Lung Graft Dysfunction, part I: Definition and grading-A 2016 Consensus Group statement of the International Society for Heart and Lung Transplantation. J Heart Lung Transplant 36(10):1097–1103
11.
go back to reference de Perrot M, Liu M, Waddell TK, Keshavjee S (2003) Ischemia-reperfusion-induced lung injury. Am J Respir Crit Care Med 167(4):490–511PubMedCrossRef de Perrot M, Liu M, Waddell TK, Keshavjee S (2003) Ischemia-reperfusion-induced lung injury. Am J Respir Crit Care Med 167(4):490–511PubMedCrossRef
12.
go back to reference Mukhopadhyay S, Parambil JG (2012) Acute interstitial pneumonia (AIP): relationship to Hamman-Rich syndrome, diffuse alveolar damage (DAD), and acute respiratory distress syndrome (ARDS). Semin Respir Crit Care Med 33(5):476–485PubMedCrossRef Mukhopadhyay S, Parambil JG (2012) Acute interstitial pneumonia (AIP): relationship to Hamman-Rich syndrome, diffuse alveolar damage (DAD), and acute respiratory distress syndrome (ARDS). Semin Respir Crit Care Med 33(5):476–485PubMedCrossRef
13.
go back to reference Fiser SM, Tribble CG, Long SM et al (2002) Ischemia-reperfusion injury after lung transplantation increases risk of late bronchiolitis obliterans syndrome. Ann Thorac Surg 73(4):1041–1047PubMedCrossRef Fiser SM, Tribble CG, Long SM et al (2002) Ischemia-reperfusion injury after lung transplantation increases risk of late bronchiolitis obliterans syndrome. Ann Thorac Surg 73(4):1041–1047PubMedCrossRef
14.
go back to reference Bharat A, Kuo E, Steward N et al (2008) Immunological link between primary graft dysfunction and chronic lung allograft rejection. Ann Thorac Surg 86(1):189–195PubMedPubMedCentralCrossRef Bharat A, Kuo E, Steward N et al (2008) Immunological link between primary graft dysfunction and chronic lung allograft rejection. Ann Thorac Surg 86(1):189–195PubMedPubMedCentralCrossRef
15.
go back to reference Anderson DC, Glazer HS, Semenkovich JW et al (1995) Lung transplant edema: chest radiography after lung transplantation--the first 10 days. Radiology 195(1):275–281PubMedCrossRef Anderson DC, Glazer HS, Semenkovich JW et al (1995) Lung transplant edema: chest radiography after lung transplantation--the first 10 days. Radiology 195(1):275–281PubMedCrossRef
16.
go back to reference Kundu S, Herman SJ, Winton TL (1998) Reperfusion edema after lung transplantation: radiographic manifestations. Radiology 206(1):75–80PubMedCrossRef Kundu S, Herman SJ, Winton TL (1998) Reperfusion edema after lung transplantation: radiographic manifestations. Radiology 206(1):75–80PubMedCrossRef
17.
go back to reference Marom EM, Choi YW, Palmer SM, DeLong DM, Stuart MD, McAdams HP (2001) Reperfusion edema after lung transplantation: effect of daclizumab. Radiology 221(2):508–514PubMedCrossRef Marom EM, Choi YW, Palmer SM, DeLong DM, Stuart MD, McAdams HP (2001) Reperfusion edema after lung transplantation: effect of daclizumab. Radiology 221(2):508–514PubMedCrossRef
18.
go back to reference Belmaati EO, Steffensen I, Jensen C et al (2012) Radiological patterns of primary graft dysfunction after lung transplantation evaluated by 64-multi-slice computed tomography: a descriptive study. Interact Cardiovasc Thorac Surg 14(6):785–791PubMedPubMedCentralCrossRef Belmaati EO, Steffensen I, Jensen C et al (2012) Radiological patterns of primary graft dysfunction after lung transplantation evaluated by 64-multi-slice computed tomography: a descriptive study. Interact Cardiovasc Thorac Surg 14(6):785–791PubMedPubMedCentralCrossRef
19.
