Grading Histopathology Features of Graft-versus-host Disease in Animal Models; A Systematic Review
Abstract
Graft-versus-host disease (GvHD), a frequent and severe complication following allogeneic hematopoietic stem cell transplantation, presents substantial morbidity and mortality risks. The crucial role of histopathological examination in diagnosing and grading GvHD, particularly within animal models, is pivotal for elucidating disease mechanisms and assessing emerging therapies. This systematic review aims to critically evaluate the various grading systems for GvHD in animal models, emphasizing histopathological characteristics. In this endeavor, we meticulously examined original research articles sourced from PubMed, Scopus, Web of Science, and Google Scholar. Our findings reveal a diverse array of grading systems, each differing in the tissues examined, criteria evaluated, severity scoring scales, and the granularity of the information provided. Predominantly, skin, liver, and gut tissues are assessed, though some systems also incorporate lung and thymus evaluations. This review will delve into the alignment between clinical and histological grading in animal models of GvHD, also casting light on prospective advancements and the impact of technological progress. In conclusion, our analysis underscores the imperative need for uniform criteria and consistent application of grading systems. Such standardization is essential to foster comparability across studies and enhance the translation of preclinical discoveries into clinical applications.
1. Ferrara JL, Levine JE, Reddy P, Holler E. Graft-versus-host disease. Lancet. 2009;373(9674):1550-61.
2. Zeiser R, Blazar BR. Pathophysiology of Chronic Graft-versus-Host Disease and Therapeutic Targets. N Engl J Med. 2017;377(26):2565-79.
3. Salemi F, Mortazavizadeh SMR, Mirmoeeni S, Azari Jafari A, Kosari F, Naghibi Irvani SS. A misdiagnosed case of blastic plasmacytoid dendritic cell neoplasm experiencing multiple recurrences who underwent allogeneic stem cell transplantation: a case report. J Med Case Rep. 2021;15(1):292.
4. Gupta M, Tieu A, Slobodian M, Shorr R, Burger D, Lalu MM, et al. Preclinical studies of MSC-derived extracellular vesicles to treat or prevent graft versus host disease: a systematic review of the literature. Stem Cell Rev Rep. 2021;17:332-40.
5. Schroeder MA, DiPersio JF. Mouse models of graft- versus-host disease: advances and limitations. Dis Model
Mech. 2011;4(3):318-33.
6. Shapiro RM, Antin JH. Therapeutic options for steroid-refractory acute and chronic GVHD: an evolving landscape. Exp Rev Hematol. 2020;13(5):519-32.
7. Shlomchik WD. Graft-versus-host disease. Nat Rev Immunol. 2007;7(5):340-52.
8. Hooijmans CR, Rovers MM, De Vries RB, Leenaars M, Ritskes-Hoitinga M, Langendam MW. SYRCLE’s risk of bias tool for animal studies. BMC Med Res Methodol. 2014;14:1-9.
9. Mestas J, Hughes CC. Of mice and not men: differences between mouse and human immunology. J Immunol. 2004;172(5):2731-8.
10. Cooke KR, Kobzik L, Martin TR, Brewer J, Delmonte JJ, Crawford JM, et al. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood. 1996;88(8):3230-9.
11. Lerner K, Kao G, Storb R, Buckner C, Clift R, Thomas E, editors. Histopathology of graft-vs.-host reaction (GvHR) in human recipients of marrow from HL-A-matched sibling donors. Transplant Proc. 1974;6(4):367-71.
12. Hill GR, Ferrara JL. The primacy of the gastrointestinal tract as a target organ of acute graft-versus-host disease: rationale for the use of cytokine shields in allogeneic bone marrow transplantation. Blood. 2000;95(9):2754-9.
13. Socié G, Blazar BR. Acute graft-versus-host disease: from the bench to the bedside. Blood. 2009;114(20):4327-36.
14. Jagasia MH, Greinix HT, Arora M, Williams KM, Wolff D, Cowen EW, et al. National Institutes of Health Consensus Development Project on Criteria for Clinical Trials in Chronic Graft-versus-Host Disease: I. The 2014 Diagnosis and Staging Working Group report. Biol Blood Marrow Transplant. 2015;21(3):389-401.e1.
15. Socié G, Mary JY, Lemann M, Daneshpouy M, Guardiola P, Meignin V, et al. Prognostic value of apoptotic cells and infiltrating neutrophils in graft-versus-host disease of the gastrointestinal tract in humans: TNF and Fas expression. Blood. 2004;103(1):50-7.
