Visual Outcomes following Descemet Stripping Automated Endothelial Keratoplasty for Corneal Endothelial Dysfunction

Abstract

Objective

To assess objective and subjective visual outcomes achieved by patients with corneal endothelial dysfunction who have undergone surgical treatment with Descemet stripping automated endothelial keratoplasty (DSAEK).

Methods

A total of 40 eyes of 36 patients with corneal endothelial dysfunction underwent DSAEK. All were followed up for 1 year. Visual acuity (VA; logMAR), mean endothelial cell density (MCD; via noncontact specular microscopy), and topography assessment were performed at baseline (preoperatively). Visual acuity and topography measurement were repeated at postoperative year 1. Subjective assessment of visual quality was evaluated using the National Eye Institute Visual Function Questionnaire (NEI-VFQ).

Results

Preoperative best-corrected VA (BCVA) was 1.29 ± 0.53 logMAR with mean optical correction of -0.33 ± 1.74 D. Postoperative BCVA, assessed after a mean of 10.8 ± 2.1 months, showed mean line gain of 7.11 ± 4.8 logMAR, with optical correction of +1.17 ± 1.54 D. Mean 6-month postoperative pachymetry was 598.2 ± 72.3 µm. Three patients experienced premature graft detachment, requiring repositioning via injection of a sterile air bubble. No other adverse events were observed. Significant improvement (p<.05 for all) in general, near, and far vision, ocular pain, difficulty in carrying out daily tasks, dependency, social life, and mental health were reflected by NEI-VFQ scores at 10.4 ± 2.1 months postoperatively versus preoperatively. No significant correlation was noted between postoperative VA line gain and NEI-VFQ-25 questionnaire score (p>0.05).

Conclusions

Descemet stripping automated endothelial keratoplasty treatment may restore corneal clarity, improve VA, and increase vision-related quality of life in patients with advanced endothelial dysfunction. Further large-scale study is needed to corroborate these findings.

Keywords

Bullous keratopathy Descemet stripping automated endothelial keratoplasty Endothelial dysfunction Fuchs dystrophy National Eye Institute Visual Function Questionnaire Subjective visual outcomes

Introduction

The current success of endothelial keratoplasty is attributable to the pioneering work of Melles et al (1), who introduced the concept of posterior lamellar keratoplasty through a posterior approach. This technique was made popular by Terry and Ousley (2) in 2001, when it was given the name deep lamellar endothelial keratoplasty. In 2004, Melles et al (3) simplified the technique by removing the Descemet membrane from the recipient cornea, in a procedure called Descemet stripping endothelial keratoplasty. Gorovoy (4) further improved the technique in 2006, with the use of a microkeratome. This updated technique was renamed Descemet stripping automated endothelial keratoplasty (DSAEK). In 2006, Melles et al (5) further developed posterior lamellar grafting by introducing the Descemet membrane endothelial keratoplasty (DMEK) technique, which has since become the gold standard technique (6–7–8), providing better postoperative visual results than DSAEK (9–10–11). In recent years, DSAEK techniques have evolved, favoring increasingly thinner and finer grafts, known as ultrathin DSAEK (UT DSAEK), with the aim of obtaining better visual results similar to those obtained with DMEK (12, 13).

Endothelial keratoplasty is now the most common surgical procedure used to treat endothelial dysfunction. Over the last decade, DSAEK has increased in popularity and was the most common (50%) type of corneal transplantation performed in the United States in 2014 (14). While surgical success of DSAEK is conventionally based on anatomical results and visual acuity (VA) gains, these criteria do not necessarily correlate with a patient's performance of daily activities (15, 16).

The current study focused on assessing both objective and subjective visual quality outcomes following DSAEK.

