- Email: [email protected]
Current indications and surgical approaches to corneal transplants at the University of Toronto: A clinical-pathological study
Current indications and surgical approaches to corneal transplants at the University of Toronto: A clinical-pathological study Ryan Le, HBSc,*,a Narain Yucel, *,†,a Shireen Khattak, HBSc,*,† Yeni H. Yucel, MD, PhD,*,†,‡,§ Gerald J. Prud’homme, MD,*,‡ Neeru Gupta, MD, PhD, MBA*,†,‡ ABSTRACT ● RÉSUMÉ Objective: To determine the most common reasons and surgical approaches for corneal graft surgery at the Kensington Eye Institute (KEI), University of Toronto. Design: Retrospective cross-sectional study. Participants: A total of 229 consecutive corneal transplants performed at the KEI. Methods: Demographic, clinical, and pathological data on all 2012 and 2013 corneal transplants were collected. Results: The mean age for corneal transplants was 65 ⫾ 16 years; 39% were full-thickness penetrating keratoplasties (PK) and 61% were partial-thickness. Graft failure (30%), infection (18%), and keratoconus (17%) were the leading indications for PK. Fuchs’ dystrophy (40%) and bullous keratopathy (24%) were main causes for partial-thickness procedures. Among partialthickness approaches, Descemet’s stripping automated endothelial keratoplasty (DSAEK), deep anterior lamellar keratoplasty (DALK), and Descemet’s membrane endothelial keratoplasty (DMEK) procedures accounted for 68%, 16%, and 16%, respectively. Fuchs’ dystrophy (40%) and bullous keratopathy (33%) were the most common indications for DSAEK. Keratoconus (57%) and corneal scarring (35%) were the most common indications for DALK, whereas Fuchs’ dystrophy (82%) accounted for most DMEK procedures. The most common reasons for all corneal grafts were Fuchs’ dystrophy (25%), bullous keratopathy (21%), graft failure (17%), and keratoconus (12%). Conclusions: Almost two-thirds of all corneal transplant procedures at the University of Toronto are partial thickness procedures. A failed graft was found to be the most common indication for full-thickness transplants. Fuchs’ dystrophy was the most common indication for a partial-thickness approach, most often treated by DSAEK. Longitudinal data are needed to determine whether partial-thickness surgeries will improve graft survival and reduce the need for regraft. Objectif : Déterminer les raisons et les approches chirurgicales les plus courantes de la greffe de la cornée au Kensington Eye Institute (KEI) de l'Université de Toronto. Nature : Étude transversale rétrospective. Participants : 229 transplantations de cornée consécutives réalisées au KEI. Méthodes : Les caractéristiques sociodémographiques, cliniques et pathologiques de tous les patients ayant subi une transplantation de la cornée effectuée entre 2012 et 2013 ont été recueillies. Résultats : L’âge moyen des patients était de 65 ± 16 ans. 39 % des patients ont subi une kératoplastie transfixiante de pleine épaisseur (KT) et 61 % une kératoplastie d’épaisseur partielle. L’échec de la greffe (30 %), l’infection (18 %) et le kératocône (17 %) étaient les indications principales de la KT. La dystrophie de Fuchs (40 %) et la kératopathie bulleuse (24 %) étaient les causes principales des interventions relatives à la kératoplastie d’épaisseur partielle. Parmi les approches relatives à cette intervention, la kératoplastie endothéliale automatisée avec détachement de la membrane de Descemet (KEADMD), la kératoplastie lamellaire antérieure profonde (KLAP) et la kératoplastie endothéliale de la membrane de Descemet (KEMD) représentaient respectivement 68 %, 16 % et 16 % des interventions. La dystrophie de Fuchs (40 %) et la kératopathie bulleuse (33 %) étaient les indications les plus courantes de la KEADMD. Le kératocône (57 %) et la cicatrisation de la cornée (35 %) étaient les indications les plus courantes de la KLAP, tandis que la dystrophie de Fuchs (82 %) expliquait la plupart des interventions de KEMD. Les raisons les plus courantes des 51 transplantations cornéennes étaient la dystrophie de Fuchs (25 %), la kératopathie bulleuse (21 %), l’échec de la greffe (17 %) et le kératocône (12 %). Conclusions : Près des deux tiers de toutes les transplantations de la cornée effectuées à l’Université de Toronto sont des kératoplasties d’épaisseur partielle. L’échec de la greffe est l’indication la plus courante des transplantations de pleine épaisseur. La dystrophie de Fuchs était l’indication la plus courante de l’approche de l’épaisseur partielle, le plus souvent par KEADMD. Des données longitudinales sont nécessaires pour déterminer si les opérations d’épaisseur partielle permettront d’améliorer la survie du greffon et diminuer la nécessité d’une nouvelle transplantation.
