Descemet membrane endothelial keratoplasty (DMEK) is the most anatomically selective endothelial keratoplasty technique, providing excellent visual outcomes and acceptable long-term endothelial cell densities (ECDs).1–4 When clinically significant cataract is present together with endothelial disease, then phacoemulsification may be performed either prior to or in combination with the transplantation.5–7 By performing the cataract surgery prior to graft placement, the donor graft is spared the phacoemulsification energy, free radicals, temperature changes, lens fragment collisions, and intraocular pressure changes, all known to be damaging to endothelial cells.8 In the absence of cataract, however, DMEK may be performed over the crystalline lens, in a technique known as “phakic DMEK.”9 Leaving the crystalline lens in situ can provide additional benefits, particularly in terms of preserving accommodation and avoiding any potential risks associated with clear lens extraction in younger patients and patients with myopia.10,11
We recently reported that phakic eyes with DMEK in a larger cohort had similar visual acuity outcomes and rates of re-bubbling as pseudophakic DMEK at 6 months.12 Additionally, the crystalline lens did not seem to be associated with additional surgical risks, thereby confirming the findings of other groups.13 However, two major potential long-term complications after phakic DMEK may be cataract formation and endothelial graft damage.9,14,15
The aim of this study was to examine the follow-up of a large cohort of phakic eyes with DMEK, to determine the incidence of cataract extraction and the effect of phacoemulsification surgery on ECD and graft performance.
Patients and Methods
Of 261 phakic eyes (191 patients) that underwent DMEK between October 2007 and March 2018, 35 eyes (13.4%) underwent phacoemulsification for cataract extraction after DMEK (Table 1). The majority of cases (80% and 87%, respectively) receiving phakic DMEK surgery were for Fuchs endothelial corneal dystrophy in both the study group and entire cohort.
Demographics of DMEK Recipients and Donors
Phacoemulsification was performed on average 18 ± 13 months after DMEK (median: 15 months; range: 3 to 69 months) (Table 2). The mean age of the patients proceeding to cataract surgery was 55.7 ± 11.5 years (median: 58 years), compared to the entire cohort, which was 55.7 ± 9.9 years (median: 57 years) (Table 1). Of the 261 phakic cases, 13 (5%) cases had diabetes mellitus at the time of DMEK and 2 cases (2 of 35, 5.7%) underwent phacoemulsification (Table 1). Seventy patients were included with bilateral DMEK, of whom 4 patients underwent bilateral phacoemulsification and 6 underwent unilateral phacoemulsification. The 4 patients with bilateral phacoemulsification did not have any known systemic diseases, diabetes mellitus, or glaucoma.
Clinical Outcomes for Eyes That Underwent Phacoemulsification After DMEK
DMEK graft preparation and surgery were performed as described previously.16,17 After positioning the DMEK graft against the recipient stroma, eyes were left with a complete air fill for 45 to 60 minutes. Thereafter, a partial air–balanced salt solution exchange was performed to leave the eye with 20% to 30% air fill. Postoperative topical medication included chloramphenicol 0.5% six times daily during the first week and twice daily during the second week and ketorolac tromethamine 0.4% and dexamethasone 0.1% four times daily for 4 weeks. This was followed by fluorometholone 0.1% four times daily, tapered to once daily at 1 year postoperatively, and once daily or once every other day indefinitely thereafter.
Patients who required phacoemulsification for cataract extraction after DMEK were referred to specialized centers and underwent phacoemulsification by experienced cataract surgeons (with a past experience of at least 1,000 cases). The ECD before and after phacoemulsification, corrected distance visual acuity (CDVA), subjective refractive outcomes, and corneal pachymetry were measured using non-contact autofocus specular microscopy (Topcon SP3000p; Topcon Medical Europe BV), Snellen visual acuity chart, and Scheimpflug imaging (Pentacam HR; Oculus Optikgeräte GmbH), respectively. Four eyes were excluded from clinical outcome analysis due to missing data before and/or after phacoemulsification, thereby precluding analysis. All patients had signed an informed consent and the study adhered to the tenets of the Declaration of Helsinki. No internal review board or ethics committee approval was required due to the retrospective nature of the study.