Methods

The study included 40 DSAEK procedures performed on 36 patients with corneal endothelial dysfunction. Approval was obtained from the local ethics committee and all procedures were carried out in accordance with the guidelines of the Declaration of Helsinki. Written informed consent was obtained from all study participants. Inclusion criteria were age at least 18 years, clinical eligibility for DSAEK (with the majority of patients presenting with either Fuchs’ dystrophy or bullous keratopathy), successful completion of DSAEK procedure, postoperative follow-up of at least 1 year, clear cornea, ability to respond to the questionnaire, and provision of written and informed consent to participate in the study. Patients with clinical edematous cornea, significant stromal opacity, major disturbances of ocular surface, or previous corneal surgery were excluded.

Surgical Procedure

Patients underwent DSAEK under local anesthetic and following the standardized technique described by Busin and Bhatt (17). The unprepared grafts required for the procedure were provided by the tissue bank and delivered in a deturgescence and shipment media (Corneajet^®, ref EYEJET00-1O; Eurobio, Les Ulis, France). Each graft was thinned on an artificial chamber (Moria single-use artificial chamber, ref 19182; Moria SA, Antony, France) using a microkeratome (CBm turbine; Moria SA) to obtain a posterior endothelial lamellar graft (thickness 100 to 150 µm). The graft was then trephined to produce an 8-mm diameter section using Hanna punch (One^®; Moria SA). After marking the epithelium with an 8-mm marker, the patient's endothelial Descemet membrane was removed under air using an inverted hook (single-use Price hook #17302; Moria SA). Another incision was made opposite the initial one, and 23-G forceps (single-use Busin forceps 23 G #17301; Moria SA) were introduced through this incision. While remaining under constant irrigation, the graft was carefully placed on a Busin spatula (single-use Busin Spatula #17300; Moria SA) before introduction into the anterior chamber using the Busin forceps. The graft was positioned centrally on the posterior surface of the recipient cornea via the rebubbling procedure, which was performed with intracameral air injection. Corneal sutures were made using nylon thread 10/0 and all patients were told to adopt a supine position for the first 12 hours after surgery.

Clinical data

Visual acuity was scored with reference to the logarithm of the minimum angle of resolution (logMAR) and its variation in line gain. Objective refraction was measured using the autorefractometer Visionix L67 (Luneau SAS; Chartres, France) with the spherical equivalent. Endothelial cell density was evaluated via noncontact specular microscopy (Nidek CEM-530, Aichi, Japan). Topographic data were collected using the Schwind Sirius system (Schwind Eye-Tech-Solutions GmbH & Co.; Kleinostheim, Germany).

Corneal aberrations assessment

The rotating Scheimpflug camera scanning system (Schwind Sirius) was used to assess higher order aberrations (HOAs) of the anterior and posterior corneal surfaces at 4 mm and 6 mm optical zones. These measurements were taken 11.2 ± 3.6 months after surgery and at least 3 months after removal of the sutures. Pachymetric maps of the recipient eyes were also analyzed for central corneal thickness and decentralization of the thinnest point.

Vision-related quality of life (QoL) questionnaire

Patients’ visual quality was self-evaluated using the National Eye Institute Visual Function Questionnaire (NEI-VFQ). The French language short version of NEI-VHQ-25 was used. This version consists of 25 items focused on general health and 11 subscales relating to vision: general vision, difficulty with near vision activities and far vision activities, peripheral vision, color vision, ocular discomfort, driving, impact on social interactions, mental health, difficulty with day-to-day tasks, and dependence on others. The questionnaire was submitted to 36 patients during consultations or by telephone. The first assessment was carried out preoperatively and the second 10.4 ± 2.1 months after surgery. Responses to each item were converted to a scale of 0 to 100, and regrouped according to subscale using the questionnaire instructions for statistical analysis.

Statistical Analysis

Statistical analyses were carried out using SAS software (version 9.1, SAS Inc., Cary, North Carolina, USA). Correlations were assessed using Pearson correlation coefficient. A p value of less than 0.05 was considered statistically significant. The Wilcoxon signed rank test was used to determine statistical significance of changes in visual-related QoL scores (overall scores before and after surgery, as well as scores for each of the 12 subscales). Each question had a yes/no answer or was given a score of 3, 4, 5, or 6 points. The score for each item was converted to a scale of 0 to 100 and an average score per section was determined.