Recent technological advances have led to the adoption of partial-thickness procedures as an alternative to fullthickness replacement of the cornea, with surgical choices guided by the location of the pathology. Selective replacement of the endothelium for diseases such as Fuchs’ & 2017 The Authors. Published by Elsevier Inc. on behalf of Canadian Journal of Opthalmology. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). http://dx.doi.org/10.1016/j.jcjo.2016.07.005 ISSN 0008-4182/17
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dystrophy can be achieved by procedures such as Descemet’s stripping automated endothelial keratoplasty (DSAEK) and Descemet’s membrane endothelial keratoplasty (DMEK). The anterior stromal layers can be targeted as in deep anterior lamellar keratoplasty (DALK)
Corneal transplants at the university of toronto—Le et al. for diseases such as keratoconus and corneal scarring. Many studies of corneal transplant surgery are derived from data spanning 2000–2010, a period of evolution and adoption of partial-thickness corneal transplants in addition to surgeon learning. During that period, significant increases in the number of partial-thickness corneal transplants were reported from Scotland,1 New Zealand,2 China,3 Colombia,4 the United Kingdom,5 Iran,6 and Canada.7–9 DSAEK leads in the treatment of corneal endothelial disease, as does DALK for anterior cornea opacity. Although corneal procedures have matured over the years, information regarding current practice patterns from major academic centres in Canada regarding the type of and indications for corneal grafts are limited. Corneal transplant surgery at the University of Toronto was only recently centralized from major teaching hospitals in the city to the Kensington Eye Institute (KEI), an academic health centre providing ambulatory surgical care. This provided a unique opportunity to evaluate the types of procedures performed and their indications from multiple academic centres and faculty. Here we report mainly 2013 data on full- and partial-thickness corneal transplantation, their indications, and patient demographics from the largest single academic centre for corneal graft surgery in Canada.
METHODS Institutional Research Ethics Board approval (REB No. 13-225) was obtained from St. Michael’s Hospital, Toronto, Canada, on October 30, 2013. This research adhered to the tenets of the Declaration of Helsinki. A retrospective review was conducted, and included clinical and pathological records of all adult corneal transplants performed at the KEI surgical center of the University of Toronto, from November 6, 2013 (date of first corneal transplant surgery at KEI), to December 31, 2013. Data were obtained from the University of Toronto Ophthalmic Pathology Laboratory and included the type
Table 1—Procedure frequency and demographics Type of Procedure Penetrating keratoplasty Partial-thickness transplant DSAEK DALK DMEK
Percent Frequency (n)
Mean Age ⫾ SD (years)
Male/Female Ratio
39 (89)
59 ⫾ 16.6
1:1
61 (140)
68 ⫾ 15.2
2:3
41 (95) 10 (23) 10 (22)
73 ⫾ 11.1 47 ⫾ 16.0 71 ⫾ 11.4
1:2 2:1 1:2
DSAEK, Descemet’s stripping endothelial keratoplasty; DALK, deep anterior lamellar keratoplasty; DMEK, Descemet’s membrane endothelial keratoplasty.
of corneal surgery performed, clinical/pathological indication, and demographic information, including age and sex. All cases with confirmed clinical and pathological diagnoses were included. The data were categorized according to the type of procedure performed, separating fullthickness transplants from partial-thickness transplants. Data on partial-thickness transplants were further categorized as DSAEK, DMEK, or DALK. Each procedure type was assessed according to its disease indications and the age and sex of patients. Three cases of DALK were converted to penetrating keratoplasties (PK). Cases in which clinical indications were not provided and pathological results showed corneal endothelial cell loss without characteristic findings of Fuchs’ dystrophy were termed “non-Fuchs’ dystrophy,” and cases of congenital hereditary endothelial dystrophy were also included here. A category of “others” included least common indications: granular dystrophy, central cloudy dystrophy of Francois, lattice dystrophy, pterygium, thick Descemet’s membrane, iridocorneal endothelial syndrome, trauma, neurotrophic keratopathy, corneal ulcer, toxic anterior segment syndrome, and uveitis.
RESULTS Two hundred and twenty-nine corneal transplants were performed from November 2012 to December 2013 (patients’ mean age 65 ⫾ 16 years). Of these, 89 (39%)
Fig. 1 — Of corneal transplant surgeries performed at University of Toronto 2012–2013 (n ¼ 229), 89 (39%) were full-thickness and 140 (61%) were partial-thickness (A). Most partial-thickness procedures were Descemet’s stripping automated endothelial keratoplasty (DSAEK) (68%), followed by deep anterior lamellar keratoplasty (DALK) (16%), and Descemet’s membrane endothelial keratoplasty (DMEK) (16%) (B). CAN J OPHTHALMOL — VOL. 52, NO. 1, FEBRUARY 2017
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Corneal transplants at the university of toronto—Le et al.
Fig. 2 — Full-thickness transplants were performed most commonly for infection, graft failure, scar, and keratoconus. Partial-thickness transplants were performed most commonly for non-Fuchs’ dystrophy (100%), Fuchs’ (98%), and bullous keratopathy cases (71%).
were full-thickness corneal transplants, and 140 (61%) were partial-thickness corneal transplants (Fig. 1A). Patients undergoing full-thickness transplants (59 ⫾ 17 years) were significantly younger compared with those who had partial-thickness transplants (68 ⫾ 15 years) (p o 0.0001). Partial-thickness procedures performed were DSAEK (68%), DALK (16%), and DMEK (16%)
(Fig. 1B). Of the partial-thickness patients, the average age was 73 ⫾ 11 years for DSAEK, 47 ⫾ 16 years for DALK, and 71 ⫾ 11 years for DMEK (Table 1). Full-thickness transplants were performed for most cases of infection (89%), graft failure (68%), other (see methods) (57%), keratoconus (54%), and corneal scarring (47%). Partial-thickness transplants were performed for most cases of non-Fuchs’ dystrophy (100%), Fuchs’ dystrophy (98%), bullous keratopathy (71%), and corneal scarring (53%) (Fig. 2). The most common indication for full-thickness transplant was graft failure (30%), followed by infection (18%) and keratoconus (17%) (Fig. 3A). The most common indication for partial-thickness transplant was Fuchs’ dystrophy (40%), followed by bullous keratopathy (24%) and both keratoconus and graft failure (9%). Among the partial-thickness procedures, keratoconus (57%) and corneal scarring (35%) were the most common indications for DALK procedures (Fig. 3B). Fuchs’ dystrophy (40%) and bullous keratopathy (33%) were the most common indications for DSAEK (Fig. 3C). Most DMEK procedures (82%) were performed for Fuchs’ dystrophy (Fig. 3D). The most common indications for all corneal graft surgery were Fuchs’ dystrophy (25%), bullous keratopathy (21%), and graft failure (17%) (Table 2). Among Fuchs’ dystrophy patients, 67% were treated with DSAEK, 31% by DMEK, and 2% by PK (Fig. 4A).