Continuous variables were reported as mean with range, and categorical variables as numbers with percentages. Continuous variables were assessed for normality by histograms and by skewness estimate with its standard error. If the standard error of skewness was double its estimate, the variables were considered skewed and were transformed into a logarithmic scale for further analysis. Continuous variables were analyzed using the t test and categorical variables using the chi-square test. The probability of requiring a cataract extraction after phakic DMEK was assessed by Kaplan-Meier survival analysis, using the log-rank test, and was presented as cumulative survival probability. Changes in ECD were analyzed as repeated measurements by linear mixed models with Bonferroni correction for multiple testing. P values of .05 were considered as statistically significant. All analyses were performed using IBM SPSS Statistics software, version 25 (IBM Corporation).
Of the 261 phakic eyes with DMEK with an average follow-up time of 51.6 ± 34 months (median: 51 months), 35 eyes (13.4%) of 29 patients underwent phacoemulsification. Although the majority of cases received phakic DMEK surgery for Fuchs endothelial corneal dystrophy, bullous keratopathy secondary to anterior chamber phakic lenses accounted for 8% (n = 22) of the entire cohort but 17% (n = 6) of the phacoemulsification group (P = .001).
The probability of cataract extraction after DMEK for the whole cohort was 0.06 (95% CI: 0.03 to 0.07) at 1 year and 0.17 (95% CI: 0.12 to 0.22) at 10 years after DMEK. No differences were seen in the probability of requiring a cataract extraction between patients younger than 57 years and patients 57 years or older (P = .10), where 57 years was the median age of the entire cohort (Figure 1)
Kaplan-Meier curve of cumulative probabilities for cataract extraction after phakic Descemet membrane endothelial keratoplasty (DMEK). Kaplan-Meier curves are shown for the entire group of phakic eyes with DMEK and for the group of phakic eyes divided into two age-based subgroups, according to the median age of the whole cohort (< 57 years and ⩾ 57 years at time-point of DMEK surgery). Cumulative probability did not differ between the two age subgroups (P = .15). Cumulative probabilities and number of eyes at risk per follow-up moments are presented in the table below the graph. Cumul = cumulative; SE = standard error
For the 31 eyes (29 patients) available for clinical outcome analysis, the mean follow-up time after phacoemulsification was 37.9 ± 27 months (range: 1 to 119 months). Four eyes were excluded from clinical outcome analysis due to missing data before and/or after phacoemulsification, thereby precluding analysis.
Thirty-five percent of the eyes (n = 11) underwent phacoemulsification between 12 and 24 months after DMEK. In the overall phacoemulsification group, the highest annual ECD decrease of 15.7% (from 1,322 ± 486 to 1,122 ± 420 cells/mm2) was seen between 12 and 24 months after DMEK (Figure 2), coinciding with the mean time of the cataract extraction (18 ± 13 months after DMEK). Overall, the ECD of the phacoemulsification group was lower at each follow-up time-point as compared to the group of phakic eyes that did not undergo phacoemulsification (Figure 2); however, this difference in ECD reached statistical significance only from 12 months of follow-up onwards (P = .095 at 1 m, P = .062 at 6 m, and all other time-points: P < .05).
Endothelial cell density (ECD) after phakic Descemet membrane endothelial keratoplasty (DMEK). ECD until the 5-year follow-up of patients who underwent phacoemulsification (PHACO) after DMEK (dashed line) and for phakic patients with DMEK without cataract extraction after DMEK (solid line). The ECD decrease between follow-up visits is presented by Δ (delta) in percentage. The arrow denotes the mean time of phacoemulsification after DMEK.