Results

As shown in Table I, 36 patients with a mean age of 73 ± 8.9 years (mean ± SD) were included in the study. The best-corrected VA (BCVA) before surgery was 1.29 ± 0.53 logMAR with a mean optical correction of -0.33 ± 1.74 D. Indications for surgery included Fuchs dystrophy in 18 patients (50%), pseudophakic bullous keratopathy in 10 patients (27.8%), and anterior transplant failure (DSAEK) in 8 patients (22.2%). Lens status was posterior chamber pseudophakia in 28 patients (77.8%), anterior chamber pseudophakia in 4 patients (11.1%), aphakia in 2 patients (5.5%) and phakia in 2 patients (5.5%). Preoperative mean endothelial cell density (MCD) was 546 ± 189 cells/mm² and mean central pachymetry was 674.4 ± 52.9 μm. The MCD findings were obtained from only 19 participants because 17 patients had noninterpretable and nonquantifiable measurements (very low number of cells obtained per mm²). Mean 6-month postoperative pachymetry was 598.2 ± 72.3 μm.

TABLE I

Demographic parameters

	Mean	SD
No.	36
Sex ratio	0.44
Age, y	73	8.9
Visual acuity, logMAR	1.29	0.53
Optical correction, D, SE	-0.33	1.64
Indications for transplant
Fuchs dystrophy	18
Pseudophakic bullous keratopathy	10
Anterior graft failure	8
Central pachymetry, μm	674.4	52.9
Lens status
Phakic	2
Pseudophakic posterior chamber implant	28
Pseudophakic anterior chamber implant	4
Aphakic	2
Endothelial cell density	546	189
Graft
Donor age, y	68	13
Endothelial cell density of the graft	2240	177
Final graft thickness, μm	161	29.8

The mean preoperative corneal graft MCD was 2,240 ± 177 cells per mm² and the mean donor age was 68 ± 13 years. Mean graft thickness prior to implant into the recipient eye was 161 ± 30 μm, as measured via ultrasound during surgery. No adverse postoperative events were observed among 33 patients (91.7%). The remaining 3 patients (8.3%) experienced premature detachment of the graft, which required a second injection of sterile air bubble to permanently reposition the graft. Postoperative VA was assessed after a mean of 10.8 ± 2.1 months, at which time, a mean line gain of 7.11 ± 4.8 logMAR was observed with an optical correction of +1.17 ± 1.54 D. No significant correlation was seen between graft thickness and postoperative gain in VA (Pearson correlation coefficient 0.29).

The mean total, anterior, and posterior corneal HOA in the central areas at 4 and 6 mm are shown in Table II. The Root Mean Square (RMS) at 4 mm was 1.59 ± 1.17 μm, 1 ± 0.9 μm, and 1.22 ± 1.12 μm for the full cornea, anterior, and posterior corneal surfaces, respectively. Similar results were obtained at 6 mm, with 1.84 ± 1.02 mm, 1.54 ± 1.32 mm, and 1.36 ± 1.45 mm, respectively, for the total cornea and the anterior and posterior surfaces. The most important subgroups of aberrations seen were trefoils, comas, and quadrifoils at either 4 or 6 mm and regardless of the part of the cornea examined.

