Congenital hereditary endothelial dystrophy (CHED), an autosomal recessive disorder, is characterized by bilateral corneal clouding with a ground-glass appearance and focal gray spots due to stromal edema and Descemet membrane (DM) thickening. Symptoms include decreased vision and nystagmus, with minimal tearing and photophobia often resulting in amblyopia. Although the primary pathology lies in the DM and endothelium, until recently, penetrating keratoplasty (PKP) has been the gold-standard surgical treatment.
Corneal transplantation in children is challenging even for experienced surgeons, resulting in increased complications due to various factors such as small eyeballs, low scleral rigidity, shallow anterior chamber, phakic status, and increased positive vitreous pressure. Children are often difficult to examine and are more prone to trauma, infection, and allograft rejection. These factors contribute to the high incidence of graft failure following PKP. Today, endothelial keratoplasties such as Descemet stripping endothelial keratoplasty (DSEK), Descemet-stripping automated endothelial keratoplasty (DSAEK), and Descemet membrane endothelial keratoplasty (DMEK) are preferred over PKP due to a decrease in the rates of suture-related complications, complications of open-sky procedures, graft rejection/failure, unstable refractive outcomes, and the need for multiple examinations under anesthesia. The effectiveness of DMEK in the management of CHED has been very recently documented in the literature with favorable visual outcomes.
Performing EK in CHED patients is associated with various intraoperative difficulties: poor visibility due to severe corneal edema and strong adherence of the DM to the underlying stroma, which may result in DM retention/tags, leading to graft detachment and failure. DM scoring is found to be much simpler in decompensated corneas such as Fuchs’ endothelial dystrophy in contrast to the CHED eyes.
In this review, we attempt to cover various surgical techniques, visual and refractive outcomes, graft-related outcomes, and complications related to endothelial keratoplasty (EK) in CHED patients.
A literature search was performed using PubMed (United States National Library of Medicine), Embase (Reed Elsevier Properties SA), Web of Science (Thomson Reuters), and Scopus (Elsevier BV) by using the following keywords: congenital hereditary endothelial dystrophy and Descemet stripping endothelial keratoplasty or Descemet stripping automated endothelial keratoplasty or Descemet membrane endothelial keratoplasty or endothelial keratoplasty or pediatric DMEK. A total of 198 articles matched our search strategy. After screening for duplication and going through the titles and abstracts, 12 relevant original articles, one case series, and six case reports were included in this review.
All relevant articles, including case reports, were also included in this review. All other studies of pediatric EK due to other causes of congenital corneal opacity have been excluded from this review. Reference lists from the selected articles were further screened to obtain further relevant articles.
We herein describe the outcomes of DSAEK and DMEK in cases of CHED.
DSAEK in CHED
DSAEK graft offers clear advantages over PKP for the treatment of endothelial failure in the pediatric age group as it is performed under a “closed system,” minimizing the risk of intraoperative complications. Since the first published series of DSAEK in CHED by Busin et al., several publications have shown that DSAEK is a safe and effective surgery in providing rapid restoration of corneal clarity with fewer complications compared to PKP.
- Surgical TechniqueDifferent techniques have been defined by various authors in their studies. To reduce the posterior vitreous pressure, intravenous mannitol 20% is routinely given for all CHED cases before beginning the procedure. The approach to the surgery might be superior or temporal cornea as per the surgeon’s preference.
- Donor tissue preparation: The donor lenticules can be either prepared preoperatively by trained technicians and appropriately stored (pre-cut donor lenticules) or they can be cut at the time of the surgery either by manual dissection or by using an automated lamellar therapeutic keratoplasty (ALTK) system. Manual dissection can be done using Melles blunt dissectors and a Moria or Barron artificial anterior chamber. A graduated diamond knife can help decide the depth of dissection depending on the donor thickness. The automated system uses microkeratome blades of various head sizes (blade depth: 300–400 mm). Femtosecond laser can also be used, which allows the precise creation of dissection planes. Following lamellar dissection, the posterior donor lamella is cut using disposable hand-held punches depending on the white-to-white diameter of the recipient. The lenticules remained well attached during the postoperative period irrespective of the donor tissue preparation method. The reported incidence of graft detachment following DSEK is 0%–82%, and that after DSAEK is 0%–43%. The highly variable rate is due to the heterogeneity in the inclusion parameters in various studies.
