Peripheral ulcerative keratitis after ultrasound-mediated cycloablation in patients with rheumatoid arthritis. A possible causal relationship

Pérez Silguero, D.; Pérez Silguero, M.Á.; Pérez-Silguero Jiménez, S.; Encinas Pisa, P.
doi:10.1016/j.oftale.2020.01.013
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75&#44; pseudophakic&#44; with systemic history of rheumatoid arthritis and diagnosed with bilateral primary open angle glaucoma &#40;OAG&#41; 5 years earlier&#46; Baseline treatment with latanoprost&#44; subsequently switched to a fixed combination of bimatoprost and timolol maleate&#46; Due to poor tolerance to the topical medication&#44; which produced ocular surface problems and poor IOP control&#44; it was decided to perform high-intensity focalized circular cycloablation in the LE utilizing the EyeOP1&#174; HIFU device &#40;Eye Tech Care&#44; Rillieux-la-Pape&#44; France&#41; after a 20-day period for clearing the drug and intensive treatment with artificial tear substitute&#46; A 12<span class="elsevierStyleHsp" style=""></span>mm probe was utilized&#46; Treatment consisted in sequential activation of 6 piezoelectric transducers activated during 8<span class="elsevierStyleHsp" style=""></span>s each&#44; with 20<span class="elsevierStyleHsp" style=""></span>s intervals between them&#46; The treatment applied after cycloablation was Tobradex &#40;Novartis Farmac&#233;utica&#44; Barcelona&#44; Spain&#41; 3 times a day during one week and topical cyclopentolate twice a day during 3 days&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">One month later the IOP was under control &#40;16<span class="elsevierStyleHsp" style=""></span>mmHg&#41; without topical hypotensive medication&#46; Forty-five days after surgery&#44; the patient visited the Emergency Dept&#46; due to pain with 6 days of evolution in said eye&#46; Examination showed paralimbar conjunctival ciliary hyperemia from 8 to 6 o&#8217;clock&#44; with half-moon corneal erosion and stromal thinning &#40;390<span class="elsevierStyleHsp" style=""></span>&#956;s thickness&#41;&#44; associated with a smaller&#44; circular and more central lesion with stromal thinning&#44; separated by healthy corneal tissue &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; At the time&#44; the patient had been one year in treatment with oral corticoids &#40;10<span class="elsevierStyleHsp" style=""></span>mg daily&#41; and 6 months with tocilizumab prescribed by the rheumatologist for rheumatoid arthritis&#44; which was adequately controlled prior to the intervention according to specialized report&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0025" class="elsevierStylePara elsevierViewall">The diagnostic was peripheral ulcerative keratitis &#40;PUK&#41; treated with topical corticoids&#44; 20&#37; autologous serum&#44; therapeutic contact lens adaptation&#44; oral doxycycline and report to Rheumatology to increase the oral corticoids dosage&#46; After 13 months of treatment and torpid evolution&#44; the condition resolved with vascularization and thick epithelial covering of the corneal defect &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Case 2</span><p id="par0030" class="elsevierStylePara elsevierViewall">Male&#44; 71&#44; pseudophakic&#44; with rheumatoid arthritis antecedent&#44; diagnosed 8 years earlier with OAG&#44; initially treated with latanoprost and replaced after 8 months with timolol maleate due to poor tolerance&#46; As the patient was diagnosed with cardiac disease&#44; the cardiologist contraindicated timolol&#46; The patient was offered LE cycloablation with EyeOP1&#174; HiFU&#46; At the time&#44; the patient was not in systemic treatment for rheumatoid arthritis&#44; which was not required according to rheumatology&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">LE surgery was carried out and 20 days later IOP was 15<span class="elsevierStyleHsp" style=""></span>mmHg&#46; Postoperative treatment was identical to that of the previous case&#46; Thirty-two days after the operation&#44; the patient visited urgently due to pain in the LE with 24 hours evolution&#46; Slit lamp showed inferior corneal lesion with slight stromal thinning and epithelial defect in addition to slight opacity of the compromised area &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; Suspecting incipient PUK&#44; the treatment described for case one was also indicated for this patient in addition to oral corticoids prescribed by Rheumatology before the ophthalmological report&#46; The case was resolved within 2 months with vascularization of the lesion &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Discussion</span><p id="par0040" class="elsevierStylePara elsevierViewall">Several devices are available to coagulate the ciliary body and reduce intraocular IOP in patients with glaucoma&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">EyeOP1&#174;&#44; the device utilized in the 2 cases described above&#44; comprises 6 miniature transducers to produce high-intensity focalized ultrasound in sequential 8-second activations for each piezoelectric transducer&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">At the histological level&#44; said activations seemed to induce a dual effect that diminished IOP&#44; the most important of which is based on segment or annular necrosis lesions due to a coagulation mechanism&#44; respecting the sclera and the lens with very limited inflammation&#46;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> The second