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Volume: 12 Issue: 6 December 2014

FULL TEXT

ARTICLE
Histopathologic and Optical Coherence Tomography Observation After Descemet’s Stripping Endothelial Keratoplasty in Rabbits

Objectives: To study the histopathologic and optical coherence tomography changes after Descemet’s Stripping Endothelial Keratoplasty in rabbits.

Materials and Methods: Descemet’s Stripping Endothelial Keratoplasty was performed in 14 rabbit eyes and descemetorhexis was performed in 10 rabbits, as control. Histopathologic examination and anterior-segment optical coherence tomography were conducted in the Descemet’s Stripping Endothelial Keratoplasty group at 1, 2, 4, and 8 weeks. For the control group, histopathologic examination was performed before surgery and at 1, 2, 4, and 8 weeks after surgery.

Results: In the Descemet’s Stripping Endothelial Keratoplasty group, corneas cleared completely within 2 weeks of surgery. Moreover, in most cases, the retained Descemet’s membrane was present at the peripheral donor-host interface. The retro-corneal fibrocellular membrane also was seen in the peripheral Descemet’s membrane stripped area without donor coverage. Anterior-segment optical coherence tomography revealed that the stroma deturgesed most rapidly between weeks 1 and 2.

Conclusions: Retained Descemet’s membrane was not the cause for graft dislocation and the retrocorneal fibrocellular membrane may be a kind of protective reaction to denuded endothelium.


Key words : Endothelial keratoplasty, Wound healing, Retrocorneal fibrous membrane, Optical coherence tomography, Histopathology

Introduction

Since the introduction of Descemet’s Stripping Endothelial Keratoplasty (DSEK), the Eye Bank of America Association has reported that 85% of all grafts in 2007 performed in the United States for endothelial disease were endothelial keratoplasty surgical procedures. Compared with the traditional penetrating keratoplasty, DSEK has several advantages including avoidance of an open-globe procedure, rapid visual rehabilitation, better tectonic stability, and fewer sutures with a lower level of astigmatism and fewer suture-related graft complications.1

However, because of the lack of sutures between the graft and recipient tissue, graft dislocation ranks as the most-frequent early postoperative complication of DSEK (which was not an issue with penetrating keratoplasty).2-12 As reported by the American Academy of Ophthalmology, dislocation rates varied from 0% to 82%, with a mean rate of 14.5%.1 Several modifications have been suggested to improve graft attachment: scraping the peripheral recipient stroma to expose stromal fibres,8 massaging to move any entrapped fluid out of the graft/host interface, extending the postoperative air bubble and face-up positioning duration, and creating small, peripheral, and stab incisions to evacuate the interface fluid have reportedly been used to decrease the rate of detachment.5 Dislocation remains still a challenge to this surgery.

The mechanism of corneal wound healing in DSEK is poorly understood. The literature has addressed the clinicopathologic findings of failed DSEK cases with the attempt to discover the causes of graft detachment as well as graft failure.13-26 In 2 case reports of failed grafts, the residual Descemet’s membrane (DM) in the interface was thought to be the cause of graft failure.19,21 However, another case report asserts the opposite.16

To our knowledge, there have been isolated reports in the observation of only dynamic corneal wound healing in EK, especially in DSEK.16,19,21 In addition, anterior-segment optical coherence tomography (AS-OCT) is used to follow the healing process after corneal surgery, helping to comprehensively clarify healing at a morphologic level. The objective of this study was to evaluate the histologic and AS-OCT findings during corneal wound healing in rabbits after DSEK.

Materials and Methods

Surgical procedure
Experiments conformed to the Association for Research in Vision and Ophthalmology (ARVO) Statement for the Use of Animals in Ophthalmic and Vision Research, and were approved by the Committee for Animal Welfare of the Eye and ear, nose, and throat Hospital of Fudan University. Fourteen New Zealand White rabbits weighing 2.5 to 3.5 kg were used as recipients (right eye each) in the DSEK group, and both eyes of 7 New Zealand White rabbits weighing 2.5 to 3.5 kg were used as donor eyes. Descemetorhexis was performed as controls in 10 New Zealand White rabbits. The operations were performed under general anesthesia, which was administered intramuscularly with a mixture of hydrochloride ketamine (2 mL:0.1 g) and diazepam injection (2 mL:10 mg) in 2:1 by 1 mL/kg body weight. Before surgery, topical 0.4% oxybuprocaine hydrochloride eye drops were also administered. After complete draping of the rabbit, an eyelid speculum was placed into the right eye. Standard aseptic techniques were used. Before the study, all protocols were in conformity with the Guide for the Care and Use of Laboratory Animals published by the National Institutes of Health 86-23, revised in 1985.