Fig. 3 — When penetrating keratoplasty (PK) was performed, the leading indications were graft failure (30%), infection (18%), and keratoconus (17%) (A). For deep anterior lamellar keratoplasty (DALK), leading indications were keratoconus (57%) and corneal scarring (35%) (B). For Descemet’s stripping automated endothelial keratoplasty (DSAEK), leading indications were Fuchs’ dystrophy (40%) and bullous keratopathy (33%) (C). For Descemet’s membrane endothelial keratoplasty (DMEK), most cases were Fuchs’ dystrophy (82%) (D).
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Corneal transplants at the university of toronto—Le et al. Table 2—Diseases and demographics Clinical Indication Fuchs’ dystrophy Bullous keratopathy Graft failure Keratoconus Infection Corneal scarring Other Non-Fuchs’ Dystrophy
Percent of All Transplants (n) 24.9 20.9 17.4 12.2 7.9 7.4 6.1 3.1
(57) (48) (40) (28) (18) (17) (14) (7)
Mean Age ⫾ SD (years) 69.9 75.2 66.8 42.0 64.7 55.4 71.3 63.8
⫾ ⫾ ⫾ ⫾ ⫾ ⫾ ⫾ ⫾
9.4 8.5 16.6 14.5 14.1 14.0 16.0 16.8
Among patients with graft failure, 68% of patients underwent PK and 32% underwent DSAEK (Fig. 4B). Bullous keratopathy patients were mostly treated by DSAEK (65%), followed by PK (29%) and DMEK (6%) (Fig. 4C). Patients with Fuchs’ dystrophy (69.9 ⫾ 9.4 years), bullous keratopathy (75.2 ⫾ 8.5 years), graft failure (66.8 ⫾ 16.6 years), infection (64.7 ⫾ 14.1 years), and nonFuchs’ dystrophy (63.8 ⫾ 16.8 years) were older than those treated for keratoconus (42.0 ⫾ 14.5 years) and corneal scarring (55.4 ⫾ 14.0 years) (Table 2).
DISCUSSION Recent centralization of corneal transplant surgery at the University of Toronto to the KEI provided an opportunity to evaluate types and indications of corneal graft surgery across multiple academic teaching hospitals and faculty. We found that approximately 61% of transplants performed in 2013 were partial-thickness grafts. Growing trends in Ontario from 2007 to 2010 have been reported,7 and advancements in partial-thickness procedures and outcomes, technology, and surgeon experience over the past decade likely play some role. Partialthickness procedures have become attractive alternatives to full-thickness procedures with evidence of improved visual outcomes, earlier visual recovery, and comparable graft survival rates of 94% and 90% for partial-thickness and full-thickness, respectively.10–17 Full-thickness
transplant recovery time is typically 1 year, whereas recovery rates for partial-thickness transplants may be 4–6 weeks.11,18,19 Among the partial-thickness procedures, a growing trend for the use of DSAEK in the surgical treatment of corneal endothelial disease has been reported.1,4 Our study showed that more DSAEK than DMEK procedures were performed for Fuchs’ dystrophy (67% vs 31%). As DMEK was relatively new at the time, it is possible that fewer surgeons were performing the procedure. Among the endothelial keratoplasty procedures (DSAEK and DMEK), DSAEK continues to be the more popular procedure. DMEK is known to be technically challenging with higher risk of the thin donor tissue dislocating or tearing.18 Continuing improvements to the DMEK procedure may increase its frequency of use in treating corneal endothelial diseases.20 In our patients with corneal scarring, 47% were treated with PK and 47% were treated with DALK. Similar proportions were found for keratoconus patients. For both of these conditions, PK was performed equally as or more often. Studies have reported increased frequency of DALK between 2001 and 2010.8,21 DALK has been found to have visual and refractive outcomes comparable to PK; however, data on long-term graft survival are variable.16,22,23 Use of one technique over the other is dependent on the disease severity and presence of risk factors, and experts agree that DALK is the preferred treatment for keratoconus unless other factors such as deep scarring are involved.24 We found that more partial-thickness transplants, specifically DSAEK and DMEK, were performed in older patients compared with full-thickness transplants. Fullthickness transplants were performed for corneal scarring and infection, which may occur across a spectrum of ages. The increasing frequency of partial-thickness techniques performed for corneal endothelial diseases like Fuchs’ dystrophy helps to explain the older demographic, given that Fuchs’ dystrophy is not typically symptomatic until the sixth decade of life. Among partial-thickness transplant patients, DSAEK and DMEK patients’ had a higher age
Fig. 4 — Procedures performed for Fuchs’ dystrophy (A), bullous keratopathy (B), and graft failure (C). Descemet’s stripping automated endothelial keratoplasty (DSAEK) was the most common procedure in Fuchs’ dystrophy and bullous keratopathy, whereas penetrating keratoplasty (PK) was the most common for graft failure. CAN J OPHTHALMOL — VOL. 52, NO. 1, FEBRUARY 2017
