Patients

The study group (DMEK after DSAEK group) of this retrospective cohort study consisted of 15 consecutive eyes from 15 patients (mean age: 67.3 ± 10.2 years, male: n = 5, female: n = 10) in which DMEK was performed for the treatment of graft failure following DSAEK using a standardized technique for graft preparation and transplantation. The indication for DSAEK was Fuchs corneal dystrophy in 14 patients (93%) and pseudophakic bullous keratopathy in 1 patient (7%). All corneas following failed DSAEK showed corneal decompensation with stromal edema. The reason for graft failure was not clear in all our patients. A presumed immunologic rejection was present in 2 eyes. All DSAEK surgeries were performed between October 2006 and December 2011, all secondary DMEK surgeries between October 6, 2009 and February 2, 2013. All surgeries (DMEK and DSAEK), which were performed in our department, were carried out by 3 experienced surgeons. The surgeons had similar learning curves and were experienced with the technique. DMEK surgeries included in this study were not among the first 75 DMEKs of each surgeon.

Our regular cohort of patients undergoing primary DMEK tends to have better values of best-corrected visual acuity (BCVA) before DMEK compared to our cohort undergoing DMEK for graft failure after DSAEK (DMEK after DSAEK group). In previous studies, patients undergoing DMEK had a preoperative BCVA between 0.6 and 0.7 logMAR (logarithm of the minimal angle of resolution); that is, BCVA was distinctly better than in the patients undergoing DMEK for failed DSAEK in the current study (1.27 ± 0.34 logMAR). Unpublished analysis of our general DMEK cohort showed a significant correlation between preoperative BCVA and BCVA 1, 3, 6, and 12 months after DMEK (n = 216, Spearman correlation coefficient 1 month: ρ 0.281, P < .001, 12 months: ρ 0.274, P = .005; Supplemental Figure , available at AJO.com ). Therefore, we compared the patients of the DMEK after DSAEK group retrospectively with 15 consecutive patients with a similarly low preoperative BCVA undergoing primary DMEK for Fuchs endothelial dystrophy.

The control group (Primary DMEK group) consisted of 15 eyes from 15 patients undergoing primary DMEK for Fuchs corneal dystrophy (mean age: 71.3 ± 10.6 years, P = .233, Mann-Whitney U ). The primary DMEK surgeries were performed between September 8, 2009 and February 27, 2013. Mean follow-up time after DMEK was 14.9 ± 10.6 months (range 1.0–31.2 months) in the DMEK after DSAEK group and 18.5 ± 9.1 months (range 1.0–30.8 months) in the Primary DMEK group ( P = .436, Mann-Whitney U ).

Donor corneas were stored in short-term culture (DMEK after DSAEK group: n = 3, primary DMEK group: n = 5) or long-term organ culture (DMEK after DSAEK group: n = 12, primary DMEK group: n = 10). DMEK grafts were prepared on the day of surgery directly prior to transplantation by the surgeon himself.

Informed consent was obtained from the patients. The study complied with the tenets of the Declaration of Helsinki and adhered to all state laws of the country. The Institutional Review Board of the University of Erlangen-Nuremberg, Germany waived the need for approval.

Surgical Technique

Graft preparation and graft transplantation for DMEK were performed as previously described in detail. The failed DSAEK grafts were removed from the stroma using an inverted hook (Price endothelial keratoplasty hook; Moria SA, Antony, France) and extracted with a forceps (DMEK after DSAEK group). In primary DMEK, the Descemet membrane of the recipient was removed in a central 9-mm area. After stripping, the graft (Descemet membrane with adherent corneal endothelial cells) spontaneously formed a roll, which was injected into the anterior chamber and positioned by repeated injections of balanced salt solution and air bubbles. At the end of the procedure, the anterior chamber was filled with an air bubble, which was reduced to 50% of the anterior chamber volume after 60 minutes.

Clinical Evaluation

The parameters analyzed in this study included BCVA, central corneal thickness (CCT) (Pentacam; Oculus, Wetzlar, Germany), and endothelial cell density (ECD) (SeaEagle; Rhine-Tec GmbH, Krefeld, Germany). The need for additional intracameral air injections after DMEK was assessed at slit-lamp examination and by the use of slit-lamp optical coherence tomography (SL-OCT; Heidelberg Engineering, Heidelberg, Germany). Examination results from the day before DMEK as well as 1, 3, 6, 12, and 18 months after grafting were analyzed.

Histologic Analysis

Removed DSAEK grafts were fixed in buffered 10% formaldehyde solution (pH 7.2), dehydrated, and embedded in paraffin. Serial sections cut at 5 μm were stained with hematoxylin-eosin and periodic acid–Schiff. Main criteria of the histologic analyses included thickness of the DSAEK graft at the thickest and thinnest part, endothelial cell count per high-power field, loss of keratocytes, and occurrence of retained Descemet membrane, retrocorneal membranes, infectious infiltrates, inflammatory cells, or melanin granules.

Transmission Electron Microscopy

For electron microscopy, 1 explanted DSAEK graft was processed according to standard protocols, as described previously. The ultrathin sections were examined with a transmission electron microscope (EM 906E; Carl Zeiss AG, Oberkochen, Germany).

