Publications by authors named "Hayate Nakagawa"

15 Publications

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The neuropeptide alpha-melanocyte-stimulating hormone is critical for corneal endothelial cell protection and graft survival after transplantation.

Am J Pathol 2021 Nov 10. Epub 2021 Nov 10.

Schepens Eye Research Institute of Massachusetts Eye and Ear, Department of Ophthalmology, Harvard Medical School, Boston, MA, USA. Electronic address:

Corneal transplantation is the most common form of tissue transplantation. The success of corneal transplantation mainly relies on the integrity of corneal endothelial cells (CEnCs), which maintain tissue transparency by pumping out excess water from the cornea. After transplantation, the rate of CEnC loss far exceeds that seen with normal aging, and this can threaten sight. The underlying mechanisms are poorly understood. Alpha-melanocyte-stimulating hormone (α-MSH) is a neuropeptide that is constitutively found in the aqueous humor with both cytoprotective and immunomodulatory effects. We found high expression of melanocortin 1 receptor (MC1R), the receptor for α-MSH, on CEnCs. We then set to determine the effect of α-MSH/MC1R signaling on endothelial function and allograft survival in vitro and in vivo using MC1R signaling-deficient mice (Mc1re/e mice with a nonfunctional MC1R). Herein, we show that in addition to its well-known immunomodulatory effect, α-MSH has cytoprotective effects on CEnCs after corneal transplantation and the loss of MC1R signaling significantly decreases long-term graft survival in vivo. In conclusion, α-MSH/MC1R signaling is critical for CEnC function and graft survival after corneal transplantation.
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http://dx.doi.org/10.1016/j.ajpath.2021.10.016DOI Listing
November 2021

Association of α-Melanocyte-Stimulating Hormone With Corneal Endothelial Cell Survival During Oxidative Stress and Inflammation-Induced Cell Loss in Donor Tissue.

JAMA Ophthalmol 2020 11;138(11):1192-1195

Schepens Eye Research Institute of Massachusetts Eye and Ear, Department of Ophthalmology, Harvard Medical School, Boston.

Importance: Corneal endothelial cell (CEnC) damage and loss are major issues in eye banking and transplantation. The underlying mechanisms for CEnC loss are incompletely understood, and cytoprotective strategies that enhance CEnC viability could have a major effect on donor tissue quality and graft survival.

Objective: To investigate the cytoprotective role of neuropeptide α-melanocyte-stimulating hormone (α-MSH) in preventing CEnC loss in eye bank cold-stored corneas under oxidative and inflammatory cytokine-induced stress.

Design, Setting, And Participants: This single-center comparative research study conducted ex vivo experiments using 16 pairs of research-grade human donor corneas (courtesy of Eversight Eye Bank). Data were collected from June 2018 to November 2019, and data were analyzed from December 2019 to January 2020.

Exposures: Two corneas from the same donor were randomized to either control or 0.1 mmol/L of α-MSH treatment and then subjected to oxidative stress (1.4 mmol/L of hydrogen peroxide-phosphate-buffered saline for 15 minutes at 37 °C; n = 8 pairs) or cytokine-induced stress (100 ng/mL of tumor necrosis factor-α and 100 ng/mL of interferon γ for 18 hours at 37 °C; n = 8 pairs). Corneas were then stored at 4 °C. Specular images were taken at baseline and repeated twice per week using a calibrated wide-field specular microscope. CEnC viability was assessed using a fluorescent live/dead viability assay.

Main Outcome And Measures: Endothelial morphometry analysis, central corneal thickness measurements, and percentage of dead cells at day 11.

Results: Of 16 donors who provided corneas, 9 (56%) were male, and the mean (SD) age was 57.9 (12.4) years. Corneas were paired, and baseline parameters were comparable between all groups. At all time points, CEnC loss was lower in the α-MSH groups compared with the control groups. This difference was statistically significant after cytokine-induced stress (20.2% vs 35.2%; sample estimate of median, -14.9; 95% CI, -23.6 to -6.3; P = .008). Compared with the control group, α-MSH treatment resulted in a smaller increase in central corneal thickness (cytokine-induced stress: 89.3 μm vs 169.8 μm; sample estimate of median, -84.9; 95% CI, -131.5 to -41.6; P = .008; oxidative stress: 43.6 μm vs 111.9 μm; sample estimate of median, -68.8; 95% CI, -100.0 to -34.5; P = .008) and a smaller proportion of cell death (cytokine-induced stress: 2.7% vs 10.4%; difference, -7.7; 95% CI, -13.1 to -2.4; P = .01; oxidative stress: 2.9% vs 12.4%; difference, 9.5; 95% CI, 5.1 to 13.9; P = .006).

