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Current Ophthalmology Reports

, Volume 6, Issue 4, pp 256–265 | Cite as

Update on the Surgical Reconstruction of Ocular Surface in Eyes with Limbal Stem Cell Deficiency

  • Jesus Cabral-Macias
  • Jaime D. Martinez
  • Andrea Naranjo
  • Guillermo Amescua
Cornea (P Hamrah and T Yamaguchi, Section Editors)
  • 4 Downloads
Part of the following topical collections:
  1. Topical Collection on Cornea

Abstract

Purpose of Review

To determine indications, advantages, disadvantages, and potential complications of current surgical approaches for reconstruction of ocular surface in subjects with limbal stem cell deficiency (LSCD).

Recent Findings

Recently, autologous limbal stem cell transplant (LSCT) has demonstrated to have positive clinical outcomes for visual rehabilitation. Simple limbal epithelial transplantation (SLET) in subjects with unilateral LSCD and wet ocular surface is a clear example of this. Keratoprosthetic devices and their late modifications remain the best option for subjects with bilateral LSCD and a wet ocular surface. Modified Osteo-Odonto KPro (MOOKP) continues to be the best option for patients with LSCD and a keratinized ocular surface. Potential sources of stem cells are being elucidated, predominantly, mesenchymal stem cells (MSCs) with encouraging results in terms of tissue regeneration along with new cell carriers.

Summary

Determining which surgery should be performed is individual to each case; however, it is imperative to control acute inflammation prior to surgery in all cases and even suppress inflammation postoperatively for successful long-term outcomes. Only long-term follow-up of novel therapies will allow to establish their effectiveness. Ideal novel surgeries must aim for long-lasting corneal transparency with high reproducibility and low cost to be available worldwide.

Keywords

Cornea Limbal stem cell deficiency Ocular surface Limbal stem cell transplantation 

Notes

Compliance with Ethical Standards

Conflict of Interest

Jesus Cabral-Macias, Jaime D. Martinez, Andrea Naranjo, and Guillermo Amescua declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Supplementary material

40135_2018_187_MOESM1_ESM.jpg (53 kb)
ESM 1 A 38 year-old male with Dua stage V corneoscleral chemical burn managed with amniotic membrane transplant in both eyes during acute phase (a and b), who afterwards developed bilateral corneal conjunctivalization (c and d). (JPG 53 kb)
40135_2018_187_MOESM2_ESM.jpg (47 kb)
ESM 2 Clinical image of a 27-year-old female with severe corneoscleral chemical burn in the left eye initially managed medically and with amniotic membrane(a). After 1 month developed corneal melting (b), tectonic cornealscleral graft, plus conjunctival /Tenon’s flap was performed (c and d). (JPG 47 kb)
40135_2018_187_MOESM3_ESM.jpg (39 kb)
ESM 3 At slit lamp examination, a 39-year-old patient with bilateral limbal stem cell deficiency due to acanthamoeba keratitis with multiple previous topical antibiotics for infectious keratitis, including self-medicated anesthetic drops; history of bilateral penetrating keratoplasty failure (a and b) who underwent a keratoprothesis type 1 (Boston KPro) (c). (JPG 39 kb)
40135_2018_187_MOESM4_ESM.jpg (98 kb)
ESM 4 Slit lamp examination showing a 55-year-old female with limbal stem cell deficiency secondary to acanthamoeba keratitis (a and b) who underwent penetrating keratoplasty + simple limbal epithelial transplantation (SLET) and cataract surgery with one year follow up. (JPG 98 kb)

References

Papers of particular interest, published recently, have been highlighted as: •• Of major importance

