Extracorporeal photopheresis in the treatment of graft-versus-host disease: Evidence and opinion

Therapeutic Advances in Hematology

Volumn 4, Issue 5, 2013, Pages 320-334

  Hart, James W ^a   Shiue, Lisa H ^b   Shpall, Elizabeth J ^a   Alousi, Amin M ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b University of Texas Health Science Center at Houston   (United States)

Author keywords

Graft versus host disease; hematopoietic stem cell transplantation; immunomodulation; photopheresis

Indexed keywords

CORTICOSTEROID; METHOXSALEN;

ACUTE GRAFT VERSUS HOST DISEASE; ALLOIMMUNITY; ANTIGEN PRESENTING CELL; APOPTOSIS; ARTICLE; ATOPIC DERMATITIS; CHRONIC GRAFT VERSUS HOST DISEASE; CROHN DISEASE; CROHN DISEASE ACTIVITY INDEX; CUTANEOUS T CELL LYMPHOMA; EXTRACORPOREAL PHOTOPHERESIS; GRAFT SURVIVAL; GRAFT VERSUS HOST REACTION; HUMAN; IMMUNOBIOLOGY; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOSTIMULATION; INSULIN DEPENDENT DIABETES MELLITUS; NEPHROGENIC SYSTEMIC FIBROSIS; NONHUMAN; PALLIATIVE THERAPY; PEMPHIGUS VULGARIS; PHOTOAGING; PHOTOSENSITIVITY; PRIORITY JOURNAL; PUVA; QUALITY OF LIFE; RHEUMATOID ARTHRITIS; SYSTEMIC LUPUS ERYTHEMATOSUS; SYSTEMIC SCLEROSIS; ULTRAVIOLET A RADIATION;

EID: 84993707671     PISSN: 20406207     EISSN: 20406215     Source Type: Journal    
DOI: 10.1177/2040620713490316     Document Type: Article

References (89)