For donor eyes, an incision depth of approximately 70% to 80% of the corneal lamellar by hand was made. After the excision of the anterior lamellar, an 8.0-mm disposable trephine was used to centrally mark the area, and then it was removed using a microscissors.

To perform DSEK, an 8.0-mm epithelial mark was made to outline an area of DM’s excision. A 2.0-mm tunnel incision was made just within the limbus, entering the anterior chamber at the marking. The chamber was filled with Healon, via an accessory limbal incision. A blunt-tipped hook made from a 5-mL syringe needle was used to gently score the DM along an 8.0-mm circle. This same blunt hook was used to strip away the DM from the overlying stromal tissue. Once fully stripped, the DM and the endothelial tissue were removed from the anterior chamber with a forceps. Then, an irrigation/aspiration cannula was used to remove almost all of the Healon from the anterior chamber and replace it with a balance salt solution. The incision was enlarged to 5.0 mm. With a small amount of Healon placed on the endothelial surface, the donor was folded in a 60 to 40 “taco” configuration with the endothelial side inward. The folded donor tissue was grasped gently with long, curved forceps and inserted into the eye. The wound was closed with interrupted 10-0 nylon sutures, and a small air bubble was slowly injected through a paracentesis site, between the lips of the taco to unfold the donor tissue and press it against the host tissue. Slight adjustment of the central aspect of the tissue was performed (if needed). All eyes were treated with Tobradex (tobramycin and dexamethasone ophthalmic suspension, 0.3%/0.1%) 4 times a day for 2 weeks.

Slit lamp and histopathologic analysis
All rabbits were subjected to postoperative slit lamp examination daily for 2 weeks and then weekly for 6 weeks. Two rabbits in each group were randomly chosen at 1, 2, 4, and 8 weeks for histopathologic examination. In addition, 2 rabbits in the control group were killed immediately after descemetorhexis surgery. All animals were killed with an overdose of hydrochloride ketamine and diazepam injection (about 4 to 5 mL) under deep anesthesia, and the corneas were excised. The corneas were fixed in formalin and embedded in paraffin, then sectioned and processed by routine hematoxylin and eosin staining.

Anterior-segment optical coherence tomography analysis
Anterior-segment optical coherence tomography was performed on all corneas in the DSEK group at 1, 2, 4, and 8 weeks. Images were acquired with an anterior segment OCT system (RTVue-100, Optovue Inc., Freemont, CA, USA) at 830 ± 10 nm wavelength and 26 000 axial scans (A-scans) per second (axial resolution, 5 μm; wider resolution, 15 μm). The entire scanning range in air was 2 to 12 mm in width and 2.0 to 2.3 mm in depth. The single line scanning mode by anterior segment wide-angle lens was selected (scanning line length, 6 mm; scanning direction, 180°). The images were obtained and processed by the same operator. Scans were centered on the vertex reflection of the central cornea. In each scan, thickness measurements of the entire cornea were taken centrally.

Results

Slit lamp and histopathologic analysis
Descemet’s Stripping Endothelial Keratoplasty was successfully performed in 14 rabbit eyes, and descemetorhexis was performed in 10 rabbits as controls. In the control group, significant opacity in the central cornea was seen in all the operated eyes throughout the 8 weeks under slit lamp (Figures 1A and 1B). The DM and the endothelium were absent by histopathologic examination after descemetorhexis surgery (Figure 1C), and the broken end of DM (Figure 1D) was observed around the peripheral cornea. At week 1, significant stromal edema was seen in areas of stripped DM without overlying DSEK graft (Figure 1E). At week 2, a layer of fibrous membrane appeared at the area absent of the DM, consisting of numerous fibrocytes (Figure 1F). However, the stromal edema seemed to be alleviated. At weeks 4 and 8, the retrocorneal fibrocellular tissue became compact with decreased numbers of fibrocytes and the stroma was no longer edematous (Figures 1G and H). Both the stromal fibers and the fibrocellular tissue were arranged in order at week 8. Retrocorneal fibrocellular tissue was connected with the broken end of the DM (Figure 1G). No endothelium was seen over the stroma during study.