Conclusions And Relevance: In this study, α-MSH treatment attenuated CEnC loss during cold storage after acute oxidative and cytokine-induced stress in human eye bank cold-stored corneas. These data suggest that supplementation of corneal storage solution with α-MSH may positively affect CEnC survival after transplant and protect the endothelium from proinflammatory cytokines and oxidative stress after full-thickness or endothelial keratoplasty, which is particularly valuable in patients at high risk of graft failure.
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http://dx.doi.org/10.1001/jamaophthalmol.2020.3413DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7499243PMC
November 2020

Blockade of costimulatory CD27/CD70 pathway promotes corneal allograft survival.

Exp Eye Res 2020 10 14;199:108190. Epub 2020 Aug 14.

Department of Ophthalmology, Tokyo Medical University, 6-7-1 Nishi-shinjuku, Shinjuku-ku, Tokyo, 160-0023, Japan.

Purpose: To determine whether the CD27/CD70 pathway plays a significant role in corneal allograft rejection by investigating the effect of blocking the CD27/CD70 pathway by anti-CD70 antibody on corneal allograft survival.

Methods: Orthotopic penetrating keratoplasty was performed using C57BL/6 donor grafts and BALB/c recipients. Expression of CD27 and CD70 on rejected cornea was examined by immunohistochemistry. Corneal transplant recipients received intraperitoneal injection of anti-CD70 antibody (FR70) or control rat IgG. Alloreactivity was measured by mixed lymphoid reaction (MLR) in recipients administered control rat IgG and those administered anti-CD70 antibody. Corneal expression of IFN-γ and IL-12 was also examined in both groups. Graft opacity was assessed over an 8-week period and graft survival was evaluated using Kaplan-Meier survival curves. Proportion of CD4CD44 memory T cells in lymph nodes was measured by flow cytometry.

Results: CD4CD27 cells and CD11cCD70 cells were present in rejected cornea. Anti-CD70 antibody administration suppressed alloreactivity in corneal allograft recipients, and inhibited IFN-γ expression in recipient cornea (p < 0.05). Anti-CD70 antibody suppressed opacity score of recipient cornea and prolonged corneal allograft survival (p < 0.05). Proportion of CD4CD44 memory T cells in recipient lymph nodes was reduced by anti-CD70 antibody treatment.

Conclusion: The CD27/CD70 pathway plays a significant role in corneal allograft rejection by initiating alloreactive Th1 cells and preserving memory T cells. Anti-CD70 antibody administration prolongs corneal allograft survival indicating the potential therapeutic effect of CD27/CD70 pathway blockade on corneal allograft rejection.
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http://dx.doi.org/10.1016/j.exer.2020.108190DOI Listing
October 2020

Corticosteroid eye drop instillation aggravates the development of Acanthamoeba keratitis in rabbit corneas inoculated with Acanthamoeba and bacteria.

Sci Rep 2019 09 6;9(1):12821. Epub 2019 Sep 6.

Department of Ophthalmology, Tokyo Medical University, Shinjuku City, Japan.