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Corneal transplants at the university of toronto—Le et al. (70s) compared with DALK patients, with the average age found to be 47.4 ⫾ 16 years (Table 1). DALK was indicated commonly to treat keratoconus and consistent with expected onset in the 20s, taking 10 to 20 years to progress to a surgical stage.25 Although published data regarding current corneal transplant indications and types in major centres are limited, data from the 2000 to 2010 period from Scotland,1 New Zealand,2 Australia,22 the United Kingdom,5 Iran,6 and Germany26 found that keratoconus was a leading indication, and as high as 41% of total transplants. Hungary19 and Colombia4 reported bullous keratopathy to be the most common cause. In China, the leading cause was infectious keratitis,3 whereas in Canada, pseudophakic corneal edema was dominant from 2000 to 2009.21 These differences reflect diverse demographics and local pathologies and may change with future treatment advances. Our study found Fuchs’ dystrophy as a leading indication for corneal transplant (25%), and Canadian data from 2010 to 2012 reported Fuchs’ dystrophy emerging as a major cause.8,9,27 Improvements in cataract surgical techniques have likely reduced the cases of pseudophakic corneal edema, coincident with the widespread adoption of partial-thickness procedures for Fuchs’ dystrophy. Bullous keratopathy (21%), graft failure (17%), and keratoconus (12%) were all important indications for corneal grafts. Most graft failures were treated with PK (68%). The cause of graft failure is an important consideration in patients undergoing surgery, and as endothelial cell loss is a common reason for graft failure, partial-thickness procedures may be more beneficial.28–30 Studies have shown that after an initial failed PK, repeat PK and DSAEK have similar graft survival rates and visual outcomes.31–34 DSAEK has been shown to result in less endothelial cell loss compared with PK.11 Long-term graft survival data show that endothelial keratoplasty procedures may be superior in regrafts, with 5-year survival rates of 86% for endothelial keratoplasty and 51% for PK.30,32 Attempts to reduce graft failure rates by increasing graft size may reduce endothelial cell loss but lead to irregularity of graft surface, among other problems.35 In cases of graft failure due to neovascularization, inflammation, or infection, many layers may be affected. For these challenging patients, partial-thickness procedures are less likely to be sufficient. Despite PK as the treatment choice for these graft failure patients, a high-risk graft bed contributes to high rates of failure in subsequent transplant procedures.36 Future improved ability to categorize the graft bed by risk and medical interventions may help address cases at higher risk of failure.37,38 Long-term survival studies of partial-thickness procedures are needed to determine whether this approach will affect the need for regrafting.
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Current practice at the KEI, University of Toronto, indicates that almost two-thirds of all corneal transplants performed are partial-thickness transplants. Fuchs’ dystrophy, bullous keratopathy, and graft failure are the most common reasons for corneal transplantation. Most Fuchs’ dystrophy and bullous keratopathy are treated with partial-thickness procedures. Full-thickness transplants remain the preferred choice for graft failure. Longitudinal data and further research are needed to determine whether longer graft survival and higher success rates with partial-thickness transplants will reduce the demand for corneal transplants due to graft failure.
REFERENCES 1. Ting DS, Sau CY, Srinivasan S, et al. Changing trends in keratoplasty in the West of Scotland: a 10-year review. Br J Ophthalmol. 2012;96:405-8. 2. Cunningham WJ, Brookes NH, Twohill HC, et al. Trends in the distribution of donor corneal tissue and indications for corneal transplantation: the New Zealand National Eye Bank Study 2000– 2009. Clin Exp Ophthalmol. 2012;40:141-7. 3. Xie L, Qi F, Gao H, et al. Major shifts in corneal transplantation procedures in north China: 5316 eyes over 12 years. Br J Ophthamol. 2009;93:1291-5. 4. Galvis V, Tello A, Gomez AJ, et al. Corneal transplantation at an ophthalmological referral center in Colombia: indications and techniques (2004–2011). Open Ophthalmol J. 2013;7:30-3. 5. Keenan TD, Jones MN, Rushton S, et al. Trends in the indications for corneal graft surgery in the United Kingdom: 1999 through 2009. Arch Ophthalmol. 2012;130:621-8. 6. Zare M, Javadi MA, Einollahi B, et al. Changing indications and surgical techniques for corneal transplantation between 2004 and 2009 at a tertiary referral center. Middle East Afr J Ophthalmol. 2012;19:323-9. 7. Lichtinger A, Yeung SN, Kim P, et al. The era of lamellar keratoplasty, evolving surgical techniques in corneal transplantation: the University of Toronto experience. Can J Ophthalmol. 2012;47:287-90. 8. Tan JC, Holland SP, Dubord PJ, et al. Evolving indications for and trends in keratoplasty in British Columbia, Canada, from 2002 to 2011: a 10 year review. Cornea. 2014;33:252-6. 9. Zhang AQ, Rubenstein D, Price AJ, et al. Evolving surgical techniques of and indications for corneal transplantation in Ontario: 2000–2012. Can J Ophthalmol. 2013;48:153-9. 