A critical analysis of rejection in vascularized composite allotransplantation: Clinical, cellular and molecular aspects, current challenges, and novel concepts

Frontiers in Immunology

Volumn 4, Issue NOV, 2013, Pages

  Sarhane, Karim A ^a   Tuffaha, Sami H ^a   Broyles, Justin M ^a   Ibrahim, Amir E ^b   Khalifian, Saami ^a   Baltodano, Pablo ^a   Santiago, Gabriel F ^c   Alrakan, Mohammed ^a   Ibrahim, Zuhaib ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

^c WALTER REED ARMY MEDICAL CENTER   (United States)

Author keywords

Banff classification; Hand face transplantation; Reconstructive transplantation; Transplant rejection; vascularized composite allotransplantation

Indexed keywords

EID: 84890350335     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00406     Document Type: Article

References (61)

1. Breidenbach WC. Hand transplantation. Med J Aust (2013) 199(4):228-9. doi: 10.5694/mja13.10637
2. Devauchelle B, Badet L, Lengelé B, Morelon E, Testelin S, Michallet M, et al. First human face allograft: early report. Lancet (2006) 368(9531):203-9. doi:10.1016/S0140-6736(06)68935-6
3. Gilbert R. Hand transplanted from cadaver is reamputated. Med Trib Med News (1964) 5:23-5.
4. Petruzzo P, Dubernard JM. The International Registry on Hand and Composite Tissue Allotransplantation. Clin Transpl (2011) 247-53.
5. Cendales LC, Kanitakis J, Schneeberger S, Burns C, Ruiz P, Landin L, et al. The Banff 2007 working classification of skin-containing composite tissue allograft pathology. Am J Transplant (2008) 8(7):1396-400. doi:10.1111/j.1600-6143.2008.02243.x
6. Dvorak HF, Mihm MC, Dvorak AM, Barnes BA, Galli SJ. The microvasculature is the critical target of the immune response in vascularized skin allograft rejection. J Invest Dermatol (1980) 74(5):280-4. doi:10.1111/1523-1747.ep12543418
7. Bhan AK, Mihm MC, Dvorak HF. T cell subsets in allograft rejection. In situ characterization of T cell subsets in human skin allografts by the use of monoclonal antibodies. J Immunol (1982) 129(4):1578-83.
8. Sarhane KA, Ibrahim Z, Leto Barone AA, Cooney DS, Lee WPA, Brandacher G. Minimization of immunosuppression and tolerance induction in reconstructive transplantation. Curr Surg Rep (2012) 1(1):40-6. doi:10.1007/s40137-012-0008-4
9. Lee WP, Yaremchuk MJ, Pan YC, Randolph MA, Tan CM, Weiland AJ. Relative antigenicity of components of a vascularized limb allograft. Plast Reconstr Surg (1991) 87(3):401-11. doi:10.1097/00006534-199103000-00001
10. Schneeberger S, Kreczy A, Brandacher G, Steurer W, Margreiter R. Steroid-and ATG-resistant rejection after double forearm transplantation responds to Campath-1H. Am J Transplant (2004) 4(8):1372-4. doi:10.1111/j.1600-6143.2004.00518.x
11. Schneeberger S, Zelger B, Ninkovic M, Margreiter R. Transplantation of the hand. Transplant Rev (2005) 19(2):100-7. doi:10.1016/j.trre.2005.07.001
12. Schuind F, Abramowicz D, Schneeberger S. Hand transplantation: the state-of-the-art. J Hand Surg Am (2007) 32(1):2-17. doi:10.1016/j.jhsb.2006.09.008
13. Kanitakis J, Badet L, Petruzzo P, Béziat JL, Morelon E, Lefrançois N, et al. Clinicopathologic monitoring of the skin and oral mucosa of the first human face allograft: Report on the first eight months. Transplantation (2006) 82(12):1610-5. doi:10.1097/01.tp.0000248780.55263.33
14. Hautz T, Zelger B, Grahammer J, Krapf C, Amberger A, Brandacher G, et al. Molecular markers and targeted therapy of skin rejection in composite tissue allotransplantation. Am J Transplant (2010) 10(5):1200-9. doi:10.1111/j.1600-6143.2010.03075.x