go back to reference Hopkins PM, Aboyoun CL, Chhajed PN et al (2002) Prospective analysis of 1,235 transbronchial lung biopsies in lung transplant recipients. J Heart Lung Transplant 21(10):1062–1067PubMedCrossRef Hopkins PM, Aboyoun CL, Chhajed PN et al (2002) Prospective analysis of 1,235 transbronchial lung biopsies in lung transplant recipients. J Heart Lung Transplant 21(10):1062–1067PubMedCrossRef
20.
go back to reference Yusen RD, Edwards LB, Kucheryavaya AY et al (2015) The Registry of the International Society for Heart and Lung Transplantation: thirty-second official adult lung and heart-lung transplantation report--2015; Focus Theme: Early Graft Failure. J Heart Lung Transplant 34(10):1264–1277PubMedCrossRef Yusen RD, Edwards LB, Kucheryavaya AY et al (2015) The Registry of the International Society for Heart and Lung Transplantation: thirty-second official adult lung and heart-lung transplantation report--2015; Focus Theme: Early Graft Failure. J Heart Lung Transplant 34(10):1264–1277PubMedCrossRef
21.
22.
23.
go back to reference Stewart S, Fishbein MC, Snell GI et al (2007) Revision of the 1996 working formulation for the standardization of nomenclature in the diagnosis of lung rejection. J Heart Lung Transplant 26(12):1229–1242PubMedCrossRef Stewart S, Fishbein MC, Snell GI et al (2007) Revision of the 1996 working formulation for the standardization of nomenclature in the diagnosis of lung rejection. J Heart Lung Transplant 26(12):1229–1242PubMedCrossRef
24.
go back to reference De Vito DA, Hoffman LA, Iacono AT, Zullo TG, McCurry KR, Dauber JH (2004) Are symptom reports useful for differentiating between acute rejection and pulmonary infection after lung transplantation? Heart Lung 33(6):372–380CrossRef De Vito DA, Hoffman LA, Iacono AT, Zullo TG, McCurry KR, Dauber JH (2004) Are symptom reports useful for differentiating between acute rejection and pulmonary infection after lung transplantation? Heart Lung 33(6):372–380CrossRef
25.
go back to reference Gotway MB, Dawn SK, Sellami D et al (2001) Acute rejection following lung transplantation: limitations in accuracy of thin-section CT for diagnosis. Radiology 221(1):207–212PubMedCrossRef Gotway MB, Dawn SK, Sellami D et al (2001) Acute rejection following lung transplantation: limitations in accuracy of thin-section CT for diagnosis. Radiology 221(1):207–212PubMedCrossRef
26.
go back to reference Park CH, Paik HC, Haam SJ et al (2014) HRCT features of acute rejection in patients with bilateral lung transplantation: the usefulness of lesion distribution. Transplant Proc 46(5):1511–1516PubMedCrossRef Park CH, Paik HC, Haam SJ et al (2014) HRCT features of acute rejection in patients with bilateral lung transplantation: the usefulness of lesion distribution. Transplant Proc 46(5):1511–1516PubMedCrossRef
27.
go back to reference Fuehner T, Simon A, Dierich M et al (2009) Indicators for steroid response in biopsy proven acute graft rejection after lung transplantation. Respir Med 103(8):1114–1121PubMedCrossRef Fuehner T, Simon A, Dierich M et al (2009) Indicators for steroid response in biopsy proven acute graft rejection after lung transplantation. Respir Med 103(8):1114–1121PubMedCrossRef
28.
go back to reference Lewis AJ, Jagadeesh D, Mukhopadhyay S, Budev M, Mehta AC (2018) Corrigendum to: Post-transplant lymphoproliferative disorder presenting on post-transplant day 35 as a pulmonary parenchymal infiltrate-a case report. Oxf Med Case Reports. 2018(12):omy100 Lewis AJ, Jagadeesh D, Mukhopadhyay S, Budev M, Mehta AC (2018) Corrigendum to: Post-transplant lymphoproliferative disorder presenting on post-transplant day 35 as a pulmonary parenchymal infiltrate-a case report. Oxf Med Case Reports. 2018(12):omy100
30.