10. Ang M, Mehta JS, Lim F, et al. Endothelial cell loss and graft survival after Descemet’s stripping automated endothelial keratoplasty and penetrating keratoplasty. Ophthalmology. 2012;119: 2239-44. 11. Gorovoy MS. Descemet-stripping automated endothelial keratoplasty. Cornea. 2006;25:886-9. 12. Kasbekar SA, Jones MN, Ahmad S, et al. Corneal transplant surgery for keratoconus and the effect of surgeon experience on deep anterior lamellar keratoplasty outcomes. Am J Ophthalmol. 2014;158: 1239-46. 13. Li JY, Terry MA, Goshe J, et al. Three-year visual acuity outcomes after Descemet’s stripping automated endothelial keratoplasty. Ophthalmology. 2012;119:1126-9. 14. Phillips PM, Phillips LJ, Much JW, et al. Descemet stripping endothelial keratoplasty: six-month results of the first 100 consecutive surgeries performed solo by a surgeon using 1 technique with 100% follow-up. Cornea. 2012;31:1361-4. 15. Ratanasit A, Gorovoy MS. Long-term results of Descemet stripping automated endothelial keratoplasty. Cornea. 2011;30:1414-8. 16. Reinhart WJ, Musch DC, Jacobs DS, et al. Deep anterior lamellar keratoplasty as an alternative to penetrating keratoplasty a report by
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the American Academy of Ophthalmology. Ophthalmology. 2011;118: 209-18. Rodriguez-Calve-de-Mora M, Quilendrino R, Ham L, et al. Clinical outcome of 500 consecutive cases undergoing Descemet’s membrane endothelial keratoplasty. Ophthalmology. 2012;122:464-70. Guerra FP, Anshu A, Price MO, et al. Endothelial keratoplasty: fellow eyes comparison of Descemet stripping automated endothelial keratoplasty and Descemet membrane endothelial keratoplasty. Cornea. 2011;30:1382-6. Tourtas T, Laaser K, Bachmann BO, et al. Descemet membrane endothelial keratoplasty versus Descemet stripping automated endothelial keratoplasty. Am J Ophthalmol. 2012;153 1082–90.e2. Hamzaoglu EC, Straiko MD, Mayko ZM, et al. The first 100 eyes of standardized Descemet stripping automated endothelial keratoplasty vs standardized Descemet membrane endothelial keratoplasty at one institution. Ophthalmology. 2015;122:2193-9. Boimer C, Lee K, Sharpen L, et al. Evolving surgical techniques of and indications for corneal transplantation in Ontario from 2000 to 2009. Can J Ophthalmol. 2011;46:360-6. Coster DJ, Lowe MT, Keane MC, et al. A comparison of lamellar and penetrating keratoplasty outcomes: a registry study. Ophthalmology. 2014;121:979-87. Jones MN, Armitage WJ, Ayliffe W, et al. Penetrating and deep anterior lamellar keratoplasty for keratoconus: a comparison of graft outcomes in the United Kingdom. Invest Ophthalmol Vis Sci. 2009;50:5265-9. Gomes JA, Tan D, Rapuano CJ, et al. Global consensus on keratoconus and ectatic diseases. Cornea. 2015;34:359-69. Rabinowitz YS. Keratoconus. Surv Ophthalmol. 1998;42:297-319. Wang J, Hasenfus A, Schirra F, et al. Changing indications for penetrating keratoplasty in Homburg/Saar from 2001 to 2010— histopathology of 1,200 corneal buttons. Graefes Arch Clin Exp Ophthalmol. 2013;251:797-802. Robert MC, Choronzey ME, Lapointe J, et al. Evolution of corneal transplantation in the province of Quebec from 2000 to 2011. Cornea. 2015;34:880-7. Thompson RW Jr, Price MO, Bowers PJ, et al. Long-term graft survival after penetrating keratoplasty. Ophthalmology. 2003;110: 1396-402. Nishimura JK, Hodge DO, Bourne WM. Initial endothelial cell density and chronic endothelial cell loss rate in corneal transplants with late endothelial failure. Ophthalmology. 1999;106:1962-5. Price MO, Fairchild KM, Price DA, et al. Descemet’s stripping endothelial keratoplasty five-year graft survival and endothelial cell loss. Ophthalmology. 2011;118:725-9. Mitry D, Bhogal M, Patel AK, et al. Descemet stripping automated endothelial keratoplasty after failed penetrating keratoplasty: survival, rejection risk, and visual outcome. JAMA Ophthamol. 2014;132:742-9. Ang M, Ho H, Wong C, et al. Endothelial keratoplasty after failed penetrating keratoplasty: an alternative to repeat penetrating keratoplasty. Am J Ophthamol. 2014;158 1221–1227.e1.
33. Jangi AA, Ritterband DC, Wu EI, et al. Descemet stripping automated endothelial keratoplasty after failed penetrating keratoplasty. Cornea. 2012;31:1148-53. 34. Tarantino-Scherrer JN, Kaufmann C, Bochmann F, et al. Visual recovery and endothelial cell survival after descemet stripping automated endothelial keratoplasty for failed penetrating keratoplasty grafts–a cohort study. Cornea. 2015;34:1024-9. 35. Romano V, Tey A, Hill NM, et al. Influence of graft size on graft survival following Descemet stripping automated endothelial keratoplasty. Br J Ophthamol. 2015;99:784-8. 36. Yu AL, Kaiser M, Schaumberger M, et al. Donor-related risk factors and preoperative recipient-related risk factors for graft failure. Cornea. 2014;33:1149-56. 37. Dekaris I, Gabric N, Draca N, et al. Three-year corneal graft survival rate in high-risk cases treated with subconjunctival and topical bevacizumab. Graefes Arch Clin Exp Ophthalmol. 2015;253:287-94. 38. Bhatti N, Qidwai U, Hussain M, et al. Efficacy of topical bevacizumab in high-risk corneal transplant survival. Pak J Med Sci. 2013;29:519-22.