effect increases uveoscleral flow as demonstrated by the findings of Aptel et al&#46; who observed a fluid space between the sclera&#44; the ciliary body and the choroids in experimentation animals&#46;<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a></p><p id="par0055" class="elsevierStylePara elsevierViewall">The efficacy of said activations has been reported in several publications both in cases of glaucoma without previous surgery&#44; achieving mean IOP reductions between 27&#46;8&#37;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> and 30&#37;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> with better results when the treatment was applied 2 or 3 times&#46;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a></p><p id="par0060" class="elsevierStylePara elsevierViewall">The safety of said treatment has been confirmed in previous publications both in single or multiple treatments&#44; with absence of significant side effects<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> or important complications during or after treatment&#46;<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3&#44;4</span></a></p><p id="par0065" class="elsevierStylePara elsevierViewall">However&#44; in a previous article the authors published a previously undescribed complication in phakic patients who underwent said treatment&#44; i&#46;e&#46;&#44; pupil ovalization and loss of accommodation&#46;<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> In this article&#44; a new complication derived from the use of said device in patients with rheumatoid arthritis is reported&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">The patients of the 2 cases reported herein were pseudophakic and shared a rheumatoid arthritis history&#46; The most frequently diseases associated to PUK are the group of collagen vascular diseases of which rheumatoid arthritis is the most frequent&#44; reaching 34&#37; of non-infectious cases&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">The exact physiopathological mechanism of PUK is unknown although it is believed that the pathogenic process is common for all PUK forms&#46; It appears that self-immune processes mediated by cells and humors are found in this entity&#46; The peripheral cornea exhibits differentiated immunological and morphological characteristics that predispose to an immune reaction against corneal antigens&#44; the deposit of immunocomplexes in circulation and hypersensitivity reactions to exogenous antigens&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">At the clinic level&#44; in biomicroscopic studies PUK cases in initial stages show a discrete opacity in the area of the lesion due to cell infiltrates in the stroma adjacent the limbus&#44; as in present case 2&#46; Subsequently&#44; a half-moon ulcer develops with epithelial defect and continues with the variable grade of vascularization and thinning of the corneal tissue&#46; These findings were observed in the present case 1&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">A differential diagnostic should take into account entities as far apart as the Mooren ulcer&#44; Terrien&#39;s marginal degeneration&#44; herpetic keratitis and catarrhal and flictenular ulcer&#44; these two being regarded by some authors as a variant of PUK&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a></p><p id="par0090" class="elsevierStylePara elsevierViewall">A possible physiopathological theory that could explain the causality of cycloablation treatment in the appearance of PUK is the fact that the 2 present cases exhibited conjunctival and episcleral iatrogenic inflammatory processes inherent to the use of the EyeOP1&#174; HIFU device&#44; because in order to apply the treatment it is necessary to place over the perilimbal conjunctiva a cone-shaped ring that applies suction and also serves as support for the transducer&#46; In addition&#44; the surgeon must apply some pressure with the probe over the conjunctiva because&#44; when ultrasound is applied&#44; the discomfort experienced by the patient &#40;which varies according to the applied systemic sedation&#41; could lead to sudden eye movements&#44; and it must be taken into account that this process lasts approximately 1 minute&#46; The day after the intervention it is frequent to find conjunctival hyperemia and even sectorial hyposphagma&#44; both with a duration of approximately one week&#46; The authors believe that these findings could have triggered a subsequent PUK process&#46; In support of the physiopathological theory of the authors&#44; it should be taken into account that the hypothesis is that the limbus and the peri-limbar conjunctival constitute a reservoir for a range of immune system effector cells and pro-inflammatory cytokins which play a significant role in the immuno-pathogenesis of PUK&#46; In addition&#44; PUK frequently presents with conjunctival and episcleral inflammation&#44; as well as scleral inflammation in some cases although in the 2 cases reported herein the latter was absent&#46; In addition&#44; the presence of said adjacent inflammation worsens the course of PUK&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">A second possible explanation is based on previously published corneal complications secondary to cyclophotocoagulation with trans-scleral diode laser&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> The time of presentation of the corneal condition is similar to ours&#44; between 20 and 32 days from treatment in