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Clinical Evaluation and Characterisation of Corneal Vascularisation Lana a Faraj,1 Dalia G Said,1,2 Mohamed Al-Aqaba,1 Ahmad M Otri,1 Harminder S Dua1

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Clinical Evaluation and Characterisation of Corneal Vascularisation Lana a Faraj,1 Dalia G Said,1,2 Mohamed Al-Aqaba,1 Ahmad M Otri,1 Harminder S Dua1 Downloaded from http://bjo.bmj.com/ on March 7, 2016 - Published by group.bmj.com Clinical science Clinical evaluation and characterisation of corneal vascularisation Lana A Faraj,1 Dalia G Said,1,2 Mohamed Al-Aqaba,1 Ahmad M Otri,1 Harminder S Dua1 1Division of Clinical ABSTRACT This is believed to be the single most important Neuroscience, Department of Background/aims To clinically characterise corneal mechanism by which the cornea remains normally Ophthalmology, University of 4 Nottingham, Nottingham, UK neovascularisation (CVas) with a view to elaborate avascular. Ectopic VEGF receptor 3 is also 2Department of Cornea and clinical presentations and to standardise descriptors for strongly expressed by corneal epithelium and could External Eye Diseases, Research clinical evaluation and research. work in a similar manner.5 Institute of Ophthalmology, Methods Corneas of 165 patients with CVas due to a Yet, the physiological and nutritional needs of Cairo, Egypt variety of corneal pathologies were observed clinically the cornea are no different from those of any other Correspondence to with the slit lamp biomicroscope and photography at tissue. In most tissues, these needs are served by Professor Harminder Singh different time points over the course of their disease. the network of blood vessels. In the cornea, the Dua, Department of Parameters assessed included location, depth, length, fluids that bathe it, the aqueous humour on the Ophthalmology, QMC, branching pattern, colour, lipid leakage, nature of blood inside and the tear film on the outside, together Derby Road, Nottingham, flow and presence of haemorrhage. A clinical grading of with the limbal vascular arcade, serve this func- NG7 2UH, UK; 1 [email protected]. CVas was applied. tion. Blood vessels also play a crucial role in host uk Results CVas can arise from the limbus, conjunctiva defence, responding to paracrine and neuronal and iris. CVas preferentially travels along planes created stimuli generated by injury or insult. When the Received 2 February 2015 by corneal incisions, suture tracks and lamellar cornea is stressed by such events, new blood vessels Revised 1 May 2015 fi Accepted 21 June 2015 keratoplasty, both deep lamellar and endothelial invade the corneal tissue to ful l this role. A multi- Published Online First keratoplasty. CVas also principally follows the depth of tude of conditions induce new blood vessels to 10 July 2015 pathology. CVas can be classified into active young, invade the cornea, resulting in ‘corneal vascularisa- active old, mature, partially regressed and regressed. tion’ (neovascularisation), a term which has clinic- Herpetic infection was the most common cause of lipid ally become a collective noun for corneal vessels keratopathy. Acanthamoeba keratitis induced the least associated with varied aetiologies. It is more a clin- amount of vascularisation. A simple and efficient clinical ical sign than a diagnosis. grading system for ascertaining the severity of CVas was The inflammation and visual impairment result- developed and validated. ing from corneal vascularisation (CVas) and the Conclusions The various clinical characteristics of CVas increased risk of immune-mediated rejection in described in this study can be used to standardise the scarred, vascularised corneas requiring transplant- nomenclature and description of CVas and clinically ation, has prompted clinicians to devise means to grade its severity. As modern, effective methods of shut vessels. Topical steroid medication, cautery, treating CVas are being introduced, it is important that argon and yellow dye laser6 and fine needle dia- – there is uniformity in the descriptors used to establish thermy (FND)7 9 have all been advocated with baseline values and evaluate outcomes of treatment. The varying degrees of success. The advent of parameters established in this study can help in this anti-VEGF antibodies has resulted in a surge of regard. interest in using these agents to treat CVas. Doses, regimes and modalities of administration are cur- rently as varied as the authors. Avastin INTRODUCTION (Bevacizumab) has been studied in both animal Transparency and lack of blood vessels are unique experiments and human trials with reported good attributes of the cornea. The latter is in many ways efficacy in shutting CVas though there is a concern a prerequisite for the former. The cornea has about its interference with nerve regeneration and – evolved to keep blood vessels away and many delayed wound healing.10 12 factors contribute to this. The compactness of the There are many other experimental agents and corneal stromal architecture is considered to be an the list is constantly growing.2 The problem rests impediment to vessel invasion. Several molecules, not only with the agent or its administration but singly or in combination, provide the milieu which equally so with the clinical variations in CVas being maintains it in an avascular state.12These include treated. We undertook an extensive study of CVas proteases and their inhibitors, growth factors, Fas by direct clinical examination of patients and ligand, angiostatin, thrombospondin and others.12 images. We were able to define certain fundamental Vascular endothelial growth factor (VEGF), a principles that would help improve the understand- potent inducer of vascularisation, is secreted by ing of CVas and guide development of protocols corneal epithelial and stromal cells and by invading for its management. 