16. Furlan SN, Watkins B, Tkachev V, Flynn R, Cooley S, Ramakrishnan S, et al. Transcriptome analysis of GVHD reveals aurora kinase A as a targetable pathway for disease prevention. Sci Trans Med. 2015;7(315):315ra191-315ra191.
17. Estenne M, Maurer JR, Boehler A, Egan JJ, Frost A, Hertz M, et al. Bronchiolitis obliterans syndrome 2001: an update of the diagnostic criteria. J Heart Lung Transplant. 2002;21(3):297-310.
18. Yousem SA, Berry GJ, Cagle PT, Chamberlain D, Husain AN, Hruban RH, et al. Revision of the 1990 working formulation for the classification of pulmonary allograft rejection: Lung Rejection Study Group. J Heart Lung Transplant. 1996;15(1 Pt 1):1-15.
19. Shulman HM, Sullivan KM, Weiden PL, McDonald GB, Striker GE, Sale GE, et al. Chronic graft-versus-host syndrome in man. A long-term clinicopathologic study of 20 Seattle patients. Am J Med. 1980;69(2):204-17.
20. Chakrabarti S, MacDonald D, Hale G, Holder K, Turner V, Czarnecka H, et al. T-cell depletion with Campath-1H "in the bag" for matched related allogeneic peripheral blood stem cell transplantation is associated with reduced graft-versus-host disease, rapid immune constitution and improved survival. Br J Haematol. 2003;121(1):109-18.
21. Ferrara JL, Cooke KR, Teshima T. The pathophysiology of acute graft-versus-host disease. Int J Hematol. 2003;78:181-7.
22. Kuzmina Z, Gounden V, Curtis L, Avila D, Rnp TT, Baruffaldi J, et al. Clinical significance of autoantibodies in a large cohort of patients with chronic graft-versus-host disease defined by NIH criteria. Am J Hematol. 2015;90(2):114-9.
23. Goker H, Haznedaroglu IC, Chao NJ. Acute graft-vs-host disease: pathobiology and management. Exp Hematol. 2001;29(3):259-77.
24. Harris AC, Young R, Devine S, Hogan WJ, Ayuk F, Bunworasate U, et al. International, multicenter standardization of acute graft-versus-host disease clinical data collection: a report from the Mount Sinai Acute GVHD International Consortium. Biol Blood Marrow Transplant. 2016;22(1):4-10.
25. Cooke KR, Gerbitz A, Crawford JM, Teshima T, Hill GR, Tesolin A, et al. LPS antagonism reduces graft-versus-host disease and preserves graft-versus-leukemia activity after experimental bone marrow transplantation. J Clin Invest. 2001;107(12):1581-9.
26. Ferrara JL, Deeg HJ. Graft-versus-host disease. New Eng J Med. 1991;324(10):667-74.
27. Hill GR, Crawford JM, Cooke KR, Brinson YS, Pan L, Ferrara JL. Total body irradiation and acute graft-versus-host disease: the role of gastrointestinal damage and inflammatory cytokines. Blood. 1997;90(8):3204-13.
28. Yousem SA. The histological spectrum of pulmonary graft-versus-host disease in bone marrow transplant recipients. Hum Pathol. 1995;26(6):668-75.
29. Cooke KR, Kobzik L, Martin TR, Brewer J, Delmonte J, Jr., Crawford JM, et al. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood. 1996;88(8):3230-9.
30. Pantanowitz L, Sinard JH, Henricks WH, Fatheree LA, Carter AB, Contis L, et al. Validating whole slide imaging for diagnostic purposes in pathology: guideline from the College of American Pathologists Pathology and Laboratory Quality Center. Arch Pathol Lab Med .2013;137(12):1710-22.
31. Swerdlow SH, Campo E, Pileri SA, Harris NL, Stein H, Siebert R, et al. The 2016 revision of the World Health Organization classification of lymphoid neoplasms. Blood. 2016;127(20):2375-90.
32. Minervini MI, Yagi Y, Marino IR, Lawson A, Nalesnik M, Randhawa P, et al. Development and experience with an integrated system for transplantation telepathology. Hum Pathol. 2001;32(12):1334-43.
33. Cooke KR, Hill GR, Crawford JM, Bungard D, Brinson YS, Delmonte J, et al. Tumor necrosis factor-alpha production to lipopolysaccharide stimulation by donor cells predicts the severity of experimental acute graft-versus-host disease. J Clin Invest. 1998;102(10):1882-91.