1. Abreu M. von Tirpitz C. Hardi R. Kaatz M. van Assche G. Rutgeerts P. et al. (2009) Extracorporeal photopheresis for the treatment of refractory Crohn's disease: results of an open-label pilot study. Inflamm Bowel Dis 15: 829–836.
2. Apisarnthanarax N. Donato M. Korbling M. Couriel D. Gajewski J. Giralt S. et al. (2003) Extracorporeal photopheresis therapy in the management of steroid-refractory or steroid-dependent cutaneous chronic graft-versus-host disease after allogeneic stem cell transplantation: feasibility and results. Bone Marrow Transplant 31: 459–465.
3. Barr M. Meiser B. Eisen H. Roberts R. Livi U. Dall'Amico R. et al. (1998) Photopheresis for the prevention of rejection in cardiac transplantation. Photopheresis Transplantation Study Group. N Engl J Med 339: 1744–1751.
4. Berger C. Hanlon D. Kanada D. Girardi M. Edelson R. (2002) Transimmunization, a novel approach for tumor immunotherapy. Transfus Apher Sci 26: 205–216.
5. Biagi E. Di Biaso I. Leoni V. Gaipa G. Rossi V. Bugarin C. et al. (2007) Extracorporeal photochemotherapy is accompanied by increasing levels of circulating CD4+CD25+GITR+Foxp3+CD62L+ functional regulatory T-cells in patients with graft-versus-host disease. Transplantation 84: 31–39.
6. Bladon J. Taylor P. (2006) Extracorporeal photopheresis: a focus on apoptosis and cytokines.J Dermatol Sci 43 (2): 85–94.
7. Brunstein C. Miller J. Cao Q. McKenna D. Hippen K. Curtsinger J. et al. (2011) Infusion of ex vivo expanded T regulatory cells in adults transplanted with umbilical cord blood: safety profile and detection kinetics. Blood 117: 1061–1070.
8. Carlens S. Ringden O. Remberger M. Lonnqvist B. Hagglund H. Klaesson S. et al. (1998) Risk factors for chronic graft-versus-host disease after bone marrow transplantation: a retrospective single centre analysis. Bone Marrow Transplant 22: 755–761.
9. Chen X. Vodanovic-Jankovic S. Johnson B. Keller M. Komorowski R. Drobyski W. (2007) Absence of regulatory T-cell control of TH 1 and TH 17 cells is responsible for the autoimmune-mediated pathology in chronic graft-versus-host disease. Blood 110: 3804–3813.
10. Child F. Ratnavel R. Watkins P. Samson D. Apperley J. Ball J. et al. (1999) Extracorporeal photopheresis (ECP) in the treatment of chronic graft-versus-host disease (GVHD). Bone Marrow Transplant 23: 881–887.
11. Chu Y. Gress R. (2008) Murine models of chronic graft-versus-host disease: insights and unresolved issues. Biol Blood Marrow Transplant 14: 365–378.
12. Cimino G. Gamper H. Isaacs S. Hearst J. (1985) Psoralens as photoactive probes of nucleic acid structure and function: organic chemistry, photochemistry, and biochemistry. Annu Rev Biochem 54: 1151–1193.
13. Clark F. Gregg R. Piper K. Dunnion D. Freeman L. Griffiths M. et al. (2004) Chronic graft-versus-host disease is associated with increased numbers of peripheral blood CD4+CD25high regulatory T cells. Blood 103: 2410–2416.
14. Cloud T. Hakim R. Griffin A. (1961) Photosensitization of the eye with methoxsalen. Arch Ophthalmol 66: 689–694.
15. Couriel D. Hosing C. Saliba R. Shpall E. Anderlini P. Rhodes B. et al. (2006) Extracorporeal photochemotherapy for the treatment of steroid-resistant chronic GVHD. Blood 107: 3074–3080.
16. Di Ianni M. Falzetti F. Carotti A. Terenzi A. Castellino F. Bonifacio E. et al. (2011) Tregs prevent GVHD and promote immune reconstitution in HLA-haploidentical transplantation. Blood 117: 3921–3928.
17. Dignan F. Greenblatt D. Cox M. Cavenagh J. Oakervee H. Apperley J. et al. (2012) Efficacy of bimonthly extracorporeal photopheresis in refractory chronic mucocutaneous GVHD. Bone Marrow Transplant 47: 824–830.
18. Edelson R. Berger C. Gasparro F. Jegasothy B. Heald P. Wintroub B. et al. (1987) Treatment of cutaneous T-cell lymphoma by extracorporeal photochemotherapy. Preliminary results. N Engl J Med 316: 297–303.