  1. 1.
    Ksander BR, Kolovou PE, Wilson BJ, Saab KR, Guo Q, Ma J, et al. ABCB5 is a limbal stem cell gene required for corneal development and repair. Nature. 2014;511(7509):353–7.Google Scholar
  2. 2.
    Sejpal K, Bakhtiari P, Deng SX. Presentation, diagnosis and management of limbal stem cell deficiency. Middle East Afr J Ophthalmol. 2013;20:5e10.Google Scholar
  3. 3.
    Le Q, Deng SX, Xu J. In vivo confocal microscopy of congenital aniridia- associated keratopathy. Eye (Lond). 2013;27:763–6.Google Scholar
  4. 4.
    Di Iorio E, Kaye SB, Ponzin D, Barbaro V, Ferrari S, Böhm E, et al. Limbal stem cell deficiency and ocular phenotype in ectrodactyly-ectodermal dysplasia- clefting syndrome caused by p63 mutations. Ophthalmology. 2012;119:74–83.Google Scholar
  5. 5.
    Aslan D, Akata R. Dyskeratosis congenita and limbal stem cell deficiency. Exp Eye Res. 2010;90:472–3.Google Scholar
  6. 6.
    Strungaru MH, Mah D, Chan CC. Focal limbal stem cell deficiency in turner syndrome: report of two patients and review of the literature. Cornea. 2014;33:207–9.Google Scholar
  7. 7.
    Merchant A, Zhao TZ, Foster CS. Chronic keratoconjunctivitis associated with congenital dyskeratosis and erythrokeratodermia variablis. Ophthalmology. 1998;105:1286–91.Google Scholar
  8. 8.
    Eschle-Meniconi M, Ahmad S, Foster C. Mucous membrane pemphigoid: an update. Curr Opin Ophthalmol. 2005;16:303–7.Google Scholar
  9. 9.
    Catt CJ, Hamilton GM, Fish J, Mireskandari K, Ali A. Ocular manifestations of Stevens-Johnson syndrome and toxic epidermal necrolysis in children. Am J Ophthalmol. 2016;166:68–75.Google Scholar
  10. 10.
    Sivaraman KR, Jivrajka RV, Soin K, Bouchard CS, Movahedan A, Shorter E, et al. Superior limbic keratoconjunctivitis-like inflammation in patients with chronic graft-versus-host disease. Ocul Surf. 2016;14:393–400.Google Scholar
  11. 11.
    Sangwan VS, Jain V, Vemuganti GK, Murthy SI. Vernal keratoconjunctivitis with limbal stem cell deficiency. Cornea. 2011;30:491–6.Google Scholar
  12. 12.
    Lichtinger A, Pe'er J, Frucht-Pery J, Solomon A. Limbal stem cell deficiency after topical mitomycin C therapy for primary acquired melanosis with atypia. Ophthalmology. 2010;117:431–7.Google Scholar
  13. 13.
    Pires RTF, Chokshi A, Tseng SCG. Amniotic membrane transplantation or conjunctival limbal autogra for limbal stem cell de ciency induced by 5- fluorouracil in glaucoma surgeries. Cornea. 2000;19(3):284–7.Google Scholar
  14. 14.
    Rossen J, Amram A, Milani B, Park D, Harthan J, Joslin C, et al. Contact lens-induced limbal stem cell deficiency. Ocul Surf. 2016;14:419e34.Google Scholar
  15. 15.
    Gupta N, Sachdev R, Tandon R. Ocular surface squamous neoplasia in xeroderma pigmentosum: clinical spectrum and outcome. Graefes Arch Clin Exp Ophthalmol. 2011;249:1217–21.Google Scholar
  16. 16.
    Atallah MR, Palioura S, Perez VL, Amescua G. Limbal stem cell transplantation: current perspectives. Clin Ophthalmol. 2016 Apr 1;10:593–602.Google Scholar
  17. 17.
    Vazirani J, Mariappan I, Ramamurthy S, Fatima S, Basu S, Sangwan VS. Surgical management of bilateral limbal stem cell deficiency. Ocul Surf. 2016;14(3):350–64.Google Scholar
  18. 18.
    Anderson DF, Ellies P, Pires RT, Tseng SC. Amniotic membrane transplantation for partial limbal stem cell deficiency. Br J Ophthalmol. 2001;85:567–75.Google Scholar
  19. 19.
    Vazirani J, Basu S, Kenia H, Ali MH, Kacham S, Mariappan I, et al. Unilateral partial limbal stem cell deficiency: contralateral versus ipsilateral autologous cultivated limbal epithelial transplantation. Am J Ophthalmol. 2014;157:584–90.Google Scholar