The anterior chamber was filled with an air bubble in the DSEK group after surgery. Corneas in the DSEK group were deturgesed and cleared completely within 2 weeks after surgery. Slit lamp examination revealed that the graft was attached well to the posterior surface of the host, and the peripheral cornea showed less dehydration than the central cornea at the 1-week examination. At the 2-week postoperative examination, the central cornea showed further dehydration, but interface fluid remained at the inferior portion of the peripheral cornea. Excellent graft attachment and no interface were observed at weeks 4 and 8. Histologic examination showed that the host cornea was much more edematous compared with the donor cornea at week 1; there was an evident dividing line between the host and donor cornea (Figure 2A).

Stromal fibers were not arranged in an orderly pattern. It seemed that the adhesion of DSEK grafts was poor and the donor graft would easily depart from the host under stretching. Though the interface was discernable at week 2, host stroma was deturgesed and arranged in order (Figure 2B). The peripheral DM stripped area that the donor failed to cover was laid over a sheet of fibrocellular tissue (Figure 2C). The graft-host interface was indistinguishable at week 4, although the donor tissue seemed more compact and hypercellular (Figure 2D). At week 8, the donor sheet could not be differentiated from the host in fibrous arrangement and cell number (Figure 2E). No scar was noted in the interface. Even when long segments of originally unstripped DM and pocket that formed because of a folded remnant DM were present at the donor-host interface, they appeared to be no problem with the adhesion (Figure 2F).

Anterior-segment optical coherence tomography analysis
Although the most significant reduction occurred from weeks 1 to 2, the central corneal thickness continued to decrease postoperatively. The host cornea appeared nonhomogenous because of severe stromal edema at week 1 and was divided from the edematous donor sheet by a visible interface. However, good attachment was seen between the graft-host interface, and the edema was markedly alleviated at week 2. The interface between host and graft in most cases was barely perceptible at week 4 at the central cornea. The interface was still clear at week 8 around the peripheral cornea. The central cornea can be described as homogenous or normal (Figure 3).

Discussion

In this study, descemetorhexis in rabbits led to endothelial injury and contributed to corneal edema for at least 8 weeks. Although it has been reported that rabbit corneal endothelium has a proliferative capacity following injury, an 8-mm circle of endothelial damage in our study could not be completely repaired after 8 weeks by migration or mitosis.27-28 Additionally, our study demonstrated that descemetorhexis could establish an endothelial defect in an animal model. However, the existence of the retrocorneal fibrocellular tissue in the control group is questionable.

Despite the lack of an endothelium, the central cornea continued to deturgess histologically, which was first observed histologically in our study. We hypothesize that the retrocorneal fibrocellular tissue was so compact that it may prevent aqueous humor from entering the stroma. A similar finding was noted in the DSEK group. The peripheral DM stripped area remained deturgesed with the retrocorneal fibrocellular tissue instead of donor coverage in histology. Nevertheless, the retrocorneal fibrocellular tissue also was found in failed DSEK/Descemet's membrane stripping (automated) endothelial keratoplasty (DSAEK) cases and was supposed as a potential cause of dislocation.16,24-25

In some researchers’ opinions, the retrocorneal fibrocellular tissue is presumably secondary to debris dragged in during insertion of the folded graft, which may induce the cellular proliferation that forms at the interface.24 This was inconsistent with our study as no graft insertion occurred in the control group. Wilson and associates29 demonstrated that the introduction of ectopic epithelial tissue into corneal stroma showed subsequent proliferation of stromal keratocytes, and the appearance of myofibroblasts, which led to stromal remodeling and scarring. Others supposed that this occurred because of persistent lenticel nonattachment or endothelial injury.25 However, it is not known if retrocorneal membrane formation is secondary to failed grafts or actually the cause. Our observation supports that the retrocorneal membrane is a reaction to endothelial injury, and that it develops to protect the stroma from edema. Thus, the retrocorneal fibrocellular tissue found in the interface may indicate tiny incomplete adherence between the graft and the host, which cannot be explored under slit lamp examination or OCT (ie, the membrane in the interface may suggest poor adherence if detected), and will not influence the clearance of the entire cornea.24 As the membrane began from the broken end of the DM, we considered that it may be secreted from the peripheral endothelium. Actually, observations have suggested that the corneal endothelial cells can transform to fibroblasts.30 Immunohistochemistry also showed retrocorneal membranes can express several cytokeratins in which normal and diseased endothelium are strongly positive.31

Compared with the persistent central cornea edema in the control group, rabbits that underwent DSEK had their corneas fully cleared within 2 weeks. There was no doubt that donor endothelia contributed in reducing corneal edema. Because of the inability of the rabbits to lie on their backs during and after surgery, there was the potential for bubble and graft decentration. Therefore, a small amount of Healon was left behind to aid in graft manipulation, which may have contributed to the longer time needed to deturgess. The graft adhesion was so poor at week 1 based on histologic analyses that it was likely to have completely separated from the host in case of any force or inappropriate positioning. The host cornea was deturgesed and the fibers were arranged regularly at week 2 by histopathology.