19. Ehrenstein M. Evans J. Singh A. Moore S. Warnes G. Isenberg D. et al. (2004) Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFalpha therapy. J Exp Med 200: 277–285.
20. Ferrara J. Reddy P. (2006) Pathophysiology of graft-versus-host disease. Semin Hematol 43: 3–10.
21. Filipovich A. Weisdorf D. Pavletic S. Socie G. Wingard J. Lee S. et al. (2005) National Institutes of Health consensus development project on criteria for clinical trials in chronic graft-versus-host disease: I. Diagnosis and staging working group report. Biol Blood Marrow Transplant 11: 945–956.
22. Fimiani M. Di Renzo M. Rubegni P. (2004) Mechanism of action of extracorporeal photochemotherapy in chronic graft-versus-host disease. Br J Dermatol 150: 1055–1060.
23. Flowers M. Apperley J. van Besien K. Elmaagacli A. Grigg A. Reddy V. et al. (2008) A multicenter prospective phase 2 randomized study of extracorporeal photopheresis for treatment of chronic graft-versus-host disease. Blood 112: 2667–2674.
24. Flowers M. Inamoto Y. Carpenter P. Lee S. Kiem H. Petersdorf E. et al. (2011) Comparative analysis of risk factors for acute graft-versus-host disease and for chronic graft-versus-host disease according to National Institutes of Health consensus criteria. Blood 117: 3214–3219.
25. Foss F. DiVenuti G. Chin K. Sprague K. Grodman H. Klein A. et al. (2005) Prospective study of extracorporeal photopheresis in steroid-refractory or steroid-resistant extensive chronic graft-versus-host disease: analysis of response and survival incorporating prognostic factors. Bone Marrow Transplant 35: 1187–1193.
26. Foss F. Gorgun G. Miller K. (2002) Extracorporeal photopheresis in chronic graft-versus-host disease. Bone Marrow Transplant 29: 719–725.
27. Fukushi N. Arase H. Wang B. Ogasawara K. Gotohda T. Good R. et al. (1990) Thymus: a direct target tissue in graft-versus-host reaction after allogeneic bone marrow transplantation that results in abrogation of induction of self-tolerance. Proc Natl Acad Sci U S A 87: 6301–6305.
28. Gasparro F. Dall'Amico R. Goldminz D. Simmons E. Weingold D. (1989) Molecular aspects of extracorporeal photochemotherapy. Yale J Biol Med 62: 579–593.
29. Gatza E. Rogers C. Clouthier S. Lowler K. Tawara I. Liu C. et al. (2008) Extracorporeal photopheresis reverses experimental graft-versus-host disease through regulatory T cells. Blood 112: 1515–1521.
30. George J. Gooden C. Guo L. Kirklin J. (2008) Role for CD4(+)CD25(+) T cells in inhibition of graft rejection by extracorporeal photopheresis.J Heart Lung Transplant 27: 616–622.
31. Giorgini A. Noble A. (2007) Blockade of chronic graft-versus-host disease by alloantigen-induced CD4+CD25+Foxp3+ regulatory T cells in nonlymphopenic hosts. J Leukoc Biol 82: 1053–1061.
32. Greinix H. Knobler R. Worel N. Schneider B. Schneeberger A. Hoecker P. et al. (2006) The effect of intensified extracorporeal photochemotherapy on long-term survival in patients with severe acute graft-versus-host disease. Haematologica 91: 405–408.
33. Greinix H. van Besien K. Elmaagacli A. Hillen U. Grigg A. Knobler R. et al. (2011) Progressive improvement in cutaneous and extracutaneous chronic graft-versus-host disease after a 24-week course of extracorporeal photopheresis - results of a crossover randomized study. Biol Blood Marrow Transplant 17: 1775–1782.
34. Greinix H. Volc-Platzer B. Kalhs P. Fischer G. Rosenmayr A. Keil F. et al. (2000) Extracorporeal photochemotherapy in the treatment of severe steroid-refractory acute graft-versus-host disease: a pilot study. Blood 96: 2426–2431.
35. Greinix H. Volc-Platzer B. Rabitsch W. Gmeinhart B. Guevara-Pineda C. Kalhs P. et al. (1998) Successful use of extracorporeal photochemotherapy in the treatment of severe acute and chronic graft-versus-host disease. Blood 92: 3098–3104.