go back to reference Sato M, Waddell TK, Wagnetz U et al (2011) Restrictive allograft syndrome (RAS): a novel form of chronic lung allograft dysfunction. J Heart Lung Transplant 30(7):735–742PubMedCrossRef Sato M, Waddell TK, Wagnetz U et al (2011) Restrictive allograft syndrome (RAS): a novel form of chronic lung allograft dysfunction. J Heart Lung Transplant 30(7):735–742PubMedCrossRef
31.
go back to reference Husain AN, Siddiqui MT, Holmes EW et al (1999) Analysis of risk factors for the development of bronchiolitis obliterans syndrome. Am J Respir Crit Care Med 159(3):829–833PubMedCrossRef Husain AN, Siddiqui MT, Holmes EW et al (1999) Analysis of risk factors for the development of bronchiolitis obliterans syndrome. Am J Respir Crit Care Med 159(3):829–833PubMedCrossRef
32.
go back to reference Estenne M, Maurer JR, Boehler A et al (2002) Bronchiolitis obliterans syndrome 2001: an update of the diagnostic criteria. J Heart Lung Transplant 21(3):297–310PubMedCrossRef Estenne M, Maurer JR, Boehler A et al (2002) Bronchiolitis obliterans syndrome 2001: an update of the diagnostic criteria. J Heart Lung Transplant 21(3):297–310PubMedCrossRef
33.
go back to reference Kramer MR, Stoehr C, Whang JL et al (1993) The diagnosis of obliterative bronchiolitis after heart-lung and lung transplantation: low yield of transbronchial lung biopsy. J Heart Lung Transplant 12(4):675–681 Kramer MR, Stoehr C, Whang JL et al (1993) The diagnosis of obliterative bronchiolitis after heart-lung and lung transplantation: low yield of transbronchial lung biopsy. J Heart Lung Transplant 12(4):675–681
34.
go back to reference Bankier AA, Van Muylem A, Knoop C, Estenne M, Gevenois PA (2001) Bronchiolitis obliterans syndrome in heart-lung transplant recipients: diagnosis with expiratory CT. Radiology 218(2):533–539PubMedCrossRef Bankier AA, Van Muylem A, Knoop C, Estenne M, Gevenois PA (2001) Bronchiolitis obliterans syndrome in heart-lung transplant recipients: diagnosis with expiratory CT. Radiology 218(2):533–539PubMedCrossRef
35.
go back to reference Morrish WF, Herman SJ, Weisbrod GL, Chamberlain DW (1991) Bronchiolitis obliterans after lung transplantation: findings at chest radiography and high-resolution CT. The Toronto Lung Transplant Group. Radiology 179(2):487–490PubMedCrossRef Morrish WF, Herman SJ, Weisbrod GL, Chamberlain DW (1991) Bronchiolitis obliterans after lung transplantation: findings at chest radiography and high-resolution CT. The Toronto Lung Transplant Group. Radiology 179(2):487–490PubMedCrossRef
36.
go back to reference Worthy SA, Park CS, Kim JS, Muller NL (1997) Bronchiolitis obliterans after lung transplantation: high-resolution CT findings in 15 patients. AJR Am J Roentgenol 169(3):673–677PubMedCrossRef Worthy SA, Park CS, Kim JS, Muller NL (1997) Bronchiolitis obliterans after lung transplantation: high-resolution CT findings in 15 patients. AJR Am J Roentgenol 169(3):673–677PubMedCrossRef
37.
go back to reference Lee ES, Gotway MB, Reddy GP, Golden JA, Keith FM, Webb WR (2000) Early bronchiolitis obliterans following lung transplantation: accuracy of expiratory thin-section CT for diagnosis. Radiology 216(2):472–477PubMedCrossRef Lee ES, Gotway MB, Reddy GP, Golden JA, Keith FM, Webb WR (2000) Early bronchiolitis obliterans following lung transplantation: accuracy of expiratory thin-section CT for diagnosis. Radiology 216(2):472–477PubMedCrossRef
38.