15. Sucher R, Fischler K, Oberhuber R, Kronberger I, Margreiter C, Ollinger R, et al. IDO and regulatory T cell support are critical for cytotoxic T lymphocyte-associated Ag-4 Ig-mediated long-term solid organ allograft survival. J Immunol (2012) 188(1):37-46. doi:10.4049/jimmunol.1002777
16. Schneeberger S, Gorantla VS, Hautz T, Pulikkottil B, Margreiter R, Lee WP. Immunosuppression and rejection in human hand transplantation. Transplant Proc (2009) 41(2):472-5. doi:10.1016/j.transproceed.2009.01.019
17. Schneeberger S, Gorantla VS, van Riet RP, Lanzetta M, Vereecken P, van Holder C, et al. Atypical acute rejection after hand transplantation. Am J Transplant (2008) 8(3):688-96. doi:10.1111/j.1600-6143.2007.02105.x
18. Pomahac B, Pribaz J, Eriksson E, Annino D, Caterson S, Sampson C, et al. Restoration of facial form and function after severe disfigurement from burn injury by a composite facial allograft. Am J Transplant (2011) 11(2):386-93. doi:10.1111/j.1600-6143.2010.03368.x
19. Lengelé BG. Current concepts and future challenges in facial transplantation. Clin Plast Surg (2009) 36(3):507-21. doi:10.1016/j.cps.2009.02.006
20. Siemionow M, Ozturk C. Face transplantation: outcomes, concerns, controversies, and future directions. J Craniofac Surg (2012) 23(1):254-9. doi:10.1097/SCS.0b013e318241b920
21. Kanitakis J. The challenge of dermatopathological diagnosis of composite tissue allograft rejection: a review. J Cutan Pathol (2008) 35(8):738-44. doi:10.1111/j.1600-0560.2007.00889.x
22. Kanitakis J, Petruzzo P, Jullien D, Badet L, Dezza MC, Claudy A, et al. Pathological score for the evaluation of allograft rejection in human hand (composite tissue) allotransplantation. Eur J Dermatol (2005) 15(4):235-8. doi:10.1097/00007890-200407271-00141
23. Siemionow M, Papay F, Alam D, Bernard S, Djohan R, Gordon C, et al. Near-total human face transplantation for a severely disfigured patient in the USA. Lancet (2009) 374(9685):203-9. doi:10.1016/S0140-6736(09)61155-7
24. Lantieri L, Meningaud J-P, Grimbert P, Bellivier F, Lefaucheur J-P, Ortonne N, et al. Repair of the lower and middle parts of the face by composite tissue allotransplantation in a patient with massive plexiform neurofibroma: a 1-year follow-up study. Lancet (2008) 372(9639):639-45. doi:10.1016/S0140-6736(08)61277-5
25. Kanitakis J, Jullien D, Petruzzo P, Hakim N, Claudy A, Revillard J-P, et al. Clinicopathologic features of graft rejection of the first human hand allograft. Transplantation (2003) 76(4):688-93. doi:10.1097/01.TP.0000079458.81970.9A
26. Cendales LC, Kirk AD, Moresi JM, Ruiz P, Kleiner DE. Composite tissue allotransplantation: classification of clinical acute skin rejection. Transplantation (2005) 80(12):1676-80. doi:10.1097/01.tp.0000185304.49987.d8
27. Levi DM, Tzakis AG, Kato T, Madariaga J, Mittal NK, Nery J, et al. Transplantation of the abdominal wall. Lancet (2003) 361(9376):2173-6. doi:10.1016/S0140-6736(03)13769-5
28. Kanitakis J. Skin rejection in human hand allografts: histological findings and grading system. In: Lanzetta MDJ editor. Hand Transplantation. Milan: Springer-Verlag (2007). 249 p.
29. Wood KJ, Goto R. Mechanisms of rejection: current perspectives. Transplantation (2012) 93(1):1-10. doi:10.1097/TP.0b013e31823cab44
30. Ponticelli C. The mechanisms of acute transplant rejection revisited. J Nephrol (2012) 25(2):150-8. doi:10.5301/jn.5000048