36. Hahn T. McCarthy P. Jr Zhang M. Wang D. Arora M. Frangoul H. et al. (2008) Risk factors for acute graft-versus-host disease after human leukocyte antigen-identical sibling transplants for adults with leukemia. J Clin Oncol 26: 5728–5734.
37. Hess A. Horwitz L. Beschorner W. Santos G. (1985) Development of graft-versus-host disease-like syndrome in cyclosporine-treated rats after syngeneic bone marrow transplantation. I. Development of cytotoxic T lymphocytes with apparent polyclonal anti-Ia specificity, including autoreactivity. J Exp Med 161: 718–730.
38. Hess A. Thoburn C. Bright E. Horwitz L. (1997) Specificity of effector mechanisms in syngeneic graft-vs-host disease: recognition of the MHC class II invariant chain peptide (CLIP). Transplant Proc 29: 725–727.
39. Hings I. Severson R. Filipovich A. Blazar B. Kersey J. Ramsay N. et al. (1994) Treatment of moderate and severe acute GVHD after allogeneic bone marrow transplantation. Transplantation 58: 437–442.
40. Hoffmann P. Ermann J. Edinger M. Fathman C. Strober S. (2002) Donor-type CD4(+)CD25(+) regulatory T cells suppress lethal acute graft-versus-host disease after allogeneic bone marrow transplantation. J Exp Med 196: 389–399.
41. Hollander G. Widmer B. Burakoff S. (1994) Loss of normal thymic repertoire selection and persistence of autoreactive T cells in graft vs host disease. J Immunol 152: 1609–1617.
42. Huang F. Platt N. Wykes M. Major J. Powell T. Jenkins C. et al. (2000) A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J Exp Med 191: 435–444.
43. Inamoto Y. Martin P. Chai X. Jagasia M. Palmer J. Pidala J. et al. (2012) Clinical benefit of response in chronic graft-versus-host disease. Biol Blood Marrow Transplant 18: 1517–1524.
44. Jansen C. Wilen G. Ylitalo P. Malmiharju T. (1983) Inter- and intraindividual variations in serum methoxsalen levels during repeated oral exposure. Curr Ther Res 33: 258–264.
45. Knobler R. Barr M. Couriel D. Ferrara J. French L. Jaksch P. et al. (2009) Extracorporeal photopheresis: past, present, and future. J Am Acad Dermatol 61: 652–665.
46. Knobler R. French L. Kim Y. Bisaccia E. Graninger W. Nahavandi H. et al. (2006) A randomized, double-blind, placebo-controlled trial of photopheresis in systemic sclerosis. J Am Acad Dermatol 54: 793–799.
47. Knobler R. Graninger W. Lindmaier A. Trautinger F. Smolen J. (1992) Extracorporeal photochemotherapy for the treatment of systemic lupus erythematosus. A pilot study. Arthritis Rheum 35: 319–324.
48. Lee S. Kim H. Ho V. Cutler C. Alyea E. Soiffer R. et al. (2006) Quality of life associated with acute and chronic graft-versus-host disease. Bone Marrow Transplant 38: 305–310.
49. Lee S. Vogelsang G. Flowers M. (2003) Chronic graft-versus-host disease. Biol Blood Marrow Transplant 9: 215–233.
50. Lim H. Edelson R. (1995) Photopheresis for the treatment of cutaneous T-cell lymphoma. Hematol Oncol Clin North Am 9: 1117–1126.
51. Ludvigsson J. Samuelsson U. Ernerudh J. Johansson C. Stenhammar L. Berlin G. (2001) Photopheresis at onset of type 1 diabetes: a randomised, double blind, placebo controlled trial. Arch Dis Child 85: 149–154.
52. MacMillan M. Weisdorf D. Wagner J. de For T. Burns L. Ramsay N. et al. (2002) Response of 443 patients to steroids as primary therapy for acute graft-versus-host disease: comparison of grading systems. Biol Blood Marrow Transplant 8: 387–394.
53. Malawista S. Trock D. Edelson R. (1991) Treatment of rheumatoid arthritis by extracorporeal photochemotherapy. A pilot study. Arthritis Rheum 34: 646–654.
54. Marks D. Rockman S. Oziemski M. Fox R. (1990) Mechanisms of lymphocytotoxicity induced by extracorporeal photochemotherapy for cutaneous T cell lymphoma. J Clin Invest 86: 2080–2085.
