ethnic variation in optic disc size by fundus photography
TRANSCRIPT
2013
Current Eye Research, 2013; 38(11): 1142–1147! Informa Healthcare USA, Inc.
ISSN: 0271-3683 print / 1460-2202 online
DOI: 10.3109/02713683.2013.809123
ORIGINAL ARTICLE
Ethnic Variation in Optic Disc Size byFundus Photography
Roland Y. Lee1, Andrew A. Kao1, Toshimitsu Kasuga1,2, Baotran N. Vo1, Qi N. Cui1,Cynthia S. Chiu1, Robert N. Weinreb3 and Shan C. Lin1
1Department of Ophthalmology, University of California, San Francisco, CA, USA,2Department of Ophthalmology, Juntendo University School of Medicine, Tokyo, Japan, and 3Department of
Ophthalmology, University of California, San Diego, California, USA
ABSTRACT
Purpose: To compare optic disc size among Caucasian, Chinese, African, Filipino and Hispanic subjects recruitedfrom a university-based general ophthalmology clinic.
Methods: In this retrospective cross-sectional study, optic disc size was calculated from fundus photographs.Differences in age, sex and spherical equivalent among the ethnic groups were examined with either Kruskal–Wallis test or Chi-square test. Ethnic differences in optic disc size were evaluated with linear mixed-effectsregression models that adjusted for age, sex, spherical equivalent, glaucoma status, lens status and use of botheyes in the same subject.
Results: Five hundred and seventy-four eyes of 305 subjects were analyzed. The mean and standard deviationof the optic disc size were 2.16� 0.41 mm2 for Caucasian, 2.30� 0.56 mm2 for Chinese, 2.31� 0.41 mm2 forFilipino, 2.38� 0.40 mm2 for African and 2.40� 0.38 mm2 for Hispanic subjects. Age and spherical equivalentdiffered among the ethnic groups by Kruskal–Wallis test (p50.05). Sex differed among the ethnic groups byChi-square test (p50.05). Ethnic differences in optic disc size were not observed among African, Hispanic,Filipino and Chinese subjects in linear mixed-effects regression analyses (p40.05). However, Caucasian differedfrom the other ethnicities in linear mixed-effects regression analyses (p50.05).
Conclusions: Optic disc size was significantly smaller in Caucasian compared to the other ethnic groups.Optic disc size differences among non-Caucasian ethnic groups were not significant.
Keywords: Ethnicity, fundus photography, glaucoma, optic disc size, race
INTRODUCTION
Glaucoma is the leading cause of irreversible blind-ness worldwide, and is projected to affect 70 millionpeople by 2020.1 A comprehensive ophthalmic exam-ination is a cornerstone to diagnosing glaucomabecause early stages of the disease are asymptomatic.2
Clinical screening of the optic disc provides usefulinformation for distinguishing patients with impend-ing glaucomatous visual field loss.3 Evaluation ofthe optic disc size is important as optic cup size, opticdisc rim area and cup-to-disc ratio vary with opticdisc size.4–9 The optic disc size may also influence the
likelihood a clinician assigns a diagnosis of glaucomaas glaucomatous optic neuropathy has been shownto be missed more frequently in glaucomatous eyeswith small optic nerve heads due to misleadingly lowcup-to-disc ratios.10
Measurements of optic disc size have previouslybeen documented in African,11–18 Caucasian,11–18
Asian,17,18 Hispanic17,18 and Filipino17 populations.However, most of these studies examined the ethnicgroups in isolation or in pairs, making it difficult tocompare variability in optic disc size across the fullspectrum of ethnic groups. A review of the literaturepublished between the years 1970 and 2004 indicated
Correspondence: Shan C. Lin, Department of Ophthalmology, University of California, San Francisco, School of Medicine, Box 0730, 10 KoretStreet, San Francisco, CA 94143-0730, USA. E-mail: [email protected]
Received 29 December 2012; revised 11 April 2013; accepted 22 May 2013; published online 9 July 2013
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that the different instruments and techniques avail-able for optic disc size measurements providedestimates that are not interchangeable.4 The compar-ability of optic disc size measurements derivedfrom a collection of studies without the contextof instrumentation and technique may be poor.This university-based retrospective cross-sectionalstudy simultaneously examined optic disc sizes inCaucasian, Chinese, African, Filipino and Hispanicsubjects using fundus photography to provide anestimation of optic disc size variability among the fiveethnic groups.
