A Hyperbaric Warm Perfusion System Preserves Tissue Composites Ex vivo and Delays the Onset of Acute Rejection

Charles Anton Fries; Carole Yasay Villamaria; Jerry Richard Spencer; Shari Lawson; Lin Wang; Thomas Raj; E. George Wolf; Bijaya Kumar Parida; Vijay Saradhi Gorantla; Rory Frederick Rickard; Michael Robert Davis

doi:10.1055/s-0038-1667298

Journal of Reconstructive Microsurgery, Table of Contents

J Reconstr Microsurg 2019; 35(02): 097-107
DOI: 10.1055/s-0038-1667298

Original Article

Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

A Hyperbaric Warm Perfusion System Preserves Tissue Composites Ex vivo and Delays the Onset of Acute Rejection

Charles Anton Fries

¹Department of Reconstructive Surgery, U.S. Army Institute of Surgical Research, Fort Sam Houston, Texas, United States

²Academic Department of Military Surgery and Trauma, Royal Centre for Defence Medicine, ICT Centre, Birmingham, United Kingdom

,

Carole Yasay Villamaria

¹Department of Reconstructive Surgery, U.S. Army Institute of Surgical Research, Fort Sam Houston, Texas, United States

³Department of Surgery, University of Texas Health Science Center at San Antonio, San Antonio, Texas, United States

,

Jerry Richard Spencer

¹Department of Reconstructive Surgery, U.S. Army Institute of Surgical Research, Fort Sam Houston, Texas, United States

⁴59 MDW/Science and Technology, Joint Base San Antonio, Texas

,

Shari Lawson

¹Department of Reconstructive Surgery, U.S. Army Institute of Surgical Research, Fort Sam Houston, Texas, United States

,

Lin Wang

¹Department of Reconstructive Surgery, U.S. Army Institute of Surgical Research, Fort Sam Houston, Texas, United States

,

Thomas Raj

⁵Department of Pathology, Brooke Army Medical Center, San Antonio, Texas, United States

,

E. George Wolf

⁶Hyperbaric Oxygen Organ Preservation Systems, San Antonio, Texas

,

Bijaya Kumar Parida

¹Department of Reconstructive Surgery, U.S. Army Institute of Surgical Research, Fort Sam Houston, Texas, United States

⁴59 MDW/Science and Technology, Joint Base San Antonio, Texas

,

Vijay Saradhi Gorantla

¹Department of Reconstructive Surgery, U.S. Army Institute of Surgical Research, Fort Sam Houston, Texas, United States

,

Rory Frederick Rickard

²Academic Department of Military Surgery and Trauma, Royal Centre for Defence Medicine, ICT Centre, Birmingham, United Kingdom

,

Michael Robert Davis

¹Department of Reconstructive Surgery, U.S. Army Institute of Surgical Research, Fort Sam Houston, Texas, United States

⁴59 MDW/Science and Technology, Joint Base San Antonio, Texas

› Author Affiliations

Abstract

Background Ischemia–reperfusion injury (IRI) precipitates acute rejection of vascularized composite allografts (VCA). Hyperbaric preservation of tissues ex vivo, between harvest and revascularization, may reduce IRI and mitigate acute rejection of VCA.

Methods A porcine heterotopic musculocutaneous gracilis flap model was used. In phase 1, control autografts (n = 5) were infused with University of Wisconsin Solution (UWS) and stored at 4°C for 3 hours. Intervention autografts (n = 5) were placed in a hyperbaric oxygen organ preservation system for 5 hours and infused with hyperoxygenated UWS at 20°C and 3 atm. Grafts were replanted into the animals' necks. In phase 2, similarly treated control (n = 8) and intervention grafts (n = 8) were allotransplanted into the necks of animals separated by a typed and standardized genetic mismatch. No systemic immunosuppression was given. Systemic markers of IRI, and clinical and histopathological assessments of necrosis and rejection were performed.

Results Autotransplanted tissue composites preserved in the hyperbaric chamber showed histopathological evidence of less muscle necrosis at 3 hours (p = 0.05). Despite a longer period of ischemia, no evidence was found of a difference in systemic markers of IRI following revascularization in these groups. Allotransplanted tissues supported ex vivo within the hyperbaric perfusion device experienced acute rejection significantly later than corresponding controls.

Conclusion Hyperbaric warm perfusion preserves musculocutaneous tissue composites ex vivo for longer than standard cold preservation in this model. This translates into a delay in acute rejection of allotransplanted tissue composites.

Keywords

vascularized composite allografts - ischemia–reperfusion injury - acute rejection