The role of topical corticosteroids in management of Acanthamoeba keratitis (AK) remains controversial. Using a rabbit AK model, we investigated whether corticosteroid use is a risk factor of AK. Acanthamoeba (1 × 10/ml) was incubated with two densities of P. aeruginosa (PA; high-PA: 1 × 10/ml, low-PA: 3 × 10/ml) before corneal inoculation. Rabbit corneas were inoculated with Acanthamoeba alone or Acanthamoeba plus PA and administered levofloxacin and betamethasone sodium phosphate (BSP) eye drops for 5 or 7 days. Infected rabbit eyes were evaluated for clinical score and Acanthamoeba by histological examination. Acanthamoeba alone and BSP treatment did not produce keratitis. Corneas inoculated with Acanthamoeba plus low-PA treated immediately with levofloxacin and BSP remained clear with few infiltrates. Corneas inoculated with Acanthamoeba plus low-PA treated with levofloxacin immediately and BSP 12 h later developed severe keratitis. Corneas inoculated with Acanthamoeba plus high-PA treated immediately with levofloxacin and BSP also developed severe keratitis. Acanthamoebae were detected by PAS staining in corneas inoculated with Acanthamoeba plus high-PA treated with levofloxacin and BSP. Topical corticosteroids have the potential to aggravate AK when cornea is infected by Acanthamoeba with a critical number of bacteria or when corticosteroids are given after infection has established by Acanthamoeba with small number of bacteria.
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http://dx.doi.org/10.1038/s41598-019-49128-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6731293PMC
September 2019

Corneal lymphangiogenesis ameliorates corneal inflammation and edema in late stage of bacterial keratitis.

Sci Rep 2019 02 27;9(1):2984. Epub 2019 Feb 27.

Department of Ophthalmology, Tokyo Medical University, Tokyo, Japan.

Lymphatic vessels play a crucial role in systemic immune response and regulation of tissue fluid homeostasis. Corneal lymphangiogenesis in bacterial keratitis has not been studied. In this study, we investigated the mechanism and the role of corneal lymphangiogenesis in a murine bacterial keratitis model using Pseudomonas aeruginosa. We first demonstrated that corneal lymphangiogenesis was enhanced mainly in the late stage of bacterial keratitis, contrary to corneal angiogenesis that started earlier. Corresponding to the delayed lymphangiogenesis, expression of the pro-lymphangiogenic factors VEGF-C and VEGFR-3 increased in the late stage of bacterial keratitis. We further found that F4/80 and CD11b positive macrophages played an essential role in corneal lymphangiogenesis. Notably, macrophages were specifically involved in corneal lymphangiogenesis in the late stage of bacterial keratitis. Finally, we demonstrated the beneficial role of corneal lymphangiogenesis in ameliorating the clinical course of bacterial keratitis. Our study showed that bacterial activity was not directly involved in the late stage of keratitis, while corneal lymphangiogenesis reduced corneal edema and clinical manifestation in the late stage of bacterial keratitis. These findings suggest that the process of lymphangiogenesis in bacterial keratitis ameliorates corneal inflammation and edema in the late stage of bacterial keratitis.
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http://dx.doi.org/10.1038/s41598-019-39876-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6393676PMC
February 2019

Reply.

Cornea 2017 09;36(9):e22

Departments of *Ophthalmology and †Microbiology, Tokyo Medical University, Tokyo, Japan.

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http://dx.doi.org/10.1097/ICO.0000000000001274DOI Listing
September 2017

Optic neuritis and acute anterior uveitis associated with influenza A infection: a case report.

Int Med Case Rep J 2017 4;10:1-5. Epub 2017 Jan 4.

Department of Ophthalmology, Tokyo Medical University Hachioji Medical Center, Tokyo, Japan.

Background: A few reports have described ocular complications of influenza A infection, such as impaired ocular movement, parasympathetic ocular nerve, keratitis, macular lesion, and frosted branch angiitis. We encountered a rare case of acute anterior uveitis and optic neuritis associated with influenza A infection.

Case Presentation: A 70-year-old man presented with symptoms of upper respiratory tract infection. A rapid diagnostic test showed a positive result for influenza A. At the same time, he developed ocular symptoms including blurred vision with optic disk edema and hemorrhage in the left eye, and bilateral red eyes. Multiplex polymerase chain reaction performed on aqueous humor sample detected no viral infection. Visual field testing with a Goldmann perimeter showed central and paracentral scotomas in the left eye. In addition to antiviral agent (oseltamivir phosphate 75 mg), the patient was prescribed topical prednisolone acetate ophthalmic suspension eye drops every 5 hours and high-dose intravenous methylprednisolone 1,000 mg daily for 3 days. Two months later, his best-corrected visual acuity improved to 20/50 with regression of visual field defects in his left eye.