METHODS
This study received institutional review board app-roval from the University of California, San Francisco(UCSF) Committee on Human Research beforecommencing data collection. Medical records frompatients who had consecutively received fundusphotography from a university-based general oph-thalmology clinic (Adult Eye Care at the UCSF,Department of Ophthalmology) between June 2006and August 2009 were retrospectively reviewed. Thefollowing information was retrieved from the medicalrecords: age, sex, visual field results, vertical cup-to-disk ratio, refractive error, glaucoma status, lensstatus and ethnicity. Visual field data were onlyavailable for patients with glaucoma or glaucomasuspicion. The patients’ self-description of ethnicitydetermined their classification into one of the follow-ing ethnic study groups: Caucasian, Chinese, African,Filipino and Hispanic. Data were mostly collectedfrom the same date in which the fundus photographswere taken. If the patient was not seen on the sameday, the record from their next clinic visit was used.
Visual field examination was performed withHumphrey Field Analyzer (model 750i; Carl ZeissMeditec, Inc., Dublin, CA). Vertical cup-to-disk ratiowas measured with the use of slit lamp biomicroscopy(model BM900; Haag-Streit AG, Koeniz, Switzerland).The spherical equivalent was derived from refractiveerror using the following formula: sphere plus half ofthe cylinder. The International Society of Geographicand Epidemiologic Ophthalmology (ISGEO) schemeprovided the basis for the diagnosis of glaucoma.19
Glaucomatous optic nerve damage is confirmed by aglaucomatous optic nerve appearance (vertical cup-to-disk ratio40.6) and a corresponding reliable visualfield defect. A glaucomatous visual field defect isconsidered present when the hemifield test is gradedoutside normal limits (with a probability of less than5% based upon comparison with age-matched con-trols in the pattern deviation plot) and showed acluster of three or more non–edge contiguous pointsthat did not cross the horizontal meridian. Visualfields were defined as reliable if they fulfilled the
following criteria: fixation losses533%, false positives520% and false negatives520%.
All fundus photographs were captured by the sametechnician using a digital fundus camera (Topcon TRC50EX; Topcon Corporation, Tokyo, Japan). If fundusphotographs of different magnification were available(either 20x or 35x magnification), the photographswith the highest magnification were utilized. Thesame glaucoma subspecialist (S.C.L) outlined theoptic disc margin in each fundus photograph byusing the magnetic lasso tool in Adobe Photoshop(version CS5; Adobe Systems, Inc., San Jose, CA). Themeasurement tool was then used to count the numberof pixels enclosed in the tracings. Due to a lack of axiallength measurements, the Littman formula couldnot be applied to determine the true size of the opticdisc in the study subjects. Heidelberg RetinaTomograph (HRT; Heidelberg Engineering, Carlsbad,CA) is widely considered the gold standard formeasuring optic disc size as it demonstrates goodreproducibility20 and correlates well with in-vivomeasurements of the optic disc obtained duringvitrectomy.21 By matching the number of pixels ina subset of fundus photos to optic disc size asdetermined by HRT, we constructed a formulathat allowed the conversion of pixel numbers tooptic disc size. The same glaucoma subspecialist(S.C.L) outlined the optic disc margin in all thecorresponding HRT images. Since fundus photo-graphs of two different magnifications (20x and 35x)were utilized, a separate conversion formula wascalculated for each magnification based on a ran-domly selected subset of 20 patients. The conversionformula for calculating optic disc size from the fundusphotographs at 20x magnification was 0.000002349�photo pixelþ 1.196 with a Pearson’s correlation coef-ficient of 0.864. The formula for calculating the opticdisc size from the fundus photographs at 35x magni-fication was 0.000006772�photo pixelþ 1.711 withPearson’s correlation coefficient of 0.621. These twoequations, corrected for magnification, were utilizedto convert the number of pixels enclosed in theoptic disc outline to optic disc size for all subjects inthe study population.
