Clinical science Visual field defect classification in the Zhongshan Ophthalmic Center–Brien Holden Vision Institute High Myopia Registry Study Xiaohu Ding,1 Robert T Chang,1,2 Xinxing Guo,1 Xing Liu,1 Chris A Johnson,3 † Brien A Holden,4, Mingguang He1

▸ Additional material is ABSTRACT myopia is rapidly becoming a major public health published online only. To view Purpose To describe a new combined myopia and problem.4 please visit the journal online fi fi (http://dx.doi.org/10.1136/ glaucoma visual eld classi cation system in order to The relationship between high myopia and bjophthalmol-2015-307942). report the visual field defects in a population of mostly POAG has been explored extensively in prior young Chinese high myopes aged 7–70 years. studies.5 However, accurate diagnosis of glaucoma fi 1 Methods A total of 1434 visual elds (including in the setting of high myopia is a challenge in clin- State Key Laboratory of confirmatory repeats of abnormal defects) from 487 high ical practice for two major reasons: (1) High Ophthalmology, Zhongshan ≤− Ophthalmic Center, myopes (sphere 6.0 D) were analysed from the myopia can cause tilted optic discs, large peripapil- Sun Yat-sen University, prospective Zhongshan Ophthalmic Center–Brien Holden lary atrophy obscuring the disc edge and shallow Guangzhou, China Vision Institute (ZOC–BHVI) High Myopia Registry Study. cupping without shifting of the vessels nasally, 2 Department of The predefined classification definitions covering high making the subjective interpretation of glaucomat- Ophthalmology, Byers Eye fi Institute at Stanford University, myopia and glaucoma categories were: normal, enlarged ous excavation more dif cult. (2) Although the Palo Alto, California, USA blind spot, abnormal suspect and abnormal with nine diagnosis of glaucoma relies upon characteristic 3Department of Ophthalmology subtypes. Two independent graders reviewed the first optic nerve cupping with associated progressive and Visual Sciences, University 150 of 1434 fields for initial grading calibration and the visual field loss, myopic degeneration can also of Iowa, Iowa City, Iowa, USA 4 remaining 1284 fields were used to assess intergrader cause similar glaucomatous-like visual field Brien Holden Vision Institute, 67 University of New South Wales, agreement. For the percentage distribution of visual defects. Therefore, patients need to be followed 8 Sydney, New South Wales, fields, the repeats and unreliable fields were excluded, over time to confirm true glaucoma progression. Australia leaving 894 fields. There is little information in the literature describ- Results The intergrader agreement of this combined ing the overall clinical characteristics of high Correspondence to fi κ fi Dr Robert T Chang, classi cation system was a value of 0.61 (95% CI myopes with visual eld defects or any prospective Byers Eye Institute at Stanford, 0.59 to 0.63). Among the 894 unique fields, the most data on how or if myopic defects change over time. 2452 Watson Ct, common visual field was normal at 33.7% followed by We were interested in determining how often Palo Alto CA 94303, USA; enlarged blind spot at 25.6%. The per cent of ‘arcuate- Chinese myopes have visual field defects that mimic [email protected] like’ field defects (combining nasal step, early arcuate glaucoma, particularly since many of those defects †Deceased 27 July 2015 and advanced arcuate) was 16.1% with advanced in young myopes may be minimally progressive and arcuate at 3.4%. not glaucomatous.9 Received 12 October 2015 Conclusions A proposed combined visual field In the present study, we first propose a broader Revised 15 February 2016 classification for high myopia and glaucoma combined classification system of visual field Accepted 22 February 2016 Published Online First demonstrates acceptable intergrader agreement. A total defects in high myopes to include both high 31 March 2016 of 16.1% of defects in young high myopes were found myopia and glaucoma types. After reporting the to mimic classic glaucomatous defects. These subjects intergrader agreement, we describe the baseline are being followed prospectively to assess which ones percentages of each field defect type in a large will progress to differentiate myopic from glaucomatous group of Chinese high myopes aged 7–70 with a field defects. median age of 17.4 years. The data collected, including visual fields, is part of an ongoing ZOC– BHVI High Myopia Registry Study that is designed INTRODUCTION to understand the natural history and pathogenesis Myopia morbidity continues to increase substan- of myopic retinopathy, initiated in November 2011 tially worldwide,1 especially in East Asians.2 in Guangzhou, China. Myopia can be corrected by spectacles, contact lens, or various intraocular or laser refractive sur- METHODS geries to achieve good vision. However, in high Ethics approval was obtained from the Zhongshan myopia, defined as worse than or equal to −6 diop- Ophthalmic Center Ethics Review Board. The tres sphere and also known as degenerative myopia, study was conducted in accordance with the tenets sight-threatening complications increase with many of the World Medical Association’s Declaration of potentially blinding conditions, such as myopic Helsinki. Written informed consent was obtained degenerative retinopathy, macular scars, increased from all participants, or their parents or legal guar- primary open-angle glaucoma (POAG) and more dians if their age was <18 years. 3 To cite: Ding X, Chang RT, frequent retinal detachment. Unlike cataract or Guo X, et al. Br J age-related macular degeneration, which mainly Study population Ophthalmol affect the elderly population, high myopia also A longitudinal observational high myope registry – 2016;100:1697 1702. affects many young adults of working age; thus study was initiated in Guangzhou in 2011 and is