31. Ravindra K, Haeberle M, Levin LS, Ildstad ST. Immunology of vascularized composite allotransplantation: a primer for hand surgeons. J Hand Surg Am (2012) 37(4):842-50. doi:10.1016/j.jhsa.2012.01.042
32. Whitelegg A, Barber LD. The structural basis of T-cell allorecognition. Tissue Antigens (2004) 63(2):101-8. doi:10.1111/j.1399-0039.2004.00188.x
33. Safinia N, Afzali B, Atalar K, Lombardi G, Lechler RI. T-cell alloimmunity and chronic allograft dysfunction. Kidney Int Suppl (2010) 119:S2-12. doi:10.1038/ki.2010.416
34. LaRosa DF, Rahman AH, Turka LA. The innate immune system in allograft rejection and tolerance. J Immunol (2007) 178(12):7503-9.
35. Khalifian S, Broyles JM, Tuffaha SH, Alrakan M, Ibrahim Z, Sarhane KA. Immune mechanisms of ischemia-reperfusion injury in transplantation. Open J Immunol (2013) 3(3):158-64. doi:10.4236/oji.2013.33020
36. Van der Touw W, Cravedi P, Kwan W, Paz-Artal E, Merad M, Heeger PS. Cutting edge: receptors for C3a and C5a modulate stability of alloantigen-reactive induced regulatory T cells. J Immunol (2013) 190(12):5921-5. doi:10.4049/jimmunol.1300847
37. Morita K, Miura M, Paolone DR, Engeman TM, Kapoor A, Remick DG, et al. Early chemokine cascades in murine cardiac grafts regulate T cell recruitment and progression of acute allograft rejection. J Immunol (2001) 167(5):2979-84.
38. Prabhune KA, Gorantla VS, Maldonado C, Perez-Abadia G, Barker JH, Ildstad ST. Mixed allogeneic chimerism and tolerance to composite tissue allografts. Microsurgery (2000) 20(8):441-7. doi:10.1002/1098-2752(2000)20:8<441::AID-MICR16>3.0.CO;2-A
39. Mengel M, Sis B, Haas M, Colvin RB, Halloran PF, Racusen LC, et al. Banff 2011 Meeting report: new concepts in antibody-mediated rejection. Am J Transplant (2012) 12(3):563-70. doi:10.1111/j.1600-6143.2011.03926.x
40. Petruzzo P, Kanitakis J, Badet L, Pialat J-B, Boutroy S, Charpulat R, et al. Long-term follow-up in composite tissue allotransplantation: in-depth study of five (hand and face) recipients. Am J Transplant (2011) 11(4):808-16. doi:10.1111/j.1600-6143.2011.03469.x
41. Hautz T, Engelhardt TO, Weissenbacher A, Kumnig M, Zelger B, Rieger M, et al. World experience after more than a decade of clinical hand transplantation: update on the Innsbruck program. Hand Clin (2011) 27(4):423-31. doi:10.1016/j.hcl.2011.07.004
42. Petruzzo P, Lanzetta M, Dubernard J-M, Landin L, Cavadas P, Margreiter R, et al. The International Registry on Hand and Composite Tissue Transplantation. Transplantation (2010) 90(12):1590-4. doi:10.1097/TP.0b013e3181ff1472
43. Unadkat JV, Schneeberger S, Horibe EH, Goldbach C, Solari MG, Washington KM, et al. Composite tissue vasculopathy and degeneration following multiple episodes of acute rejection in reconstructive transplantation. Am J Transplant (2010) 10(2):251-61. doi:10.1111/j.1600-6143.2009.02941.x
44. Mundinger GS, Munivenkatappa R, Drachenberg CB, Ha JS, Vaca EE, Shipley ST, et al. Histopathology of chronic rejection in a nonhuman primate model of vascularized composite allotransplantation. Transplantation (2013) 95(10):1204-10. doi:10.1097/TP.0b013e31828d1528
45. Kaufman CL, Ouseph R, Blair B, Kutz JE, Tsai TM, Scheker LR, et al. Graft vasculopathy in clinical hand transplantation. Am J Transplant (2012) 12(4):1004-16. doi:10.1111/j.1600-6143.2011.03915.x
46. Marco ML. The Fischer-Lewis model of chronic allograft rejection-a summary. Nephrol Dial Transplant (2006) 21(11):3082-6. doi:10.1093/ndt/gfl451
