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Corneal Deformation Response and Ocular Geometry: a Noninvasive Diagnostic Strategy in Marfan Syndrome

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Corneal Deformation Response and Ocular Geometry: a Noninvasive Diagnostic Strategy in Marfan Syndrome Corneal Deformation Response and Ocular Geometry: A Noninvasive Diagnostic Strategy in Marfan Syndrome LAUREN C. BEENE, ELIAS I. TRABOULSI, IBRAHIM SEVEN, MATTHEW R. FORD, ABHIJIT SINHA ROY, ROBERT S. BUTLER, AND WILLIAM J. DUPPS, JR PURPOSE: To evaluate corneal air-puff deformation syndrome, including increased deformation, decreased responses and ocular geometry as predictors of Marfan bending resistance, and decreased energy dissipation syndrome. capacity. A predictive model incorporating HLA and DESIGN: Prospective observational clinical study. corneal curvature shows greatest potential for noninva- METHODS: Sixteen investigator-derived, 4 standard sive clinical diagnosis of Marfan syndrome. (Am J Ocular Response Analyzer (ORA), and geometric vari- Ophthalmol 2016;161:56–64. Ó 2016 by Elsevier Inc. ables from corneal tomography and optical biometry using All rights reserved.) Oculus Pentacam and IOL Master were assessed for discriminative value in Marfan syndrome, measuring right eyes of 24 control and 13 Marfan syndrome sub- ARFAN SYNDROME IS AN AUTOSOMAL DOMI- jects. Area under the receiver operating characteristic nant connective tissue disorder caused by muta- 1 (AUROC) curve was assessed in univariate and multivar- M tions in FBN1. Clinical diagnosis currently iate analyses. conforms to the Ghent criteria, most recently revised in 2 RESULTS: Six investigator-derived ORA variables suc- 2010. These diagnostic criteria have evolved since the cessfully discriminated Marfan syndrome. The best lone original description by Antoine-Bernard Marfan in 1896, disease predictor was Concavity Min (Marfan syndrome reflecting challenges presented by a broad phenotypic spec- 47.5 ± 20, control 69 ± 14, P [ .003; AUROC [ trum and the age-dependent nature of individual abnor- 0.80). Corneal hysteresis (CH) and corneal resistance malities, as well as advances in our understanding of the factor (CRF) were decreased (Marfan syndrome CH genetic etiology of Marfan syndrome and differentiation 2–6 9.45 ± 1.62, control CH 11.24 ± 1.21, P [ .01; Marfan from related conditions. Early diagnosis is of crucial syndrome CRF 9.77 ± 1.65, control CRF 11.03 ± 1.72, importance in Marfan syndrome owing to the life- P [ .01) and corneas were flatter in Marfan syndrome threatening sequelae of cardiac and vascular pathology. (Marfan syndrome Kmean 41.25 ± 2.09 diopter, control While the estimated prevalence of Marfan syndrome has Kmean 42.70 ± 1.81 diopter, P [ .046). No significant been cited at 2–3 in 10 000, an exact prevalence is difficult differences were observed in central corneal thickness, to measure owing to presumed underdiagnosis of this 7,8 axial eye length, or intraocular pressure. A multivariate condition. regression model incorporating corneal curvature and The role of the ocular examination in diagnosing Marfan hysteresis loop area (HLA) provided the best predictive syndrome has gained prominence with the revised Ghent value for Marfan syndrome (AUROC [ 0.85). criteria, as the presence of ectopia lentis with aortic dila- >_ 2 CONCLUSIONS: This study describes novel biodynamic tion (Z-score 2) is currently sufficient for diagnosis. How- features of corneal deformation responses in Marfan ever, the only other ocular feature officially considered in diagnosis is myopia greater than 3 diopters (D), which has questionable specificity for this condition.2 The poten- Accepted for publication Sep 22, 2015. tial for ocular abnormalities to aid in diagnosis may be From the Case Western Reserve University School of Medicine (L.C.B.); the Center for Genetic Eye Diseases (L.C.B., E.I.T.) and much greater than currently acknowledged, as fibrillin-1 Ocular Biomechanics & Imaging Laboratory (I.S., M.R.F., A.S.R., microfibrils that are abnormally formed owing to the W.J.D.), Cole Eye Institute, Cleveland Clinic Foundation; the disease-causing mutations in FBN1 are widely distributed Department of Biomedical Engineering, Case Western Reserve 9 University (M.R.F., W.J.D.); and Quantitative Health Sciences (R.S.B.) in the human eye. Histologic study of fibrillin-1 microfi- and the Department of Biomedical Engineering (W.J.D.), Cleveland brils in the Marfan syndrome eye found differences in Clinic Lerner Research Institute, Cleveland, Ohio. both quantity and quality of microfibrils, and it is possible Lauren Beene is now affiliated with Rainbow Babies & Children’s Hos- pital, University Hospitals Case Medical Center, Cleveland, Ohio. Abhi- that the impact of their malformation likely leads to global 10,11 jit Sinha Roy is now affiliated with Biomechanics and Mathematical ocular changes. Modeling Solutions Lab, Narayana Nethralaya, Bangalore, India. Investigation of biomechanical and dynamic changes in Inquiries to William J. Dupps, Jr, Cole Eye Institute, Cleveland Clinic, 9500 Euclid Ave/i-32, Cleveland, OH 44195; e-mail: bjdupps@sbcglobal. tissues that contain abnormal fibrillin-1 is a reasonable net next step in refining the approach to diagnosing Marfan 56 Ó 2016 BY ELSEVIER INC.ALL RIGHTS RESERVED. 