All statistical analyses were conducted withR-statistics (v2.15.1 software for Macintosh; RFoundation for Statistical Computing, Vienna,Austria) and p values 50.05 were considered toindicate statistical significance. Differences in age,spherical equivalent and optic disc size among theethnic groups were examined with the Kruskal–Wallistest, while differences in sex among the ethnic groupswere examined with the Chi-square test. The associ-ation between optic disc size and glaucoma statuswas examined with a linear mixed-effects regressionmodel that adjusted for age, sex, spherical equivalent,lens status, ethnicity and use of both eyes in the samesubject. The association between optic disc size and
Ethnic Variation in Optic Disc Size 1143
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lens status was examined with a linear mixed-effectsregression model that adjusted for age, sex, sphericalequivalent, glaucoma status, ethnicity and use of botheyes in the same subject. Ethnic differences in opticdisc size were analyzed first by pairwise comparisonsof optic disc size among Chinese, African, Hispanicand Filipino subjects and then followed by a com-parison of optic disc size between Caucasian andother ethnicities. The linear mixed-effects regressionmodels used to analyze the ethnic differences in opticdisc size were adjusted for age, sex, glaucoma status,lens status, spherical equivalent and use of both eyesin the same subject.
RESULTS
Five hundred and seventy-four eyes of 305 subjectswere included in the analysis. The inability to assessthe excluded 36 eyes encompassed the followingreasons: 22 had poor quality photographs due tocataract, five had choroidal nevus, three had enucle-ation, two had phthisis, three had photographs thatdid not capture the entire optic nerve and one hadsevere age-related macular degeneration. Table 1summarizes the demographics, clinical characteristics,glaucoma status, lens status and optic disc size of thestudy subjects by ethnicity. The mean and standarddeviation of the optic disc size were 2.16� 0.41 mm2
for Caucasian, 2.30� 0.56 mm2 for Chinese, 2.31�0.41 mm2 for Filipino, 2.38� 0.40 mm2 for African and2.40� 0.38 mm2 for Hispanic subjects. Optic disc size,age, and spherical equivalent significantly differedamong the ethnic groups by the Kruskal–Wallis test(p50.05). Sex was significantly different amongthe ethnic groups by the Chi-square test (p50.05).
The association between optic disc size and glaucomastatus was not significant in the linear mixed-effectsregression analysis, which adjusted for age, sex,spherical equivalent, lens status, ethnicity and useof both eyes in the same subject (p40.05).The association between optic disc size and lensstatus was not significant in the linear mixed-effectsregression analysis, which adjusted for age, sex,spherical equivalent, glaucoma status, ethnicity anduse of both eyes in the same subject (p40.05).
Table 2 shows the pairwise comparisons of opticdisc size among Chinese, African, Hispanic andFilipino subjects. Ethnic differences in optic disc sizewere not observed among the African, Hispanic,Filipino and Chinese subjects in the linear mixed-effects regression analyses (p40.05). The optic discsize was significantly smaller in Caucasian comparedto the other ethnic groups in linear mixed-effectsregression analyses (p50.05). The linear mixed-effectsregression models used to analyze the ethnic differ-ences in optic disc size were adjusted for age, sex,glaucoma status, lens status, spherical equivalent anduse of both eyes in the same subject.
Optic disc size was calculated from fundus photo-graphs based on conversion formulas developedby corresponding pixel counts from the fundusphotographs with optic disc size in the HRT images.Since our study utilized fundus photographs of twodifferent magnifications, 20x and 35x, a separateconversion equation was calculated for each magni-fication based on a randomly selected subset of 20patients with fundus photographs of that magnifica-tions. The number of fundus photographs in eachmagnification for the five ethnic groups are listedin the following as (numbers of 20x magnification:numbers of 35x magnification): Caucasian (115:35);
TABLE 1 Demographics and clinical characteristics of the study population.
