Endothelial Keratoplasty After Failed Penetrating Keratoplasty: An Alternative to Repeat Penetrating Keratoplasty MARCUS ANG, HENRIETTA HO, CHEEWAI WONG, HLA MYINT HTOON, JODHBIR S. MEHTA, AND DONALD TAN  PURPOSE:

To analyze graft survival of endothelial keratoplasty (EK) under a previous failed penetrating keratoplasty (PK) compared to repeat PK.  DESIGN: Retrospective, comparative case series.  METHODS: Analysis involved consecutive patients who underwent either a repeat PK or EK under PK, after failed PK, whose primary surgical indication was pseudophakic bullous keratopathy at a single tertiary center. Clinical data and donor and recipient characteristics were recorded from our prospective cohort from the Singapore Corneal Transplant Study. Main outcome measure was graft survival up to 5 years follow-up.  RESULTS: We included a total of 113 eyes that underwent a repeat PK (n [ 81) or EK under a failed PK (n [ 32). Cumulative graft survival probabilities comparing repeat PK with EK under PK were at 91.9% vs 96.2% (1 year), 82.6% vs 91.6% (2 years), 66.8% vs 86.4% (3 years), and 51.3% vs 86.4% up to 5 years follow-up, respectively (log-rank P value [ .013). Multivariate Cox regression analysis was performed, which adjusted for: age, sex, risk factors for graft failure (corneal neovascularization, ocular surface disease, glaucoma, active corneal inflammation, anterior synechiae), donor endothelial cell count, and repeat donor size. Repeat PK was a significant risk factor for graft failure compared to performing an EK under PK (hazard ratio: 10.17; 95% CI 1.10–93.63; P [ .041).  CONCLUSION: In our study of eyes with bullous keratopathy, endothelial keratoplasty under a previously failed PK provided better graft survival outcomes than repeat PK, adjusting for potential confounders and risk factors for graft failure. (Am J Ophthalmol 2014;158: 1221–1227. Ó 2014 by Elsevier Inc. All rights reserved.)







replacing penetrating keratoplasty (PK) for the treatment of endothelial disease leading to corneal

Accepted for publication Aug 15, 2014. From Singapore National Eye Centre (M.A., H.H., C.W., J.S.M., D.T.); Singapore Eye Research Institute (M.A., C.W., H.M.H., J.S.M., D.T.); Department of Ophthalmology, National University Health System (D.T.); Department of Clinical Sciences, Duke-National University of Singapore Graduate Medical School (J.S.M.); and Lee Kong Chian School of Medicine, Nanyang Technological University (D.T.), Singapore. Inquiries to Prof Donald Tan, Singapore National Eye Centre, 11 Third Hospital Avenue, Singapore 168751; e-mail: [email protected] 0002-9394/$36.00 http://dx.doi.org/10.1016/j.ajo.2014.08.024


2014 BY

decompensation.1–3 The main advantages of EK over PK include rapid postoperative visual rehabilitation and less allograft rejection.3–8 Despite these advantages, most studies have suggested that graft survival between PK and EK are actually similar (though few have been direct comparative studies).9 Nonetheless, after a failed primary PK, a surgeon may now choose to selectively replace the endothelium by performing an EK under the existing PK, instead of the traditional repeat PK, which has been shown to have poor long-term survival rates of 21%–70%.10–18 As EK has been shown to potentially have a lower rejection risk compared to PK, one advantage of performing EK over PK would be the potential for a reduced risk of rejection, as compared to a repeat PK.19,20 Initial studies have found graft survival rates of EK under a failed PK to be around 55%–100% at 1 year.21–23 However, many of these studies were noncomparative case series, with a limited follow-up period.21,23–27 Of the few studies that examined long-term graft survival, Anshu and associates found a graft survival rate of 74% at 4 years (up to 96% in a subgroup of patients without previous glaucoma shunt surgery).22 Kitzmann and associates found a trend toward better 3-year graft survival in 7 eyes that underwent EK compared to 17 eyes that had a repeat PK (57.9% vs 68.6%, P ¼ .507), although this result was not statistically significant (likely owing to the small sample size).23 In addition, the authors found no statistically significant differences in postoperative best-corrected visual acuity (BCVA) between the 2 groups at 1, 2, or 3 years,23 although others have reported significant improvements in postoperative BCVA in EK after failed PK.22,24,26,27 To date, there are no studies that have conclusively shown better outcomes for EK after failed PK, compared to repeat PK. Without a direct comparative study (with an adequate sample size) from the same cohort, we are unable to support or refute claims that EK after a failed PK is indeed a useful alternative to performing a repeat PK.22 Therefore, we conducted this current study to better clarify the graft survival rates after repeat PK compared to EK after the first failed PK.