Conclusion: We report a case of bilateral acute anterior uveitis and unilateral optic neuritis concomitant with influenza A infection. Topical and systemic corticosteroids were effective to resolve acute anterior uveitis and neuritis. Analysis of aqueous humor sample suggested that acute anterior uveitis and optic neuritis in this case were not caused by influenza A virus infection per se but by autoimmune mechanism.
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http://dx.doi.org/10.2147/IMCRJ.S113217DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5221811PMC
January 2017

Number of Bacteria and Time of Coincubation With Bacteria Required for the Development of Acanthamoeba Keratitis.

Cornea 2017 Mar;36(3):353-357

Departments of *Ophthalmology, Tokyo Medical University, Tokyo, Japan; and †Microbiology, Tokyo Medical University, Tokyo, Japan.

Purpose: We hypothesized that bacteria may be a factor contributing to the development of Acanthamoeba keratitis (AK). We investigated interactions between Acanthamoeba and Pseudomonas aeruginosa for the development of keratitis in rabbit corneas.

Methods: Acanthamoeba castellanii (ATCC50492) and P. aeruginosa (PAO-1) were used. Two densities of P. aeruginosa (high, 1 × 10/mL; low, 3 × 10/mL) and 2 durations of coincubation (long, 6 h; short, 2 h) of Acanthamoeba with 1 × 10/mL of P. aeruginosa were tested. Acanthamoeba alone or Acanthamoeba coincubated with P. aeruginosa was inoculated into rabbit corneas. After inoculation, levofloxacin (LVFX) eye drops were administered. The clinical score of the cornea was evaluated after inoculation.

Results: Acanthamoeba alone did not produce keratitis during a 5-day observation period. Rabbit corneas inoculated with Acanthamoeba coincubated with low-density P. aeruginosa followed by topical LVFX were clear with few infiltrates. Corneas inoculated with Acanthamoeba coincubated with high-density P. aeruginosa followed by LVFX treatment developed severe keratitis, and clinical scores were significantly higher compared with high-density P. aeruginosa alone followed by LVFX treatment (scores 7, 9.6, 8.5 vs. 3, 3.5, 3.25 on days 1-3, all P < 0.01). The long (6 h) coincubation time of Acanthamoeba with high-density P. aeruginosa resulted in more severe keratitis compared with short (2 h) coincubation (scores, 9.7, 12.7, 12.1, 9.8, 8.7 vs. 7, 9.6, 8.5, 6.9, 5.6 on days 1-5, all P < 0.01).

Conclusions: These results suggest that the presence of bacteria is essential and a critical number of bacteria is required for the development of AK. The time of coexistence with bacteria may be an important determinant of the severity of AK.
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http://dx.doi.org/10.1097/ICO.0000000000001129DOI Listing
March 2017

Cytokines and Recurrence of Macular Edema after Intravitreal Ranibizumab in Patients with Branch Retinal Vein Occlusion.

Ophthalmologica 2016 11;236(4):228-234. Epub 2016 Nov 11.

Department of Ophthalmology, Hachioji Medical Center, Tokyo Medical University, Tokyo, Japan.

The aqueous humor levels of cytokines and growth/inflammatory factors were measured in 46 branch retinal vein occlusion (BRVO) patients with macular edema (ME) who were treated with intravitreal ranibizumab injection (IRI). Patients with recurrence of ME received further IRI as needed. The number of IRIs was significantly correlated with age, baseline best-corrected visual acuity, and baseline central macular thickness (CMT), as well as the baseline aqueous levels of 5 cytokines/factors (soluble vascular endothelial growth factor receptor-1, platelet-derived growth factor-AA [PDGF-AA], soluble intercellular adhesion molecule-1, interleukin-6 [IL-6], and IL-8). Multivariate linear regression analysis with stepwise selection confirmed that age, baseline CMT, and baseline PDGF-AA level were independent determinants of the number of IRIs. These findings suggest that inflammatory factors may influence the recurrence of ME in BRVO patients, and that PDGF-AA might be a useful indicator of the number of IRIs required to control ME.
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http://dx.doi.org/10.1159/000451062DOI Listing
January 2017

Comparative Effects of Topical Diclofenac and Betamethasone on Inflammation After Vitrectomy and Cataract Surgery in Various Vitreoretinal Diseases.