Ethnicity Caucasian Chinese Filipino African Hispanic p Value
DemographicsNumber of patients 79 73 35 70 48Number of eyes 150 136 66 130 92Age (years)a 65.6� 14.8 71.0� 11.9 63.7� 16.2 68.0� 13.9 66.0� 14.6 0.007b
Sex (male:female) 87:63 55:81 29:37 47:83 36:56 0.002c
Glaucoma statusNon-glaucoma 12 12 8 22 16Glaucoma suspect 73 70 47 53 60Glaucoma 65 54 11 55 16
Non-glaucoma eyesDiabetes 2 10 0 6 1Age-related macular degeneration 2 0 0 0 2Hypertension 1 0 0 0 2Pseudophakic 21.3% 21.3% 25.8% 30.0% 16.3%
Clinical characteristicsSpherical equivalent (diopters)a �0.86� 2.63 �1.43� 3.44 �1.13� 3.71 �0.443� 2.27 0.55� 2.27 0.003b
Optic disc size (mm2)a 2.16� 0.41 2.30� 0.56 2.31� 0.41 2.38� 0.40 2.40� 0.38 50.0001b
aData are expressed as mean value� standard deviation.bp Value by Kruskal–Wallis test.cp Value by Chi-square test.
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Chinese (111:25); Filipino (49:17); African (80:50) andHispanic (53:39).
DISCUSSION
This study evaluated the optic disc size amongCaucasian, Chinese, African, Hispanic and Filipinosubjects from a university-based general ophthalmol-ogy clinic using fundus photography. Our resultsshowed that optic disc size was significantly smallerin Caucasian compared to other ethnic groups.Comparisons of optic disc size among the ethnicgroups were corrected for age, sex, glaucoma status,lens status and spherical equivalent. These findingssuggest that ethnicity is an independent determinantof optic disc size.
This study provided strong evidence thatCaucasians possess smaller optic disc size comparedto Chinese, African, Hispanic and Filipino subjects.This finding is in line with results from otherethnicity-based comparisons of optic disc size usingnumerous imaging modalities. In particular, a smalleroptic disc size in Caucasians compared to Africanshas been confirmed by fundus photography,11
Rodenstock optic disc analyzer,12 Stratus opticalcoherence tomography,13 HRT14–17 and Cirrus high-definition optical coherence tomography,18 while asmaller optic disc size in Caucasians compared toHispanic, Asians, Chinese and Filipino have beenverified by HRT17 and Cirrus high-definition opticalcoherence tomography.18 Despite the multitude ofstudies, however, the different instruments usedfor measuring optic disc size provide estimationsthat are not interchangeable and readily comparable.Even if the same instruments were used in separatestudies, measurements were likely still affected by theposition of the camera with respect to the eye and/ora reliance on an operator to outline the optic discmargin to define a reference plane before automatedcalculations. Therefore, a key value of our study lies inits standardization of instruments and techniquesthrough simultaneous comparisons of optic disc sizeacross multiple ethnicities. A direct measurement ofoptic disc size is only possible during intraocularprocedures involving the posterior pole or throughhistological preparations.22 On the other hand, values
derived from imaging modalities are not absolute andshould be utilized as a gauge of the variability in opticdisc size among ethnic groups. As such, the use of asingle instrument and operator across separate ethnicgroups is very important.