  20. 20.
    Tsai RJ, Sun TT, Tseng SC. Comparison of limbal and conjunctival autograft transplantation in corneal surface reconstruction in rabbits. Ophthalmology. 1990;97:446–55.Google Scholar
  21. 21.
    Pellegrini G, Traverso CE, Franzi AT, Zingirian M, Cancedda R, De Luca M. Long-term restoration of damaged corneal surfaces with autologous cultivated corneal epithelium. Lancet. 1997;349(9057):990–3.Google Scholar
  22. 22.
    Sangwan VS, Basu S, Vemuganti GK, Sejpal K, Subramaniam SV, Bandyopadhyay S, et al. Clinical outcomes of xeno- free autologous cultivated limbal epithelial transplantation: a 10-year study. Br J Ophthalmol. 2011;95(11):1525–9.Google Scholar
  23. 23.
    Sangwan VS, Basu S, MacNeil S, Balasubramanian D. Simple limbal epithelial transplantation (SLET): a novel surgical technique for the treatment of unilateral limbal stem cell deficiency. Br J Ophthalmol. 2012;96(7):931–4.Google Scholar
  24. 24.
    Basu S, Mohamed A, Chaurasia S, Sejpal K, Vemuganti GK, Sangwan VS. Clinical outcomes of penetrating keratoplasty after autologous cultivated limbal epithelial transplantation for ocular surface burns. Am J Ophthalmol. 2011;152(6):917–24.Google Scholar
  25. 25.
    Sabater AL, Perez VL. Amniotic membrane use for management of corneal limbal stem cell deficiency. Curr Opin Ophthalmol. 2017 Jul;28(4):363–9.Google Scholar
  26. 26.
    Şapte E, Costea CF, Carauleanu A, Danca C, et al. Histological, immunohistochemical and clinical considerations on amniotic membrane transplant for ocular surface reconstruction. Romanian J Morphol Embryol. 2017;58(2):363–9.Google Scholar
  27. 27.
    Sharma N, Kaur M, Agarwal T, Sangwan VS, Vajpayee RB. Treatment of acute ocular chemical burns. Surv Ophthalmol. 2018;63:214–35.Google Scholar
  28. 28.
    Malhotra C, Jain AK. Human amniotic membrane transplantation: different modalities of its use in ophthalmology. World J Transplant. 2014;4:111–21.Google Scholar
  29. 29.
    Ma KN, Thanos A, Chodosh J, Shah AS, Mantagos IS. A novel technique for amniotic membrane transplantation in patients with acute Stevens-Johnson syndrome. Ocul Surf. 2016;14(1):31–6.Google Scholar
  30. 30.
    •• Baradaran-Rafii A, Eslani M, Haq Z, Shirzadeh E, Huvard MJ, Djalilian AR. Current and upcoming therapies for ocular surface chemical injuries. The Ocular Surface. 2017;15(1):48–64. This manuscript gives a detailed and description of the current options for different stages of injuries leading to LSCD.Google Scholar
  31. 31.
    Casas VE, Kheirkhah A, Blanco G, Tseng SC. Surgical approach for scleral ischemia and melt. Cornea. 2008;27:196–201.Google Scholar
  32. 32.
    Wang S, Tian Y, Zhu H, Cheng Y, Zheng X, Wu J. Tenonplasty combined with free oral buccal mucosa autografts for repair of sclerocorneal melt caused by chemical burns. Cornea. 2015;34:1240–4.Google Scholar
  33. 33.
    Takeda K, Nakamura T, Inatomi T, Sotozono C, Watanabe A, Kinoshita S. Ocular surface reconstruction using the combination of autologous cultivated oral mucosal epithelial transplantation and eyelid surgery for severe ocular surface disease. Am J Ophthalmol. 2011;152:195–201.Google Scholar
  34. 34.
    Eslani M, Baradaran-Rafii A, Ahmad S. Cultivated limbal and oral mucosal epithelial transplantation. Semin Ophthalmol. 2012;27(3–4):80–93.Google Scholar
  35. 35.