Ding X, et al. Br J Ophthalmol 2016;100:1697–1702. doi:10.1136/bjophthalmol-2015-307942 1697 Clinical science

expected to run until 2021. Subjects with high myopia, defined as worse than or equal to −6 dioptres sphere (not spherical equivalent) in both eyes, were recruited from both optometric clinic and a previous community screening population study in order to have more subjects older than 50 years.10 At baseline, a total of 895 participants were eligible and enrolled in the regis- try. However, only 487 subjects had visual field data. Baseline data collected in the high myopia registry included: cycloplegic refraction, best-corrected visual acuity, ocular biom- etry, external motility and slit lamp exam, lens opacity by the Lens Opacities Classification System (LOCS III) grading scale, intraocular pressure (IOP) measurement by Goldmann applana- tion, standard automatic perimetry, B-scan ultrasound, digital stereo fundus photography (Canon CX-1), autofluorescence (Heidelberg Spectralis) and spectral domain optical coherence tomography (SD-OCT Optovue). Refraction was performed with an autorefractor (Topcon KR-8800) after cycloplegia. Ocular biometric parameters including axial length were obtained by optical low-coherence reflectometry (Lenstar LS-900, Haag-Streit AG). Figure 1 The schema of our recruitment. Visual field examination A total of 487 subjects underwent bilateral standard automatic perimetry (Zeiss Humphrey Visual Field 750i, Carl Zeiss the established criteria to determine final percentages reported Meditec, Dublin, California, USA) on a separate return visit, from the unique 894 fields in which repeat or unreliable fields using the 24-2 Swedish interactive threshold algorithm (SITA) had been removed. A total of 167 unreliable fields (13%) were fast, white-on-white, performed on a single machine. All visual removed. If the original and repeat field were both reliable, then fi elds were conducted in a single dark room without distraction the field with fewer false positives was chosen or fewer fixation (ambient light <5 lux) with a trained technician who explained losses if the false positives were the same. Thus, 167 unreliable to all subjects how to complete the test reliably. Each subject and 373 repeat visual fields were removed, arriving at the 894 fi had a short demonstration test before commencing the of cial visual field total for analysis (figure 1). examination. During the test, the technician also monitored the subject’s eye movement, and made adjustments as necessary to maintain proper fixation. Unreliable fields, defined as reach one Statistical analysis – of three criteria: false positive ≥15%, false negative ≥33% and Median, range and 25th 75th percentile were used to describe fixation loss ≥33%, were repeated immediately (up to two the non-normal distribution parameters. The agreement κ times) as well as any abnormal fields. From November 2011 to between two graders was assessed by , whose values of >0.7 August 2012, a total of 1434 visual fields (including repeats of are generally considered excellent and between 0.4 and 0.7 are abnormals) from 487 patients were available for our current considered as moderate. p<0.05 was considered statistically sig- fi visual field analysis, the outline of the recruitment was shown in ni cant. All statistics were performed using STATA (V.12.0, figure 1. Stata, College Station, Texas, USA).

