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1 JOURNAL CLUB CLINICAL SCIENCES Postoperative Visual Acuity in Patients With Fuchs Dystrophy Undergoing Descemet Membrane Stripping Automated Endothelial Keratoplasty Correlation With the Severity of Histologic Changes Dorrie M. Happ, MD; David A. Lewis, MD; Kevin H. Eng, MS; Heather D. Potter, MD; Aneesh Neekhra, MD; Christopher R. Croasdale, MD; David R. Hardten, MD; Sarah Nehls, MD; Michael Eide, MD; Jocelyn Rowe, MD; Sherif Khedr, MD; Daniel M. Albert, MD, MS Objective: To investigate a correlation between the severity of histologic changes of the Descemet membrane in patients with Fuchs endothelial dystrophy and the bestcorrected visual acuity (VA) after Descemet membrane stripping automated endothelial keratoplasty (DSAEK). Methods: In a retrospective study design, we created a histologic grading system based on common characteristics observed histologically among 92 DSAEK specimens sent to the University of Wisconsin Eye Pathology Laboratory with a clinical diagnosis of Fuchs dystrophy from 3 separate corneal surgeons. Cases were graded as mild, moderate, or severe on the basis of guttae dispersion, presence of a laminated Descemet membrane, presence of embedded guttae, and density of guttae. Regression models were built to study the relationship among preoperative VA, histologic findings, and bestcorrected VA 6 months and 1 and 2 years after DSAEK. Results: No correlation was found between the severity of histologic changes of Descemet membrane and preoperative VA. However, a correlation was noted between the preoperative and final VA. Cases with a laminated Descemet membrane but no embedded guttae (n=8) appeared to be less responsive to DSAEK. Otherwise, the severity of histologic changes of Descemet membrane observed in patients with Fuchs corneal dystrophy after DSAEK did not show a statistically significant correlation with final VA. Conclusions: Our analysis fails to show an inverse relationship between the severity of histologic changes of the Descemet membrane and the best-corrected VA of at least after DSAEK for Fuchs endothelial dystrophy. However, in a subset of patients with Fuchs dystrophy who develop a laminated Descemet membrane without embedded guttae, the visual recovery after DSAEK is less than expected. The laminated architecture of Descemet membrane without embedded guttae may facilitate separation between the membrane layers and, thus, incomplete removal of the recipient s Descemet membrane during DSAEK, which may then limit the postoperative visual outcome. Arch Ophthalmol. 2012;130(1):33-38 Author Affiliations are listed at the end of this article. FUCHS DYSTROPHY IS A COMmon, usually bilateral and typically asymmetrical progressive cause of corneal blindness in the United States. The exact cause of Fuchs dystrophy remains unknown, but there appears to be a genetic component combined with environmental factors. The inheritance most closely resembles an autosomal dominant pattern; however, incomplete penetrance is observed, and the disease seems to be expressed much more frequently in women. 1 The disease becomes clinically evident in the fourth or fifth decade of life, but it does not produce visually significant symptoms until approximately a decade later. Several stages of the disease exist. The first stage is asymptomatic, but guttae can be seen centrally on the posterior aspect of a thickened Descemet membrane. 2 In the second stage, the patient may experience increased glare and a painless decrease in vision due to corneal edema. 2 Journal Club slides available at The cornea may begin to decompensate. In the third stage, vision deteriorates further owing to advanced corneal edema, and the patient may experience pain from the formation of epithelial and subepithelial bul- 33
2 lae. 2 The fourth stage is characterized by profound vision loss due to subepithelial scarring, which histologically appears as diffuse avascular subepithelial connective tissue. 2 Cataracts are common in patients with Fuchs dystrophy, and the course of the disease may be accelerated after cataract removal or other intraocular procedures. WhenmedicalmanagementofFuchsdystrophyisnolonger adequate to control symptoms or if vision loss becomes unacceptable, surgery is the treatment of choice. Descemet membrane stripping automated endothelial keratoplasty (DSAEK) hasbecomethepreferredtreatment, replacingpenetrating keratoplasty for treating Fuchs dystrophy because of its distinct advantages, including quicker visual rehabilitation and reduced risk of intraoperative and postoperative injury. In addition, DSAEK creates minimal change in corneal surface topography, resulting in a reduced incidence of induced astigmatism, increased predictability in postoperative corneal power, decreased risk of neurotrophic ulcers because of protection of corneal innervation, and reduced rejection. Mostpatientsexperienceabestspectacle-corrected visual acuity (VA) of at least after DSAEK. 