the publication mentioned above and one month and a half in present case 1 &#40;although it should have been before onset because the patient visited with advanced PUK&#41; and 32 days in case 2&#46; The authors propose that the corneal condition could have been caused by a lesion in the long ciliary nerves due to temperature elevation beyond the irradiated target tissue&#46; According to the authors&#44; in said cases an excessively high energy was applied over a large surface &#40;an extension of 270&#8211;360&#176;&#41; and patients exhibited added risk factors&#46; In addition&#44; the condition was neurotrophic keratitis and not PUK as in the present cases&#46; In the treatment applied by the authors&#44; the circular shape of the probe followed the macroscopic anatomy of the ciliary body&#44; thus enabling high coupling precision with the target tissue without injuring adjacent structures&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> In order to achieve a selective impact on the ciliary body&#44; ultrasound is focused at a depth of 2<span class="elsevierStyleHsp" style=""></span>mm under the sclera&#46; The treatment comprises only 45&#37; of the entire ciliary body&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">In case 1&#44; the diagnostic was reached at an advanced stage of the disease despite the fact that the patient was at the time in treatment with tocilizumab&#44; a monoclonal antibody that joins the cellular receptor of interleukin-6&#46; This drug is part of a group of medicaments that has been proposed precisely for treating PUK&#46; In case 2 the disease was diagnosed at the initial stage as demonstrated by the slight opacity in the compromised corneal area&#44; with the patient responded positively to the prescribed treatment&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">It is clear that a higher number of patients with this complication is required to establish a causal relationship between ultrasound cycloablation and PUK in patients with rheumatoid arthritis&#46; However&#44; the authors believe that the corneal condition is severe to the extent that said possibility must be known&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">In the knowledge of the authors&#44; the complications experienced by the 2 cases described above have not been previously described and should be taken into account when prescribing treatment in patients with rheumatoid arthritis as well as included in the informed consent for said intervention&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Funding</span><p id="par0115" class="elsevierStylePara elsevierViewall">The present paper has not received specific funding from agencies of the public or private sectors or nonprofit institutions&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Conflict of interest</span><p id="par0120" class="elsevierStylePara elsevierViewall">None declared&#46;</p></span></span>"
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            0 => "Peripheral ulcerative keratitis"
            1 => "Ultrasound-mediated cycloablation"
            2 => "Rheumatoid arthritis"
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            0 => "Queratitis ulcerativa perif&#233;rica"
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        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">The cases concern a corneal complication not previously described&#44; to our knowledge&#44; after the application of ultrasound-mediated circular cycloablation&#44; in 2 cases of primary open-angle glaucoma in patients diagnosed with rheumatoid arthritis&#46;</p></span>"
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      "es" => array:2 [
        "titulo" => "Resumen"
        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Presentamos una complicaci&#243;n corneal no descrita con anterioridad&#44; seg&#250;n nuestro conocimiento&#44; tras la aplicaci&#243;n de cicloablaci&#243;n circular mediada por ultrasonidos&#44; en 2 casos de glaucoma primario de &#225;ngulo abierto en pacientes con antecedente de artritis reumatoide&#46;</p></span>"
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        "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as&#58; P&#233;rez Silguero D&#44; P&#233;rez Silguero M&#193;&#44; P&#233;rez-Silguero Jim&#233;nez S&#44; Encinas Pisa P&#46; Queratitis ulcerativa perif&#233;rica tras cicloablaci&#243;n mediada por ultrasonidos en pacientes con artritis reumatoide&#46; Una posible relaci&#243;n causal&#46; Arch Soc Esp Oftalmol&#46; 2020&#59;95&#58;196&#8211;200&#46;</p>"
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          "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Upper half&#58; &#40;A&#41; left&#58; peripheral corneal ulceration in LE&#44; with another more central ulcerated lesion&#46; &#40;B&#41; Right&#58; OCT longitudinal section showing the ulcerated corneal lesion of the LE in the initial stage&#44; with contact lens and occupation of the corneal defect due to tear&#46; Corneal thickness 390<span class="elsevierStyleHsp" style=""></span>&#956;s&#46; lower half&#58; &#40;A&#41; left&#58; resolution of condition with epithelization and corneal vascularization&#46; &#40;B&#41; Right&#58; OCT after recovery&#44; showing a residual corneal leukoma and epithelium covering the resulting defect&#44; shown without contact lens&#46; Corneal thickness 410<span class="elsevierStyleHsp" style=""></span>&#956;s&#46;</p>"
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