47. White E, Hildemann WH, Mullen Y. Chronic kidney allograft reactions in rats. Transplantation (1969) 8(5):602-17. doi:10.1097/00007890-196911000-00007
48. Hautz T, Zelger B, Brandacher G, Mueller H, Grahammer J, Zelger B, et al. Histopathologic characterization of mild rejection (grade I) in skin biopsies of human hand allografts. Transplant Int (2012) 25(1):56-63. doi:10.1111/j.1432-2277.2011.01369.x
49. Kanitakis J, McGregor B, Badet L, Petruzzo P, Morelon E, Devauchelle B, et al. Absence of c4d deposition in human composite tissue (hands and face) allograft biopsies: an immunoperoxidase study. Transplantation (2007) 84(2):265-7. doi:10.1097/01.tp.0000266899.93315.52
50. Landin L, Cavadas PC, Ibañez J, Roger I, Vera-Sempere F. CD3+-mediated rejection and C4d deposition in two composite tissue (bilateral hand) allograft recipients after induction with alemtuzumab. Transplantation (2009) 87(5):776-81. doi:10.1097/TP.0b013e318198dbc7
51. Morelon E, Kanitakis J, Petruzzo P. Immunological issues in clinical composite tissue allotransplantation: where do we stand today? Transplantation (2012) 93(9):855-9. doi:10.1097/TP.0b013e31824728b8
52. Wu S, Xu H, Chen B, Wen Y, Ikusika OM, Ocker A, et al. Sensitized recipients exhibit accelerated but not hyperacute rejection of vascularized composite tissue allografts. Transplantation (2011) 92(6):627-33. doi:10.1097/TP.0b013e31822b9264
53. Sellarés J, de Freitas DG, Mengel M, Reeve J, Einecke G, Sis B, et al. Understanding the causes of kidney transplant failure: the dominant role of antibody-mediated rejection and nonadherence. Am J Transplant (2012) 12(2):388-99. doi:10.1111/j.1600-6143.2011.03840.x
54. Unadkat JV, Schneeberger S, Goldbach C, Solari MG, Washington KM, Afrooz PN, et al. Investigation of antibody-mediated rejection in composite tissue allotransplantation in a rat limb transplant model. Transplant Proc (2009) 41(2):542-5. doi:10.1016/j.transproceed.2009.01.024
55. Baldwin WM, Valujskikh A, Fairchild RL. Antibody-mediated rejection: emergence of animal models to answer clinical questions. Am J Transplant (2010) 10(5):1135-42. doi:10.1111/j.1600-6143.2010.03065.x
56. Marcussen N, Olsen TS, Benediktsson H, Racusen L, Solez K. Reproducibility of the Banff classification of renal allograft pathology. Inter-and intraobserver variation. Transplantation (1995) 60(10):1083-9.
57. Furness PN, Taub N. Interobserver reproducibility and application of the ISN/RPS classification of lupus nephritis-a UK-wide study. Am J Surg Pathol (2006) 30(8):1030-5. doi:10.1097/00000478-200608000-00015
58. Volk H-D, Sawitzki B, Reinke P. Molecular analysis of renal allograft biopsies-more than a nice toy for researchers? Am J Transplant (2013) 13(3):539-40. doi:10.1111/ajt.12081
59. Sarhane KA. Tissue CLN3: A Potential Biomarker for Breast Cancer? [MSc Thesis]. Beirut: Department of Biochemistry and Molecular Genetics, Faculty of Medicine, American University of Beirut (2012).
60. Starzl R, Brandacher G, Lee WPA, Carbonell J, Zhang W, Schnider J, et al. Review of the early diagnoses and assessment of rejection in vascularized composite allotransplantation. Clin Dev Immunol (2013) 2013:402980. doi:10.1155/2013/402980
61. Hautz T, Zelger BG, Weissenbacher A, Zelger B, Brandacher G, Landin L, et al. Standardizing skin biopsy sampling to assess rejection in vascularized composite allotransplantation. Clin Transplant (2013) 27(2):E81-90. doi:10.1111/ctr.12086