3 Factors that can limit VA after DSAEK include preexisting retinal disease or amblyopia, preexisting stromal scarring, and, potentially, age. 4 In 2007, the Eye Bank of America Association reported that 85% of all grafts performed in the United States for endothelial disease were DSAEK procedures, approximating corneal transplant procedures. Another potential limitation to best spectaclecorrected VA after DSAEK in patients with Fuchs dystrophy could include stromal scarring due to longstanding disease. In this study, we created a histologic grading system to systematically evaluate DSAEK specimens received in our pathology laboratory to determine whether a correlation existed between the severity of pathologic changes noted in the specimen and post- DSAEK visual outcome. Assuming that more severe pathologic changes among DSAEK specimens correlate with the severity of stromal changes, we hypothesize that lowerthan-expected post-dsaek VA can be attributed to these stromal changes that remain even after the removal and replacement of the pathologic Descemet membrane. Therefore, early DSAEK in Fuchs dystrophy could prevent formation of these secondary stromal changes and result in improved postoperative visual outcome. In contrast, if an association does not exist between histopathologic findings and postoperative VA, then we suggest that stromal changes may not be a significant factor in determining outcome. It is also possible that the histopathologic severity of Descemet membrane changes does not correlate with the severity of stromal changes. METHODS The study design was retrospective and included 92 DSAEK specimens that were sent to the University of Wisconsin Eye Pathology Laboratory with a clinical diagnosis of Fuchs dystrophy from 3 separate corneal surgeons (C.R.C., D.R.H., and S.N.). All corneal tissue was prepared using an automated microkeratome. The specimens were fixed in a buffered solution of 10% formalin and processed for light microscopy. Staining for light microscopy included hematoxylin-eosin and periodic acid-schiff stains. Table 1. Grading System for Histologic Changes Observed in DM Light Microscopy Histologic Grading Characteristics Description of Grading Score Guttae dispersion None present 0 Present along 30% of DM 1 Present along 30% to 70% of DM 2 Present along 70% of DM 3 Laminated DM a Absent 0 Present 1 Embedded guttae b Absent 0 Present 1 Density of guttae c to to Overall grade d Mild 0 to 3 Moderate 4 to 6 Severe 7 to 9 Abbreviation: DM, Descemet membrane. a Indicates presence of a less brightly staining periodic acid-schiff layer. b Indicates guttae found buried within the fibrillar layer. c Calculated as the average of 10 high-power fields at 40 magnification. d Category is based on total score. We created a histologic grading system based on common characteristics observed under light microscopy among DSAEK specimens. Table 1 describes the 4 characteristics and grading system used to calculate a total histologic score. The 4 characteristics include guttae dispersion, presence of a laminated Descemet membrane, presence of embedded guttae, and density of guttae. Based on the total score, cases were divided into mild, moderate, or severe categories. Institutional review board approval was obtained and clinical data were recorded for each patient, including preoperative VA and postoperative VA at 2, 3, and 6 months and 1 and 2 years. Comorbid ocular diseases and surgical complications, including intraoperative complications, graft dehiscence, graft decentration, the need for rebubbling, graft failure, donor folds, and interface haze, were all recorded if observed. Snellen VA scores were converted to a logmar scale for ease of statistical analysis. Regression models were built between the preoperative VA and the 6-month and 1- and 2-year postoperative VAs. The components of the histologic score are listed in Table 1. RESULTS A total of 92 cases were sent to the University of Wisconsin Eye Pathology Laboratory during the study period. Thirteen cases were excluded from the study because of either graft failure(n=3) or visually significant comorbid ocular disease (n=10). A significant number of patients had correctable comorbid ocular disease, such as a cataract or posterior capsular opacity, and were included in the study if they received corrective surgery at the time of their DSAEK or afterward. Three patients underwent corrective procedures for cataract or posterior capsular opacity after their initial DSAEK, and their best-corrected VA after the corrective procedure was used for statistical analysis of postoperative VA. The data from 2 additional patients with unusual results were omitted from regression analysis but are included in Figure 1 and Figure 2. 34
