Whole-eye transplantation: a look into the past and vision for the future (original) (raw)

Eye volume 31, pages 179–184 (2017) Cite this article

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Abstract

Blindness afflicts ~39 million people worldwide. Retinal ganglion cells are unable to regenerate, making this condition irreversible in many cases. Whole-eye transplantation (WET) provides the opportunity to replace diseased retinal ganglion cells, as well as the entire optical system and surrounding facial tissue, if necessary. Recent success in face transplantation demonstrates that this may be a promising treatment for what has been to this time an incurable condition. An animal model for WET must be established to further enhance our knowledge of nerve regeneration, immunosuppression, and technical aspects of surgery. A systematic review of the literature was performed to evaluate studies describing animal models for WET. Only articles in which the eye was completely enucleated and reimplanted were included. Study methods and results were compared. In the majority of published literature, WET can result in recovery of vision in cold-blooded vertebrates. There are a few instances in which mammalian WET models demonstrate survival of the transplanted tissue following neurovascular anastomosis and the ability to maintain brief electroretinogram activity in the new host. In this study we review in cold-blooded vertebrates and mammalian animal models for WET and discuss prospects for future research for translation to human eye transplantation.

References

  1. WHO. Global Data on Visual Impairment. Available at: http://www.who.int/blindness/publications/globaldata/en/ (accessed on 2 October 2014).
  2. Ellenberg D, Shi J, Jain S, Chang JH, Brady S, Melhem E et al. Impediments to eye transplantation: ocular viability following optic nerve transection or enucleation. Br J Ophthalmol 2009; 93: 1134–1140.
    Article CAS Google Scholar
  3. Scientists urged to hold firm to eye transplant goal. JAMA 1978; 240 (12) 1227.
  4. Carty MJ, Bueno EM, Soleymani Lehmann L, Pomahac B . A position paper in support of face transplantation in the blind. Plast Reconstr Surg 2012; 130: 319–324.
    Article CAS Google Scholar
  5. Stone LS . Heteroplastic transplantation of the eyes between the larvae of two species of Amblystoma. J Exp Zool 1930; 55: 193–261.
    Article Google Scholar
  6. Stone LS, Cole HS . Grafted eyes of young and old adult salamanders (amblystoma punctatum showing return of vision. Yale J Biol Med 1943; 15: 735–755.
    CAS PubMed PubMed Central Google Scholar
  7. Stone L, Ussher N, Beers D . Reimplantation and transplantation of larval eyes into the salamander Amblystoma punctum. J Exp Zool 1937; 77: 13–47.
    Article Google Scholar
  8. Stone L, Zaur L . Reimplantation and transplantation of adult eyes in the salamander (triturus viridescens with return of vision. J Exp Zool 1940; 85: 243–269.
    Article Google Scholar
  9. Stone L, Ellison F . Return of vision in eyes exchanged between adult salamanders of different species. J Exp Zool 1945; 100: 217–227.
    Article CAS Google Scholar
  10. Stone LS . Return of vision in larval eyes exchanged between Amblystoma punctatum and the cave salamander, Typhlotriton spelaeus. Investig Ophthalmol 1964; 3 (6): 555–565.
    CAS Google Scholar
  11. Stone LS . Return of vision in transplanted larval eyes of cave salamanders. J Exp Zool 1964; 156: 219–227.
    Article CAS Google Scholar
  12. Pietsch P, Schneider C . Transplanted eyes of foreign donors can reinstate the optically activated skin camouflage reactions in bilaterally enucleated salamanders (Ambystoma). Brain Behav Evol 1988; 32 (6): 364–370.
    Article CAS Google Scholar
  13. Koppányi T, Baker C . Further studies on eye transplantation in the spotted rat. Am J Physiol 2014; 71: 344–348.
    Article Google Scholar
  14. Sperry R . Restoration of vision after crossing of optic nerves and after contralateral transplantation of eye. J Neurophysiol 1945; 8: 15–28.
    Article Google Scholar
  15. Sedohara A, Komazaki S, Asashima M . In vitro induction and transplantation of eye during early Xenopus development. Dev Growth Differ 2003; 45 (5-6): 463–471.
    Article Google Scholar
  16. Blackiston DJ, Levin M . Ectopic eyes outside the head in Xenopus tadpoles provide sensory data for light-mediated learning. J Exp Biol 2013; 216 (Pt 6): 1031–1040.
    Article Google Scholar
  17. May C . Enucleation with transplantation and reimplantation of eyes. Med Rec 1886; 29 (22): 613–621.
    Google Scholar
  18. Freed W, Wyatt RJ . Transplantation of eyes to the adult rat brain: histological findings and light-evoked potential response. Life Sci 1980; 27 (6): 503–510.
    Article CAS Google Scholar
  19. Sher H, Cohen RJ . Revascularization of isolated extracorporeal canine eyes by direct microsurgical anastomosis. J Microsurg 1981; 1 (5): 399–402.
    Article Google Scholar
  20. Sher H . Revascularization of autotransplanted ovine eyes by microsurgical anastomosis. J Microsurg 1981; 2 (4): 269–272.
    Article CAS Google Scholar
  21. Shi J, Ellenberg D, Kim JY, Qian H, Ripps H, Jain S et al. Restoration of electroretinogram activity in exenterated swine eyes following ophthalmic artery anastomosis. Restor Neurol Neurosci 2009; 27 (4): 351–357.
    PubMed Google Scholar
  22. Bradford H . A case of enucleation with replacement of the human globe by that of a rabbit. Bost Med Surg J 1885; 113 (12): 269–270.
    Article Google Scholar
  23. O’Brian S . Science and Technology Milestones in 1969. Available at: seniorliving.about.com/od/boomernostalgia/tp/1969-milestones-science.htm (accessed on 3 September 2016).
  24. Washington KM, Solari MG, Sacks JM, Horibe EK, Unadkat JV, Carvell GE et al. A model for functional recovery and cortical reintegration after hemifacial composite tissue allotransplantation. Plast Reconstr Surg 2009; 123 (2 Suppl): 26S–33S.
    Article CAS Google Scholar
  25. Morrison JC, Johnson EC, Cepurna WO, Funk RHW . Microvasculature of the rat optic nerve head. Invest Ophthalmol Vis Sci 1999; 40 (8): 1702–1709.
    CAS PubMed Google Scholar
  26. National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals. Guide for the Care and Use of Laboratory Animals. National Academies Press (US): Washington (DC), 2011.
  27. Chiaki K, Bo W, Maxine RM, Hongkun W, Yolandi van der M, Leon CH et al. Evaluation of viability, structural integrity and functional outcome after whole eye transplantation. Plastic Reconstr Surg 2015; 135: 82.
    Google Scholar
  28. Keeler C . The functional capacity of transplanted adult frog eyes. J Exp Zool 1929; 54 (3): 461–472.
    Article Google Scholar