go back to reference Choi YW, Rossi SE, Palmer SM, DeLong D, Erasmus JJ, McAdams HP (2003) Bronchiolitis obliterans syndrome in lung transplant recipients: correlation of computed tomography findings with bronchiolitis obliterans syndrome stage. J Thorac Imaging 18(2):72–79PubMedCrossRef Choi YW, Rossi SE, Palmer SM, DeLong D, Erasmus JJ, McAdams HP (2003) Bronchiolitis obliterans syndrome in lung transplant recipients: correlation of computed tomography findings with bronchiolitis obliterans syndrome stage. J Thorac Imaging 18(2):72–79PubMedCrossRef
39.
go back to reference Konen E, Gutierrez C, Chaparro C et al (2004) Bronchiolitis obliterans syndrome in lung transplant recipients: can thin-section CT findings predict disease before its clinical appearance? Radiology 231(2):467–473PubMedCrossRef Konen E, Gutierrez C, Chaparro C et al (2004) Bronchiolitis obliterans syndrome in lung transplant recipients: can thin-section CT findings predict disease before its clinical appearance? Radiology 231(2):467–473PubMedCrossRef
40.
go back to reference Gunn ML, Godwin JD, Kanne JP, Flowers ME, Chien JW (2008) High-resolution CT findings of bronchiolitis obliterans syndrome after hematopoietic stem cell transplantation. J Thorac Imaging 23(4):244–250PubMedPubMedCentralCrossRef Gunn ML, Godwin JD, Kanne JP, Flowers ME, Chien JW (2008) High-resolution CT findings of bronchiolitis obliterans syndrome after hematopoietic stem cell transplantation. J Thorac Imaging 23(4):244–250PubMedPubMedCentralCrossRef
41.
go back to reference Ofek E, Sato M, Saito T et al (2013) Restrictive allograft syndrome post lung transplantation is characterized by pleuroparenchymal fibroelastosis. Mod Pathol 26(3):350–356PubMedCrossRef Ofek E, Sato M, Saito T et al (2013) Restrictive allograft syndrome post lung transplantation is characterized by pleuroparenchymal fibroelastosis. Mod Pathol 26(3):350–356PubMedCrossRef
42.
go back to reference Verleden SE, de Jong PA, Ruttens D et al (2014) Functional and computed tomographic evolution and survival of restrictive allograft syndrome after lung transplantation. J Heart Lung Transplant 33(3):270–277PubMedCrossRef Verleden SE, de Jong PA, Ruttens D et al (2014) Functional and computed tomographic evolution and survival of restrictive allograft syndrome after lung transplantation. J Heart Lung Transplant 33(3):270–277PubMedCrossRef
43.
go back to reference Arakawa H, Kurihara Y, Niimi H, Nakajima Y, Johkoh T, Nakamura H (2001) Bronchiolitis obliterans with organizing pneumonia versus chronic eosinophilic pneumonia: high-resolution CT findings in 81 patients. AJR Am J Roentgenol 176(4):1053–1058PubMedCrossRef Arakawa H, Kurihara Y, Niimi H, Nakajima Y, Johkoh T, Nakamura H (2001) Bronchiolitis obliterans with organizing pneumonia versus chronic eosinophilic pneumonia: high-resolution CT findings in 81 patients. AJR Am J Roentgenol 176(4):1053–1058PubMedCrossRef
44.
go back to reference Konen E, Weisbrod GL, Pakhale S, Chung T, Paul NS, Hutcheon MA (2003) Fibrosis of the upper lobes: a newly identified late-onset complication after lung transplantation? AJR Am J Roentgenol 181(6):1539–1543PubMedCrossRef Konen E, Weisbrod GL, Pakhale S, Chung T, Paul NS, Hutcheon MA (2003) Fibrosis of the upper lobes: a newly identified late-onset complication after lung transplantation? AJR Am J Roentgenol 181(6):1539–1543PubMedCrossRef
45.
