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• W2017010838 abstract "In this issue of Ophthalmology, 2 articles examine the anatomic features that largely determine the corneal tissue response in the performance of 2 evolving corneal transplantation procedures: Descemet's membrane endothelial keratoplasty (DMEK), by Schlötzer-Schrehardt et al,1Schlötzer-Schrehardt U. Bachmann B.O. Tourtas T. et al.Reproducibility of graft preparations in Descemet's membrane endothelial keratoplasty.Ophthalmology. 2013; 120: 1769-1777Abstract Full Text Full Text PDF PubMed Scopus (54) Google Scholar and deep anterior lamellar keratoplasty (DALK), by Dua et al.2Dua H.S. Faraj L.A. Said D.G. et al.Human corneal anatomy redefined: a novel pre-Descemet's layer (Dua's layer).Ophthalmology. 2013; 120: 1778-1785Abstract Full Text Full Text PDF PubMed Scopus (243) Google Scholar These articles have similar themes, exploring the structural biology that may determine the success or failure of these 2 different surgical procedures, both of which operate on the very posterior limits of the corneal stroma and posterior limiting lamina (Descemet's membrane). Importantly, both articles intersect the often neglected but increasingly important fields of structural biology and biomechanics, in that DMEK and DALK apply strain to different corneal layers to induce delamination of Descemet's membrane from the posterior stroma. Perhaps the first investigator to recognize the importance of corneal structure to mechanics was William Bowman,3Bowman W. Lectures on the parts concerned in the operations on the eye, and on the structure of the retina. Royal London Ophthalmic Hospital, Moorfields, London1847Google Scholar who identified collagen fibers that ran in slanting directions from the anterior limiting lamina (Bowman's layer) across stromal lamellae, as shown in his classic drawing from his 1847 monograph (Fig 1). At that time, Bowman made this insightful comment: “This arrangement might, I imagine, be shown on mechanical principals, to be the best possible for the maintenance of the convexity of the front of the cornea.” This structural and mechanical relationship also was suggested by the work of Linda Muller, who used extreme swelling of the cornea to show that the anterior stroma resisted swelling to maintain corneal curvature, a property at the time associated with lamellar interweaving.4Muller L.J. Pels E. Vrensen G.F. The specific architecture of the anterior stroma accounts for maintenance of corneal curvature.Br J Ophthalmol. 2001; 85: 437-443Crossref PubMed Scopus (308) Google Scholar More recent studies have demonstrated that the resistance of the stroma to transverse shear strain is highest in the anterior stroma and decreases with depth5Petsche S.J. Chernyak D. Martiz J. et al.Depth-dependent transverse shear properties of the human corneal stroma.Invest Ophthalmol Visual Sci. 2012; 53: 873-880Crossref PubMed Scopus (93) Google Scholar and that these mechanical differences are associated with collagen fiber intertwining and branching, as shown originally by Bowman3Bowman W. Lectures on the parts concerned in the operations on the eye, and on the structure of the retina. Royal London Ophthalmic Hospital, Moorfields, London1847Google Scholar and more recently by Winkler et al6Winkler M. Chai D. Kriling S. et al.Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics.Invest Ophthalmol Visual Sci. 2011; 52: 8818-8827Crossref PubMed Scopus (147) Google Scholar using nonlinear optical imaging (Fig 2). Atomic force microscopy also has shown that different layers of the cornea have different mechanical stiffness and associated collagen fiber organization.7Last J.A. Thomasy S.M. Croasdale C.R. et al.Compliance profile of the human cornea as measured by atomic force microscopy.Micron. 