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      Role of Chronic Inflammation in Myopia Progression: Clinical Evidence and Experimental Validation

      research-article
      Author(s): a , b , c , d , e , f , g , h , a , b , i , b , e , j , *
      Publication date (Electronic):
      Journal: EBioMedicine
      Publisher: Elsevier
      Keywords: Systemic lupus erythematosus, SLE, type 1 diabetes mellitus, T1DM, monocular form deprivation, MFD, nuclear factor κB, NFκB, interleukin, IL, tumor necrosis factor α, TNF-α, cyclosporine A, CSA, lipopolysaccharide, LPS, peptidoglycan, PGN, collagen I, COL1, muscarinic acetylcholine receptor, mAChR, transforming growth factor β, TGF-β, matrix metalloproteinase 2, MMP2, juvenile chronic arthritis, JCA, refractive error, RE, National Health Insurance Research database, NHIRD, International Classification of Diseases, 9th Revision, Clinical Modification, ICD-9-CM, phosphate-buffered saline, PBS, Dulbecco’s Modified Eagle Medium, DMEM, fetal bovine serum, FBS, Tris-buffered saline, TBS, 4',6-diamidino-2-phenylindole, DAPI, extracellular signal-regulated kinase, ERK, protein kinase B, AKT, phosphoinositide 3-kinase, PI3K, hazard ratio, HR, confidence interval, CI, retinal pigment epithelial cell, RPE, Myopia, Inflammation, Interleukin 6, Tumor necrosis factor alpha, Nuclear factor κB, c-Fos

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          Abstract

          Prevention and treatment of myopia is an important public problem worldwide. We found a higher incidence of myopia among patients with inflammatory diseases such as type 1 diabetes mellitus (7.9%), uveitis (3.7%), or systemic lupus erythematosus (3.5%) compared to those without inflammatory diseases ( p < 0.001) using data from children (< 18 years old) in the National Health Insurance Research database. We then examined the inhibition of myopia by atropine in Syrian hamsters with monocular form deprivation (MFD), an experimental myopia model. We found atropine downregulated inflammation in MFD eyes. The expression levels of c-Fos, nuclear factor κB (NFκB), interleukin (IL)-6, and tumor necrosis factor (TNF)-α were upregulated in myopic eyes and downregulated upon treatment with atropine. The relationship between the inflammatory response and myopia was investigated by treating MFD hamsters with the immunosuppressive agent cyclosporine A (CSA) or the inflammatory stimulators lipopolysaccharide (LPS) or peptidoglycan (PGN). Myopia progression was slowed by CSA application but was enhanced by LPS and PGN administration. The levels of c-Fos, NF-κB, IL-6, and TNF-α were upregulated in LPS- and PGN-treated eyes and downregulated by CSA treatment. These findings provide clinical and experimental evidence that inflammation plays a crucial role in the development of myopia.

          Highlights

          • •

            Patients with inflammatory diseases have a higher incidence of myopia compared to those without inflammatory diseases.

          • •

            The expression levels of c-Fos, NFκB, IL-6, and TNF-α, which have known roles in chronic inflammation, were upregulated in myopic eyes.

          • •

            Atropine inhibited the progression of myopia by downregulating c-Fos, NFκB, IL-6, and TNF-α.

          Myopia is an important and common eye disease that can lead to legal blindness. The relationship between myopia and inflammatory responses has never been studied. We demonstrated that increased inflammation in the eye promotes progression of myopia, whereas decreased inflammation slows the development of myopia.

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          Most cited references62

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          Relative peripheral hyperopic defocus alters central refractive development in infant monkeys.