- Recipient bed preparation: Gentle debridement of host epithelium usually aids in better visualization in edematous corneas. A circular marker (7.5–9.0 mm) using gentian violet can be used to outline the limits of the internal surface from which DM-endothelium has to be peeled off. The area of DM removal is usually 1 mm larger in diameter than the planned donor graft. Phakic DSAEK is considered challenging in terms of both intraoperative difficulties and the risk of subsequent cataract formation. Mechanical damage during the procedure may be a contributing factor in the development of early or latent secondary cataracts. Safety measures such as using viscoelastic devices, pupil constriction so the iris acts as a barrier, and maintaining the anterior chamber using a constant inflow of air or saline should be adopted to prevent lenticular trauma. The incision sites can be moved approximately 1 mm superiorly from the standard 9- and 3-o’clock positions so that the entire graft pull-through maneuver is performed using the superior part of the iris to protect the underlying crystalline lens. [Fig. 1] Despite these strategies, the incidence of post-DSAEK cataracts has been reported between 7% and 37%. Trypan blue (0.06%) solution can also be used to increase the visibility of DM through the edematous cornea. [Fig. 1] Chandelier illumination has been proven to improve visualization during DM stripping and graft centration.DM scoring is more difficult to perform in eyes with CHED. Most surgeons demonstrated successful descemetorrhexis with reverse Sinskey hook [Fig. 1]; however, Busin et al. and Lenhart et al. used cystotome to carefully cut through the DM in cases with adherent DM. Scoring can also be performed using a cannula, Terry scraper, or DM stripper and forceps. Descemetorrhexis can be performed under balanced salt solution, air, or viscoelastic material depending on the surgeon’s preference. Poor visibility due to severe corneal edema and strict adherence of DM to underlying stroma, especially in infants, makes descemetorrhexis difficult to accomplish in CHED eyes. However, there are no significant differences in visual or graft-related outcomes with any of these techniques.
However, stripping the DM has several disadvantages, especially in recipients with severe corneal edema. The scope of the stripped DM is difficult to control, which may result in incomplete donor graft coverage and persistent edema postoperatively. In contrast, n-DSAEK, which does not require the removal of the DM, has its own merits. It has been shown to simplify the procedure, shorten the surgical time, and reduce inflammatory reactions. n-DSAEK is preferred in cases where DM cannot be identified, such as in infants (age less than 1 year), poor visibility due to severe corneal edema, and when DM stripping is difficult even after numerous attempts.
- Donor lenticule insertion: Lenticule insertion and unfolding are technically challenging, and a rise in IOP should be avoided to reduce the chance of lenticule dropout. Donor lenticule can be introduced into the anterior chamber by using different techniques such as combined use of Busin glide and suture-assisted donor lenticule insertion; alternatively, the donor lenticule can be loaded onto Busin glide, Sheet’s IOL glide, or Tan Endoglide and pulled into the AC by using an internal limiting membrane peeling forceps from the clear corneal side port on the opposite end. The donor graft can be placed as a 60/40 under fold or 50/50 “taco” configuration and inserted into the AC. However, Price et al. reported that curling the DSAEK graft into a cylindrical shape for insertion causes less endothelial cell loss and improved graft longevity than folding the graft for insertion. To prevent postoperative pupillary block, a peripheral iridectomy should be performed and a complete air fill in the AC should be maintained for 10 min. Partial-thickness venting incisions till the graft interface at a 45° angle is a good option in cases where the graft is found to be excessively mobile due to interface fluid. This is followed by the partial release of air to maintain 60%–75% air volume in the AC [Fig. 1]. Variable time periods for postoperative maintenance of supine position have been recommended, ranging from 2 h, 4h, and up to 12 h.Table 1 summarizes the preoperative parameters and surgical techniques of DSAEK in CHED.
- Outcomes of DSAEK in CHED
- Visual outcomesIn various studies, the preoperative corrected distance visual acuity (CDVA) ranged from counting fingers to 20/63. Improvement in vision in pre-verbal children and infants was as early as 1 week to up to 2 years of follow-up. Similar results were found in older children, whose postoperative CDVA ranged from 20/160 at 12 months follow-up to near 20/20 (0.03 logMAR) at 2–9 years follow-up. This wide range can be attributed to different preoperative visual acuity, varied age at surgery, amblyopia, and surgeon’s bias.