When stratifying the ECD values for the time-point of phacoemulsification, the preoperative mean ECD of 1,314 ± 524 cells/mm2 (n = 31) was recorded at the mean of 3.9 months (range: 2 weeks to 23 months) prior to phacoemulsification (Table 2). The postoperative ECD values were recorded for the 1- to 6-month period after phacoemulsification and showed a decrease of 11% (1,167 ± 443 cells/mm2) compared to values before phacoemulsification (P = .333). At the 7- to 18-month period after phacoemulsification, ECD decreased by 19%, compared to preoperative values and was 1,039 ± 414 cells/mm2 (n = 29) (P = .001) (Figure A, available in the online version of this article). The decrease in ECD between 1 to 6 and 7 to 18 months after phacoemulsification was not significant (P = .096). Furthermore, an approximately 3.3% decrease in ECD was recorded between 1 and 2 years (n = 24) and 4.0% between 2 and 3 years (n = 17) after phacoemulsification.
Specular microscopy images of 4 eyes with Descemet membrane endothelial keratoplasty (DMEK) before (top row) and 1 to 6 months (middle row) and 7 to 18 months (bottom row) after phacoemulsification (PHACO). Endothelial cell density (ECD) in cells/mm2 is represented at the top of each image. ECD loss in percentage compared to before phacoemulsification is indicated by an *.
The mean central corneal thickness (CCT) changed from 532 ± 46 µm (n = 31) prior to phacoemulsification cataract surgery to 539 ± 56 µm (n = 29) at 1 to 6 months and to 534 ± 38 µm (n = 29) at 7 to 18 months postoperatively (Table 2). The mean CDVA prior to cataract surgery was 0.27 ± 0.13 logMAR (n = 30) (decimal VA 0.54), 0.07 ± 0.12 logMAR (n = 30) (decimal VA 0.85) at 1 to 6 months and 0.07 ± 0.09 logMAR (n = 28) (decimal VA 0.85) at 7 to 18 months after cataract surgery (Figure 3). No detachment of the DMEK graft was observed during phacoemulsification and cataract surgery itself was uneventful in 33 of 35 eyes (94%). One case was complicated by a nuclear drop that required subsequent vitrectomy. In another patient with an extensive history of vitreoretinal surgeries, it was not possible to implant an intraocular lens and the patient was left aphakic.
Corrected distance visual acuity (CDVA) outcomes before phakic Descemet membrane endothelial keratoplasty (DMEK), before and 1 to 6 months and 7 to 18 months after phacoemulsification (PHACO). Bar graphs present the percentage of eyes reaching the CDVA levels given in decimals (Snellen). Number of eyes available is presented underneath the follow-up time-points.
One patient required a re-transplantation 2 months after phacoemulsification (23 months after DMEK) due to a preexisting low ECD. A second patient with a glaucoma drainage tube needed a repeated graft 24 months after phacoemulsification (39 months after DMEK) due to secondary graft failure.
This study evaluated the incidence of cataract extraction in phakic eyes after DMEK and the effect of phacoemulsification on the DMEK graft. A low incidence of cataract extraction after DMEK and an acceptable ECD decrease were observed.
Although relatively high rates of cataract formation within 1 year were reported for the older posterior lamellar keratoplasty techniques,18,19 this was improved upon by Descemet stripping (automated) endothelial keratoplasty (DS(A)EK), for which rates of 5% to 40% were reported.20-24 DMEK appears to confer an even lower rate, and although the number of phakic DMEK cases requiring cataract surgery reported here (13.1%) was higher than our previously reported rates of 4%25 and 4.7%,15 this is more indicative of the extended follow-up period.
Previous reports calculated that the probability of a patient requiring cataract surgery within 1 year of phakic DMEK was 27%, which rose to approximately 45% in patients older than 50 years.14 This is considerably higher than our finding of 6% at 1 year (Figure 1), and also 6% for those older than 57 years. This difference may be due to the presence of cataract preoperatively, as Burkart et al14 noted that 31% of their phakic DMEK cases had evidence of cataract preoperatively. A preexisting cataract is a known risk factor for cataract progression after penetrating keratoplasty,26 even though this has not been yet confirmed for DMEK. As a result, the presence of even a mild cataract is usually considered a contraindication to phakic DMEK in our center.