Footnotes and Disclosure: a
Ryan Le and Narain Yucel contributed equally to this work and should be considered joint first authors. The authors have no proprietary or commercial interest in any materials discussed in this article. The authors would like to acknowledge the Dorothy Pitts Chair and the Thor and Nicky Eaton Fund. From the *Keenan Research Centre for Biomedical Science at the Li Ka Shing Knowledge Institute of St. Michael’s Hospital, Toronto, Ont; †Ophthalmology & Vision Sciences, St. Michael’s Hospital, University of Toronto, Toronto, Ont; ‡Laboratory Medicine & Pathobiology, St. Michael’s Hospital, University of Toronto, Toronto, Ont; §Ophthalmic Pathology Laboratory, University of Toronto, Toronto, Ont. Originally received Dec. 18, 2015. Final revision Jun. 7, 2016. Accepted Jul. 6, 2016. Correspondence to Neeru Gupta, MD, PhD, MBA, St. Michael’s Hospital, 30 Bond Street, Cardinal Carter Wing, 8-072, Toronto, Ont. M5B 1W8; [email protected]
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Recent technological advances have led to the adoption of partial-thickness procedures as an alternative to fullthickness replacement of the cornea, with surgical choices guided by the location of the pathology. Selective replacement of the endothelium for diseases such as Fuchs’ & 2017 The Authors. Published by Elsevier Inc. on behalf of Canadian Journal of Opthalmology. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). http://dx.doi.org/10.1016/j.jcjo.2016.07.005 ISSN 0008-4182/17
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dystrophy can be achieved by procedures such as Descemet’s stripping automated endothelial keratoplasty (DSAEK) and Descemet’s membrane endothelial keratoplasty (DMEK). The anterior stromal layers can be targeted as in deep anterior lamellar keratoplasty (DALK)
Corneal transplants at the university of toronto—Le et al. for diseases such as keratoconus and corneal scarring. Many studies of corneal transplant surgery are derived from data spanning 2000–2010, a period of evolution and adoption of partial-thickness corneal transplants in addition to surgeon learning. During that period, significant increases in the number of partial-thickness corneal transplants were reported from Scotland,1 New Zealand,2 China,3 Colombia,4 the United Kingdom,5 Iran,6 and Canada.7–9 DSAEK leads in the treatment of corneal endothelial disease, as does DALK for anterior cornea opacity. Although corneal procedures have matured over the years, information regarding current practice patterns from major academic centres in Canada regarding the type of and indications for corneal grafts are limited. Corneal transplant surgery at the University of Toronto was only recently centralized from major teaching hospitals in the city to the Kensington Eye Institute (KEI), an academic health centre providing ambulatory surgical care. This provided a unique opportunity to evaluate the types of procedures performed and their indications from multiple academic centres and faculty. Here we report mainly 2013 data on full- and partial-thickness corneal transplantation, their indications, and patient demographics from the largest single academic centre for corneal graft surgery in Canada.
METHODS Institutional Research Ethics Board approval (REB No. 13-225) was obtained from St. Michael’s Hospital, Toronto, Canada, on October 30, 2013. This research adhered to the tenets of the Declaration of Helsinki. A retrospective review was conducted, and included clinical and pathological records of all adult corneal transplants performed at the KEI surgical center of the University of Toronto, from November 6, 2013 (date of first corneal transplant surgery at KEI), to December 31, 2013. Data were obtained from the University of Toronto Ophthalmic Pathology Laboratory and included the type
Table 1—Procedure frequency and demographics Type of Procedure Penetrating keratoplasty Partial-thickness transplant DSAEK DALK DMEK
Percent Frequency (n)
Mean Age ⫾ SD (years)
Male/Female Ratio
39 (89)
59 ⫾ 16.6
1:1
61 (140)
68 ⫾ 15.2
2:3
41 (95) 10 (23) 10 (22)
73 ⫾ 11.1 47 ⫾ 16.0 71 ⫾ 11.4
1:2 2:1 1:2
DSAEK, Descemet’s stripping endothelial keratoplasty; DALK, deep anterior lamellar keratoplasty; DMEK, Descemet’s membrane endothelial keratoplasty.
of corneal surgery performed, clinical/pathological indication, and demographic information, including age and sex. All cases with confirmed clinical and pathological diagnoses were included. The data were categorized according to the type of procedure performed, separating fullthickness transplants from partial-thickness transplants. Data on partial-thickness transplants were further categorized as DSAEK, DMEK, or DALK. Each procedure type was assessed according to its disease indications and the age and sex of patients. Three cases of DALK were converted to penetrating keratoplasties (PK). Cases in which clinical indications were not provided and pathological results showed corneal endothelial cell loss without characteristic findings of Fuchs’ dystrophy were termed “non-Fuchs’ dystrophy,” and cases of congenital hereditary endothelial dystrophy were also included here. A category of “others” included least common indications: granular dystrophy, central cloudy dystrophy of Francois, lattice dystrophy, pterygium, thick Descemet’s membrane, iridocorneal endothelial syndrome, trauma, neurotrophic keratopathy, corneal ulcer, toxic anterior segment syndrome, and uveitis.
RESULTS Two hundred and twenty-nine corneal transplants were performed from November 2012 to December 2013 (patients’ mean age 65 ⫾ 16 years). Of these, 89 (39%)
Fig. 1 — Of corneal transplant surgeries performed at University of Toronto 2012–2013 (n ¼ 229), 89 (39%) were full-thickness and 140 (61%) were partial-thickness (A). Most partial-thickness procedures were Descemet’s stripping automated endothelial keratoplasty (DSAEK) (68%), followed by deep anterior lamellar keratoplasty (DALK) (16%), and Descemet’s membrane endothelial keratoplasty (DMEK) (16%) (B). CAN J OPHTHALMOL — VOL. 52, NO. 1, FEBRUARY 2017
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Corneal transplants at the university of toronto—Le et al.