55. Martin P. Weisdorf D. Przepiorka D. Hirschfeld S. Farrell A. Rizzo J. et al. (2006) National Institutes of Health Consensus Development Project on Criteria for Clinical Trials in Chronic Graft-versus-Host Disease: VI. Design of Clinical Trials Working Group report. Biol Blood Marrow Transplant 12: 491–505.
56. Mathur K. Morris S. Deighan C. Green R. Douglas K. (2008) Extracorporeal photopheresis improves nephrogenic fibrosing dermopathy / nephrogenic systemic fibrosis: three case reports and review of literature. J Clin Apher 23: 144–150.
57. McLeod B. Sniecinski I. Ciavarella D. Owen H. Price T. Randels M. et al. (1999) Frequency of immediate adverse effects associated with therapeutic apheresis. Transfusion 39: 282–288.
58. Messina C. Locatelli F. Lanino E. Uderzo C. Zacchello G. Cesaro S. et al. (2003) Extracorporeal photochemotherapy for paediatric patients with graft-versus-host disease after haematopoietic stem cell transplantation. Br J Haematol 122: 118–127.
59. Miyara M. Amoura Z. Parizot C. Badoual C. Dorgham K. Trad S. et al. (2005) Global natural regulatory T cell depletion in active systemic lupus erythematosus. J Immunol 175: 8392–8400.
60. Morelli A. Larregina A. Shufesky W. Zahorchak A. Logar A. Papworth G. et al. (2003) Internalization of circulating apoptotic cells by splenic marginal zone dendritic cells: dependence on complement receptors and effect on cytokine production. Blood 101: 611–620.
61. Mutis T. van Rijn R. Simonetti E. Aarts-Riemens T. Emmelot M. van Bloois L. et al. (2006) Human regulatory T cells control xenogeneic graft-versus-host disease induced by autologous T cells in RAG2-/-gammac-/- immunodeficient mice. Clin Cancer Res 12: 5520–5525.
62. Owsianowski M. Gollnick H. Siegert W. Schwerdtfeger R. Orfanos C. (1994) Successful treatment of chronic graft-versus-host disease with extracorporeal photopheresis. Bone Marrow Transplant 14: 845–848.
63. Pavletic S. Martin P. Lee S. Mitchell S. Jacobsohn D. Cowen E. et al. (2006) Measuring therapeutic response in chronic graft-versus-host disease: National Institutes of Health Consensus Development Project on Criteria for Clinical Trials in Chronic Graft-versus-Host Disease: IV. Response Criteria Working Group report. Biol Blood Marrow Transplant 12: 252–266.
64. Perfetti P. Carlier P. Strada P. Gualandi F. Occhini D. van Lint M. et al. (2008) Extracorporeal photopheresis for the treatment of steroid refractory acute GVHD. Bone Marrow Transplant 42: 609–617.
65. Perotti C. Del Fante C. Tinelli C. Viarengo G. Scudeller L. Zecca M. et al. (2010) Extracorporeal photochemotherapy in graft-versus-host disease: a longitudinal study on factors influencing the response and survival in pediatric patients. Transfusion 50: 1359–1369.
66. Przepiorka D. Weisdorf D. Martin P. Klingemann H. Beatty P. Hows J. et al. (1995) 1994 Consensus Conference on Acute GVHD Grading. Bone Marrow Transplant 15: 825–828.
67. Quaranta S. Shulman H. Ahmed A. Shoenfeld Y. Peter J. McDonald G. et al. (1999) Autoantibodies in human chronic graft-versus-host disease after hematopoietic cell transplantation. Clin Immunol 91: 106–116.
68. Radenhausen M. Michelsen S. Plewig G. Bechara F. Altmeyer P. Hoffmann K. (2004) Bicentre experience in the treatment of severe generalised atopic dermatitis with extracorporeal photochemotherapy. J Dermatol 31: 961–970.
69. Rieger K. Loddenkemper C. Maul J. Fietz T. Wolff D. Terpe H. et al. (2006) Mucosal FOXP3+ regulatory T cells are numerically deficient in acute and chronic GvHD. Blood 107: 1717–1723.
70. Rook A. Heald P. Nahass G. Macey W. Witmer W. Lazarus G. et al. (1989) Treatment of autoimmune disease with extracorporeal photochemotherapy: pemphigus vulgaris - preliminary report. Yale J Biol Med 62: 647–652.
71. Rubegni P. Cuccia A. Sbano P. Cevenini G. Carcagni M. D'Ascenzo G. et al. (2005) Role of extracorporeal photochemotherapy in patients with refractory chronic graft-versus-host disease. Br J Haematol 130: 271–275.
