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      Imaging and Quantification of Subbasal Nerve Plexus in Healthy Volunteers and Diabetic Patients with or without Retinopathy

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          Abstract

          Background

          The alterations of subbasal nerve plexus (SBP) innervation and corneal sensation were estimated non-invasively and compared with the values in healthy volunteers. Additionally, this study addressed the relation of SBP changes to the retinal status, glycemic control and diabetes duration.

          Methodology/Principal Findings

          Eighteen eyes of diabetic patients with peripheral diabetic neuropathy aged 68.8±8.8 years and twenty eyes of healthy volunteers aged 66.3±13.3 yrs. were investigated with in vivo confocal laser-scanning microscopy (CLSM). An adapted algorithm for image analysis was used to quantify the morphological and topological properties of SBP. These properties were correlated to incidence of diabetic retinopathy (DR) and corneal sensation (Cochet-Bonnet esthesiometer). The developed algorithm allows a fully automated analysis of pre-segmented SBP structures. Altogether, 10 parameters were analysed, and all of them revealed significant differences between diabetic patients and healthy volunteers. The nerve fibre density, total fibre length and nerve branches were found to be significantly lower in patients with diabetes than those of control subjects (nerve fibre density 0.006±0.002 vs. 0.020±0.007 mm/mm 2; total fibre length 6223±2419 vs. 19961±6553 µm; nerve branches 25.3±28.6 vs. 141.9±85.7 in healthy volunteers). Also the corneal sensation was significantly lower in diabetic group when compared to controls (43±11 vs. 59±18 mm). There was found no difference in SBP morphology or corneal sensation in the subgroups with (DR) or without (NDR) diabetic retinopathy.

          Conclusions/Significance

          SBP parameters were significantly reduced in diabetic patients, compared to control group. Interestingly, the SBP impairment could be shown even in the diabetic patients without DR. Although automatic adapted image analysis simplifies the evaluation of in vivo CLSM data, image acquisition and quantitative analysis should be optimised for the everyday clinical practice.

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          Most cited references39

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          Corneal confocal microscopy: a non-invasive surrogate of nerve fibre damage and repair in diabetic patients.

          N Efron, Wiley Abbott, P Kallinikos … (2003)
          The accurate detection, characterization and quantification of human diabetic neuropathy are important to define at risk patients, anticipate deterioration, and assess new therapies. Corneal confocal microscopy is a reiterative, rapid, non-invasive in vivo clinical examination technique capable of imaging corneal nerve fibres. The aim of this study was to define the ability of this technique to quantify the extent of degeneration and regeneration of corneal nerve fibres in diabetic patients with increasing neuropathic severity. We scanned the cornea and collected images of Bowman's layer (containing a rich nerve plexus) from 18 diabetic patients and 18 age-matched control subjects. Corneal nerve fibre density (F(3)=9.6, p<0.0001), length (F(3)=23.8, p<0.0001), and branch density (F(3)=13.9, p<0.0001) were reduced in diabetic patients compared with control subjects, with a tendency for greater reduction in these measures with increasing severity of neuropathy. Corneal confocal microscopy is a rapid, non-invasive in vivo clinical examination technique which accurately defines the extent of corneal nerve damage and repair and acts as a surrogate measure of somatic neuropathy in diabetic patients. It could represent an advance to define the severity of neuropathy and expedite assessment of therapeutic efficacy in clinical trials of human diabetic neuropathy.
          Article 0 comments Cited 132 times – based on 0 reviews     Review now
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            Corneal Confocal Microscopy