prospective cohort study that tracks and records all clinical




data, surgical complications, and outcomes in patients who undergo corneal transplants at the Singapore National Eye Center (SNEC).28 For this study, we included consecutive patients who first underwent PK for pseudophakic bullous keratopathy (PBK) at the SNEC from January 1, 1991 to December 31, 2008, and subsequently underwent either EK or a PK, after the first PK suffered from graft failure (January 1, 1993 to December 31, 2010). All surgeries were performed by the 5 corneal surgeons at our center, which included cases performed or partially performed by corneal fellows in training under direct supervision. Our study followed the principles of the Declaration of Helsinki, with ethics approval obtained from the Singapore Health Services Centralized Institutional Review Board. We reviewed patients’ demographics, clinical features, and surgical techniques. Visual acuity (VA) was measured using the Snellen VA chart and we analyzed results using logarithm of the minimal angle of resolution (logMAR) equivalent units.29 The Singapore Eye Bank provides all donor corneas with standard internal guidelines for PK and EK grafts and we obtained all donor information from their database, including donor endothelial cell counts.28 Our main outcome measure was percent graft survival up to 5 years postoperatively. Graft failure was defined as irreversible loss of optical clarity, sufficient to compromise vision for a minimum of 3 consecutive months.30  SURGICAL TECHNIQUE: PENETRATING KERATOPLASTY:

Penetrating keratoplasties were performed using a standard technique with a Hanna vacuum trephine system (Moria Inc, Antony, France), as previously described.28 The original failed PK was either surgically removed or excised using the Hanna trephine. A 0.25- to 0.50-mm oversized donor cornea then was punched out, endothelial side up, and sutured onto the recipient with 10-0 nylon, using either an 8-bite, 100 nylon double continuous running suture or a combination of a single 8-bite 10-0 nylon continuous and 8 interrupted sutures. Intraoperative astigmatic control was achieved using a microscope-mounted keratoscope. A bandage contact lens was placed at the end of the surgery, and subconjunctival dexamethasone (0.1%) (Decadron; Merck & Co Inc, Rahway, New Jersey, USA), gentamicin (14 mg/mL) (Garamycin; Schering AG, Berlin-Wedding, Germany), and cefazolin (50 mg/mL) (Ancef; GlaxoSmithKline, Research Triangle Park, North Carolina, USA) was injected (0.1 mL of each).  SURGICAL TECHNIQUE: ENDOTHELIAL KERATOPLASTY UNDER FAILED PENETRATING KERATOPLASTY: All EK

surgeries were performed using a technique previously described, with slight modifications and no stripping of Descemet membrane.31,32 Donors were prepared by the surgeon using an automated lamellar therapeutic keratoplasty system (ALTK; Moria SA, Antony, France) and generally oversized by 0.5–1.0 mm over the original PK in order to cover the previous graft-host junction. 1222