3 To cite: Faraj LA, Said DG, macrophages. However, a soluble variant of the Al-Aqaba M, et al. Br J VEGF receptor 1 (VEGFR-1 or sFlt) is also MATERIALS AND METHODS Ophthalmol 2016;100: expressed by corneal epithelial cells.4 This molecule One hundred and sixty-five patients with CVas – 315 322. binds to and sequestrates the available VEGF. were prospectively observed, clinically with the slit Faraj LA, et al. Br J Ophthalmol 2016;100:315–322. doi:10.1136/bjophthalmol-2015-306686 315 Downloaded from http://bjo.bmj.com/ on March 7, 2016 - Published by group.bmj.com Clinical science lamp biomicroscope at different time points over the course of An independent subjective assessment of the specific morpho- the disease process. All patients had slit lamp photomicrographs logical characteristics was carried out by three observers. To test taken. Clinical images and notes of 104 of these were prospect- the reliability of the observations a random selection of 75 ively and retrospectively reviewed at different time points. images from the records of 20 patients was examined and Parameters assessed during clinical evaluation of the eyes and scored. Inter-rater agreement was tested using κ measurement, review of the photographs (a combination of diffuse, slit and which is a chance-adjusted measure of agreement.13 Three raters retro illuminated images) were as follows: (LAF, DGS and AMO) were enrolled in the study to judge for Source: conjunctival, limbal or iris. Patients with pterygium the presence or absence of vessel characteristics in our cases. and diffuse keratoconjunctival proliferation were excluded. Randolph’s free-marginal multirater κ was used for statistical Location and depth: quadrants affected (1–4) and whether analysis of the intra-rater and inter-rater agreement. SPSS statis- superficial, anterior stromal, posterior stromal or a combin- tical package (V.17) was used for further analysis.14 Values of κ ation of these. can range from −1.0 to 1.0, with −1.0 representing perfect dis- Length: peripheral or extending centrally (see details below). agreement below chance, 0.0 indicative of agreement which is Branching pattern: straight loops, tortuous, arborising. due to chance and 1.0 perfect agreement above chance. A κ of Colour: bright or dull red, grey or white. 0.70 or above indicates adequate or substantial inter-rater agree- Leakage: presence of lipid and corneal oedema. ment. The study was accorded approval from the audit commit- Nature of the blood flow: cattle trucking or fragmented, con- tee of Queens Medical Centre, Nottingham (approval number tinuous, tumbling of red blood cells. Presence of corneal 2882), and by the ethics committee (reference number 10/ haemorrhages. H0408/12). Features of associated pathology were also noted. All patients were evaluated by direct observation on the slit lamp and a RESULTS study of clinical images. Clinical records were also reviewed to Causes of CVas ascertain diagnosis. The corneal images were taken using anter- The cause for CVas included infection, inflammation, degenera- ior segment slit lamp camera (Topcon SL-7F slit lamp, Topcon tions, trauma including chemical burns, corneal grafts and 4059 Flash and Nikon 5207550 Digital Camera) at the magnifi- contact lens wear. The distribution of different aetiological cat- cation required to delineate the fine details of the vessels. egories among this study cohort of CVas is provided in table 1. Severity of vascularisation secondary to infective keratitis was Viral keratitis was the most common cause of CVas in our ascertained according to the following scoring system which study, contributing to 24.9% of the cases. Corneal transplant- included number of quadrants involved (1–4), depth of involve- ation accounted for almost a similar number (23.7%) with pene- ment (superficial=anterior one-third of corneal thickness or trating keratoplasty accounting for 15.8%, anterior lamellar deep=posterior two-thirds) and location of vessels (periphera- keratoplasty for 7.3% and endothelial keratoplasty for 0.6%. Of l=outer one-third, mid-peripheral=middle third and central=- the cases, 15.8% were related to bacterial keratitis. central third). At the other end of the range were conditions such as acanth- A score of 1 was given for each quadrant affected; a score of amoeba keratitis (9.1%) and limbal stem cell deficiency (4.2%). 1 for superficial vessels and 2 for deep vessels; and a score of 1 for peripheral vessels, 2 for mid-peripheral vessels and 3 for Morphology of CVas central vessels. When one quadrant had more than one vessel, Corneal vascularisation usually commenced from the limbus the score attributed to the worst vessel(s) was counted for that (see also section titled ‘Sources’ below).
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