Fig. 2 — Full-thickness transplants were performed most commonly for infection, graft failure, scar, and keratoconus. Partial-thickness transplants were performed most commonly for non-Fuchs’ dystrophy (100%), Fuchs’ (98%), and bullous keratopathy cases (71%).
were full-thickness corneal transplants, and 140 (61%) were partial-thickness corneal transplants (Fig. 1A). Patients undergoing full-thickness transplants (59 ⫾ 17 years) were significantly younger compared with those who had partial-thickness transplants (68 ⫾ 15 years) (p o 0.0001). Partial-thickness procedures performed were DSAEK (68%), DALK (16%), and DMEK (16%)
(Fig. 1B). Of the partial-thickness patients, the average age was 73 ⫾ 11 years for DSAEK, 47 ⫾ 16 years for DALK, and 71 ⫾ 11 years for DMEK (Table 1). Full-thickness transplants were performed for most cases of infection (89%), graft failure (68%), other (see methods) (57%), keratoconus (54%), and corneal scarring (47%). Partial-thickness transplants were performed for most cases of non-Fuchs’ dystrophy (100%), Fuchs’ dystrophy (98%), bullous keratopathy (71%), and corneal scarring (53%) (Fig. 2). The most common indication for full-thickness transplant was graft failure (30%), followed by infection (18%) and keratoconus (17%) (Fig. 3A). The most common indication for partial-thickness transplant was Fuchs’ dystrophy (40%), followed by bullous keratopathy (24%) and both keratoconus and graft failure (9%). Among the partial-thickness procedures, keratoconus (57%) and corneal scarring (35%) were the most common indications for DALK procedures (Fig. 3B). Fuchs’ dystrophy (40%) and bullous keratopathy (33%) were the most common indications for DSAEK (Fig. 3C). Most DMEK procedures (82%) were performed for Fuchs’ dystrophy (Fig. 3D). The most common indications for all corneal graft surgery were Fuchs’ dystrophy (25%), bullous keratopathy (21%), and graft failure (17%) (Table 2). Among Fuchs’ dystrophy patients, 67% were treated with DSAEK, 31% by DMEK, and 2% by PK (Fig. 4A).
Fig. 3 — When penetrating keratoplasty (PK) was performed, the leading indications were graft failure (30%), infection (18%), and keratoconus (17%) (A). For deep anterior lamellar keratoplasty (DALK), leading indications were keratoconus (57%) and corneal scarring (35%) (B). For Descemet’s stripping automated endothelial keratoplasty (DSAEK), leading indications were Fuchs’ dystrophy (40%) and bullous keratopathy (33%) (C). For Descemet’s membrane endothelial keratoplasty (DMEK), most cases were Fuchs’ dystrophy (82%) (D).
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Corneal transplants at the university of toronto—Le et al. Table 2—Diseases and demographics Clinical Indication Fuchs’ dystrophy Bullous keratopathy Graft failure Keratoconus Infection Corneal scarring Other Non-Fuchs’ Dystrophy
Percent of All Transplants (n) 24.9 20.9 17.4 12.2 7.9 7.4 6.1 3.1
(57) (48) (40) (28) (18) (17) (14) (7)
Mean Age ⫾ SD (years) 69.9 75.2 66.8 42.0 64.7 55.4 71.3 63.8
⫾ ⫾ ⫾ ⫾ ⫾ ⫾ ⫾ ⫾
9.4 8.5 16.6 14.5 14.1 14.0 16.0 16.8
Among patients with graft failure, 68% of patients underwent PK and 32% underwent DSAEK (Fig. 4B). Bullous keratopathy patients were mostly treated by DSAEK (65%), followed by PK (29%) and DMEK (6%) (Fig. 4C). Patients with Fuchs’ dystrophy (69.9 ⫾ 9.4 years), bullous keratopathy (75.2 ⫾ 8.5 years), graft failure (66.8 ⫾ 16.6 years), infection (64.7 ⫾ 14.1 years), and nonFuchs’ dystrophy (63.8 ⫾ 16.8 years) were older than those treated for keratoconus (42.0 ⫾ 14.5 years) and corneal scarring (55.4 ⫾ 14.0 years) (Table 2).