The Tan EK forceps (ASICO, Westmont, Illinois, USA) or EndoGlide donor insertion forceps (Angiotech, Reading, Pennsylvania, USA/Network Medical Products, North Yorkshire, UK) was then used to pull the donor cornea through the scleral incision using nonfolding techniques: over either a Sheets glide (n ¼ 16, BD Visitec, New Jersey, USA)31,32 or the EndoGlide donor inserter device (n ¼ 16; Angiotech, Reading, Pennsylvania, USA/ Network Medical Products, North Yorkshire, UK).33 An inferior peripheral iridectomy was performed through a limbal stab incision in all cases. The scleral wound and anterior maintainer paracentesis incisions were secured with 10/0 nylon interrupted sutures, and a full air tamponade (8 minutes) under slight compression was achieved with a large bubble in the anterior chamber, with removal of interface fluid using venting incisions. Similarly, subconjunctival corticosteroid and antibiotic injections, as described above, completed the procedure.  POSTOPERATIVE CARE:

All patients received a standard postoperative topical antibiotic (levofloxacin 0.5%) and corticosteroid regime: 1 drop of topical prednisolone acetate 1% every 3 hours for a month, 4 times daily for 2 months, and tapered by 1 drop per 3 months down to 1 drop per day dosing by 1 year, and thereafter continued indefinitely. Bandage contact lenses were generally removed after re-epithelialization, usually 1–2 weeks after surgery. In selected cases, patients were also started on oral prednisolone 1 mg/kg, slowly tapered postoperatively over 2 months; and other systemic immunosuppression (oral mycophenolate mofetil [MMF] 2 g daily, or oral cyclosporin A [CsA]) was tapered to achieve therapeutic levels, at the discretion of the surgeons. These cases tended to be younger patients or patients deemed at relatively higher risk of allograft rejection, for example those with significant corneal vascularization, detailed in previous studies.28


Statistical analysis included descriptive statistics, where the mean and standard deviation (SD) were calculated for the continuous variables; while frequency distribution and percentages were used for categorical variables. Comparisons between categorical variables were conducted by the Pearson x2 test/Fisher exact tests and for continuous data Mann-Whitney U test to compare between repeat PK and EK under PK groups. Visual acuity (logMAR) was compared using the paired-sample t test/Wilcoxon signed rank test comparing baseline to 12 months follow-up; Kaplan-Meier survival analysis using the log-rank test was conducted to compare and determine the survival probabilities of repeat PK and EK under PK groups. The survival period of failed grafts was defined as the time between the date of surgery and recorded date of graft failure. Statistical Package for the Social Sciences version 17.0 (SPSS Inc, Chicago, Illinois, USA) was used to analyze the data. A P value _0.75 mm Reason for original PK failure Endothelial failure Graft rejection Glaucoma Infection Other




(N ¼ 113)

(N ¼ 81)

(N ¼ 32)

69.1 (12.7)

70.9 (11.7)

61 (54) 52 (46)

P Value

64.4 (14.1)


47 (58) 34 (42)

14 (43.8) 18 (56.3)


90 (79.6) 8 (7.1) 6 (5.3) 9 (8.0)

65 (80.2) 7 (8.6) 4 (4.9) 5 (6.1)

25 (78.1) 1 (3.1) 2 (6.3) 4 (12.5)


59 (16–76) 2792 (380) 8.2 (0.5)

62 (17–76) 2756 (392) 8.0 (0.4)

57 (16–76) 2922 (367) 8.6 (0.4)

40 (38.1) 15 (14.3) 23 (21.9) 27 (24.5)

34 (44.2) 14 (18.2) 18 (23.4) 11 (14.3)

6 (21.4) 1 (3.6) 5 (17.9) 16 (57.2)

70 (61.9) 27 (23.9) 5 (4.4) 6 (5.3) 5 (4.4)

45 (55.6) 22 (27.2) 4 (4.9) 6 (7.4) 4 (4.9)

25 (78.1) 5 (15.6) 1 (3.1) 0 1 (3.1)