0002-9394/$36.00 http://dx.doi.org/10.1016/j.ajo.2015.09.027 syndrome. Abnormalities in corneal biomechanical prop- of Marfan syndrome per the 1996 or 2010 Ghent criteria, erties, or, more precisely, behavior as measured by the tech- based on clinical examinations from ophthalmology, cardi- niques used in the present study, have been detected in a ology, and medical genetics, and were all established pa- variety of corneal disorders and postoperative conditions, tients from the Cole Eye Institute, Cleveland Clinic or including Fuchs dystrophy,12 post–laser in situ keratomil- the University Hospitals Case Medical Center. Partici- eusis (LASIK) eyes,12,13 and keratoconus,12,14–16 a disease pants were evaluated between October 2012 and July characterized by stromal degeneration and disruption of 2013. Individuals who had undergone any kind of ocular Bowman membrane, of which fibrillin-1 is a component.9 surgery or who only had a suspected diagnosis of Marfan Differences between normal and Marfan syndrome corneas syndrome were excluded from this study. The second group have been previously observed at the microscopic and clin- included healthy age-matched volunteers without history of ical levels. Specifically, Iordanidou and associates evalu- Marfan syndrome or other connective tissue diseases or con- ated Marfan syndrome corneas using confocal microscopy ditions that could affect the health and shape of the cornea, and found highly reflective interconnected lines between such as keratoconus. In total, 13 right eyes of participants keratocytes in the extracellular matrix of over half of with a confirmed diagnosis of Marfan syndrome and 24 right Marfan syndrome corneas, and brightly reflective particles eyes of age-matched controls were evaluated in this study. in the endothelium in Marfan syndrome corneas exclu- 17 sively. Additionally, clinical differences in corneal curva- MEASUREMENTS: The ORA (Reichert Ophthalmic In- ture have been observed repeatedly, as numerous studies struments, Buffalo, New York, USA) assesses corneal have found the Marfan syndrome cornea to be flatter biomechanical behavior through measurement of corneal than non–Marfan syndrome corneas.18–21 Based on these hysteresis (CH) and other features of the corneal deforma- many observations of differences in the Marfan syndrome tion response. Hysteresis is a measurement of the energy cornea, it is reasonable to suspect that corneal absorptive capacity of viscoelastic tissues that undergo deformation responses in Marfan syndrome may also be time-dependent strain upon deformation. The ORA mea- altered.20 sures corneal hysteresis through application of a variable Biomechanical behaviors of the cornea can be assessed air impulse to the central cornea with simultaneous moni- in vivo using the Ocular Response Analyzer (ORA). To toring of the magnitude of corneal deformation using an date, only 1 study has investigated the biomechanical infrared electro-optical collimation detector system.12 behavior in the corneas of individuals with Marfan syn- The pressure and deformation data can be exported for drome.22 Here we expand on the investigation of alter- custom analysis. An illustrative example is provided in ations in biomechanical behavior in corneas of the Figure, with the solid line depicting the pressure individuals with Marfan syndrome, using investigator- applied to the cornea and the dotted line representing derived ORA variables described by Hallahan and associ- corneal deformation. The intensity of photons reflected ates and found to have high predictive value for detecting off the cornea is greatest when the corneal surface is rela- keratoconus.16 We assess the capacity of the corneal defor- tively planar, which occurs at relative applanation. The mation responses to predict a diagnosis of Marfan syndrome cornea passes through 2 points of applanation as it indents both independently and in conjunction with geometric and regains shape. The ORA measures corneal hysteresis as measurements of the Marfan cornea, including corneal cur- the difference in external pressure at these 2 points of vature, central corneal thickness, and axial eye length. applanation, P1 and P2.12 Through this investigation, we explore the possibility of a The ORA also measures the corneal resistance factor novel diagnostic algorithm that may be clinically useful (CRF), which is related to the same pressure values from which in diagnosing future cases of Marfan syndrome. corneal hysteresis is derived. CRF is biased toward the pressure
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