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Atypical Cellular Elements of Unknown Origin in the Subbasal Nerve Plexus of a Diabetic Cornea Diagnosed by Large-Area Confocal Laser Scanning Microscopy

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Atypical Cellular Elements of Unknown Origin in the Subbasal Nerve Plexus of a Diabetic Cornea Diagnosed by Large-Area Confocal Laser Scanning Microscopy diagnostics Interesting Images Atypical Cellular Elements of Unknown Origin in the Subbasal Nerve Plexus of a Diabetic Cornea Diagnosed by Large-Area Confocal Laser Scanning Microscopy Katharina A. Sterenczak 1,* , Oliver Stachs 1,2, Carl Marfurt 3, Aleksandra Matuszewska-Iwanicka 4, Bernd Stratmann 5, Karsten Sperlich 1,2 , Rudolf F. Guthoff 1,2, Hans-Joachim Hettlich 4, Stephan Allgeier 6 and Thomas Stahnke 1,2 1 Department of Ophthalmology, Rostock University Medical Center, 18057 Rostock, Germany; [email protected] (O.S.); [email protected] (K.S.); [email protected] (R.F.G.); [email protected] (T.S.) 2 Department Life, Light & Matter, University of Rostock, 18059 Rostock, Germany 3 Department of Anatomy, Cell Biology & Physiology, Indiana University School of Medicine-Northwest, Gary, Indianapolis, IN 46204, USA; [email protected] 4 Eye Clinic, Johannes Wesling Klinikum Minden, Ruhr-University Bochum, 32429 Minden, Germany; [email protected] (A.M.-I.); [email protected] (H.-J.H.) 5 Heart and Diabetes Center NRW, Ruhr-University Bochum, 32545 Bad Oeynhausen, Germany; [email protected] 6 Institute for Automation and Applied Informatics, Karlsruhe Institute of Technology, 76344 Eggenstein-Leopoldshafen, Germany; [email protected] * Correspondence: [email protected] Citation: Sterenczak, K.A.; Stachs, O.; Abstract: In vivo large-area confocal laser scanning microscopy (CLSM) of the human eye using Marfurt, C.; Matuszewska-Iwanicka, A.; Stratmann, B.; Sperlich, K.; EyeGuidance technology allows a large-scale morphometric assessment of the corneal subbasal nerve Guthoff, R.F.; Hettlich, H.-J.; Allgeier, plexus (SNP). Here, the SNP of a patient suffering from diabetes and associated late complications S.; Stahnke, T. Atypical Cellular was analyzed. The SNP contained multiple clusters of large hyperintense, stellate-shaped, cellular- Elements of Unknown Origin in the like structures. Comparable structures were not observed in control corneas from healthy volunteers. Subbasal Nerve Plexus of a Diabetic Two hypotheses regarding the origin of these atypical structures are proposed. First, these structures Cornea Diagnosed by Large-Area might be keratocyte-derived myofibroblasts that entered the epithelium from the underlying stroma Confocal Laser Scanning Microscopy. through breaks in Bowman’s layer. Second, these structures could be proliferating Schwann cells Diagnostics 2021, 11, 154. https:// that entered the epithelium in association with subbasal nerves. The nature and pathophysiological doi.org/10.3390/diagnostics11020154 significance of these atypical cellular structures, and whether they are a direct consequence of the patient’s diabetic neuropathy/or a non-specific secondary effect of associated inflammatory processes, Academic Editor: Zhen Cheng are unknown. Received: 16 December 2020 Accepted: 19 January 2021 Keywords: in vivo large-area confocal laser scanning microscopy; subbasal nerve plexus; keratocyte- Published: 21 January 2021 derived myofibroblasts; Schwann cells; diabetes Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- iations. In vivo confocal laser scanning microscopy of the cornea. The cornea represents a biological barrier to and mediator of the external environment and consists of five dis- tinct layers: The epithelium, including the subbasal nerve plexus (SNP); Bowman’s layer; stroma; Descemet’s membrane; and the endothelium [1]. Each of these layers fulfills spe- cific biological functions which are crucial to ocular homeostasis. In addition, the cornea Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. is highly innervated by sensory nerves that exert important influences on the regulation This article is an open access article of corneal epithelial integrity and wound healing [2]. Corneal nerves lose their myelin distributed under the terms and sheathes soon after entering the cornea at the limbus and become essentially transparent; conditions of the Creative Commons thus, their clinical appearance was not amenable to in vivo evaluation until the develop- Attribution (CC BY) license (https:// ment of confocal laser scanning microscopy (CLSM) [3]. During in vivo CLSM, corneal creativecommons.org/licenses/by/ elements, including cells, the extracellular matrix, and nerves, scatter light at various 4.0/). degrees, making it possible to obtain high signal-to-noise images leading to high contrast Diagnostics 2021, 11, 154. https://doi.org/10.3390/diagnostics11020154 https://www.mdpi.com/journal/diagnostics Diagnostics 2021, 11, x