J Ocul Pharmacol Ther 2016 12 18;32(10):677-684. Epub 2016 Oct 18.

Department of Ophthalmology, Tokyo Medical University Hachioji Medical Center , Tokyo, Japan .

Purpose: To compare the effects of topical diclofenac and betamethasone on postoperative inflammation after combined sutureless cataract and vitreoretinal surgery in patients with macular hole (MH), epiretinal membrane (ERM), diabetic macular edema (DME), and rhegmatogenous retinal detachment (RRD).

Methods: The study involved 180 eligible eyes that underwent the combined surgery, followed by treatment with topical diclofenac (n = 100) or betamethasone (n = 80) for 12 weeks. Maximum postoperative inflammation index (maxPOI), assessed by laser flare-cell meter, and intraocular pressure (IOP) were monitored. The relationships between maxPOI and total operation time or number of endophotocoagulations during surgery were investigated.

Results: Postoperative inflammation peaked at 2 weeks and decreased thereafter in all 4 diseases, without significant differences between 2 treated groups. Postoperative IOP in MH and ERM was significantly higher in the betamethasone group. In DME and RRD, a greater number of endophotocoagulations increased maxPOI in both diclofenac and betamethasone groups, while longer operation time increased maxPOI only in diclofenac groups.

Conclusions: In MH and ERM, topical diclofenac and betamethasone equally suppressed postoperative inflammation after the combined surgery, although diclofenac better controlled postoperative IOP. In DME and RRD, both drugs were equally effective in suppressing inflammation and controlling IOP, but diclofenac showed weaker suppression following longer operation.
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http://dx.doi.org/10.1089/jop.2016.0099DOI Listing
December 2016

Intravitreal Ranibizumab and Aqueous Humor Factors/Cytokines in Major and Macular Branch Retinal Vein Occlusion.

Ophthalmologica 2016 23;235(4):203-7. Epub 2016 Mar 23.

Department of Ophthalmology, Hachioji Medical Center, Tokyo Medical University, Tokyo, Japan.

Aqueous humor levels of cytokines and growth/inflammatory factors were measured in 38 patients with macular edema who had major branch retinal vein occlusion (BRVO) or macular BRVO and were treated with intravitreal ranibizumab injection (IRI). Patients with recurrence of macular edema received further IRI as needed. Aqueous humor levels of vascular endothelial growth factor (VEGF), soluble VEGF receptor-1 (sVEGFR-1), and other cytokines/factors were measured. Compared with major BRVO, macular BRVO was associated with lower aqueous humor levels of sVEGFR-1, its ligands (VEGF and placental growth factor), and other growth/inflammatory factors (platelet-derived growth factor-AA, monocyte chemotactic protein-1, soluble intercellular adhesion molecule-1, interleukin-6, and interleukin-8). The mean number of IRI over 6 months was significantly lower in the macular BRVO group than in the major BRVO group. These findings suggest that macular BRVO requires fewer IRI than major BRVO and is associated with lower aqueous humor levels of various growth/inflammatory factors and cytokines.
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http://dx.doi.org/10.1159/000444923DOI Listing
January 2017

Investigation of the Role of Bacteria in the Development of Acanthamoeba Keratitis.

Cornea 2015 Oct;34(10):1308-15

Departments of *Ophthalmology, †Microbiology, and ‡Molecular Pathology, Tokyo Medical University, Shinjuku-ku, Japan.

Purpose: Recently, much interest has been shown in bacteria extracted from Acanthamoeba strains isolated from patients with Acanthamoeba keratitis (AK). We hypothesized that the bacteria in Acanthamoeba strains may be a contributing factor in the development of AK. To prove this hypothesis, we investigated the involvement of bacteria harbored by Acanthamoeba in causing progressive ocular infection in rabbit corneas.

Methods: One Acanthamoeba strain (T4 genotype) that harbored bacteria was isolated from a patient with AK. The Acanthamoeba strain pretreated or not pretreated with levofloxacin (LVFX) was inoculated into rabbit corneas. We also tested the effect of LVFX eye drops on keratitis induced by the Acanthamoeba strain. The infected rabbit eyes were evaluated for clinical scores, Acanthamoeba 18S rDNA and bacterial 16S rDNA numbers were analyzed by the real-time polymerase chain reaction, and the presence of Acanthamoeba was analyzed by histological examination.