46.
go back to reference Solyanik O, Hollmann P, Dettmer S et al (2015) Quantification of pathologic air trapping in lung transplant patients using CT density mapping: comparison with other CT air trapping measures. PLoS One 10(10)PubMedPubMedCentralCrossRef Solyanik O, Hollmann P, Dettmer S et al (2015) Quantification of pathologic air trapping in lung transplant patients using CT density mapping: comparison with other CT air trapping measures. PLoS One 10(10)PubMedPubMedCentralCrossRef
47.
go back to reference Mortani Barbosa EJ Jr, Shou H, Simpsom S, Gee J, Tustison N, Lee JC (2018) Quantitative computed tomography metrics from the transplanted lung can predict forced expiratory volume in the first second after lung transplantation. J Thorac Imaging 33(2):112–123PubMedCrossRef Mortani Barbosa EJ Jr, Shou H, Simpsom S, Gee J, Tustison N, Lee JC (2018) Quantitative computed tomography metrics from the transplanted lung can predict forced expiratory volume in the first second after lung transplantation. J Thorac Imaging 33(2):112–123PubMedCrossRef
48.
go back to reference Saito T, Horie M, Sato M et al (2016) Low-dose computed tomography volumetry for subtyping chronic lung allograft dysfunction. J Heart Lung Transplant 35(1):59–66PubMedCrossRef Saito T, Horie M, Sato M et al (2016) Low-dose computed tomography volumetry for subtyping chronic lung allograft dysfunction. J Heart Lung Transplant 35(1):59–66PubMedCrossRef
49.
go back to reference Renne J, Lauermann P, Hinrichs JB et al (2015) Chronic lung allograft dysfunction: oxygen-enhanced T1-mapping MR imaging of the lung. Radiology 276(1):266–273PubMedCrossRef Renne J, Lauermann P, Hinrichs JB et al (2015) Chronic lung allograft dysfunction: oxygen-enhanced T1-mapping MR imaging of the lung. Radiology 276(1):266–273PubMedCrossRef
50.
go back to reference Voskrebenzev A, Greer M, Gutberlet M et al (2018) Detection of chronic lung allograft dysfunction using ventilation-weighted Fourier decomposition MRI. Am J Transplant 18(8):2050–2060PubMedCrossRef Voskrebenzev A, Greer M, Gutberlet M et al (2018) Detection of chronic lung allograft dysfunction using ventilation-weighted Fourier decomposition MRI. Am J Transplant 18(8):2050–2060PubMedCrossRef
51.
go back to reference Moher Alsady T, Voskrebenzev A, Greer M et al (2019) MRI-derived regional flow-volume loop parameters detect early-stage chronic lung allograft dysfunction. J Magn Reson Imaging 27(10):26799 Moher Alsady T, Voskrebenzev A, Greer M et al (2019) MRI-derived regional flow-volume loop parameters detect early-stage chronic lung allograft dysfunction. J Magn Reson Imaging 27(10):26799
52.
go back to reference Verleden SE, Gheysens O, Goffin KE et al (2019) Role of 18F-FDG PET/CT in restrictive allograft syndrome after lung transplantation. Transplantation 103(4):823–831PubMedCrossRef Verleden SE, Gheysens O, Goffin KE et al (2019) Role of 18F-FDG PET/CT in restrictive allograft syndrome after lung transplantation. Transplantation 103(4):823–831PubMedCrossRef
Metadata
Title
Imaging indications and findings in evaluation of lung transplant graft dysfunction and rejection
Authors
Mnahi Bin Saeedan
Sanjay Mukhopadhyay
C. Randall Lane
Rahul D. Renapurkar
Publication date
01-12-2020
Publisher
Springer Berlin Heidelberg
Published in
Insights into Imaging / Issue 1/2020
Electronic ISSN: 1869-4101
DOI
https://doi.org/10.1186/s13244-019-0822-7

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