DISCUSSION Recent centralization of corneal transplant surgery at the University of Toronto to the KEI provided an opportunity to evaluate types and indications of corneal graft surgery across multiple academic teaching hospitals and faculty. We found that approximately 61% of transplants performed in 2013 were partial-thickness grafts. Growing trends in Ontario from 2007 to 2010 have been reported,7 and advancements in partial-thickness procedures and outcomes, technology, and surgeon experience over the past decade likely play some role. Partialthickness procedures have become attractive alternatives to full-thickness procedures with evidence of improved visual outcomes, earlier visual recovery, and comparable graft survival rates of 94% and 90% for partial-thickness and full-thickness, respectively.10–17 Full-thickness
transplant recovery time is typically 1 year, whereas recovery rates for partial-thickness transplants may be 4–6 weeks.11,18,19 Among the partial-thickness procedures, a growing trend for the use of DSAEK in the surgical treatment of corneal endothelial disease has been reported.1,4 Our study showed that more DSAEK than DMEK procedures were performed for Fuchs’ dystrophy (67% vs 31%). As DMEK was relatively new at the time, it is possible that fewer surgeons were performing the procedure. Among the endothelial keratoplasty procedures (DSAEK and DMEK), DSAEK continues to be the more popular procedure. DMEK is known to be technically challenging with higher risk of the thin donor tissue dislocating or tearing.18 Continuing improvements to the DMEK procedure may increase its frequency of use in treating corneal endothelial diseases.20 In our patients with corneal scarring, 47% were treated with PK and 47% were treated with DALK. Similar proportions were found for keratoconus patients. For both of these conditions, PK was performed equally as or more often. Studies have reported increased frequency of DALK between 2001 and 2010.8,21 DALK has been found to have visual and refractive outcomes comparable to PK; however, data on long-term graft survival are variable.16,22,23 Use of one technique over the other is dependent on the disease severity and presence of risk factors, and experts agree that DALK is the preferred treatment for keratoconus unless other factors such as deep scarring are involved.24 We found that more partial-thickness transplants, specifically DSAEK and DMEK, were performed in older patients compared with full-thickness transplants. Fullthickness transplants were performed for corneal scarring and infection, which may occur across a spectrum of ages. The increasing frequency of partial-thickness techniques performed for corneal endothelial diseases like Fuchs’ dystrophy helps to explain the older demographic, given that Fuchs’ dystrophy is not typically symptomatic until the sixth decade of life. Among partial-thickness transplant patients, DSAEK and DMEK patients’ had a higher age
Fig. 4 — Procedures performed for Fuchs’ dystrophy (A), bullous keratopathy (B), and graft failure (C). Descemet’s stripping automated endothelial keratoplasty (DSAEK) was the most common procedure in Fuchs’ dystrophy and bullous keratopathy, whereas penetrating keratoplasty (PK) was the most common for graft failure. CAN J OPHTHALMOL — VOL. 52, NO. 1, FEBRUARY 2017
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Corneal transplants at the university of toronto—Le et al. (70s) compared with DALK patients, with the average age found to be 47.4 ⫾ 16 years (Table 1). DALK was indicated commonly to treat keratoconus and consistent with expected onset in the 20s, taking 10 to 20 years to progress to a surgical stage.25 Although published data regarding current corneal transplant indications and types in major centres are limited, data from the 2000 to 2010 period from Scotland,1 New Zealand,2 Australia,22 the United Kingdom,5 Iran,6 and Germany26 found that keratoconus was a leading indication, and as high as 41% of total transplants. Hungary19 and Colombia4 reported bullous keratopathy to be the most common cause. In China, the leading cause was infectious keratitis,3 whereas in Canada, pseudophakic corneal edema was dominant from 2000 to 2009.21 These differences reflect diverse demographics and local pathologies and may change with future treatment advances. Our study found Fuchs’ dystrophy as a leading indication for corneal transplant (25%), and Canadian data from 2010 to 2012 reported Fuchs’ dystrophy emerging as a major cause.8,9,27 Improvements in cataract surgical techniques have likely reduced the cases of pseudophakic corneal edema, coincident with the widespread adoption of partial-thickness procedures for Fuchs’ dystrophy. Bullous keratopathy (21%), graft failure (17%), and keratoconus (12%) were all important indications for corneal grafts. Most graft failures were treated with PK (68%). The cause of graft failure is an important consideration in patients undergoing surgery, and as endothelial cell loss is a common reason for graft failure, partial-thickness procedures may be more beneficial.28–30 Studies have shown that after an initial failed PK, repeat PK and DSAEK have similar graft survival rates and visual outcomes.31–34 DSAEK has been shown to result in less endothelial cell loss compared with PK.11 Long-term graft survival data show that endothelial keratoplasty procedures may be superior in regrafts, with 5-year survival rates of 86% for endothelial keratoplasty and 51% for PK.30,32 Attempts to reduce graft failure rates by increasing graft size may reduce endothelial cell loss but lead to irregularity of graft surface, among other problems.35 In cases of graft failure due to neovascularization, inflammation, or infection, many layers may be affected. For these challenging patients, partial-thickness procedures are less likely to be sufficient. Despite PK as the treatment choice for these graft failure patients, a high-risk graft bed contributes to high rates of failure in subsequent transplant procedures.36 Future improved ability to categorize the graft bed by risk and medical interventions may help address cases at higher risk of failure.37,38 Long-term survival studies of partial-thickness procedures are needed to determine whether this approach will affect the need for regrafting.
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Current practice at the KEI, University of Toronto, indicates that almost two-thirds of all corneal transplants performed are partial-thickness transplants. Fuchs’ dystrophy, bullous keratopathy, and graft failure are the most common reasons for corneal transplantation. Most Fuchs’ dystrophy and bullous keratopathy are treated with partial-thickness procedures. Full-thickness transplants remain the preferred choice for graft failure. Longitudinal data and further research are needed to determine whether longer graft survival and higher success rates with partial-thickness transplants will reduce the demand for corneal transplants due to graft failure.
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Footnotes and Disclosure: a
Ryan Le and Narain Yucel contributed equally to this work and should be considered joint first authors. The authors have no proprietary or commercial interest in any materials discussed in this article. The authors would like to acknowledge the Dorothy Pitts Chair and the Thor and Nicky Eaton Fund. From the *Keenan Research Centre for Biomedical Science at the Li Ka Shing Knowledge Institute of St. Michael’s Hospital, Toronto, Ont; †Ophthalmology & Vision Sciences, St. Michael’s Hospital, University of Toronto, Toronto, Ont; ‡Laboratory Medicine & Pathobiology, St. Michael’s Hospital, University of Toronto, Toronto, Ont; §Ophthalmic Pathology Laboratory, University of Toronto, Toronto, Ont. Originally received Dec. 18, 2015. Final revision Jun. 7, 2016. Accepted Jul. 6, 2016. Correspondence to Neeru Gupta, MD, PhD, MBA, St. Michael’s Hospital, 30 Bond Street, Cardinal Carter Wing, 8-072, Toronto, Ont. M5B 1W8; [email protected]
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