.137 .039 21 mm Hg) Graft rejection episode Graft detachment Corneal infection Persistent epitheliopathy Resuture Wound dehiscence Herpetic keratitis Suprachoroidal hemorrhage Endophthalmitis

PK-PK (N ¼ 81) N (%)

PK-EK (N ¼ 32) N (%)

P Value

32 (39.5)

8 (25)


11 (13.6) 0 5 (6.2) 9 (11.1) 3 (3.7) 2 (2.5) 1 (1.2) 0 0

1 (3.1) 2 (6.3) 3 (9.4) 0 0 0 0 0 0

.174 .078 .685 .059 .557 .590 1.000 NA NA

EK ¼ endothelial keratoplasty; IOP ¼ intraocular pressure; NA ¼ not applicable; PK ¼ penetrating keratoplasty; PK-EK ¼ EK under PK; PK-PK ¼ repeat PK; SD ¼ standard deviation. a Complications as recorded in our prospective Singapore Cornea Transplant Study database.

decompensation from pseudophakic bullous keratopathy. Our 3-year graft survival rate for EK under PK was 86.4%, whereas other EK under PK studies reported 69%– 81%,14,23 and 21%–70% for repeat PK.10–18 Of note, graft rejection episodes were more common in the repeat PK group compared to the EK under PK group, albeit nonsignificant, likely owing to the small sample size (13.6% vs 3.1%, P ¼ .174)—despite having no significant differences in immunosuppression regime.20 Nonetheless, further studies with larger numbers could certainly show a lower risk of rejection, consistent with the evidence from studies that show that a primary EK has a lower risk of endothelial rejection compared to a primary PK.20 In terms of visual acuity outcomes, most studies report significant improvement in BCVA after EK for failed PK.24,25,27 Anshu and associates studied 60 eyes and found an improvement in median BCVA from 1.00 logMAR preoperatively to 0.40 logMAR at 1 year (P < .0001).14 Heitor de Paula and associates reported an improvement in BCVA from 1.43 logMAR preoperatively to 0.55 logMAR at 1 year in 22 eyes (P ¼ .001).26 However, there is a lack of comparative studies to conclude if visual improvement is better in EK under a failed PK or repeat PK. Kitzmann and associates found no statistically significant differences in postoperative BCVA between the 2 groups at 1, 2, or 3 years.23 Similarly, we found significant improvement in postoperative BCVA in both groups and at 1 year, but no significant differences in BCVA at the 1 year follow-up between the repeat PK group and EK under PK group (P ¼ .185). Our graft dislocation rate (6.3%) without Descemet membrane (DM) stripping was similar to the lowest reported dislocation rates in the literature for EK under a VOL. 158, NO. 6

failed PK (Nottage and Nirankari: 6% dislocation rate without DM stripping27; Straiko and associates: 5.9% dislocation rate with DM stripping, and without any cases of PK wound dehiscence38). Clements and associates studied complications in EK under a failed PK and found the presence of a glaucoma drainage device and donor grafts that were smaller than the previous PK to be significant risk factors for graft dislocation, while DM stripping did not reduce the graft dislocation rate in their series.39 Similarly, we achieved a relatively low graft dislocation rate without stripping the DM, which can be more challenging in these patients with a failed PK, and which may also lead to inadvertent disruption of the graft-host junction. The main limitation of our study is its retrospective nature, which allows for possible selection bias. However, given the known clinical advantages of EK over PK, it would be difficult to perform a prospective randomized clinical trial; hence we conducted this nested study within our prospective cohort, as the next-best alternative. We then performed multivariate analysis to account for any confounders or differences in risk factors between comparisons and still found that EK under PK had better graft survival compared to a repeat PK. Moreover, differences in factors such as the longer time between PK and EK grafts compared to repeat PK could mean that risk factors and secondary changes such as increased scarring, anterior synechiae, and corneal vascularization would be potentially worse in the EK under PK group—which could actually further strengthen our finding that EK under PK may be a better alternative to repeat PK. Ideally, it would have been interesting to examine endothelial cell density as an outcome measure, but we did not have sufficient data for any useful analysis. We also recognize that more advanced cases of corneal decompensation with more significant stromal scarring may have been more likely to receive a repeat PK. However, we do routinely attempt EK even in severe cases of corneal decompensation after graft failure, as long as there is only moderate anterior stromal scarring present— and in any cases of significant residual stromal scarring, a deep anterior lamellar keratoplasty may be performed after the EK under PK.40 As EK was a relatively newer corneal transplantation technique at the time these cases were performed, we recognize the higher number of repeat PK performed for failed PK in our cohort and the different learning curves of our corneal surgeons. However, we already observed a significant superior graft survival among the EK under PK cases; with the learning curve removed, this would only strengthen the results of our study. In conclusion, our study suggests that in eyes with bullous keratopathy after a failed penetrating keratoplasty, endothelial keratoplasty is a better alternative to a repeat penetrating keratoplasty with superior graft survival for up to 5 years. Larger corroborative studies would be useful to confirm the improved graft survival rates and fewer postoperative complications we have observed in this study with endothelial keratoplasty in the management of regrafts.