Visual field classification system and grading RESULTS In order to include visual field defect types associated with high Among the 487 participants, 229 (47.0%) were male and 258 myopia, new visual field grading criteria were drafted, consisting (53.0%) were female. The median age was 17.4 years, range of four major types: normal, enlarged blindness spot (at least 7–70 years, the 25% percentile was 13.3 years and 75% per- two abnormal edge point around the blind spot), suspicious for centile was 28.1 years. The median refraction was −8.6 D, range abnormal (minimum criteria for a defect but no pattern) and −6to−35 D, 25% and 75% percentiles were −7.4 and definitely abnormal (figure 2). The grading criteria for glau- −11.0 D, respectively. The median axial length was 27.2 mm, comatous defects were adapted from the Ocular Hypertension range 23.8–32.0 mm and the 25% and 75% percentiles were Treatment Study visual field criteria: nasal step, early arcuate, 26.3 and 28.1 mm, respectively (table 1). advanced arcuate with additional myopic related defects added Of the 1284 visual fields available for the reader agreement including generalised (widespread) sensitivity loss, paracentral analysis, the κ index of agreement before adjudication was 0.61 defect, central defect, rim artefacts, tilted disc (crosses at least (95% CI 0.59 to 0.63). Given that the agreement would be two outer rims crossing vertical and horizontal midlines) and higher with a higher percentage of normal visual fields, after cecocentral defect. We used the first 150 of 1434 visual fields to removing the fields both graders read as normal, the κ value was train two grading ophthalmologists to reach the final assessment 0.56 (95% CI 0.54 to 0.58) revealing moderate correlation.11 shown in figure 2, and the visual field grading schematic Of the 1434 visual fields, 540 were removed due to unreli- depicted in figure 3. ability (167) or repeats (373), leaving 894 unique visual fields Minus the calibration training set of 150 fields, 1284 visual used for distribution description. Table 2 displays the percentage fields were independently graded by two ophthalmologists (XD distribution of visual field defects in high myopes, the most and RTC) for calculating the intergrader agreement. When the common one being normal, which accounted for 33.7% (95% agreement estimation was completed, all visual fields were CI 30.6% to 36.9%). Based on our definitions, the next most pooled and the ones in disagreement were readjudicated with common defects were enlarged blind spots at 25.6% (95% CI

1698 Ding X, et al. Br J Ophthalmol 2016;100:1697–1702. doi:10.1136/bjophthalmol-2015-307942 Clinical science

Figure 2 The visual field defect classification. MD, mean deviation; PSD, pattern SD. GHT, glaucoma hemifield test.

22.8% to 28.6%) and generalised reduction in sensitivity at 16.1% of all field defects in our young high myopic population 23.4% (95% CI 20.6% to 26.3%). The arcuate-like visual field had this pattern. To assess this group further in terms of glau- defects, grouped together as either nasal step (5.1%), early coma risk, baseline clinical data on IOP,central corneal thickness arcuate (7.6%) and advanced arcuate (3.4%), contributed up to (CCT), fundus photos and SD-OCTwere reviewed for these 144 16.1% (95% CI 13.8% to 18.9%). Relatively rarer types were: subjects. Elevated IOP (>21 mm Hg, with adjustment for CCT), paracentral defect at 5.9% (95% CI 4.4% to 7.7%), rim arte- as well as glaucomatous optic nerve appearances in fundus facts at 2.5% (95% CI 1.5% to 3.7%), tilted disc defects at photos (including optic nerve notching, retinal nerve fibre layer 1.6% (95% CI 0.8% to 2.6%) and central defects at 1.0% (95% (RNFL) defect, optic haemorrhage, enlarged cup–disc ratio and CI 0.4% to 1.9%), with the least common being cecocentral asymmetry between two eyes) were considered as signs of high defect which only accounted for about 0.3% (0.0% to 0.9%). risk glaucoma suspects when correlated with the field defects. Classically, nasal step, early arcuate and advanced arcuate RNFL map and quadrant values provided by SD-OCT helped to defects are strongly associated with glaucoma, and we found localise areas of RNFL loss when reviewing the fundus photos.

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Figure 3 The grading schema of visual field grading. PSD, pattern SD.

Nineteen (2.1%) eyes in this young population were finally cate- sectional sample, longitudinal prospective data is still being col- gorised as high-risk glaucoma suspect, and the others appeared lected and will be reported in the future. Approximately 16.1% lower risk but would need follow-up testing to assess for progres- had repeatable arcuate-like field defects with 2.1% eyes judged sion. Two typical cases with high and low risk of glaucoma sus- to be at high risk of glaucoma after IOP, CCT, fundus photos pects were shown in the online supplementary materials. and OCT were also reviewed and correlated. There is much