3 A Simple linear regression 6 mo B Piecewise linear regression 6 mo No benefit from DSAEK Linear model estimate C 12 mo D 12 mo E 24 mo F 24 mo Figure 1. Simple linear regression of preoperative and postoperative visual acuity (VA) (A, C, and E) and a piecewise linear regression (B, D, and F). For the preoperative VA, data points are staggered slightly to show multiple points that have the same value. Patients vision improved regardless of preoperative vision. This trend is observed at the 6-, 12-, and 24-month end points. DSAEK indicates Descemet membrane stripping automated endothelial keratoplasty. We found no significant relationship between the individual histologic features in Table 1 and preoperative VA using individual regressions and stepwise selection among the 4 features. Furthermore, there was no significant association between preoperative vision and the histologic score (regression, P=.58). Preoperative and final VA were mildly correlated (regression, P=.005) as shown in Figure 1A, C, and E. The 35
4 A 6-Month Postoperative VA, Log MARScale No benefit from DSAEK Simple regression line Neither Both B 6-Month No benefit from DSAEK Simple regression line Figure 2. Correlation of laminated appearance and embedded guttae in patients undergoing Descemet membrane stripping automated endothelial keratoplasty (DSAEK). A, Patients with no concordant lamination and no embedded guttae (neither) and with both concordant lamination and embedded guttae (both). B, Patients with lamination without embedded guttae. For the preoperative visual acuity (VA), data points are staggered slightly to show multiple points that have the same value. The subgroup of patients with lamination and no embedded guttae appears to be less responsive to DSAEK. Although axes are logmar scale, equivalent Snellen lines are indicated. Table 2. Coincidence of Laminated Appearance and Embedded Guttae a Lamination Present Embedded Guttae Present No All Patients estimated improvement, starting from the study average preoperative VA of, was 0.18 (95% CI, ), suggesting that the average benefit of DSAEK and postoperative follow-up was approximately 2 Snellen lines. The regression slope was 0.14 (95% CI, 4-4), implying that patients with poorer preoperative vision had greater postoperative gains. A slope of 1 implies a constant benefit of DSAEK regardless of preoperative vision; if DSAEK were to restore every person to the same vision, we would find a 0 slope. As a result of this observed insensitivity to preoperative VA, patients with a starting VA worse than or or better were regressed separately. The linear models (Figure 1B, D, and F) suggest that patients visual improvement was relative to their preoperative vision until a plateau was reached at a starting VA of. At that point, patients appeared to have constant improvement to a postoperative VA of at 6 months and approaching at 24 months. Although the univariate regression of preoperative VA was associated with postoperative VA (R 2 =0.115 [overall F test, P=.002]), models that included the 4 graded histologic factors did not explain substantially Yes No Yes All Patients a Data are expressed as number of patients. more variation and did not improve this association significantly (guttae, R 2 =0.126 [analysis of variance (ANOVA) F test, P=.99]; embedded guttae, R 2 =0.143 [ANOVA F test, P=.30]; lamination, R 2 =0.120 [ANOVA F test, P=.81]; and density of guttae, R 2 =0.174 [ANOVA F test, P=.77]). Laminated appearance and embedded guttae were highly correlated (Table 2), but there was a small subset of patients with lamination (8 of 79) who did not have embedded guttae. These patients appeared to not share the same benefits of DSAEK as were received by patients with concordant lamination and embedding (ANOVA F test, P.001). Although they improved by 2 Snellen lines on average, patients in this subgroup with extremely poor vision