34. Yanik G, Hellerstedt B, Custer J, Hutchinson R, Kwon D, Ferrara JL, et al. Etanercept (Enbrel) administration for idiopathic pneumonia syndrome after allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2002;8(7):395-400.
35. Shlomchik WD, Couzens MS, Tang CB, McNiff J, Robert ME, Liu J, et al. Prevention of graft versus host disease by inactivation of host antigen-presenting cells. Science. 1999;285(5426):412-5.
2. Zeiser R, Blazar BR. Pathophysiology of Chronic Graft-versus-Host Disease and Therapeutic Targets. N Engl J Med. 2017;377(26):2565-79.
3. Salemi F, Mortazavizadeh SMR, Mirmoeeni S, Azari Jafari A, Kosari F, Naghibi Irvani SS. A misdiagnosed case of blastic plasmacytoid dendritic cell neoplasm experiencing multiple recurrences who underwent allogeneic stem cell transplantation: a case report. J Med Case Rep. 2021;15(1):292.
4. Gupta M, Tieu A, Slobodian M, Shorr R, Burger D, Lalu MM, et al. Preclinical studies of MSC-derived extracellular vesicles to treat or prevent graft versus host disease: a systematic review of the literature. Stem Cell Rev Rep. 2021;17:332-40.
5. Schroeder MA, DiPersio JF. Mouse models of graft- versus-host disease: advances and limitations. Dis Model
Mech. 2011;4(3):318-33.
6. Shapiro RM, Antin JH. Therapeutic options for steroid-refractory acute and chronic GVHD: an evolving landscape. Exp Rev Hematol. 2020;13(5):519-32.
7. Shlomchik WD. Graft-versus-host disease. Nat Rev Immunol. 2007;7(5):340-52.
8. Hooijmans CR, Rovers MM, De Vries RB, Leenaars M, Ritskes-Hoitinga M, Langendam MW. SYRCLE’s risk of bias tool for animal studies. BMC Med Res Methodol. 2014;14:1-9.
9. Mestas J, Hughes CC. Of mice and not men: differences between mouse and human immunology. J Immunol. 2004;172(5):2731-8.
10. Cooke KR, Kobzik L, Martin TR, Brewer J, Delmonte JJ, Crawford JM, et al. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood. 1996;88(8):3230-9.
11. Lerner K, Kao G, Storb R, Buckner C, Clift R, Thomas E, editors. Histopathology of graft-vs.-host reaction (GvHR) in human recipients of marrow from HL-A-matched sibling donors. Transplant Proc. 1974;6(4):367-71.
12. Hill GR, Ferrara JL. The primacy of the gastrointestinal tract as a target organ of acute graft-versus-host disease: rationale for the use of cytokine shields in allogeneic bone marrow transplantation. Blood. 2000;95(9):2754-9.
13. Socié G, Blazar BR. Acute graft-versus-host disease: from the bench to the bedside. Blood. 2009;114(20):4327-36.
14. Jagasia MH, Greinix HT, Arora M, Williams KM, Wolff D, Cowen EW, et al. National Institutes of Health Consensus Development Project on Criteria for Clinical Trials in Chronic Graft-versus-Host Disease: I. The 2014 Diagnosis and Staging Working Group report. Biol Blood Marrow Transplant. 2015;21(3):389-401.e1.
15. Socié G, Mary JY, Lemann M, Daneshpouy M, Guardiola P, Meignin V, et al. Prognostic value of apoptotic cells and infiltrating neutrophils in graft-versus-host disease of the gastrointestinal tract in humans: TNF and Fas expression. Blood. 2004;103(1):50-7.
16. Furlan SN, Watkins B, Tkachev V, Flynn R, Cooley S, Ramakrishnan S, et al. Transcriptome analysis of GVHD reveals aurora kinase A as a targetable pathway for disease prevention. Sci Trans Med. 2015;7(315):315ra191-315ra191.
17. Estenne M, Maurer JR, Boehler A, Egan JJ, Frost A, Hertz M, et al. Bronchiolitis obliterans syndrome 2001: an update of the diagnostic criteria. J Heart Lung Transplant. 2002;21(3):297-310.
18. Yousem SA, Berry GJ, Cagle PT, Chamberlain D, Husain AN, Hruban RH, et al. Revision of the 1990 working formulation for the classification of pulmonary allograft rejection: Lung Rejection Study Group. J Heart Lung Transplant. 1996;15(1 Pt 1):1-15.