72. Sakoda Y. Hashimoto D. Asakura S. Takeuchi K. Harada M. Tanimoto M. et al. (2007) Donor-derived thymic-dependent T cells cause chronic graft-versus-host disease. Blood 109: 1756–1764.
73. Salvaneschi L. Perotti C. Zecca M. Bernuzzi S. Viarengo G. Giorgiani G. et al. (2001) Extracorporeal photochemotherapy for treatment of acute and chronic GVHD in childhood. Transfusion 41: 1299–1305.
74. Seaton E. Szydlo R. Kanfer E. Apperley J. Russell-Jones R. (2003) Influence of extracorporeal photopheresis on clinical and laboratory parameters in chronic graft-versus-host disease and analysis of predictors of response. Blood 102: 1217–1223.
75. Shimada M. Onizuka M. Machida S. Suzuki R. Kojima M. Miyamura K. et al. (2007) Association of autoimmune disease-related gene polymorphisms with chronic graft-versus-host disease. Br J Haematol 139: 458–463.
76. Shulman H. Kleiner D. Lee S. Morton T. Pavletic S. Farmer E. et al. (2006) Histopathologic diagnosis of chronic graft-versus-host disease: National Institutes of Health Consensus Development Project on Criteria for Clinical Trials in Chronic Graft-versus-Host Disease: II. Pathology Working Group Report. Biol Blood Marrow Transplant 12: 31–47.
77. Smith E. Sniecinski I. Dagis A. Parker P. Snyder D. Stein A. et al. (1998) Extracorporeal photochemotherapy for treatment of drug-resistant graft-versus-host disease. Biol Blood Marrow Transplant 4: 27–37.
78. Sniecinski I. Parker P. Dagis A. Collier T. Wang S. Richard K. et al. (1998) Extracorporeal photopheresis is effective treatment for chronic refractory graft-versus-host disease. In: American Society of Hematology, 40th Annual Meeting, Miami Beach, FL, December 4–8, 1998.
79. Steinman R. Turley S. Mellman I. Inaba K. (2000) The induction of tolerance by dendritic cells that have captured apoptotic cells. J Exp Med 191: 411–416.
80. Teshima T. Reddy P. Liu C. Williams D. Cooke K. Ferrara J. (2003) Impaired thymic negative selection causes autoimmune graft-versus-host disease. Blood 102: 429–435.
81. Therakos (2001) Photopheresis. Available from: http://www.therakos.com/healthcare-professionals (accessed 15 May 2012).
82. Toubai T. Sun Y. Reddy P. (2008) GVHD pathophysiology: is acute different from chronic? Best Pract Res Clin Haematol 21: 101–117.
83. Tsirigotis P. Kaloyannidis P. Papalexandri A. Baltadakis I. Karakasis D. Batsis I. et al. (2012) Extracorporeal photopheresis in the treatment of chronic graft-versus-host disease. The Hellenic experience: a study by the Hellenic association of hematology. Transfus Apher Sci 46: 173–180.
84. Vowels B. Cassin M. Boufal M. Walsh L. Rook A. (1992) Extracorporeal photochemotherapy induces the production of tumor necrosis factor-alpha by monocytes: implications for the treatment of cutaneous T-cell lymphoma and systemic sclerosis. J Invest Dermatol 98: 686–692.
85. Weisdorf D. Haake R. Blazar B. Miller W. McGlave P. Ramsay N. et al. (1990) Treatment of moderate / severe acute graft-versus-host disease after allogeneic bone marrow transplantation: an analysis of clinical risk features and outcome. Blood 75: 1024–1030.
86. Zhao D. Zhang C. Yi T. Lin C. Todorov I. Kandeel F. et al. (2008) In vivo-activated CD103+CD4+ regulatory T cells ameliorate ongoing chronic graft-versus-host disease. Blood 112: 2129–2138.
87. Zic J. (2003) The treatment of cutaneous T-cell lymphoma with photopheresis. Dermatol Ther 16: 337–346.
88. Zic J. Miller J. Stricklin G. King L. Jr (1999) The North American experience with photopheresis. Ther Apher 3: 50–62.
89. Zorn E. Kim H. Lee S. Floyd B. Litsa D. Arumugarajah S. et al. (2005) Reduced frequency of FOXP3+ CD4+CD25+ regulatory T cells in patients with chronic graft-versus-host disease. Blood 106: 2903–2911.