Although there is evidence for an increased incidence of cataract formation in diabetic patients,27 our cohort included only 5% (n = 13) of diabetic patients, with only 2 of them undergoing phacoemulsification after DMEK. Based on the small sample size, we cannot state whether or not diabetic patients in our study group appeared to be at a higher risk for cataract formation after DMEK. On the other hand, a significantly higher percentage of eyes with bullous keratopathy were represented in the study group that underwent phacoemulsification when compared to the entire group of phakic eyes. Due to the relatively small group of eyes with bullous keratopathy, it is not possible to draw any definite conclusion whether those eyes with bullous keratopathy were more prone to developing cataract because of the indication itself or because the surgery for these eyes may have been technically more challenging. Additionally, a higher dose and a longer use of steroids may expedite cataract development after DMEK. At our institute, we routinely transition to topical fluorometholone drops 1 month postoperatively after all DMEK surgeries and we suspect the lower penetration of the steroid has less of an influence on the crystalline lens. More potent corticosteroids are only applied to treat allograft rejection, which occurs rarely after DMEK.
One of the main concerns with phakic DMEK is the potential risk of a future phacoemulsification surgery on the donor graft. Phacoemulsification in normal corneas is associated with a range of endothelial cell loss, from between 6% and 17%.28–31 In addition, the normal rate of endothelial decline of approximately 0.6% per year increases to 2.5%32 per year from 1 to 10 years after surgery,33 but little is known about how donor endothelium responds. Data from penetrating keratoplasties after phacoemulsification is conflicted, with some reporting losses of 19% to 32% after 6 months,34–37 whereas a small comparative clinical trial reported no difference in ECD when these cases were compared with the standard “triple” approach. Data from phacoemulsification after DS(A)EK are similarly lacking, although one report suggested that the effects of phacoemulsification were also minimal.20 In our cohort, we found an initial 11% ECD loss within the first 6 months of the phacoemulsification surgery, which increased to 19% after 7 to 18 months. Although this is an improvement over our previous report,15 it does suggest that the effect of phacoemulsification surgery on donor endothelium persists over time, similar to normal corneas.33 CCT did not change significantly over this period, indicating that the residual endothelial cells were still functional and competent.
It might be noteworthy that the study group undergoing phacoemulsification after DMEK included significantly more eyes with bullous keratopathy compared to the whole cohort (17% vs 8%, respectively). It has previously been reported that eyes with bullous keratopathy, compared to eyes with Fuchs endothelial corneal dystrophy, have significantly lower ECD at 6 months after DMEK.12 Therefore, this could have influenced the early ECD decrease in the phacoemulsification group and may partly explain why the ECD was already lower in the study group as compared to the entire group of phakic eyes before the first phacoemulsification had taken place.
In cases where the ECD is borderline prior to the cataract surgery, or where a hard lens is expected, a small incision approach may also be considered. Although phacoemulsification is the most routine approach for cataract surgeons, small incision cataract surgery has the advantage of avoiding the need for phacoemulsification energy entirely.
There are some limitations to this study that should be addressed. Because the cataract surgeries were not performed in our center, but instead by the patient's referring ophthalmologist, it was not possible to standardize the surgical technique or to obtain all of the surgical data. Although all surgeons were known to be experienced in cataract surgery, no data are available regarding the total phacoemulsification energy used, surgical time, or the types of ophthalmic viscosurgical devices used, all of which influence in the endothelium during cataract surgery.8,38 Additionally, like every retrospective cohort, our study was prone to loss to follow-up, which could have potentially lead to an underestimation of the phacoemulsification effect on ECD loss, CDVA, and CCT. If there was a delayed effect of the phacoemulsification on the DMEK graft, we could have missed the clinical outcomes for those cases that were lost early after phacoemulsification. However, our clinical outcome group had at most 9.7% of random lost to follow-up data, which should have not affected the validity of the study.39 Although phakic DMEK surgery is typically reserved for only younger patients, we report a low rate of cataract development in a cohort with a mean age of 55.7 years. As long as the crystalline lens remains clear before DMEK, the cataract surgery may be deferred, reducing associated risks from surgery and allowing the patient to benefit from future developments and improvements in intraocular lens technology. When cataract does develop, phacoemulsification can be performed safely with no impact on CCT, and endothelial cell losses lower than we previously reported.