    Iyer G, Pillai VS, Srinivasan B, Guruswami S, Padmanabhan P. Mucous membrane grafting for lid margin keratinization in Stevens-Johnson syndrome: results. Cornea. 2010;29(2):146–51.Google Scholar
  36. 36.
    Fu Y, Liu J, Tseng SC. Oral mucosal graft to correct lid margin pathologic features in cicatricial ocular surface diseases. Am J Ophthalmol. 2011;152(4):600–8.Google Scholar
  37. 37.
    Kheirkhah A, Ghaffari R, Kaghazkanani R, Hashemi H, Behrouz MJ, Raju VK. A combined approach of amniotic membrane and oral mucosa transplantation for fornix reconstruction in severe symblepharon. Cornea. 2013;32(2):155–60.Google Scholar
  38. 38.
    Basu S, Shanbhag SS, Gokani A, Kedar R, Bahuguna C, Sangwan VS. Chronic ocular sequelae of Stevens-Johnson syndrome in children: long-term impact of appropriate therapy on natural history of disease. Am J Ophthalmol. 2018;189:17–28.Google Scholar
  39. 39.
    Wakamatsu TH, SantʼAnna AEBPP, Cristovam PC, Alves VAF, Wakamatsu A, Gomes JAP. Minor salivary gland transplantation for severe dry eyes. Cornea. 2017 Nov;36(Suppl 1):S26–33.Google Scholar
  40. 40.
    Murube J, Manyari A, ChenZhuo L, et al. Labial salivary gland transplantation in severe dry eye. Oper Tech Oculoplast Orbital Reconstr Surg. 1998;1:104–10.Google Scholar
  41. 41.
    Soares EJ, França VP. Transplantation of labial salivary glands for severe dry eye treatment. Arq Bras Oftalmol. 2005;68:481–9.Google Scholar
  42. 42.
    Marinho DR, Burmann TG, Kwitko S. Labial salivary gland transplantation for severe dry eye due to chemical burns and Stevens-Johnson syndrome. Ophthal Plast Reconstr Surg. 2010;26:182–4.Google Scholar
  43. 43.
    Sant’Anna AE, Hazarbassanov RM, de Freitas D, et al. Minor salivary glands and labial mucous membrane graft in the treatment of severe symblepharon and dry eye in patients with Stevens-Johnson syndrome. Br J Ophthalmol. 2012;96:234–9.Google Scholar
  44. 44.
    Daya SM. Conjunctival-limbal autograft. Curr Opin Ophthalmol. 2017;28:370–6.Google Scholar
  45. 45.
    Moreira PB, Magalhães RS, Pereira NC, Oliveira LA, Sousa LB. Limbal transplantation at a tertiary hospital in Brazil: a retrospective study. Arq Bras Oftalmol. 2015 Jul-Aug;78(4):207–11.Google Scholar
  46. 46.
    Basu S, Ali H, Sangwan VS. Clinical outcomes of repeat autologous cultivated limbal epithelial transplantation for ocular surface burns. Am J Ophthalmol. 2012;153(4):643–50.Google Scholar
  47. 47.
    Baylis O, Figueiredo F, Henein C, Lako M, Ahmad S. 13 years of cultured limbal epithelial cell therapy: a review of the outcomes. J Cell Biochem. 2011;112:993–1002.Google Scholar
  48. 48.
    Movahedan A, Cheung AY, Eslani M, Mogilishetty G, Govil A, Holland EJ. Long-term outcomes of ocular surface stem cell allograft transplantation. Am J Ophthalmol. 2017 Dec;184:97–107.Google Scholar
  49. 49.
    Zhao Y, Ma L. Systematic review and meta-analysis on transplantation of ex vivo cultivated limbal epithelial stem cell on amniotic membrane in limbal stem cell deficiency. Cornea. 2015;34:592–600.Google Scholar
  50. 50.
    Rama P, Matuska S, Paganoni G, Spinelli A, de Luca M, Pellegrini G. Limbal stem-cell therapy and long-term corneal regeneration. N Engl J Med. 2010;363:147–55.Google Scholar
  51. 51.
    Amescua G, Atallah M, Nikpoor N, Galor A, Perez VL. Modified simple limbal epithelial transplantation using cryopreserved amniotic membrane for unilateral limbal stem cell deficiency. Am J Ophthalmol. 2014;158(3):469–475.e2.Google Scholar
  52. 52.
    Gupta N, Joshi J, Farooqui JH, Mathur U. Results of simple limbal epithelial transplantation in unilateral ocular surface burn. Indian J Ophthalmol. 2018;66:45–52.Google Scholar