still had poor visual outcomes (Figure 2). After exclusion of the 13 cases, 79 were graded histologically and divided into mild, moderate, or severe histologic findings on the basis of the grading system created to evaluate changes observed on the Descemet membrane (Table 1). This resulted in a total of 20 mild cases (score, 0-3), 40 moderate cases (score, 4-6), and 19 severe cases (score, 7-9). Ten mild cases (50%), 22 moderate cases (55%), and 13 severe cases (68%) had a 6-month postoperative VA of or better (Table 3). No association between histologic score and 6-month postoperative VA of or better was seen ( 2 test, P=.48). Overall, 23 of the 79 cases (29%) achieved a VA of or better at the 6-month postoperative follow-up (Table 3). Among these 23 cases, 6 were graded as histologically mild; 12, histologically moderate; and 5, histologically severe. No association between histologic score and 6-month postoperative VA of or better was seen ( 2 test, P=.95). 36
5 Because VA improved uniformly over time (Figure 1), no association between improvement and histologic score was apparent at later time points (at 12 months, 2 test, P=.21; at 24 months, 2 test, P=.41). Notably, 19 of 49 patients with 2 years of follow-up had improved VA to better than. COMMENT The goal of this study was to examine whether changes occurring within the corneal stroma in patients with Fuchs dystrophy would limit their best-corrected VA after undergoing DSAEK. Although we had hypothesized that more advanced disease would be associated with poor visual outcomes, our results indicated that postoperative vision is not related to the histologic severity of disease. Histologic factors were also not associated with preoperative vision. We identified a subgroup of patients, those with laminated Descemet membrane and no embedded guttae, who appear to not share the same benefits of DSAEK. Postoperative vision in these patients improved by a fixed amount relative to their starting vision. The laminated architecture of the Descemet membrane without embedded guttae may facilitate the separation between the layers of membrane and, thus, incomplete removal of the recipient s Descemet membrane during DSAEK, which may then limit the postoperative visual outcome. 5 This histologic presentation warrants further study because it was rare and did not seem to fit the expected progression of disease. Descemet membrane is produced by corneal endothelial cells and becomes thickened in Fuchs dystrophy. Normally, it consists of 2 layers. The anterior banded layer is present at birth and remains approximately 3 µm thick, whereas the posterior nonbanded layer becomes progressively thicker with age, ranging from approximately 3 µm at 20 years of age to 10 µm at 80 years of age. 2 In patients with Fuchs dystrophy, the anterior layer remains relatively constant and the posterior nonbanded layer thins. This posterior layer is often replaced by as many as 2 additional layers: a banded layer and a loose collagen fibrillar layer. 6 When present, the fibrillar layer is located between the endothelium and the abnormal posterior layer. This fibrillar layer is thought to become more prominent as the disease progresses. 2 Descemet membrane can increase in thickness up to 20 µm. 2 The presence of these additional layers is not pathognomonic for Fuchs dystrophy because they have also been observed in other forms of bullous keratopathies. 6 Fuchs dystrophy is characterized by the presence of centrally located, anvil-shaped excrescences, termed guttae, along the posterior surface of the Descemet membrane, which become more numerous and spread peripherally as the disease progresses. 2 Guttae seen in Fuchs dystrophy are contiguous with the abnormal posterior banded layer. Histologically, the fibrillar layer creates a laminated appearance and can bury guttae within the thickened Descemet membrane. The buried guttae are best distinguished with periodic Table 3. Histologic Score Groupings and Correlation With Best-Corrected VA a Histologic Score 6-mo Postoperative Best-Corrected VA b All Patients Mild Moderate Severe All Scores c Mild Moderate Severe All Scores Abbreviation: VA, visual acuity. a Data are expressed as number of patients. Differences between groups were tested using the 2 test (df = 2). b P =.48. c P =.95. acid-schiff stain, which stains the guttae and the surrounding basement membrane with variable intensity. The other clinical hallmark of Fuchs dystrophy is corneal edema. As progressive endothelial cell loss occurs, the surviving cell population flattens and spreads to maintain an intact monolayer of endothelium. Stromal edema develops as endothelial cells become progressively less able to maintain their barrier and pump function. Stromal changes seen under electron microscopy in Fuchs dystrophy include lipid keratopathy, intrakeratocytic and extrakeratocytic granular material, and degenerated keratocytes. 