          Earl Smith, Li-Fang Hung, Juan Huang (2009)
          Understanding the role of peripheral defocus on central refractive development is critical because refractive errors can vary significantly with eccentricity and peripheral refractions have been implicated in the genesis of central refractive errors in humans. Two rearing strategies were used to determine whether peripheral hyperopia alters central refractive development in rhesus monkeys. In intact eyes, lens-induced relative peripheral hyperopia produced central axial myopia. Moreover, eliminating the fovea by laser photoablation did not prevent compensating myopic changes in response to optically imposed hyperopia. These results show that peripheral refractive errors can have a substantial impact on central refractive development in primates.
          Article 0 comments Cited 116 times – based on 0 reviews     Review now
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            Peripheral vision can influence eye growth and refractive development in infant monkeys.

            Ying Qiao, Jennifer Smith, Hsiao-Fang Hung … (2005)
            Given the prominence of central vision in humans, it has been assumed that visual signals from the fovea dominate emmetropization. The purpose of this study was to examine the impact of peripheral vision on emmetropization. Bilateral, peripheral form deprivation was produced in 12 infant monkeys by rearing them with diffusers that had either 4- or 8-mm apertures centered on the pupils of each eye, to allow 24 degrees or 37 degrees of unrestricted central vision, respectively. At the end of the lens-rearing period, an argon laser was used to ablate the fovea in one eye of each of seven monkeys. Subsequently, all the animals were allowed unrestricted vision. Refractive error and axial dimensions were measured along the pupillary axis by retinoscopy and A-scan ultrasonography, respectively. Control data were obtained from 21 normal monkeys and 3 infants reared with binocular plano lenses. Nine of the 12 treated monkeys had refractive errors that fell outside the 10th- and 90th-percentile limits for the age-matched control subjects, and the average refractive error for the treated animals was more variable and significantly less hyperopic/more myopic (+0.03 +/- 2.39 D vs. +2.39 +/- 0.92 D). The refractive changes were symmetric in the two eyes of a given animal and axial in nature. After lens removal, all the treated monkeys recovered from the induced refractive errors. No interocular differences in the recovery process were observed in the animals with monocular foveal lesions. On the one hand, the peripheral retina can contribute to emmetropizing responses and to ametropias produced by an abnormal visual experience. On the other hand, unrestricted central vision is not sufficient to ensure normal refractive development, and the fovea is not essential for emmetropizing responses.
            Article 0 comments Cited 97 times – based on 0 reviews     Review now
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              Comorbidity profiles among patients with ankylosing spondylitis: a nationwide population-based study.

              Jiunn-Horng Kang, Shun-Hua Chen, Ching-Po Lin (2010)
              Ankylosing spondylitis (AS) is a systemic inflammatory disease that can result in chronic pain and disability. This study aimed to analyse the prevalence and risk of medical comorbidities in patients with AS compared with the general population. 11 701 patients with AS and 58 505 matching controls were selected for analysis from the National Health Insurance Research Dataset (NHIRD) in Taiwan. The Elixhauser comorbidity index was used for selecting medical comorbidities. Pearson chi2 tests and conditional logistic regression a nalyses were performed to examine the prevalence and risk of comorbidities between these two groups. Patients with AS were at increased risk for multiple systemic comorbidities including cardiovascular, neurological, pulmonary, gastrointestinal, endocrine, haematological and mental illness. The most prevalent comorbidities in patients with AS were hypertension (16.4%), peptic ulcers (13.9%) and headaches (10.2%). The results show that patients with AS have a higher prevalence of multiple comorbidities than the general population in Taiwan. These findings are consistent with previous studies done in Western populations. The results could be useful for both the clinical management of patients with AS and for researching the underlying pathological mechanisms.
              Article 0 comments Cited 69 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Lei Wan
                Journal
                Journal ID (nlm-ta): EBioMedicine
                Journal ID (iso-abbrev): EBioMedicine
                Title: EBioMedicine
                Publisher: Elsevier
                ISSN (Electronic): 2352-3964
                Publication date PMC-release: 19 July 2016
                Publication date Collection: August 2016
                Publication date (Electronic): 19 July 2016
                Volume: 10
                Pages: 269-281
                Affiliations
                [a ]Department of Ophthalmology, China Medical University Hospital, Taichung, Taiwan
                [b ]School of Chinese Medicine, China Medical University, Taichung, Taiwan
                [c ]Department of Pediatrics, China Medical University Hospital, Taichung, Taiwan
                [d ]College of Medicine, China Medical University, Taichung, Taiwan
                [e ]Department of Biotechnology, Asia University, Taichung, Taiwan
                [f ]Department of Medical Research, China Medical University Hospital, Taichung, Taiwan
                [g ]Graduate Institute of Veterinary Pathobiology, National Chung Hsing University, Taichung, Taiwan
                [h ]Institute of Molecular Medicine, National TsingHua University, Hsinchu, Taiwan
                [i ]Management Office for Health Data, China Medical University Hospital, Taichung, Taiwan
                [j ]Department of Gynecology, China Medical University Hospital, Taichung, Taiwan
                Author notes
                [* ]Corresponding author at: School of Chinese Medicine, China Medical University, No. 91, Hsueh-Shih Road, Taichung 40402, Taiwan.School of Chinese MedicineChina Medical UniversityNo. 91, Hsueh-Shih RoadTaichung40402Taiwan leiwan@ 123456mail.cmu.edu.tw lei.joseph@ 123456gmail.com
                Article
                Publisher ID: S2352-3964(16)30326-7
                DOI: 10.1016/j.ebiom.2016.07.021
                PMC ID: 5006729
                PubMed ID: 27470424
                SO-VID: d5968a65-cb49-4337-9342-2c78f6ac260b
                Copyright © © 2016 The Authors
                License:

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                Date received : 4 May 2016
                Date revision received : 16 July 2016
                Date accepted : 17 July 2016
                Categories
                Subject: Research Paper

                Keywords: systemic lupus erythematosus, sle,type 1 diabetes mellitus, t1dm,monocular form deprivation, mfd,nuclear factor κb, nfκb,interleukin, il,tumor necrosis factor α, tnf-α,cyclosporine a, csa,lipopolysaccharide, lps,peptidoglycan, pgn,collagen i, col1,muscarinic acetylcholine receptor, machr,transforming growth factor β, tgf-β,matrix metalloproteinase 2, mmp2,juvenile chronic arthritis, jca,refractive error, re,national health insurance research database, nhird,international classification of diseases, 9th revision, clinical modification, icd-9-cm,phosphate-buffered saline, pbs,dulbecco’s modified eagle medium, dmem,fetal bovine serum, fbs,tris-buffered saline, tbs,4',6-diamidino-2-phenylindole, dapi,extracellular signal-regulated kinase, erk,protein kinase b, akt,phosphoinositide 3-kinase, pi3k,hazard ratio, hr,confidence interval, ci,retinal pigment epithelial cell, rpe,myopia,inflammation,interleukin 6,tumor necrosis factor alpha,nuclear factor κb,c-fos
                Data availability:
                Keywords: systemic lupus erythematosus, sle, type 1 diabetes mellitus, t1dm, monocular form deprivation, mfd, nuclear factor κb, nfκb, interleukin, il, tumor necrosis factor α, tnf-α, cyclosporine a, csa, lipopolysaccharide, lps, peptidoglycan, pgn, collagen i, col1, muscarinic acetylcholine receptor, machr, transforming growth factor β, tgf-β, matrix metalloproteinase 2, mmp2, juvenile chronic arthritis, jca, refractive error, re, national health insurance research database, nhird, international classification of diseases, 9th revision, clinical modification, icd-9-cm, phosphate-buffered saline, pbs, dulbecco’s modified eagle medium, dmem, fetal bovine serum, fbs, tris-buffered saline, tbs, 4',6-diamidino-2-phenylindole, dapi, extracellular signal-regulated kinase, erk, protein kinase b, akt, phosphoinositide 3-kinase, pi3k, hazard ratio, hr, confidence interval, ci, retinal pigment epithelial cell, rpe, myopia, inflammation, interleukin 6, tumor necrosis factor alpha, nuclear factor κb, c-fos

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