- Deng SX, Lee WB, Hammersmith KM, et al. Descemet membrane endothelial keratoplasty: safety and outcomes: a report by the American Academy of Ophthalmology. Ophthalmology. 2018;125(2):295–310. doi:10.1016/j.ophtha.2017.08.015 [CrossRef]
- Melles GR, Lander F, Rietveld FJ. Transplantation of Descemet's membrane carrying viable endothelium through a small scleral incision. Cornea. 2002;21(4):415–418. doi:10.1097/00003226-200205000-00016 [CrossRef]
- Stuart AJ, Romano V, Virgili G, Shortt AJ. Descemet's membrane endothelial keratoplasty (DMEK) versus Descemet's stripping automated endothelial keratoplasty (DSAEK) for corneal endothelial failure. Cochrane Database Syst Rev. 2018;6(6):CD012097. doi:10.1002/14651858.CD012097.pub2 [CrossRef]
- Flockerzi E, Maier P, Böhringer D, et al. all German Keratoplasty Registry Contributors. Trends in corneal transplantation from 2001 to 2016 in Germany: a report of the DOG-Section Cornea and its Keratoplasty Registry. Am J Ophthalmol. 2018;188:91–98. doi:10.1016/j.ajo.2018.01.018 [CrossRef]
- Chaurasia S, Price FW Jr, Gunderson L, Price MO. Descemet's membrane endothelial keratoplasty: clinical results of single versus triple procedures (combined with cataract surgery). Ophthalmology. 2014;121(2):454–458. doi:10.1016/j.ophtha.2013.09.032 [CrossRef]
- Schoenberg ED, Price FW Jr, Miller J, McKee Y, Price MO. Refractive outcomes of Descemet membrane endothelial keratoplasty triple procedures (combined with cataract surgery). J Cataract Refract Surg. 2015;41(6):1182–1189. doi:10.1016/j.jcrs.2014.09.042 [CrossRef]
- Laaser K, Bachmann BO, Horn FK, Cursiefen C, Kruse FE. Descemet membrane endothelial keratoplasty combined with phacoemulsification and intraocular lens implantation: advanced triple procedure. Am J Ophthalmol. 2012;154(1):47–55.e2. doi:10.1016/j.ajo.2012.01.020 [CrossRef]
- Takahashi H. Corneal endothelium and phacoemulsification. Cornea. 2016;35(suppl 1):S3–S7. doi:10.1097/ICO.0000000000000990 [CrossRef]
- Dapena I, Ham L, Tabak S, Balachandran C, Melles G. Phacoemulsification after Descemet membrane endothelial keratoplasty. J Cataract Refract Surg. 2009;35(7):1314–1315. doi:10.1016/j.jcrs.2008.12.050 [CrossRef]
- Alió JL, Grzybowski A, El Aswad A, Romaniuk D. Refractive lens exchange. Surv Ophthalmol. 2014;59(6):579–598. doi:10.1016/j.survophthal.2014.04.004 [CrossRef]
- Daien V, Le Pape A, Heve D, Carriere I, Villain M. Incidence, risk factors, and impact of age on retinal detachment after cataract surgery in France: a national population study. Ophthalmology. 2015;122(11):2179–2185. doi:10.1016/j.ophtha.2015.07.014 [CrossRef]
- Birbal RS, Baydoun L, Ham L, et al. Effect of surgical indication and preoperative lens status on Descemet membrane endothelial keratoplasty outcomes. Am J Ophthalmol. 2020;212:79–87. doi:10.1016/j.ajo.2019.12.011 [CrossRef]
- Godin MR, Boehlke CS, Kim T, Gupta PK. Influence of lens status on outcomes of Descemet membrane endothelial keratoplasty. Cornea. 2019;38(4):409–412. doi:10.1097/ICO.0000000000001872 [CrossRef]