TABLE II

Total, anterior, and posterior aberrations in the central regions at 4 and 6 mm

	Total cornea		Anterior surface		Posterior surface
	Mean	SD	Mean	SD	Mean	SD
4 mm
Total HOA	1.59	1.17	1	0.9	1.22	1.12
Trefoil	0.94	0.82	0.59	0.56	0.63	0.7
Coma	0.61	0.83	0.43	0.31	0.45	0.41
Quadrifoil	0.46	0.51	0.35	0.45	0.38	0.38
Astigmatism II	0.35	0.33	0.2	0.22	0.27	0.29
Spherical aberration	0.26	0.33	0.12	0.23	0.14	0.31
Pentafoil	0.33	0.4	0.21	0.31	0.28	0.39
Trefoil II	0.27	0.23	0.12	0.11	0.24	0.23
Coma II	0.21	0.27	0.1	0.1	0.19	0.28
6 mm
Total HOA	1.81	1.02	1.54	1.32	1.36	1.45
Trefoil	1.04	0.67	0.88	0.69	0.53	0.44
Coma	0.77	0.33	0.7	0.94	0.63	0.98
Quadrifoil	0.58	0.55	0.46	0.48	0.53	0.4
Astigmatism II	0.37	0.27	0.31	0.23	0.32	0.34
Spherical aberration	0.33	0.43	0.03	0.62	0.29	0.6
Pentafoil	0.37	0.33	0.26	0.19	0.27	0.32
Trefoil II	0.27	0.22	0.16	0.12	0.24	0.28
Coma II	0.27	0.2	0.21	0.2	0.28	0.33

HOA = higher order aberration.

The subgroups for total, anterior, and posterior corneal HOA in the central regions at 4 and 6 mm are shown in Table II. Each subgroup corresponds to a Zernicke polynomial: trefoil = Z³₃, coma = Z³₁, quadrifoil = Z⁴₄, astigmatism II = Z²₄, spherical aberration = Z⁰₄, pentafoil = Z⁶₀, trefoil II = Z⁵₃, and coma II = Z⁵₁. Various statistical correlations between line gain and HOA in different subgroups were assessed. As shown in Table III, significant correlations (p<.05%) were as follows: RMS total at 4 mm (r = 0.38), posterior RMS at 4 mm (r = 0.40), and quadrifoils at 4 mm (r = 0.37). A negative correlation was also observed between decentralization of the thinnest point (on the pachymetric map) and the line gain (r = 0.29) (p>0.05).

TABLE III

Significant correlations between line gain at 12 months and higher order aberrations

Correlation line gain at M12/RMS	Mean	SD	Pearson correlation coefficient	p
RMS total 4 mm	1.59	1.17	0.38	0.0401
RMS anterior 4 mm	1.05	0.87	0.26	0.1715
RMS posterior 4 mm	1.22	1.12	0.40	0.0298
Trefoil 4 mm	0.6	0.70	0.34	0.0672
Coma 4 mm	0.45	0.41	0.32	0.0904
Quadrifoil 4 mm	0.38	0.38	0.37	0.0482
Astigmatism II 4 mm	0.27	0.29	0.27	0.1566
Spherical aberration 4 mm	0.14	0.31	0.25	0.183
Pentafoil 4 mm	0.28	0.39	0.28	0.1481
Trefoil II 4 mm	0.24	0.23	0.33	0.0779
Coma II 4 mm	0.19	0.28	0.33	0.0772
RMS total 6 mm	1.81	1.02	0.23	0.226

RMS = Root Mean Square.

Table IV shows the change in overall score and the different aspects of NEI-VFQ-25 before and after surgery. Significant differences were observed for overall score (p<.05) and the following aspects of the questionnaire (p<.05 for all): general vision, near vision, far vision, ocular pain, difficulty in day-to-day tasks, dependency, social life, and mental health. No significant differences were noted for aspects involving overall health (p>0.05), driving (p>0.05), color vision (p>0.05), or peripheral vision (p>0.05). Likewise, no significant correlation was seen between VA line gain and variation in NEI-VFQ-25 questionnaire score (p>0.05).