Full Text

References

References
1 Shores JT, Brandacher G, Lee WP. Hand and upper extremity transplantation: an update of outcomes in the worldwide experience. Plast Reconstr Surg 2015; 135 (02) 351e-360e
2 Siemionow M, Gharb BB, Rampazzo A. Successes and lessons learned after more than a decade of upper extremity and face transplantation. Curr Opin Organ Transplant 2013; 18 (06) 633-639
3 Hollenbeck ST, Erdmann D, Levin LS. Current indications for hand and face allotransplantation. Transplant Proc 2009; 41 (02) 495-498
4 Weissenbacher A, Hautz T, Pratschke J, Schneeberger S. Vascularized composite allografts and solid organ transplants: similarities and differences. Curr Opin Organ Transplant 2013; 18 (06) 640-644
5 Giele H, Bendon C, Reddy S. , et al. Remote revascularization of abdominal wall transplants using the forearm. Am J Transplant 2014; 14 (06) 1410-1416
6 Khalil AA, Aziz FA, Hall JC. Reperfusion injury. Plast Reconstr Surg 2006; 117 (03) 1024-1033
7 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 (03) 401-411
8 Wolf EG. . Hyperbaric oxygen organ preservation system. US Patent: us 6794182; 2004
9 Boerema I, Meyne NG, Brummelkamp WK. , et al. [ Life without blood]. Ned Tijdschr Geneeskd 1960; 104: 949-954
10 Good surgical practices. Available at: http://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFRSearch.cfm?CFRPart=58&showFR=1 . Accessed September, 2012
11 National Research Council. Guide for the Care and Use of Laboratory Animals, 8th ed. Washington, DC: The National Academies Press; 2011
12 Villamaria CY, Rasmussen TE, Spencer JR, Patel S, Davis MR. Microvascular porcine model for the optimization of vascularized composite tissue transplantation. J Surg Res 2012; 178 (01) 452-459
13 Hammers DW, Matheny Jr RW, Sell C. , et al. Impairment of IGF-I expression and anabolic signaling following ischemia/reperfusion in skeletal muscle of old mice. Exp Gerontol 2011; 46 (04) 265-272
14 Zdichavsky M, Jones JW, Ustuner ET. , et al. Scoring of skin rejection in a swine composite tissue allograft model. J Surg Res 1999; 85 (01) 1-8
15 Cendales LC, Kanitakis J, Schneeberger S. , et al. The Banff 2007 Working Classification of Skin-Containing Composite Tissue Allograft Pathology. Am J Transplant 2008; 8 (07) 1396-1400
16 Villamaria CY, Fries CA, Spencer JR, Roth M, Davis MR. Hydrogen sulfide mitigates reperfusion injury in a porcine model of vascularized composite autotransplantation. Ann Plast Surg 2014; 72 (05) 594-598
17 Kirk AD. Crossing the bridge: large animal models in translational transplantation research. Immunol Rev 2003; 196: 176-196
18 Leto Barone AA, Leonard DA, Torabi R. , et al. The gracilis myocutaneous free flap in swine: an advantageous preclinical model for vascularized composite allograft transplantation research. Microsurgery 2013; 33 (01) 51-55
19 Bonastre J, Landin L, Diez J, Casado-Sanchez C, Casado-Perez C. Factors influencing acute rejection of human hand allografts: a systematic review. Ann Plast Surg 2012; 68 (06) 624-629
20 Pradka SP, Ong YS, Zhang Y. , et al. Increased signs of acute rejection with ischemic time in a rat musculocutaneous allotransplant model. Transplant Proc 2009; 41 (02) 531-536
21 Tullius SG, Reutzel-Selke A, Egermann F. , et al. Contribution of prolonged ischemia and donor age to chronic renal allograft dysfunction. J Am Soc Nephrol 2000; 11 (07) 1317-1324
22 Xiao B, Xia W, Zhang J, Liu B, Guo S. Prolonged cold ischemic time results in increased acute rejection in a rat allotransplantation model. J Surg Res 2010; 164 (02) e299-e304
23 Shimizu F, Okamoto O, Katagiri K, Fujiwara S, Wei F-C. Prolonged ischemia increases severity of rejection in skin flap allotransplantation in rats. Microsurgery 2010; 30 (02) 132-137
24 Caterson EJ, Lopez J, Medina M, Pomahac B, Tullius SG. Ischemia-reperfusion injury in vascularized composite allotransplantation. J Craniofac Surg 2013; 24 (01) 51-56
25 Halloran PF, Homik J, Goes N. , et al. The “injury response”: a concept linking nonspecific injury, acute rejection, and long-term transplant outcomes. Transplant Proc 1997; 29 (1–2): 79-81
26 Yuan X, Theruvath AJ, Ge X. , et al. Machine perfusion or cold storage in organ transplantation: indication, mechanisms, and future perspectives. Transpl Int 2010; 23 (06) 561-570
27 Bathini V, McGregor T, McAlister VC, Luke PPW, Sener A. Renal perfusion pump vs cold storage for donation after cardiac death kidneys: a systematic review. J Urol 2013; 189 (06) 2214-2220
28 Ardehali A, Esmailian F, Deng M. , et al; PROCEED II trial investigators. Ex-vivo perfusion of donor hearts for human heart transplantation (PROCEED II): a prospective, open-label, multicentre, randomised non-inferiority trial. Lancet 2015; 385 (9987): 2577-2584
29 Dhital KK, Iyer A, Connellan M. , et al. Adult heart transplantation with distant procurement and ex-vivo preservation of donor hearts after circulatory death: a case series. Lancet 2015; 385 (9987): 2585-2591
30 Constantinescu MA, Knall E, Xu X. , et al. Preservation of amputated extremities by extracorporeal blood perfusion; a feasibility study in a porcine model. J Surg Res 2011; 171 (01) 291-299
31 Salgado CJ, Jamali AA, Ortiz JA. , et al. Effects of hyperbaric oxygen on the replanted extremity subjected to prolonged warm ischaemia. J Plast Reconstr Aesthet Surg 2010; 63 (03) 532-537
32 Edwards RJ, Im MJ, Hoopes JE. Effects of hyperbaric oxygen preservation on rat limb replantation: a preliminary report. Ann Plast Surg 1991; 27 (01) 31-35
33 Lebranchu Y, Baan C, Biancone L. , et al. Pretransplant identification of acute rejection risk following kidney transplantation. Transpl Int 2014; 27 (02) 129-138
34 Shaheen MF, Shaheen FA, Attar B, Elamin K, Al Hayyan H, Al Sayyari A. Impact of recipient and donor nonimmunologic factors on the outcome of deceased donor kidney transplantation. Transplant Proc 2010; 42 (01) 273-276