Results: Inoculation of nonpretreated Acanthamoeba resulted in severe keratitis. In contrast, inoculation of LVFX-pretreated Acanthamoeba did not induce keratitis (mean clinical score, 17.3 vs. 2.3; P < 0.05). Rabbit corneas inoculated with nonpretreated Acanthamoeba followed by topical LVFX therapy developed severe keratitis. In corneas inoculated with nonpretreated Acanthamoeba followed by LVFX therapy, the number of Acanthamoeba 18S rDNA copies was significantly higher than in other groups (P < 0.05), whereas the bacterial 16S rDNA gene was undetectable. Acanthamoeba cysts were detected by Fungiflora Y staining only in corneas inoculated with nonpretreated Acanthamoeba followed by LVFX therapy.

Conclusions: These results suggest that the presence of bacteria in Acanthamoeba may be required for the development of AK.
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http://dx.doi.org/10.1097/ICO.0000000000000541DOI Listing
October 2015

Peroxisome proliferator-activated receptor-γ agonist pioglitazone suppresses experimental autoimmune uveitis.

Exp Eye Res 2013 Nov 6;116:291-7. Epub 2013 Oct 6.

Department of Ophthalmology, Tokyo Medical University, 6-7-1 Nishishinjuku, Shinjuku-ku, Tokyo 160-0023, Japan. Electronic address:

Peroxisome proliferator-activated receptor (PPAR)-γ agonists are clinically used as anti-diabetes agents. Recent research has discovered that an anti-inflammatory effect of PPAR agonist may have the potential to treat autoimmune disease. In the present study, we investigated the anti-inflammatory effects of PPAR-γ agonist, pioglitazone, on murine model of endogenous uveitis. Experimental autoimmune uveoretinitis (EAU) was induced by immunizing C57BL/6 mice with human interphotoreceptor retinoid binding protein-derived peptide (1-20). Pioglitazone or vehicle was injected intravenously from day -1 (whole phase treatment) or day 8 (effector phase study) until day 20. Severity of EAU was assessed clinically and pathologically on day 21. Immunological status was assessed by measuring intraocular inflammatory factors, and activation and regulatory markers of CD4(+) T cells in draining lymph nodes (LNs). Treatment with pioglitazone suppressed both whole-phase and effector-phase of EAU. In effector-phase treatment, intraocular concentrations of TNF-α and IL-6 were significantly suppressed, and CD4(+)Foxp3(+) regulatory T cells and CD4(+)CD62L(high) naïve T cells increased in draining LNs, although there were no differences in CD4(+)CD44(high) effector T cells and IL-17 producing CD4(+) T cells between pioglitazone- and vehicle-treated mice. Administration of pioglitazone before and after the onset of EAU significantly reduced disease severity. The present results suggest that pioglitazone may be a novel therapeutic agent for endogenous uveitis.
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http://dx.doi.org/10.1016/j.exer.2013.09.017DOI Listing
November 2013

Non-Descemet's stripping automated endothelial keratoplasty for bullous keratopathy secondary to iridoschisis.

Clin Ophthalmol 2013 3;7:1353-5. Epub 2013 Jul 3.

Department of Ophthalmology, Tokyo Medical University, Shinjukuku, Tokyo, Japan.

Purpose: To report a case of bullous keratopathy secondary to iridoschisis treated by non-Descemet's stripping automated endothelial keratoplasty (nDSAEK).

Case Report: A 79-year-old woman was referred to our hospital with loss of vision in the left eye. Slit lamp examination of her left eye showed a shallow anterior chamber with cataract and schisis in the inferior quadrant of iris stroma. Bullous keratopathy secondary to iridoschisis was diagnosed. Cataract surgery with iridectomy succeeded to deepen the anterior chamber and remove the floating iris leaf, although corneal edema remained. Four days later, nDSAEK was performed, which resolved corneal edema and restored visual acuity.

Conclusion: The two-step surgery of cataract surgery plus iridectomy followed by nDSAEK may be an effective strategy for treating bullous keratopathy secondary to iridoschisis.
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http://dx.doi.org/10.2147/OPTH.S43180DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3704543PMC
July 2013
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