            Mitra Tavakoli, Cristian Quattrini, Caroline Abbott … (2010)
            OBJECTIVE The accurate quantification of human diabetic neuropathy is important to define at-risk patients, anticipate deterioration, and assess new therapies. RESEARCH DESIGN AND METHODS A total of 101 diabetic patients and 17 age-matched control subjects underwent neurological evaluation, neurophysiology tests, quantitative sensory testing, and evaluation of corneal sensation and corneal nerve morphology using corneal confocal microscopy (CCM). RESULTS Corneal sensation decreased significantly (P = 0.0001) with increasing neuropathic severity and correlated with the neuropathy disability score (NDS) (r = 0.441, P 3) defined an NFD of 6) defined a NFD cutoff of <20.8/mm2 with a sensitivity of 0.71 (0.42–0.92) and specificity of 0.64 (0.54–0.74). CONCLUSIONS CCM is a noninvasive clinical technique that may be used to detect early nerve damage and stratify diabetic patients with increasing neuropathic severity.
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              Morphology of corneal nerves using confocal microscopy.

              N Efron, P Soto (2001)
              The aim of the current study was to evaluate the distribution and morphology of corneal nerves as seen by means of white light confocal microscopy. This study analyzed images of corneal nerves that were obtained using the Tomey Confoscan slit scanning confocal microscope (40x/0.75 objective lens). The images were classified according to their location within the cornea. The objective and subjective evaluation of the images involved measuring, grading, or judging a number of parameters from both individual pictures and from each single nerve fiber within any image. The in vivo observations made in this work are in agreement with those of previous histologic studies. The general scheme of corneal innervation is described as originating from thick and straight stromal nerve trunks that extend lateral and anteriorly and give rise to plexiform arrangements of progressively thinner nerve fibers at several levels within the stroma. From there, nerve fibers perforate Bowman's layer and eventually form a dense neural plexus just beneath the basal epithelial cell layer, which is characterized by tortuous and thin beaded nerve fibers interconnected by numerous nerve elements; nerve fibers from this plexus are known to be responsible for the innervation of the epithelium. This study provides convincing evidence of the suitability of confocal microscopy to image corneal nerves, the only drawback being the limited resolution in terms of the differentiation of the ultrastructure of nerve bundles.
              Article 0 comments Cited 88 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Friedemann Paul: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, USA )
                ISSN (Electronic): 1932-6203
                Publication date Collection: 2013
                Publication date (Electronic): 15 January 2013
                Volume: 8
                Issue: 1
                Electronic Location Identifier: e52157
                Affiliations
                [1 ]Department of Ophthalmology, University of Rostock, Rostock, Germany
                [2 ]Translational Centre for Regenerative Medicine (TRM), University of Leipzig, Leipzig, Germany
                [3 ]Clinic of Internal Medicine I, Klinikum Südstadt, Rostock, Germany
                [4 ]Institute for Biostatistics and Informatics in Medicine and Ageing Research, University of Rostock, Rostock, Germany
                [5 ]Institute of Medical Biochemistry and Molecular Biology, University of Rostock, Rostock, Germany
                Charité University Medicine Berlin, Germany
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AZ HS RFG OS. Performed the experiments: AZ SP VH HS. Analyzed the data: AZ KW MH GK SB OS. Wrote the paper: AZ KW MH RFG OS.

                Article
                Publisher ID: PONE-D-12-10080
                DOI: 10.1371/journal.pone.0052157
                PMC ID: 3546080
                PubMed ID: 23341892
                SO-VID: d3b066c7-8449-4877-8a79-f7f9d793fe63
                Copyright statement: Copyright @ 2013
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 10 April 2012
                Date accepted : 12 November 2012
                Page count
                Pages: 8
                Funding
                The study was generously supported by the DFG (Deutsche Forschungsgemeinschaft) (Transregio 37, Micro- and Nanosystems in Medicine – Reconstruction of Biological Functions). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Medicine
                Subject: Anatomy and Physiology
                Subject: Ocular System
                Subject: Ocular Anatomy
                Subject: Endocrinology
                Subject: Diabetic Endocrinology
                Subject: Diabetes Mellitus Type 2
                Subject: Neurology
                Subject: Neuroimaging
                Subject: Ophthalmology
                Subject: Corneal Disorders
                Subject: Retinal Disorders

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                ScienceOpen disciplines: Uncategorized

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