TABLE IV

Comparison of QoL before and after DSAEK using the NEI-VFQ-25 questionnaire

	No.	Before		After		p value^a
	No.	Mean	SD	Mean	SD	p value^a
Global	36	64.5	5.2	75.8	7.1	<.0001
General health	36	54.9	11.7	56.3	12.5	0.5
General vision	36	43.3	10.1	56.9	12.8	<.0001
Near vision	36	44.7	8.7	58.1	13.4	<.0001
Far vision	36	45.1	9.4	66.4	12.2	<.0001
Driving	5	50.0	8.8	67.5	6.8	0.06
Ocular discomfort	36	64.9	13.3	86.8	12.7	<.0001
Task difficulties	36	54.5	10.8	71.1	12.5	<.0001
Dependency	36	55.3	9.6	69.6	12.2	<.0001
Social function	36	68.1	9.2	75.3	13.1	<.0001
Mental health	36	73.3	9.4	76.4	8.3	0.04
Color vision	36	98.6	5.8	99.3	4.2	1.0
Peripheral vision	36	100.0	0.0	100.0	0.0	–

DSAEK = Descemet stripping automated endothelial keratoplasty; NEI-VFQ-25 = National Eye Institute Visual Function Questionnaire; QoL = quality of life.

Wilcoxon signed rank test for nonparametric samples.

Discussion

Descemet stripping automated endothelial keratoplasty is a recognized treatment of corneal endothelial dysfunction. It involves the transplantation of the posterior layers of cornea from a donor eye into a recipient eye. Studies assessing the efficacy of this procedure report improved VA outcomes similar to the mean VA gain of 7.11 ± 4.8 logMAR observed in the current study. Specifically, the study by Chen et al (18) of endothelial keratoplasty outcomes reported a postoperative VA gain of at least 4 lines. In the current study, the effect of VA was measured in terms of lines gained rather than final BCVA because 13 patients (44.4%) had at least one associated ophthalmic pathology likely to affect VA (macular disorders, glaucoma, amblyopia).

The gain seen in VA was concomitant with a modification of the objective refraction, with DSAEK inducing hypermetropia of approximately 1 D among the participants. This phenomenon has been described previously in a meta-analysis by Lee et al (19), in which a mean induced hyperopia of 1.1 D (0.7-1.5 D) was observed, and in a study by Koenig et al (20), where induced hyperopia of 1.19 ± 1.32 D occurred. These values are close to those documented in the current study. Dupps et al (21) explained the phenomenon as the result of nonuniformity of the graft profile, which occurs when the lens is thicker at the periphery compared to the center. In a study of elevation topography, Scorcia et al (22) explained that this difference in thickness between the center and the edges of the graft results in a change in the posterior curvature that causes a hyperopic shift. They also noted that this development of hypermetropia has a tendency to decrease over time.

While patients with various disease etiologies, namely Fuchs dystrophy, pseudophakic bulbous keratopathy, and anterior graft failure, were included in the study, analysis of outcomes was not performed in relation to these disease subgroups. We acknowledge that this is a potential study limitation, as analyzing the data in this manner may have provided some insight into the correlation between DSAEK outcomes and cause of endothelial dysfunction. However, given the small study group size, and even smaller etiology-based subgroup sizes, any findings made could not have been taken as conclusive. As such, larger-scale studies designed specifically to assess DSAEK outcomes according to endothelial dysfunction cause are needed and are better placed for this type of evaluation.

In the current study, the main postoperative complication observed was partial or total graft detachment; however, the 8.3% rate of detachment observed was lower than the 14.5% rate reported by Lee et al (19). The detachment typically occurred within 1 week after surgery and was remedied using a second intracameral injection of sterile air bubble to achieve permanent fixation of the graft.

No correlation was seen between graft thickness and gain in VA in the current study, a result consistent with Terry et al (23), who also found no correlation when grafts of typical thicknesses (100-200 μm) were used. In contrast, Dickman et al (24) reported a correlation between VA and graft thickness, but only in patients with no other ocular pathologies.