- Burkhart ZN, Feng MT, Price FW Jr, Price MO. One-year outcomes in eyes remaining phakic after Descemet membrane endothelial keratoplasty. J Cataract Refract Surg. 2014;40(3):430–434. doi:10.1016/j.jcrs.2013.08.047 [CrossRef]
- Musa FU, Cabrerizo J, Quilendrino R, Dapena I, Ham L, Melles GR. Outcomes of phacoemulsification after Descemet membrane endothelial keratoplasty. J Cataract Refract Surg. 2013;39(6):836–840. doi:10.1016/j.jcrs.2012.12.032 [CrossRef]
- Groeneveld-van Beek EA, Lie JT, van der Wees J, Bruinsma M, Melles GR. Standardized 'no-touch' donor tissue preparation for DALK and DMEK: harvesting undamaged anterior and posterior transplants from the same donor cornea. Acta Ophthalmol. 2013;91(2):145–150. doi:10.1111/j.1755-3768.2012.02462.x [CrossRef]
- Dapena I, Ham L, Droutsas K, van Dijk K, Moutsouris K, Melles GR. Learning curve in Descemet's membrane endothelial keratoplasty: first series of 135 consecutive cases. Ophthalmology. 2011;118(11):2147–2154. doi:10.1016/j.ophtha.2011.03.037 [CrossRef]
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- Terry MA, Wall JM, Hoar KL, Ousley PJ. A prospective study of endothelial cell loss during the 2 years after deep lamellar endothelial keratoplasty. Ophthalmology. 2007;114(4):631–639. doi:10.1016/j.ophtha.2006.11.024 [CrossRef]
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Demographics of DMEK Recipients and Donors
|Parameter||Study Group||Total Group of Phakic DMEK Eyes|
|No. of eyes (patients)||35 (31)||261 (191)|
|Mean ± SD patient age, years (median)||55.7 ± 11.5 (58)||55.7 ± 9.9 (57)|
|Patient gender, n (%)|
| Male||17 (48.6%)||99 (52%)|
| Female||18 (51.4%)||91 (48%)|
|Indication for DMEK, n (%)|
| Fuchs endothelial corneal dystrophy||28 (80%)||227 (87%)|
| Bullous keratopathy||6 (17%)||22 (8%)|
| Failed graft (PK/DSAEK)||–||7 (3%)|
| Other (corneal dystrophies, corneal decompensation due to trauma, Acanthamoeba keratitis)||1 (3%)a||5 (2%)|
|Diabetes mellitus, n (%)||2 (5.7%)||13 (5%)|
|Mean ± SD donor age, years||62.3 ± 9.1||62.9 ± 9.8|
|Mean ± SD donor ECD, cells/mm2||2,525 ± 192||2,590 ± 191|
|Mean ± SD follow-up time after DMEK, months (median)||54.2 ± 28 (57)||51.6 ± 34 (51)|
Clinical Outcomes for Eyes That Underwent Phacoemulsification After DMEK
|Time between DMEK and PHACO, months|
| Mean ± SD||18 ± 13|
| Range||3 to 69|
|FU after PHACO, months|
| Mean ± SD||37.9 ± 27|
| Range||1 to 119|
| Mean ± SD donor ECD, cells/mm2||2,513 ± 188 (n = 31)|
| Mean ± SD CDVA, logMAR||0.31 ± 0.20 (n = 30)|
| Mean ± SD CCT, µm||660 ± 85 (n = 31)|
|After DMEK, before PHACO|
| Mean ± SD ECD, cells/mm2||1,314 ± 524 (n = 31)|
| Mean ± SD CDVA, logMAR||0.27 ± 0.13 (n = 30)|
| Mean ± SD CCT, µm||532 ± 46 (n = 31)|
|1 to 6 months after PHACO|
| Mean ± SD ECD, cells/mm2||1,167 ± 443 (n = 28)|
| Mean ± SD ECD decrease, %a||11 ± 14 (range: 0 to 41)|
| Mean ± SD CDVA, logMAR||0.07 ± 0.12 (n = 30)|
| Mean ± SD CCT, µm||539 ± 56 (n = 29)|
|7 to 18 months after PHACO|
| Mean ± SD ECD, in cells/mm2||1,039 ± 414 (n = 29)|
| Mean ± SD ECD decrease, %a||19 ± 17 (range: 0 to 54)|
| Mean ± SD CDVA, logMAR||0.07 ± 0.09 (n = 28)|
| Mean ± SD CCT, µm||534 ± 38 (n = 29)|