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Author notes

  1. D Bourne and Y Li: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Plastic Surgery, University of Pittsburgh Medical Center, Pittsburgh, PA, USA
    D Bourne, Y Li, C Komatsu, M R Miller, E H Davidson, L He, I A Rosner, H Tang, W Chen, M G Solari & K M Washington
  2. Department of Plastic and Reconstructive Surgery, XiJing Hospital, Fourth Military Medical University, Xi’an, China
    Y Li & L He
  3. Department of Ophthalmology, Eye and Ear Institute, Ophthalmology and Visual Science Research Center, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
    M R Miller
  4. Department of Emergency, The First Affiliated Hospital of GuangXi Medical University, Nanning, GuangXi, China
    H Tang
  5. Department of Ophthalmology, New York University School of Medicine, New York, USA
    J S Schuman
  6. Veterans Administration Pittsburgh Healthcare System, Pittsburgh, PA, USA
    K M Washington

Authors

  1. D Bourne
  2. Y Li
  3. C Komatsu
  4. M R Miller
  5. E H Davidson
  6. L He
  7. I A Rosner
  8. H Tang
  9. W Chen
  10. M G Solari
  11. J S Schuman
  12. K M Washington

Corresponding author

Correspondence toK M Washington.

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The authors declare no conflict of interest.

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Bourne, D., Li, Y., Komatsu, C. et al. Whole-eye transplantation: a look into the past and vision for the future.Eye 31, 179–184 (2017). https://doi.org/10.1038/eye.2016.272

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