DISCUSSION The ZOC–BHVI Myopia Registry Study was initiated to observe the natural history of high myopia and to explore the Table 2 The distribution of each visual field defects in high potential risk factors for visual acuity damage. This current ana- myopia lysis of the visual field data from 487 young high myopes Category Number Per cent (95% CI) derived from the ZOC–BHVI study has led to proposing an updated visual field classification system for high myopia and Normal 301 33.7% (30.6% to 36.9%) glaucoma. While this study is a retrospective review of a cross- Enlarged blind spot 229 25.6% (22.8% to 28.6%) Abnormal suspect 55 6.2% (4.7% to 7.9%) Nasal step 46 5.1% (3.8% to 6.8%) Table 1 The demographic characteristics of the studied population Early arcuate 68 7.6% (6.0% to 9.5%) Advanced arcuate 30 3.4% (2.3% to 4.8%) 25%–75% Generalised reduction in sensitivity 209 23.4% (20.6% to 26.3%) Median percentile Range Paracentral defect 53 5.9% (4.4% to 7.7%) Age (year) 17.4 13.1–28.1 7–70 Central defect 9 1.0% (0.4% to 1.9%) Gender (male/female) 229/258 Rim artefacts 22 2.5% (1.5% to 3.7%) Spherical equivalent (dioptre) −8.6 −7.4 to −11.0 −6.0 to −35.0 Tilted disc defects 14 1.6% (0.8% to 2.6%) Axial length (mm) 27.2 26.3–28.1 23.8–32.0 Cecocentral defects 3 0.3% (0.0% to 0.9%)

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interest in this area because young high myopes may be at risk Furthermore, in a study conducted among inexperienced glau- for normal tension glaucoma (NTG) but diagnosing glaucoma coma and normal subjects to explore the sensitivity and specifi- in this setting can be a challenge given the overlap in structural city of SITA fast versus SITA standard on glaucoma diagnosis, and functional testing. The high myopes with arcuate-like visual the authors found both strategies had similar results.22 fields will be followed to watch for visual field progression over The intergrader agreement κ value in our study was 0.61, the next 10 years. Those results may be able to confirm the which was similar to OHTS,11 whose agreement among three natural history of a previously reported small series of young graders was 0.64–0.66, but the agreement between two graders Chinese high myopes followed over 7 years who had minimally was better than ours. The κ in our study was not significantly progressive visual field defects.9 better than OHTS because our classification allowed up to two When designing the visual field classification, we decided not categories for each field (ie, generalised depression and arcuate), to use mean deviation (MD) since the MD significantly and we did not analyse the upper and lower hemifield separately. decreases as the degree of myopia increases. A study by Aung et The most common defect was an enlarged blind spot, which is al of 146 patients with an average refraction of −6.4±3.7 D more likely in high myopes due to elongation of the eye and (range −0.5 to −14.0 D) using a regression model, found that resultant displacement of the optic nerve insertion. Several epi- when myopia increased by 1 dioptre, the MD decreased by demiological studies have found that the tilted disc (structural about 0.2 dB.12 This relationship held for high myopia alone, changes) is very high, about 50%–70% in myopia or high and also for glaucoma with myopia. In Mayama’s study,13 the myopia23 24 and only about 10% in emmetropic individuals.24 mean refraction was −2.4±3.5 D (range +4.0 to −13.0 D) and, The enlarged blind spot may be due to the peripapillary similarly, more negative spherical equivalent was associated with atrophy25 or elongated axial length with a tilted optic nerve greater visual defects in advanced stage both POAG and NTG in insertion that maps outside of the normal blind spot on static per- central 10° field. Similar results were also found in a Japanese imetry. Peripapillary atrophy was reported to be as high as 80% cohort of high myopes in Araie’s study.14 In a retrospective ana- in the high myopia study (SE≤−6.0 D) by Chang et al23 in which lysis conducted by Perdicchi et al15 exploring the effect of subjects were enrolled from three population-based investiga- various degrees of myopia on glaucoma visual field progression tions, age 40 years and older and the peripapillary atrophy was over a study duration from 24 to 64 months, the results of 110 based on fundus photos using Curtin and Karlin classification.26 patients revealed a significant decrease of MD in highly myopic The main strength of this study is the large number and a patients. Thus, a new pattern-based visual field defect classifica- priori systematic description of the visual pattern of visual field tion system helps to describe more accurately the distribution of defects in high myopic patients validated with acceptable agree- abnormal points for pathological myopia combined with glau- ment between independent readers. Although the classification comatous defects. appears complicated, it encompasses both myopic and glau- To the best of our knowledge, this is the first comprehensive comatous common categories with specific subtypes. visual field classification in high myopes. In a study carried out Nonetheless, several limitations should be noted. First, the by Fledelius and Goldschmidt,16 the authors used Goldmann patients were mostly recruited from specialised outpatient clinics Kinetic perimetry with a large test stimulus (V/4e) to explore lacking the random distribution of prospective population-based the visual field characteristics in high myopia in a sample size of study designs. Second, although we were selecting from a large 52 eyes (31 patients), using three defined types: significant sample size of over 1000 subjects enrolled in the high myopia visual field defects, marginal peripheral constriction and normal registry, only about half of them had visual fields tested at base- without further descriptive details. There were also several line, so the percentage may not be representative of the entire visual field defect categories, but they were specifically designed group. Third, the number of first time test takers was not for staging glaucoma or glaucoma suspects, so the defect types recorded, but this effect was minimised by having unreliable did not match those commonly found in high myopia. For the exams repeated. Fourth, our classification scheme for abnormal enhanced glaucoma staging system (GSS-2) classification,17 the defects produced a κ of 0.61, which may have been higher if we stage (stage 0–5) and type (localised, generalised and mixed had fewer categories where subjects could have two subtypes. For defects) was totally based on MD and corrected pattern SD or example, if we only focus on glaucomatous defect (adding cat- corrected loss variance, but did not include various field defect egories 4A–4C together), then the κ improves to 0.74. Fifth, the distribution patterns. In the Ocular Hypertension Treatment high myopia registry study had chosen 24-2 SITA fast testing Study (OHTS) visual field classification,11 the defects strategy which may be a possible limitation for those who use were divided into three major types: glaucoma-related defects, 24-2 SITA standard. However, it is unlikely as a study by neurological defects and artefacts. We did reference the Saunders21 demonstrated that SITA fast and SITA standard result glaucoma-related defects, such as: nasal step, early arcuate, differences were similar and only small differences were found at advanced arcuate, paracentral defect, generalised reduction sen- low sensitivity values. Thus having used SITA fast would not sig- sitivity, rim artefacts, but we also added some classic myopic nificantly affect our classification system. field defects, such as: enlarged or off-set blind spot, tilted disc In conclusion, we have defined and validated a comprehensive defect and cecocentral defect. visual field defect classification system for high myopia com- All subjects had undergone 24-2 SITA fast testing strategy. bined with glaucomatous defects. We have reported on a new The 24-2 pattern covers the central 24° visual field and is com- finding of the percentage of arcuate-like visual field defects that parable to the 30-2 pattern in diagnosing glaucoma,18 and the need to be followed because of the risk of NTG. Finally, we 24-2 pattern is expected to have fewer lens rim artefacts. SITA plan to review serial fields from the ZOC–BHVI subjects who strategy has become the most commonly used in glaucoma diag- have high risk of glaucoma. nosis due to its time saving without reducing its effectiveness.19 20 21 Two studies indicated that SITA standard strategy was less Correction notice The author affiliation information for the authors Brien A Holden variable and more precise than SITA fast in patients with glau- and Mingguang He has been updated since this paper was first published online. coma, but only for low sensitivity spots. Most of the high Contributors XD: collected the data, conducted the analysis, organised the writing myopes were normal, so SITA fast was a better choice. and compiled the initial draft. RTC: collected the data, organised the writing and