Although two previous studies published byKnight et al.18 and Seider et al.17 also examinedmore than two ethnic groups, there are notabledifferences between their studies and the presentstudy. The study by Knight et al.18 enrolled 284subjects from four different ethnic groups (Caucasian,Chinese, African and Hispanic) across multiple siteswith separate imaging devices and different techni-cians. As such, discrepancies in examination tech-niques, patient positioning and machine calibrationmay well have contributed to measurement incon-sistencies. Our study avoids the issue of inter-observer reliability by utilizing a single imagingdevice and a single technician to examine all subjects.Furthermore, the present study recruited all fivedifferent ethnic groups (Caucasian, Chinese, African,Filipino and Hispanic) from a single site, therebyeliminating interfacility variability. The study bySeider et al.17 was a prior publication from our owngroup, which examined five ethnic groups (African,Asian, Caucasian, Hispanic and Filipino) using HRT.Although both studies compare five different ethnicgroups, there are two notable distinctions. First, in thestudy by Seider et al., subjects were recruited froma glaucoma clinic and the study utilized an opticnerve imaging device that is primary used in patientswith glaucoma or suspicion for glaucoma. Therefore,the majority of the subjects (99%) from the studycarried a diagnosis of glaucoma or were glaucomasuspects. The present study recruited subjects froma general ophthalmology clinic and utilized fundusphotography. Therefore, a significant portion of thisstudy population are not glaucoma suspects and donot carry a diagnosis of glaucoma. To account for thepotential bias of including subjects with a diagnosisof glaucoma or are considered glaucoma suspects,we adjusted for the subjects’ glaucoma status in ouranalyses. Second, the Seider et al. study used the termAsian in a broad sense, covering all populationsfrom South Asia to East Asia, and incorporated manydifferent Asian subgroups (Indian, Chinese, Japanese,Korean and Vietnamese) into a single broad Asiangroup. The present study recognizes that the types ofglaucoma varies substantially among the differentAsian subgroups and has further divided the broadethnic classification of Asian subjects into distinct twoAsian subgroups (i.e. Chinese and Filipino).
Despite the fact that there is some consensusregarding the existence of ethnic differences in opticdisc size, there has been no study on the effect ofethnic differences in optic disc size. We believe thatthe results of our study, supplemented by the Seideret al. study, may help to address this question. The
TABLE 2 p Values for pairwise comparisons of optic disc sizeby linear mixed-effects regression analyses.a
African Hispanic Filipino Chinese
African 0.7808 0.7058 0.2369Hispanic 0.4302 0.2224Filipino 0.6400
ap Values by linear mixed-effects regression model, adjustedfor age, sex, glaucoma status, lens status, spherical equivalentand use of both eyes in the same subject.
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optic disc measurements for the two studies are listedin Table 3 for comparison; while Caucasians havesimilar optic disc size in both the glaucoma andgeneral ophthalmology clinics, Chinese, African,Hispanic and Filipino subjects had considerablyhigher mean values in optic disc size in the glaucomaclinic compared to subjects from the general ophthal-mology clinic. The optic disc size influences thelikelihood a clinician assigns a diagnosis of glaucoma.Indeed, glaucomatous optic neuropathy has beenshown to be missed more frequently in glaucomatouseyes with smaller optic discs because they naturallymanifest a lower cup-to-disc ratio.10 Since glaucomasubspecialists are more likely referred patients withlarger optic disc size and more suspicious cup-to-discratios, the comparable optic disc sizes of Caucasiansin both the general ophthalmology and glaucomaclinics suggest that there might be a tendency forunder-diagnosis and under-referral of Caucasianglaucoma suspects.
The Blue Mountains Eye Study found that eyeswith larger optic disc size tend to exhibit higher cup-to-disc ratios.6 The correlation between optic disc sizeand cup-to-disc ratio is pertinent because whereashigh cup-to-disc ratios can be physiologic in eyeswith large optic discs, high cup-to-disc ratios in eyeswith small optic discs may indicate the presence ofglaucomatous optic neuropathy.4 Some histologicalstudies have reported a positive correlation betweenoptic disc size and the number of axons; the numberof axons increases linearly with increased optic discsize.23,24 The relatively large reserve of axons in an eyewith a large disc may explain why a high cup-to-discratio may be normal in an eye with a large opticdisc but not in an eye with a small optic disc. Since asmaller optic disc is more likely to manifest a lowercup-to-disc ratio, an eye with a small optic disc and acup-to-disc ratio greater than 0.6 is more likely tosuffer from glaucomatous optic neuropathy.Conversely, a larger optic disc characteristically mani-fests a higher cup-to-disc ratio, and a cup-to-disc ratio
greater than 0.6 in such an eye is less likely to equatewith glaucomatous optic neuropathy. SinceCaucasians have smaller optic disc sizes on average,they are more likely to manifest a lower physiologiccup-to-disc ratio. A general ophthalmologist whoscreens for glaucoma based on the ISGEO schememight use a cup-to-disk of 0.7 as the threshold forfurther evaluation such as visual field testing. Thus,cup-to-disc ratio alone could influence the diagnosisof glaucoma by a general ophthalmologist and sub-sequent referrals to glaucoma subspecialists. Theoverall effect might be an under-diagnosis andunder-referral of Caucasian glaucoma suspects.