6 These stromal changes have occurred with greater incidence in Fuchs dystrophy compared with bullous keratopathy, potentially because of prolonged corneal edema. 6 Although we were not able to evaluate the host corneal stroma directly, we hypothesized that increasing severity of pathologic findings among DSAEK specimens corresponded with increasing severity of stromal changes. However, our study found no correlation between the severity of histologic changes observed in the Descemet membrane and best-corrected postoperative VA. Therefore, it is possible that the stromal changes are not permanent or do not correlate with the severity of pathologic changes observed in Descemet membrane specimens. Submitted for Publication: December 7, 2010; final revision received April 28, 2011; accepted April 29, Author Affiliations: Duluth Family Medicine Residency Program, Duluth, Minnesota (Dr Happ); Department of Ophthalmology and Visual Sciences, University of Wisconsin School of Medicine and Public Health (Drs Lewis, Potter, Croasdale, Nehls, Rowe, Khedr, and Albert), Department of Statistics, University of Wisconsin- Madison (Mr Eng), and Davis Duehr Dean Clinic (Dr Croasdale), Madison, Wisconsin; Department of Neurology, University of Louisville, Louisville, Kentucky (Dr Neekhra); Department of Ophthalmology, University of Minnesota, Minneapolis (Dr Hardten); and Ophthalmology LTD, Sioux Falls, South Dakota (Dr Eide). 37
6 Correspondence: Daniel M. Albert, MD, MS, Department of Ophthalmology and Visual Sciences, University of Wisconsin Madison, Room K6/412 Clinical Science Center, 600 Highland Ave, Madison, WI Financial Disclosure: None reported. Funding/Support: This study was supported by core grant for vision research P30 EY from the National Institutes of Health and by an unrestricted department award from Research to Prevent Blindness. Disclaimer: Dr Albert is the editor of the Archives of Ophthalmology. He was not involved in the editorial evaluation or decision to accept this article for publication. Online-Only Material: This article is featured in the Archives Journal Club. Go to to download teaching PowerPoint slides. REFERENCES 1. Klintworth GK. Corneal dystrophies. Orphanet J Rare Dis. 2009;4:7. doi: / Borboli S, Colby K. Mechanisms of disease: Fuchs endothelial dystrophy. Ophthalmol Clin North Am. 2002;15(1): Koenig SB, Covert DJ. Early results of small-incision Descemet s stripping and automated endothelial keratoplasty. Ophthalmology. 2007;114(2): Price MO, Price FW Jr. Descemet s stripping with endothelial keratoplasty: comparative outcomes with microkeratome-dissected and manually dissected donor tissue. Ophthalmology. 2006;113(11): Dapena I, Ham L, Moutsouris K, Melles GRJ. Incidence of recipient Descemet membrane remnants at the donor-to-stromal interface after descemetorhexis in endothelial keratoplasty. Br J Ophthalmol. 2010;94(12): Yuen HK, Rassier CE, Jardeleza MS, et al. A morphologic study of Fuchs dystrophy and bullous keratopathy. Cornea. 2005;24(3): Archives Web Quiz Winner C ongratulations to the winner of our August quiz, Bikramjit P. Pal, DNB, DO, FICO, Shri Bhagwan Mahavir Vitreoretinal Services, Sankara Nethralaya, Chennai, India. The correct answer to our August challenge was acquired vasoproliferative retinal tumor. For a complete discussion of this case, see the Research Letters section in the September Archives (Chow CC, Blair MP, Shapiro MJ. Acquired vasoproliferative retinal tumor: a late sequela of retinopathy of prematurity. Arch Ophthalmol. 2011;129[9]: ). Be sure to visit the Archives of Ophthalmology Web site ( and try your hand at Clinical Challenge Interactive Quiz. We invite visitors to make a diagnosis based on selected information from a case report or other feature scheduled to be published in the following month s print edition of the Archives. The first visitor to our Web editors with the correct answer will be recognized in the print journal and on our Web site and will also be able to choose one of the following books published by AMA Press: Clinical Eye Atlas, Clinical Retina, orusers Guides to the Medical Literature. 38
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