19. Shulman HM, Sullivan KM, Weiden PL, McDonald GB, Striker GE, Sale GE, et al. Chronic graft-versus-host syndrome in man. A long-term clinicopathologic study of 20 Seattle patients. Am J Med. 1980;69(2):204-17.
20. Chakrabarti S, MacDonald D, Hale G, Holder K, Turner V, Czarnecka H, et al. T-cell depletion with Campath-1H "in the bag" for matched related allogeneic peripheral blood stem cell transplantation is associated with reduced graft-versus-host disease, rapid immune constitution and improved survival. Br J Haematol. 2003;121(1):109-18.
21. Ferrara JL, Cooke KR, Teshima T. The pathophysiology of acute graft-versus-host disease. Int J Hematol. 2003;78:181-7.
22. Kuzmina Z, Gounden V, Curtis L, Avila D, Rnp TT, Baruffaldi J, et al. Clinical significance of autoantibodies in a large cohort of patients with chronic graft-versus-host disease defined by NIH criteria. Am J Hematol. 2015;90(2):114-9.
23. Goker H, Haznedaroglu IC, Chao NJ. Acute graft-vs-host disease: pathobiology and management. Exp Hematol. 2001;29(3):259-77.
24. Harris AC, Young R, Devine S, Hogan WJ, Ayuk F, Bunworasate U, et al. International, multicenter standardization of acute graft-versus-host disease clinical data collection: a report from the Mount Sinai Acute GVHD International Consortium. Biol Blood Marrow Transplant. 2016;22(1):4-10.
25. Cooke KR, Gerbitz A, Crawford JM, Teshima T, Hill GR, Tesolin A, et al. LPS antagonism reduces graft-versus-host disease and preserves graft-versus-leukemia activity after experimental bone marrow transplantation. J Clin Invest. 2001;107(12):1581-9.
26. Ferrara JL, Deeg HJ. Graft-versus-host disease. New Eng J Med. 1991;324(10):667-74.
27. Hill GR, Crawford JM, Cooke KR, Brinson YS, Pan L, Ferrara JL. Total body irradiation and acute graft-versus-host disease: the role of gastrointestinal damage and inflammatory cytokines. Blood. 1997;90(8):3204-13.
28. Yousem SA. The histological spectrum of pulmonary graft-versus-host disease in bone marrow transplant recipients. Hum Pathol. 1995;26(6):668-75.
29. Cooke KR, Kobzik L, Martin TR, Brewer J, Delmonte J, Jr., Crawford JM, et al. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood. 1996;88(8):3230-9.
30. Pantanowitz L, Sinard JH, Henricks WH, Fatheree LA, Carter AB, Contis L, et al. Validating whole slide imaging for diagnostic purposes in pathology: guideline from the College of American Pathologists Pathology and Laboratory Quality Center. Arch Pathol Lab Med .2013;137(12):1710-22.
31. Swerdlow SH, Campo E, Pileri SA, Harris NL, Stein H, Siebert R, et al. The 2016 revision of the World Health Organization classification of lymphoid neoplasms. Blood. 2016;127(20):2375-90.
32. Minervini MI, Yagi Y, Marino IR, Lawson A, Nalesnik M, Randhawa P, et al. Development and experience with an integrated system for transplantation telepathology. Hum Pathol. 2001;32(12):1334-43.
33. Cooke KR, Hill GR, Crawford JM, Bungard D, Brinson YS, Delmonte J, et al. Tumor necrosis factor-alpha production to lipopolysaccharide stimulation by donor cells predicts the severity of experimental acute graft-versus-host disease. J Clin Invest. 1998;102(10):1882-91.
34. Yanik G, Hellerstedt B, Custer J, Hutchinson R, Kwon D, Ferrara JL, et al. Etanercept (Enbrel) administration for idiopathic pneumonia syndrome after allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2002;8(7):395-400.
35. Shlomchik WD, Couzens MS, Tang CB, McNiff J, Robert ME, Liu J, et al. Prevention of graft versus host disease by inactivation of host antigen-presenting cells. Science. 1999;285(5426):412-5.
| Files | ||
| Issue | Vol 23 No 3 (2024) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/ijaai.v23i3.15634 | |
| Keywords | ||
| Animal model Grading system Graft-versus-host disease GvHD Histopathology | ||
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How to Cite
1.
Ashraf H, Kosari F. Grading Histopathology Features of Graft-versus-host Disease in Animal Models; A Systematic Review. Iran J Allergy Asthma Immunol. 2024;23(3):235-244.