Ding X, et al. Br J Ophthalmol 2016;100:1697–1702. doi:10.1136/bjophthalmol-2015-307942 1701 Clinical science compiled the initial draft. XG: collected the data and organised the writing. XL: 11 Keltner JL, Johnson CA, Cello KE, et al. Classification of visual field abnormalities reviewed the literatures. CAJ: reviewed the literatures. BAH: conceived and designed in the ocular hypertension treatment study. Arch Ophthalmol 2003;121: the study. MH: conceived and designed the study and organised the writing. 643–50. 12 Aung T, Foster PJ, Seah SK, et al. Automated static perimetry: the influence of Funding The study was supported by the Fundamental Research Funds of the State myopia and its method of correction. Ophthalmology 2001;108:290–5. Key Laboratory in Ophthalmology, the National Natural Science Foundation of China 13 Mayama C, Suzuki Y, Araie M, et al. Myopia and advanced-stage open-angle (81125007) and a research grant from the Brien Holden Vision Institute. The glaucoma. Ophthalmology 2002;109:2072–7. funding sources had no role in study design, data collection and analysis, decision to 14 Araie M, Arai M, Koseki N, et al.Influence of myopic refraction on visual field publish or preparation of the manuscript. defects in normal tension and primary open angle glaucoma. Jpn J Ophthalmol Ethics approval Ethics approval was provided by the Zhongshan Ophthalmic 1995;39:60–4. Center Ethics Review Board. 15 Perdicchi A, Iester M, Scuderi G, et al. Visual field damage and progression in – Competing interests None declared. glaucomatous myopic eyes. Eur J Ophthalmol 2007;17:534 7. 16 Fledelius HC, Goldschmidt E. Eye shape and peripheral visual field recording in high Patient consent Obtained. myopia at approximately 54 years of age, as based on ultrasonography and Provenance and peer review Not commissioned; externally peer reviewed. Goldmann kinetic perimetry. Acta Ophthalmol 2010;88:521–6. 17 Brusini P, Filacorda S. 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