This study has several limitations. First, a commonlimitation in most studies exploring ethnic differencesin disease characteristics lies in the ethnic classifica-tion of study subjects. Ethnic groups in our study arenot stratified according to specific anthropologicallybased criteria. Instead, the classification used in ourstudy is based on the subjects’ self-identified ethnicity,as listed in our medical record system. Second,subjects with darker fundi (i.e. Chinese, Filipino andAfrican subjects) may be less likely to have goodquality high magnification fundus photos becauseof less reflected light and lower exposure values.However, Fisher’s Exact test did not demonstrate adifference in the proportion of high magnificationphotos between Caucasians and subjects with darkerfundi (i.e. Chinese, Filipino and African subjects;p = 0.3717). Third, our study population may sufferfrom selection bias because recruitment took placein a university-based general ophthalmology clinic.There is a possibility that patients with larger opticdiscs and more suspicious cup-to-disc ratios are moreoften referred to an academic institution such asUCSF, and are therefore more likely to receive opticdisc photography. Furthermore, fundus photographyis not a part of the routine ophthalmic examinationand is not usually ordered unless a reason such asglaucomatous cup-to-disc appearance is present.Lastly, our retrospective study did not have accessto axial length data normally used in the Littmannformula to calculate the actual size of objects onfundus photographs. Despite these limitations, ourstudy may provide a valuable addition to the existingliterature because of the use of a single standardizedinstrument and operator for all five different ethnicgroups.
In summary, this study demonstrated thatCaucasians possess smaller optic discs compared toChinese, African, Hispanic and Filipino subjects in astudy population recruited from a university-basedgeneral ophthalmology clinic. The results of our studyprovide strong support for the existence of ethnicvariations in optic disk size and that these differencesshould be taken into consideration in the diagnosisand treatment of glaucoma. Ethnic differences in opticdisc size may well affect the diagnostic capability of
TABLE 3 Comparison of optic disc size in subjects recruitedthrough general ophthalmology and glaucoma clinics.a
EthnicityOptic disc size (mm2)
[present study]bOptic disc size (mm2)
[Seider et al.17]c
Caucasian 2.16� 0.41 2.15� 0.58Chinese 2.30� 0.56 2.38� 0.54Filipino 2.31� 0.40 2.48� 0.70African 2.38� 0.40 2.55� 0.51Hispanic 2.39� 0.38 2.57� 0.55
aData are expressed as mean value� standard deviation.bSubjects recruited from a general ophthalmology clinic(Adult Eye Care at the University of California San Francisco,Department of Ophthalmology).cSubjects recruited from a glaucoma clinic (Beckman VisionCenter at the University of California San Francisco,Department of Ophthalmology).
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quantitative imaging modalities to separate normalfrom glaucomatous eyes due to a reliance on device-specific normative ranges that do not account forethnic differences. While a high cup-to-disc ratio canbe physiologic in an eye with a large optic disc size,the presence of a high cup-to-disc ratio in an eye witha small optic disc size may be indicative of glau-comatous optic nerve damage. This relationshipbetween optic disc size and cup-to-disc ratio maylead to an under-diagnosis of glaucoma in eyes withsmall optic discs such as those of Caucasians. Finally,further studies on a larger population are warrantedto confirm our findings.
DECLARATION OF INTEREST
The authors have no financial or other conflicts ofinterest concerning this study.
This study was supported by NIH-NEI EY002162 –Core Grant for Vision Research, Research to PreventBlindness and That Man May See, Inc.
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