2012; 43: 1293-1298Crossref PubMed Scopus (91) Google ScholarFigure 2A, Composite 3-dimensional reconstruction of the posterior human cornea at 0.22 μm/pixel resolution. Collagen fibers (magenta) were reconstructed based on second harmonic generated signals. Cell nuclei (green) were stained for using ethidium homodimer and imaged using confocal fluorescence microscopy. B, Cross-sectional view of the posterior human cornea taken from the same scan. Two nuclei are visible within 5 μm of the posterior limiting lamina (arrowheads). C, Close-up view of the highlighted region from (B). The dashed line is drawn 10 μm from the posterior limiting lamina. D = Descemet's membrane; S = stroma.View Large Image Figure ViewerDownload Hi-res image Download (PPT) Although interweaving of collagen fibers was noted first by Kokott8Kokott W. Uber mechanisch funktionelle strukturen des auges.Graefes Arch. 1938; 138: 425-485Crossref Scopus (61) Google Scholar in his seminal study published in 1938 (Fig 3), interlacing of collagen fibers within the stroma has been demonstrated more recently by Radner et al9Radner W. Mallinger R. Interlacing of collagen lamellae in the midstroma of the human cornea.Cornea. 2002; 21: 598-601Crossref PubMed Scopus (46) Google Scholar and Radner and Mallinger. 10Radner W. Zehetmayer M. Aufreiter R. Mallinger R. Interlacing and cross-angle distribution of collagen lamellae in the human cornea.Cornea. 1998; 17: 537-543Crossref PubMed Scopus (111) Google Scholar In these studies, it was evident that collagen fiber interlacing extends throughout the corneal stroma and may explain, in part, the puzzle posed by Maurice11Maurice D.M. Some puzzles in the microscopic structure of the stroma.J Refract Surg. 1999; 15: 692-694PubMed Google Scholar in 1999 regarding the cohesion of the cornea that keeps thin sections of the stroma from falling apart in water. As shown using nonlinear optical imaging, collagen fibers are not simply interwoven or interlaced, but are intertwined, suggesting that individual collagen fibrils, which are bundled together to form the fibers, may branch and anastomose independently with multiple fibers as they extend across the cornea (Fig 2). This effectively would interlink the entire stroma into one common fabric, with the density of intertwining defining the relative stiffness of the cornea moving from the anterior to posterior stroma and from the center to the periphery to control corneal shape. It also should be noted that collagen fibers show physical insertions into the anterior and posterior limiting laminas (Bowman's layer and Descemet's membrane, respectively),12Binder P.S. Rock M.E. Schmidt K.C. Anderson J.A. High-voltage electron microscopy of normal human cornea.Invest Ophthalmol Vis Sci. 1991; 32: 2234-2243PubMed Google Scholar, 13Mathew J.H. Bergmanson J.P. Doughty M.J. Fine structure of the interface between the anterior limiting lamina and the anterior stromal fibrils of the human cornea.Invest Ophthalmol Vis Sci. 2008; 49: 3914-3918Crossref PubMed Scopus (19) Google Scholar, 14Komai Y. Ushiki T. The three-dimensional organization of collagen fibrils in the human cornea and sclera.Invest Ophthalmol Vis Sci. 1991; 32: 2244-2258PubMed Google Scholar and that these attachments account for the cohesive properties of the cornea that keep both the corneal epithelium and endothelium effectively attached. In the context of our current understanding of the complex relationship between corneal structure and mechanical attributes of the cornea, the 2 articles published in this issue of Ophthalmology help us to define the implications of these interactions for DMEK and DALK. In DMEK, the cohesive forces that attach the posterior limiting lamina to the stroma, whether through direct collagen fiber insertions, as shown by Binder et al12Binder P.S. Rock M.E. Schmidt K.C. Anderson J.A. High-voltage electron microscopy of normal human cornea.Invest Ophthalmol Vis Sci. 1991; 32: 2234-2243PubMed Google Scholar and Komai and Ushiki,14Komai Y. Ushiki T. The three-dimensional organization of collagen fibrils in the human cornea and sclera.Invest Ophthalmol Vis Sci. 1991; 32: 2244-2258PubMed Google Scholar or through the presence of adhesive glycoproteins, as suggested in the report by Schlötzer-Schrehardt et al, show important individual variations that impact on the successful detachment of this membrane. In DALK, the behavior of the big bubble separation of the very posterior stroma suggests an inherent structural weakness in the interlamellar adhesive strength of the central cornea that was measured first by Smolek and McCarey,15Smolek M.K. McCarey B.E. Interlamellar adhesive strength in human eyebank corneas.Invest Ophthalmol Vis Sci. 1990; 31: 1087-1095PubMed Google Scholar and that is likely the result of the logarithmic decline in collagen fiber intertwining.6Winkler M. Chai D. Kriling S. et al.Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics.Invest Ophthalmol Visual Sci. 2011; 52: 8818-8827Crossref PubMed Scopus (147) Google Scholar The observation by Dua et al,2Dua H.S. Faraj L.A. Said D.G. et al.Human corneal anatomy redefined: a novel pre-Descemet's layer (Dua's layer).Ophthalmology. 2013; 120: 1778-1785Abstract Full Text Full Text PDF PubMed Scopus (243) Google Scholar indicating that the big bubble approach more frequently induces the separation of a 6- to 13-μm thick posterior stromal layer, suggests important spatial variations in stromal cohesiveness. Although the observations presented are novel and illuminate an important mechanical response to acutely introduced nonphysiologic strain, in our opinion, the data presented do not warrant the assignation of a new anatomic layer to the cornea. At the very least, it is premature without rigorous verification using optimally preserved specimens. As described above, detailed anatomic descriptions have been provided previously, and a very brief analysis in our hands demonstrates the presence of keratocytes within 5 μm of the posterior limiting lamina (Figure 2, Figure 4). This observation runs counter to a supposed hallmark of this so-called new layer, that is, acellularity. Using the terminology proposed is not justified in our opinion at this point and will only confuse the literature. It is also not in keeping with the recommended descriptive terminology outlined by Terminologia Anatomica.16Federative Committee on Anatomical Terminology (FCAT) Terminologia Anatomica. Thieme, Stuttgart1998Google Scholar In conclusion, these 2 articles help to fill in part an important gap in our understanding of the mechanical consequences of the structural biology of the cornea and how this relationship is critical to corneal surgery. It would be ideal to have a complete structural blueprint of the cornea on which new and more precise therapeutic and refractive procedures could be developed based on sound mechanical principles. In the meantime, we should all remember the admonition from Ecclesiastes 1:9: “There is nothing new under the sun.” Human Corneal Anatomy Redefined: A Novel Pre-Descemet's Layer (Dua's Layer)OphthalmologyVol. 120Issue 9PreviewTo define and characterize a novel pre-Descemet's layer in the human cornea. Full-Text PDF Reproducibility of Graft Preparations in Descemet's Membrane Endothelial KeratoplastyOphthalmologyVol. 120Issue 9PreviewTo assess the reproducibility of manual graft preparation and evaluate the incidence rate and nature of structural anomalies of Descemet's membrane (DM) preventing successful graft preparation in DM endothelial keratoplasty (DMEK). Full-Text PDF ErratumOphthalmologyVol. 120Issue 12PreviewPlease note that one of the authors' degrees in the publication entitled, “Lessons in Corneal Structure and Mechanics to Guide the Corneal Surgeon” (Ophthalmology 2013;120:1715-1717) had errors. The correct degrees for Dr. Jan P.G. Bergmanson should have been OD, PhD. Full-Text PDF Re: Jester et al.: Lessons in Corneal Structure and Mechanics to Guide the Corneal Surgeon (Ophthalmology 2013;120:1715-1717)OphthalmologyVol. 121Issue 4PreviewWe appreciate the well-constructed arguments and comments made by Jester et al1 in their editorial, part of which relates to our publication in the same issue of Ophthalmology.2 We acknowledge and accept their comments related to nomenclature and terminology. Full-Text PDF" @default.
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