  53. 53.
    •• Basu S, Sureka SP, Shanbhag SS, Kethiri AR, Singh V, Sangwan VS. Simple limbal epithelial transplantation: long-term clinical outcomes in 125 cases of unilateral chronic ocular surface burns. Ophthalmology. 2016;123:1000–10. This study shows results over 1 year, identifying a high success rate for epithelization of ocular surface and improvement in visual acuity. Also, complications and risk factors for failure are described. Google Scholar
  54. 54.
    Jain R, Kanaujia V, Sahu S, Das S. Management of unilateral limbal stem cell deficiency by simple limbal epithelial transplantation-our experience. MOJ Surg. 2014;1:00002.Google Scholar
  55. 55.
    Vazirani J, Ali MH, Sharma N, et al. Autologous simple limbal epithelial transplantation for unilateral limbal stem cell deficiency: multicentre results. Br J Ophthalmol. 2016;100:1416–20.Google Scholar
  56. 56.
    Nishida K, Yamato M, Hayashida Y, Watanabe K, Yamamoto K, Adachi E, et al. Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium. N Engl J Med. 2004;351:1187–96.Google Scholar
  57. 57.
    Nakamura T, Inatomi T, Sotozono C, Amemiya T, Kanamura N, Kinoshita S. Transplantation of cultivated autologous oral mucosal epithelial cells in patients with severe ocular surface disorders. Br J Ophthalmol. 2004;88:1280–4.Google Scholar
  58. 58.
    Burillon C, Huot L, Justin V, Nataf S, Chapuis F, Decullier E, et al. Cultured autologous oral mucosal epithelial cell sheet (CAOMECS) transplantation for the treatment of corneal limbal epithelial stem cell deficiency. Invest Ophthalmol Vis Sci. 2012;53(3):1325–31.Google Scholar
  59. 59.
    Sotozono C, Inatomi T, Nakamura T, Koizumi N, Yokoi N, Ueta M, et al. Visual improvement after cultivated oral mucosal epithelial transplantation. Ophthalmology. 2013;120(1):193–200.Google Scholar
  60. 60.
    Satake Y, Higa K, Tsubota K, Shimazaki J. Long-term outcome of cultivated oral mucosal epithelial sheet transplantation in treatment of total limbal stem cell deficiency. Ophthalmology. 2011;118(8):1524–30.Google Scholar
  61. 61.
    Nakamura T, Yokoo S, Bentley AJ, Nagata M, Fullwood NJ, Inatomi T, et al. Development of functional human oral mucosal epithelial stem/progenitor cell sheets using a feeder-free and serum-free culture system for ocular surface reconstruction. Sci Rep. 2016;6:37173.Google Scholar
  62. 62.
    Cheung AY, Holland EJ. Keratolimbal allograft. Curr Opin Ophthalmol. 2017;28:377–81.Google Scholar
  63. 63.
    Chan CC, Biber JM, Holland EJ. The modified Cincinnati procedure: combined conjunctival limbal autografts and keratolimbal allografts for severe unilateral ocular surface failure. Cornea. 2012;31:1264–72.Google Scholar
  64. 64.
    Cheung AY, Sarnicola E, Govil A, Holland EJ. Combined conjunctival limbal autografts and living-related conjunctival limbal allografts for severe unilateral ocular surface failure. Cornea. 2017 Dec;36(12):1570–5.Google Scholar
  65. 65.
    Biber JM, Skeens HM, Neff KD, Holland EJ. The Cincinnati procedure: technique and outcomes of combined living-related conjunctival limbal allografts and keratolimbal allografts in severe ocular surface failure. Cornea. 2011;30(7):765–71.Google Scholar
  66. 66.
    Hou JH, de la Cruz J, Djalilian AR. Outcomes of Boston keratoprosthesis implantation for failed keratoplasty after keratolimbal allograft. Cornea. 2012;31:1432–5.Google Scholar
  67. 67.