- Refractive outcomesEK is associated with a lower and more predictable postoperative refractive error with early stabilization. This offers an added advantage for better amblyopia management, less frequent change of glasses, and better compliance of the parents to therapy. DSAEK grafts usually induce a hyperopic of 0.75–1.5 D. Postoperative cycloplegic refraction in CHED eyes ranged from − 7 DS to + 10 DS (up to 4 DC) in various studies. In one of the largest case series by Mohebbi et al., the residual postoperative refractive error was + 2.57 ± 3.3 DS in the age group of 3–16 years at follow-up of 38 months.
- Graft-related outcomesThough the cornea becomes relatively clear following successful EK, the clarity never reaches the pristine quality of PKP due to the stromal–stromal interface haze. Despite this, the visual acuity remains comparable between groups. It may be claimed that persistent haze may by itself account for amblyopia and decrease in contrast; however, early visual stabilization, predictable refraction, and avoiding suture-related complications might offer more advantages in terms of amblyopia management. All corneas are expected to clear between 1 week and a month following EK, and clarity continues to improve until a year. Infants seem to have a faster improvement in corneal clarity compared to older children due to the lesser duration of pre-existed corneal edema. Due to the stromal–stromal interface in DSEK, residual haze is often present until a year. Graft detachment or dislocation is the most common graft-related complication postoperatively and can be managed with re-bubbling on the immediate postoperative day. Slight graft decentration may be observed without any need for intervention. Other less common complications include immunologic graft rejection, which can be easily reverted with topical and systemic steroids, and graft failure due to traumatic wound dehiscence.
- ComplicationsThere were no intraoperative complications, such as lenticular touch, in any of the case series. However, the completion of DM scoring was not attempted in a few cases either due to incomplete visualization or very adherent DM, especially in infants. DM tags were left in place in a few cases even after unsuccessful attempts of DM removal. Mohebbi et al. reported a case of pupillary block on the first postoperative day and increased IOP in 61.1% of cases. Yang et al. demonstrated that infants show a lower rate of complications, faster recovery, and better outcomes of DSAEK compared to children >1 year of age as infants are more likely to remain supine postoperatively for graft attachment and commencement of amblyopia management at an earlier age.
Table 2 summarizes the visual, refractive, and graft-related outcomes and complications of DSAEK in CHED.
DMEK in CHED
DMEK, a recent addition to EK, is advantageous over DSAEK due to relatively faster visual recovery and a lower rejection rate. DMEK has been ineffectively attempted in an infant’s eye with posterior polymorphous corneal dystrophy, whereas it has shown good visual and functional outcomes in a Kearns–Sayre syndromic child with endothelial dysfunction. To date, only four studies have evaluated the anatomical and functional outcomes of DMEK and n-DMEK in CHED eyes.
- Surgical Technique
- Donor tissue preparation: In all the studies, donor DM stripping was performed intraoperatively before DMEK surgery by using a standard approach. After scoring of the peripheral endothelium–Descemet membrane (EDM), it is carefully separated from the underlying stroma by using a pair of McPherson forceps under 1–2 drops of the storage medium (submerged cornea under backgrounds away technique) till 1–2 mm short of completion such that a peripheral hinge of stromal–EDM adhesion is left. The stripped EDM is floated back using the storage medium, leaving one-half of the corneal stroma exposed for the creation of a stromal window. The inked F-stamp/S-mark is lightly applied to DM through the 2-mm stromal window with the replacement of the stromal plug.
- Recipient bed preparation: DM stripping is performed encompassing a larger area of 9 mm in CHED eyes with thickened DM that can be visualized preoperatively on ASOCT. Saad et al. and Fogla et al. reported 57% and 50% of CHED eyes to have thickened DM, respectively; however, Fogla et al. recommended DM stripping in all cases irrespective of the DM morphology.
- Donor lenticule insertion: A glass injector connected to a fluid-filled syringe is used to insert the donor lenticule into the AC. After securing the main wound with 10-0 nylon sutures, a no-touch tapping technique is used to unroll the lenticule. The graft unfolding and correct orientation can be confirmed by the F-stamp/S-mark and Mi-OCT. For tamponade to support the donor DM, air or 20% sulfur hexafluoride gas can be injected, especially in non-stripping Descemet membrane EK (nDMEK) cases for longer tamponade.Table 1 summarizes the preoperative parameters and surgical techniques of DMEK in CHED.
- Outcomes of DMEK in CHED
- Visual outcomesSaad et al. showed a significant improvement in CDVA from 0.9 ± 0.3 to 0.4 ± 0.2 logMAR irrespective of stripping or non-stripping of DM at 16.9 ± 8.1 months. Similarly, Fogla et al. reported marked improvement in the mean CDVA from 0.8 ± 0.3 to 0.3 ± 0.2 logMAR at 7.8 ± 2.5 months. A study comparing standard DMEK versus nDMEK demonstrated only a minor visual gain in either group and similar outcomes between both groups. This could be due to amblyopia as most of these patients were operated on at an older age (13–39 years).