Mondloch and Kymionis19,21 assumed retained DM to be responsible for graft dislocation and failure. On the contrary, it was demonstrated by Caldwell that residual interface DM did not appear to hinder graft adhesion.16 However, the findings were based on failed DSEK grafts and needed experimental studies to confirm this hypothesis. We have confirmed the results in successful and cleared DSEK cases. From the histology of our study, retained DM at the periphery was observed in most cases, and it did create a small interface pocket, though it did not appear to affect adhesion. Moreover, it was believed that retained DM was more adhesive to the graft than to the host stroma.16 What is more, studies have shown that DM removal is not necessary for DSEK graft adherence in humans, including eyes with previous failed penetrating keratoplasty.32 Therefore, endothelial keratoplasty without DM removal may increase graft adhesion and facilitate surgical manipulation.

As a noncontact imaging device, AS-OCT allows for safe and comfortable imaging in the early postoperative period and succeeding follow-ups. Many studies have documented DSEK graft over time in humans by AS-OCT.33-37 At week 1, it was difficult to identify whether the graft was dislocated or not because of the presence of significant edema. Even on the slit lamp, small degrees of peripheral separation or slight fluid collection at the interface may not be well identified. Anterior-segment optical coherence tomography is extremely useful in diagnosing and delineating DM detachment, particularly when graft stromal edema obscures direct visualization.33 It has been reported that the recovery of endothelial pump after DSEK takes place between 1 week and 1 month postoperatively,35 which was consistent with our findings as the most significant reduction of central corneal occurred from week 1 to week 2 both in OCT and histologic performance.

This study gives evidence that AS-OCT can be used practically to evaluate dynamic histologic behavior to some extent, as well as for the quantitative and qualitative assessment of graft-host interface after endothelial keratoplasty Though it seemed that the corneal wound healing process had reached its climax at week 8 by the indication of the disappearing interface from OCT, we failed to follow after 8 weeks for comparison. However, interface was still discernable around the peripheral stroma throughout the course of the 8 weeks. A bubble that was not sufficient to cover all of the graft may account for the change. Also, the shape of the bubble caused the central cornea to receive the maximum force and thus heal more quickly than the peripheral. Finally, we reported that serial monitoring of cornea thickness after DSEK provides a surrogate estimate of endothelial function33 and an important predictor of DSEK failure.37 This idea was supported in our study, as continued dehydration was observed throughout the healing. Otherwise, the cornea would have remained edematous without enough healthy endothelium.

The cornea wound achieved nearly complete healing based on histologic and OCT images at 8 weeks, but we failed to continue to follow-up, which also was a limitation of our study. Although DSEK graft histology has been well-studied in human eyes postmortem, and the use of a rabbit model is questionable, we hope our study will provide new clinically relevant information.

In the study, we correlate the histologic change and OCT appearance in corneal wound healing in rabbits after DSEK. Of which, descemetorhexis can completely strip the DM and endothelium and could be a way to establish an endothelial defect model. The retrocorneal fibrocellular tissue found in previous failed DSEK/- DSAEK cases was demonstrated both in the endothelial defect control group and the successful DSEK group. Our observations support that the membrane occurred because of persistent lenticel nonattachment or endothelial injury, and may indicate incomplete adherence between the graft and the host. Also, retained DM may not be the cause of graft dislocation.


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Volume : 12
Issue : 6
Pages : 548 - 554
DOI : 10.6002/ect.2013.0282


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From the Department of Ophthalmology, EYE and ENT Hospital of Fudan University, Shanghai, China
Acknowledgements: The authors declare they have no conflicts of interest to declare. This
work was supported by Grants 81300792 from the National Natural Science Foundation of China.
Corresponding author: Lan Gong, EYE and ENT Hospital of Fudan University, No.83, Fenyang Road, Shanghai 200031 China
Phone: +21 6431 0068
Fax: +21 6437 7134*281
E-mail: gong_lan70@yahoo.com.cn