    Sejpal K, Yu F, Aldave AJ. The Boston keratoprosthesis in the management of corneal limbal stem cell deficiency. Cornea. 2011;30(11):1187–94.Google Scholar
  68. 68.
    Aldave AJ, Sangwan VS, Basu S, Basak SK, Hovakimyan A, Gevorgyan O, et al. International results with the Boston type I keratoprosthesis. Ophthalmology. 2012;119:1530–8.Google Scholar
  69. 69.
    Saeed HN, Shanbhag S, Chodosh J. The Boston keratoprosthesis. Curr Opin Ophthalmol. 2017;28:390–6.Google Scholar
  70. 70.
    Ciolino JB, Belin MW, Todani A, al-Arfaj K, Rudnisky CJ, Boston Keratoprosthesis Type 1 Study Group. Boston keratoprosthesis type 1 study group. Retention of the Boston keratoprosthesis type 1: multicenter study results. Ophthalmology. 2013;120:1195–200.Google Scholar
  71. 71.
    Aravena C, Bozkurt TK, Yu F, Aldave AJ. Long-term outcomes of the Boston type I keratoprosthesis in the management of corneal limbal stem cell deficiency. Cornea. 2016 Sep;35(9):1156–64.Google Scholar
  72. 72.
    Aravena C, Yu F, Aldave AJ. Long-term visual outcomes, complications, and retention of the Boston type I keratoprosthesis. Cornea. 2018;37:3–10.Google Scholar
  73. 73.
    Srikumaran D, Munoz B, Aldave AJ, Aquavella JV, Hannush SB, Schultze R, et al. Long-term outcomes of Boston type 1 keratoprosthesis implantation: a retrospective multicenter cohort. Ophthalmology. 2014;121:2159–64.Google Scholar
  74. 74.
    Gomaa A, Comyn O, Liu C. Keratoprostheses in clinical practice - a review. Clin Exp Ophthalmol. 2010;38:211–24.Google Scholar
  75. 75.
    Pujari S, Siddique SS, Dohlman CH, Chodosh J. The Boston keratoprosthesis type II: the Massachusetts eye and ear infirmary experience. Cornea. 2011;30(12):1298–303.Google Scholar
  76. 76.
    Strampelli B. Keratoprosthesis with osteodental tissue. Am J Ophthalmol. 1963;89:1029–39.Google Scholar
  77. 77.
    Falcinelli G, Falsini B, Taloni M, Colliardo P, Falcinelli G. Modified osteo-odonto-keratoprosthesis for treatment of corneal blindness: long-term anatomical and functional outcomes in 181 cases. Arch Ophthalmol. 2005;123(10):1319–29.Google Scholar
  78. 78.
    Basu S, Sureka S, Shukla R, Sangwan V. Boston type 1 based keratoprosthesis (Auro Kpro) and its modification (LVP Kpro) in chronic Stevens Johnson syndrome. BMJ Case Rep. 2014;2014:bcr2013202756.  https://doi.org/10.1136/bcr-2013-202756.
  79. 79.
    Espandar L, Pathan MF, Afshari NA. Adult corneal stem cells and alternative sources for regenerative therapy for the cornea: an update. CML Ophthalmology. 2015;25(4):97–104.Google Scholar
  80. 80.
    Basu S, Hertsenberg AJ, Funderburgh ML, Burrow MK, Mann MM, du Y, et al. Human limbal biopsy-derived stromal stem cells prevent corneal scarring. Sci Transl Med. 2014 December 10;6(266):266ra172.Google Scholar
  81. 81.
    Javorkova E, Trosan P, Zajicova A, et al. Modulation of the early inflammatory microenvironment in the alkali-burned eye by systemically administered interferon-gamma-treated mesenchymal stromal cells. Stem Cells Dev. 2014;15(23):2490–500.Google Scholar
  82. 82.
    Oh JY, Roddy GW, Choi H, Lee RH, Ylostalo JH, Rosa RH, et al. Anti-inflammatory protein TSG- 6 reduces inflammatory damage to the cornea following chemical and mechanical injury. Proc Natl Acad Sci U S A. 2010;107(39):16875–80.Google Scholar
  83. 83.
    Hayashi R, Ishikawa Y, Ito M, Kageyama T, Takashiba K, Fujioka T, et al. Generation of corneal epithelial cells from induced pluripotent stem cells derived from human dermal fibroblast and corneal limbal epithelium. PLoS One. 2012;7(9):e45435.Google Scholar