ALL AUTHORS HAVE COMPLETED AND SUBMITTED THE ICMJE FORM FOR DISCLOSURE OF POTENTIAL CONFLICTS OF INTEREST. Financial disclosures: Donald Tan and Jodhbir S. Mehta, inventors of the EndoGlide, have financial interests in the device (AngioTech, Reading, Pennsylvania, USA/Network Medical Products, North Yorkshire, UK). Funding/support: Singapore National Research Foundation Translational & Clinical Research (TCR) Programme Grant (NMRC/TCR/002-SERI/2008-TCR 621/41/2008). Contributions of authors: design and conduct of the study (M.A., D.T., J.S.M.); collection (M.A., H.H., C.W., H.M.H., D.T., J.S.M.), management (D.T., J.S.M.), analysis (M.A., H.H., C.W., H.M.H., D.T., J.S.M.), and interpretation of the data (M.A., H.H., C.W., H.M.H., D.T., J.S.M.); and preparation of the manuscript (M.A., H.H., C.W., H.M.H., D.T., J.S.M.).

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survival after 10 years in the Cornea Donor Study. Ophthalmology 2013;120(12):2419–2427. Mitry D, Bhogal M, Patel AK, et al. Descemet stripping automated endothelial keratoplasty after failed penetrating keratoplasty: survival, rejection risk, and visual outcome. JAMA Ophthalmol 2014;132(6):742–749. Straiko MD, Terry MA, Shamie N. Descemet stripping automated endothelial keratoplasty under failed penetrating keratoplasty: a surgical strategy to minimize complications. Am J Ophthalmol 2011;151(2):233–237.e2. Clements JL, Bouchard CS, Lee WB, et al. Retrospective review of graft dislocation rate associated with descemet stripping automated endothelial keratoplasty after primary failed penetrating keratoplasty. Cornea 2011;30(4):414–418. Pang A, Mohamed-Noriega K, Chan AS, Mehta JS. Confocal microscopy findings in deep anterior lamellar keratoplasty performed after Descemet’s stripping automated endothelial keratoplasty. Clin Ophthalmol 2014;8:243–249.



Biosketch Dr Marcus Ang is currently Associate Consultant, Cornea and External Eye Diseases Service at the Singapore National Eye Center. He attained a Masters in Clinical Investigation for research at the National University of Singapore. His research interests include Cornea and Refractive surgery, Ocular inflammation and Uveitis.




Endothelial keratoplasty after failed penetrating keratoplasty: an alternative to repeat penetrating keratoplasty.

To analyze graft survival of endothelial keratoplasty (EK) under a previous failed penetrating keratoplasty (PK) compared to repeat PK...
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