A study by Rudolph et al (25), which presents HOA results for eyes that have not undergone surgery, suggests that HOAs occurred more frequently in the current study compared with healthy surgery-free eyes. Specifically, total corneal RMS at 4 and 6 mm were 0.763 ± 0.573 μm and 0.605 ± 0.347 μm, respectively. These findings are consistent with the results of Yamaguchi et al (26), Seery et al (27), and Chamberlain et al (28), which all show greater HOA in eyes that have undergone DSAEK compared with healthy eyes. The impact of these HOA on the VA of patients who have undergone DSAEK was low in the current study (weak correlations [r<.5]). This is consistent with findings from studies by Seery et al (27) and Chamberlain et al (28), which also revealed a weak relationship between HOA and VA. Moreover, the correlation between HOA and the gain in VA is difficult to define because the latter is dependent on associated ocular pathologies. Some previous studies have demonstrated that spherical and coma aberrations have the most impact on visual quality (29, 30). In our study, the main aberration subgroup observed was trefoil, which may explain why the HOAs seen appeared to have less impact on vision.

Published literature has shown that better visual results are achieved with DMEK than DSAEK (9–10–11). Busin et al (12) suggest that the evolution of DSAEK towards ultrathin DSAEK may further improve its outcomes, making them more similar to those achieved with DMEK. Endothelial graft outcomes are traditionally evaluated using conventional measures such as corrected final VA, final corneal transparency, final corneal thickness, graft thickness, keratometry, and interface disorders (13). Although these parameters are useful, they do not always reflect the ability of a patient to carry out day-to-day tasks (15, 16). Furthermore, a surgeon's definition of success does not always match what the patient perceives. Even with a clear cornea and good far VA, some patients are still dissatisfied with their vision and the limitations it imposes on their daily activities. Conversely, some patients who gain only a modest degree of VA might be satisfied with the surgery and perceive a subjective improvement in vision (16). Often, these observations can be attributed to different expectations (realistic or not), inadequate preoperative consultation, fluctuating capacity to adapt, or a combination of these factors (15, 31).

For this reason and with growing interest in vision-related QoL, new questionnaires have been developed over the last couple of decades. In the current study, the NEI-VFQ-25 questionnaire was used to assess vision-related QoL because it is reliable, available in French (32), and has already been used for various ocular disorders (33, 34).

The patients included in the present study had primary or secondary endothelial decompensation, with the latter involving stromal edema. Stromal edema results in a sense of reduced VA that is not distressing, sometimes including photophobia, a feeling of being veiled, and halos around bright lights. In advanced stages, bubbles appear beneath the epithelial layer, occasionally with pain, tearing, blepharospasm, and even rupture. Surgery significantly improved all the subgroups explored by the questionnaire, except for general health, ability to drive, mental health, color vision, and peripheral vision. These results corroborate those recently published by Puri et al (35), who used the VF-14 questionnaire and also reported improved QoL among patients older than 65 years who had undergone DSAEK. In terms of evaluating general health, systemic diseases and comorbidities can affect the NEI-VFQ-25 score. To limit this effect, study subgroups should be set up to take nonocular disease into account. However, the small sample size of the current study did not permit this. Even for patients with related ophthalmic disorders, the number of patients limited the creation of subgroups. No significant difference in preoperative versus postoperative driving ability was observed in the current study. Of note, there was a small number of patients in the study group who were drivers (n = 5), most likely owing to the age of the patients and the presence of general disorders that make driving difficult. Color and peripheral vision are not greatly affected by endothelial decompensation, which explains why no significant differences in these aspects were seen before versus after surgery.

Over the last decade, DSAEK, UT DSAEK, and DMEK have become accepted treatments for endothelial decompensation. Findings from the current study show that eyes treated with this intervention experience significant improvement in VA, exhibit restored corneal clarity, and have increased corneal HOA. However, these aberrations show weak correlation with the significant gain in VA seen postoperatively. Descemet stripping automated endothelial keratoplasty, UT DSAEK, and DMEK also appear to significantly improve vision-related QoL in patients with advanced endothelial dysfunction.

Footnotes

Financial support: No financial support was received for this submission.

Conflict of interest: None of the authors has conflict of interest with this submission.

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