  84. 84.
    Gomes JA, Geraldes Monteiro B, Melo GB, et al. Corneal reconstruction with tissue-engineered cell sheets composed of human immature dental pulp stem cells. Invest Ophthalmol Vis Sci. 2010;51(3):1408–14.Google Scholar
  85. 85.
    Ilari L, Daya SM. Long-term outcomes of keratolimbal allograft for the treatment of severe ocular surface disorders. Ophthalmology. 2002;109:1278–84.Google Scholar
  86. 86.
    Solomon A, Ellies P, Anderson DF, Touhami A, Grueterich M, Espana EM, et al. Long-term outcome of keratolimbal allograft with or without penetrating keratoplasty for total limbal stem cell deficiency. Ophthalmology. 2002;109:1159–66.Google Scholar
  87. 87.
    Sepsakos L, Cheung AY, Holland EJ. Outcomes of keratoplasty after ocular surface stem cell transplantation. Cornea. 2017 Sep;36(9):1025–30.Google Scholar
  88. 88.
    Shimazaki J, Maruyama F, Shimmura S, Fujishima H, Tsubota K. Immunologic rejection of the central graft after limbal allograft transplantation combined with penetrating keratoplasty. Cornea. 2001;20:149–52.Google Scholar
  89. 89.
    Lai JY, Lue SJ, Cheng HY, Ma HA. Effect of matrix nanostructure on the functionality of carbodiimide crosslinked amniotic membranes as limbal epithelial cell scaffolds. J Biomed Nanotechnol. 2013;9(12):2048–62.Google Scholar
  90. 90.
    Buznyk O, Pasyechnikova N, Islam MM, Iakymenko S, Fagerholm P, Griffith M. Bioengineered corneas grafted as alternatives to human donor corneas in three high-risk patients. Clinical and Translational Science. 2015;8:558–62.Google Scholar
  91. 91.
    Liu W, Merrett K, Griffith M, Fagerholm P, Dravida S, Heyne B, et al. Recombinant human collagen for tissue engineered corneal substitutes. Biomaterials. 2008;29(9):1147–58.Google Scholar
  92. 92.
    Levis HJ, Menzel-Severing J, Drake RA, Daniels JT. Plastic compressed collagen constructs for ocular cell culture and transplantation: a new and improved technique of confined fluid loss. Curr Eye Res. 2013;38(1):41–52.Google Scholar
  93. 93.
    Brown KD, Low S, Mariappan I, Abberton KM, Short R, Zhang H, et al. Plasma polymer-coated contact lenses for the culture and transfer of corneal epithelial cells in the treatment of limbal stem cell deficiency. Tissue Eng A. 2014;20(3–4):646–55.Google Scholar
  94. 94.
    Guan L, Ge H, Tang X, Su S, Tian P, Xiao N, et al. Use of a silk fibroin-chitosan scaffold to construct a tissue-engineered corneal stroma. Cells Tissues Organs. 2013;198(3):190–7.Google Scholar
  95. 95.
    Albert R, Veréb Z, Csomós K, et al. Cultivation and characterization of cornea limbal epithelial stem cells on lens capsule in animal material-free médium. PLoS ONE. 2012;7(10):e47187.Google Scholar
  96. 96.
    Reichl S, Borrelli M, Geerling G. Keratin films for ocular surface reconstruction. Biomaterials. 2011;32(13):3375–86.Google Scholar
  97. 97.
    Gimeno FL, Lavigne V, Gatto S, Croxatto JO, et al. One-year follow-up of epithelial corneal cell sheet allografts mounted on platelet poor plasma in rabbits. Mol Vis. 2009;15:2771–9.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Jesus Cabral-Macias
    • 1
  • Jaime D. Martinez
    • 2
  • Andrea Naranjo
    • 2
  • Guillermo Amescua
    • 2
  1. 1.Cornea and Refractive Surgery DepartmentInstituto de Oftalmología Fundación Conde de ValencianaMexico CityMexico
  2. 2.Department of Ophthalmology, Anne Bates Leach Eye Hospital, Bascom Palmer Eye InstituteUniversity of Miami Miller School of MedicineMiamiUSA

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