Statistical Analysis

Statistical evaluation was performed using IBM SPSS software version 20.0 (SPSS, Armonk, New York, USA). Differences of samples between groups were assessed by Mann-Whitney U test. Categorical data were analyzed with χ ² test and Fisher exact test, if the expected value of each group was less than 5. Differences of parameter values within groups were assessed using the Wilcoxon test. The significance level was set at P = .05.

Visual Acuity

The average time between DSAEK and DMEK was 26 ± 17 months (range: 4–70 months). DMEK surgery was successful in all procedures. No primary graft failure occurred. Corneal edema, thickening, and opacification of the cornea improved in all patients after DMEK.

Four eyes in the DMEK after DSAEK group were excluded from the analysis of the visual acuity owing to amblyopia, ischemic optic neuropathy, macular pucker, and age-related macular degeneration. In the Primary DMEK group 4 eyes were excluded because of epithelial basement membrane dystrophy (Map-dot-fingerprint), subepithelial haze/scarring (n = 2), and a macular hole. There was no difference in the number of eyes with ocular comorbidities limiting the visual acuity in both groups (Fisher exact test, P = .659).

Mean BCVA in the DMEK after DSAEK group was 1.27 ± 0.34 before DMEK and increased significantly, to 0.43 ± 0.33 (Wilcoxon, P = .003) at 1 month and to 0.23 ± 0.21 (Wilcoxon, P = .012) at 3 months after DMEK ( Table 1 ). At the following visits 6, 12, and 18 months after DMEK, mean BCVA did not increase significantly compared to the previous visit ( P > .05). In the Primary DMEK group, mean BCVA increased significantly from 1.0 ± 0.40 before surgery to 0.32 ± 0.09 (Wilcoxon, P = .027) 1 month and to 0.29 ± 0.23 (Wilcoxon, P = .042) 3 months postoperatively ( Table 1 ). Thereafter, mean BCVA increased slightly but not significantly up to 0.10 ± 0.09 at the follow-up visit 18 months after surgery ( P > .05). Comparative analysis of mean BCVA values at baseline and at each follow-up visit showed no significant differences between both groups ( Table 1 , Figure 1 ).

Best-corrected visual acuity after Descemet membrane endothelial keratoplasty. Box plot showing best-corrected visual acuity at baseline and at 5 follow-up visits within the first 18 months after Descemet membrane endothelial keratoplasty (DMEK): comparison between the DMEK after DSAEK (Descemet stripping automated endothelial keratoplasty) group and the Primary DMEK group. The increase in visual acuity was significant in both groups between baseline (preoperatively) and the follow-up visit after 1 and 3 months, respectively. There were no significant differences in mean BCVA at each visit between both groups. Significant differences between 2 groups are marked by an asterisk.

Central Corneal Thickness

In the DMEK after DSAEK group, mean CCT decreased significantly, from 917 ± 184 μm before DMEK to 480 ± 68 μm 1 month after DMEK (Wilcoxon, P = .005), and in the Primary DMEK group from 727 ± 79 μm to 506 ± 61 μm (Wilcoxon, P = .018, Table 2 ). There was no significant difference in CCT at each follow-up visit after DMEK surgery between both groups. During the following months no significant change in mean CCT could be observed within both groups ( P > .05 between each follow-up visit, Table 2 , Figure 2 ).

Central corneal thickness after Descemet membrane endothelial keratoplasty. Box plot showing central corneal thickness at baseline and at 5 follow-up visits within the first 18 months after Descemet membrane endothelial keratoplasty (DMEK): comparison between the DMEK after DSAEK (Descemet stripping automated endothelial keratoplasty) group and the Primary DMEK group. The decrease in central corneal thickness was significant in both groups between baseline (preoperatively) and the follow-up visit 1 month after surgery. There were no significant differences in the CCT at the following visits between both groups. Significant differences between 2 groups are marked by an asterisk.

Endothelial Cell Density

Mean ECD decreased by 39%, from 2470 ± 120 cells/mm² to 1496 ± 311 cells/mm², in the DMEK after DSAEK group ( P = .005, Wilcoxon) within the first month after surgery. In the Primary DMEK group, mean ECD decreased by 45%, from 2455 ± 181 cells/mm² to 1341 ± 201 cells/mm² ( P = .043, Wilcoxon) within the first month after surgery. During the following months mean ECD did not change significantly. There was no significant difference in the endothelial cell counts between both groups at baseline and at each follow-up examination ( Table 3 , Figure 3 ).

Table 3

Endothelial Cell Density of the Donor Graft and 1, 3, 6, 12, and 18 Months After Secondary Descemet Membrane Endothelial Keratoplasty for Graft Failure Following Descemet Stripping Automated Endothelial Keratoplasty and After Primary Descemet Membrane Endothelial Keratoplasty, Respectively

Follow-up (Months After DMEK)	DMEK After DSAEK Group (Cell Count/mm² ± SD)	Primary DMEK Group (Cell Count/mm² ± SD)	P Value (Mann-Whitney U )
Donor	2470 ± 120	2455 ± 181	.683
1	1496 ± 311	1341 ± 201	.428
3	1545 ± 294	1591 ± 193	.573
6	1611 ± 265	1519 ± 272	.679
12	1393 ± 223	1499 ± 306	.536
18	1390 ± 239	1391 ± 193	1.00

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