- Refractive outcomesDMEK is associated with minimal changes in the refractive error, that is, surgically induced corneal astigmatism of <1 D and a minimal change in the spherical equivalent of 0.5–1 D induced at the anterior corneal surface. This is because the DM graft has an equal thickness over its entire diameter unlike that of DSAEK.
- Graft related outcomesFollowing DMEK, the stromal collagen fibers seem to appear more compact on ASOCT, with a reduction in corneal thickness. Corneal thickness was shown to decrease significantly in all studies from 991 ± 65 mm to 590 ± 70 mm following DMEK and 895 ± 51 mm to 603 ± 46 mm following nDMEK. Average endothelial cell loss (ECL) at 6 months after routine DMEK ranges from 25% to 47%. The mean ECL in CHED eyes following DMEK was 33% at 16.9 ± 8.1 months (32.3% in the nDMEK group and 33.6% in the DMEK group at 17.6 ± 6.8 months and 10.5 ± 4 months, respectively). These data suggest that ECL following DMEK is comparable to DSAEK in CHED eyes. Fogla et al. reported the presence of abnormal corneal folds in the anterior stroma in one-third of the eyes despite having a good resolution of corneal edema. These folds were restricted to the anterior stroma of the recipient cornea, suggesting that this could be due to the rapid resolution of corneal edema and an accompanying change in corneal curvature. This could be because the collagen fibers in the posterior half of the cornea become more compact following DMEK than the anterior half because of the poor water retentive capacity of keratan sulfate, resulting in a possible curvature mismatch between them. In addition, the anterior collagen fibers have greater rigidity, making them less pliable after the resolution of edema. A similar appearance has been noted postoperatively following DSAEK in CHED.
- Intraoperative: Due to repeated intraocular manipulation during difficult DM stripping, a case of intraoperative aqueous misdirection has been reported that was managed with pars plana core vitrectomy.
- Postoperative: Donor graft detachment is the most common postoperative complication, which could be related to eye rubbing or failure to maintain a supine position, with a reported incidence of 0%–43%. Graft failure was noted in a single case at the 5-month follow-up and required a repeat DMEK surgery.
EK can be challenging, especially in children. Good visual outcomes can be achieved following EK in CHED eyes if intervened early with effective amblyopia management. Although the optimal age for EK remains controversial, early surgical intervention should be advocated to avoid amblyopia. EK should be preferred over PKP due to lesser complications, early visual recovery and refractive stability, better amblyopia management, and comparable visual outcomes. AlArrayedh et al. demonstrated poor outcomes from PKP in CHED due to dense amblyopia and a high risk of long-term graft failure.
Various intraoperative difficulties discussed require adequate surgical expertise to efficiently address them. The DM remnants/tags that might hinder the graft apposition and lead to detachment can be visualized better and removed using intraoperative chandelier illumination, intraoperative OCT, or by using the metal surface of the crescent blade against the stained DM. Ashar et al. compared DSEK with and without Descemet stripping and concluded similar outcomes. Similar results were reported by Asif et al. that there was no significant difference in terms of graft detachment irrespective of whether DM was stripped in CHED eyes.
Partial and peripheral graft detachment following DMEK rates have been reported for around 62%–63% and complete detachment for around 30%; however, with improved techniques and surgical experience, this has significantly reduced to 34.6% in a multicenter study and to as low as 4% in one case series. Therefore, a learning curve for DMEK surgery, including postoperative care, is highly relevant.
Intraoperatively, graft adhesion can be confirmed by the double ring sign; however, this is not always possible in CHED eyes due to thick and hazy corneas. An acute-angled bevel sign on Mi-OCT can also be useful in confirmation of the graft orientation in these cases. During DMEK, the staining of the donor DM and the S-mark/F-stamp can facilitate in visualizing and confirming the orientation of the graft intraoperatively. The orientation of the DM scroll in the AC can also be confirmed using Mi-OCT intraoperatively before air tamponade.
To conclude, EK is a preferred treatment in CHED eyes, and it can be performed safely with certain modifications compared to that in adults. EK can be planned early to prevent the development of amblyopia. EK results in optimal visual and refractive outcomes compared to PKP with much lesser complications.
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Conflicts of interest
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