FOR PEER REVIEW 2 of 7 Diagnostics 2021, 11, 154 2 of 7 elements, including cells, the extracellular matrix, and nerves, scatter light at various de- grees, making it possible to obtain high signal-to-noise images leading to high contrast microscopic imaging of the native cornea at the cellular level [4]. Several studies have shownmicroscopic that SNP imaging changes of the are nativenot characteristic cornea at the of cellularone specific level corneal [4]. Several pathology, studies but have re- flectshown non-specific that SNP changes pathological are not processes characteristic which of oneare specificpresent cornealin many pathology, corneal, butocular, reflect or systemicnon-specific diseases pathological [5,6] or processesarise as a whichresult areof a present therapy in regime, many corneal, such as ocular, that used or systemic to treat multiplediseases [myeloma5,6] or arise [7]. as The a result in vivo of aCLSM therapy scans regime, of the such SNP as within that used this tostudy treat were multiple per- formedmyeloma by [ 7using]. The Heidelbergin vivo CLSM Retina scans Tomograph of the SNP withinII (HRT this II,study Heidelberg were performed Engineering by GmbH,using Heidelberg Heidelberg, Retina Germany) Tomograph in combination II (HRT II, with Heidelberg an in-house Engineering modified GmbH, version Heidel- of the Rostockberg, Germany) Cornea Module in combination (RCM, Heidelberg with an in-house Engineering modified GmbH, version Heidelberg, of the Rostock Germany)— Cornea theModule RCM (RCM, 2.0—and Heidelberg the EyeGuidance Engineering system, GmbH, wh Heidelberg,ich enabled Germany)—the large-scale imaging RCM 2.0—and of the SNPthe EyeGuidance [8–10]. During system, conventional which enabledCLSM, single large-scale images imaging represent of thea standard SNP [8– 10area]. Duringof 0.16 2 mmconventional2 (Figure CLSM,1, inset single B), thereby images covering represent approximately a standard area 0.2% of 0.16 of mmthe average(Figure1 complete, inset B), cornealthereby surface, covering which approximately is insufficient 0.2% for of conducting the average a completereliable morphometric corneal surface, assessment which is ofinsufficient the complete for conducting SNP [5]. In a the reliable past, morphometric mosaicking approaches assessment of of single the complete images SNPhave [ 5been]. In proposedthe past, mosaicking in order to examine approaches the of SNP single on a images larger havescale. been The proposedEyeGuidance in order system to examineapplied inthe this SNP study on arepresents larger scale. a highly The automated EyeGuidance computer-controlled system applied in technique this study that represents facilitates a thehighly generation automated of mosaic computer-controlled images by using technique a moving that fixation facilitates target the which generation is presented of mosaic to theimages contralateral by using eye a moving [8,9]. Figures fixation 1 target and S1 which display is presented a normal toSNP the of contralateral a healthy volunteer eye [8,9]. usingFigure large-area1 and Figure CLSM. S1 display a normal SNP of a healthy volunteer using large-area CLSM. Figure 1. NormalNormal subbasal subbasal nerve nerve plexus plexus (SNP) (SNP) of ofa healthy a healthy volunteer volunteer obtained obtained from from a 55-year-old a 55-year-old male male using using large-area large- confocal laser scanning microscopy (CLSM). Numerous hyperintense subbasal nerves of varying diameters, many of area confocal laser scanning microscopy (CLSM). Numerous hyperintense subbasal nerves of varying diameters, many which are associated with dendritic cells, are visible (§, nerves of the SNP, and , dendritic cell) (high-resolution image of which are associated with dendritic cells, are visible (§, nerves of the SNP, and , dendritic cell) (high-resolution supplementary Figure S1). Inset (A): subbasal nerve (§) and dendritic cell (), and inset (B): single CLSM image (area 400 ×image 400 µm supplementary2). Figure S1). Inset (A): subbasal nerve (§) and dendritic cell (), and inset (B): single CLSM image (area 400 × 400 µm2). Patient’s history. The patient presented here has suffered from type 2 diabetes melli- Patient’s history. The patient presented here has suffered from type 2 diabetes melli- tus (DM) since 2005, with poorly adjusted blood-sugar control (HbA1c 9.5%). Further key tus (DM) since 2005, with poorly adjusted blood-sugar control (HbA1c 9.5%). Further key diagnoses include bilateral diabetic nephropathy (actual grade II), diabetic polyneuropa- diagnoses include bilateral diabetic nephropathy (actual grade II), diabetic polyneuropathy, thy, steatosis hepatitis, coronary vascular disease, arteriosclerosis, sleep apnea syndrome, steatosis hepatitis, coronary vascular disease, arteriosclerosis, sleep apnea syndrome, adi- adipositas grade III, and hyperlipidemia.
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