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1From the Institute of Ophthalmology, University College London, United Kingdom; the 2Key Laboratory of Ophthalmology, Sun Yat-sen University, Ministry of Education, Zhongshan Ophthalmic Center, Guangzhou, China; the 3Glaucoma Research Unit, Moorfields Eye Hospital, London, United Kingdom; and the 4Wilmer Eye Institute, Johns Hopkins University, Baltimore, Maryland.
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Abstract |
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METHODS. Random clustering sampling was used to identify adults aged 50 years and over in Liwan District, Guangzhou. Glaucoma was diagnosed with the ISGEO (International Society of Geographical and Epidemiological Ophthalmology) classification scheme. All subjects underwent gonioscopy.
RESULTS. In the study, 1504 subjects (75.3% participation rate) were examined, with a crude prevalence of all glaucoma of 3.8% (95% confidence interval [CI], 2.8%–4.8%). Primary open-angle glaucoma (POAG) was found in 2.1% (95% CI, 1.4%–2.8%) and primary angle-closure glaucoma (PACG) in 1.5% (95% CI, 0.8%–2.1%). The prevalence of all glaucoma was significantly higher in older people and men.
CONCLUSIONS. POAG was more common than PACG in this southern Chinese population, with rates similar to those reported in Chinese Singaporeans. The age-adjusted rate of POAG was similar to that found in European-derived populations, but PACG was more common among Chinese, indicating that there is a large burden of glaucoma in the Chinese people.
We therefore performed a population-based study of glaucoma prevalence in the city of Guangzhou in southern China. To promote the use of uniform definitional standards in glaucoma research we adhered to a widely accepted scheme for reporting the prevalence of glaucoma in epidemiologic research.15
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Methods |
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Study subjects were enrolled in Liwan District, Guangzhou. Liwan district is 1 of 10 administrative districts in Guangzhou, with a population of 514,600 (National Census 2000.) The decision to select this district for the survey was taken because of its stable, older population and a socioeconomic profile representative of Guangzhou as a whole.16 One street block of Fengyuan Street, with a population of 62,815 occupying 0.77 square kilometers was selected, because it is a mainly residential area with a limited number of commercial and industrial buildings. Ten clusters within this street block were identified, defined geographically by Residence Administrative Committees (RACs) subdivisions, each with an approximately equal number of residents (6000).
Individuals aged 50 years or more who had been resident in the selected study districts for more than 6 months were considered eligible during the enumeration. Using the Household Resident Register record kept by the district government, we identified households with eligible subjects by the address, name of household head, name of subjects, and date of birth. A total of 2313 eligible subjects were identified from this register. These households were then individually visited to verify that the enumerated subjects were still resident at the address and to arrange appointments for examination. Written, informed consent was obtained after explaining the purpose of the study and the risks and benefits of the examination.
Eye Examination
An examination site was set up in the community within half an hour’s walking distance for most subjects. Identity of the subjects was verified using the subjects’ official photo identity cards. A standard questionnaire was administered by a trained interviewer to collect details of ophthalmic history, general medical history, income, and education. A nurse used a handheld autorefractor (ARK-30; Nidek Corp., Gamagori, Japan) to measure the noncycloplegic refraction. Distance visual acuity was measured using an Early Treatment Diabetic Retinopathy Study (ETDRS) logMAR (logarithm of the minimum angle of resolution) E chart (Precision Vision, Villa Park, IL) with a standard illumination box at a distance of 4 m. The presenting visual acuity with habitual correction was recorded. In those with presenting visual acuity of less than 6/12 in either eye, best corrected vision was assessed using the results of autorefraction with necessary subjective refinement.
Intraocular pressure (IOP) was measured by a nurse using a handheld tonometer (Tonopen; Mentor, Norwell, MA) device after instilling topical anesthesia (0.4% Benoxil; Oxybuprocaine, Santen, Japan). The internal calibration program was run before use every day. The measurement was repeated if the SE of the measurement was more than 5%. If three consecutive measurements were not able to achieve SE < 5% or the patients could not cooperate, the IOPs were considered not measurable (27 right and 28 left eyes). One measurement was taken and recorded for each eye. The decision to employ the Tonopen handheld tonometer was taken in light of our previous manometric studies into IOP measurement error in Chinese eyes that suggest that Tonopen gives the most accurate clinical estimates of true IOP.17
Slit lamp examination (model SL-8Z; Topcon, Tokyo, Japan; with D1x digital image system; Nikon, Tokyo, Japan) was then performed by an experienced ophthalmologist (MGH) to identify abnormalities of the anterior segment, including evidence of ischemic sequelae of angle-closure, secondary glaucoma, and lens opacity. Gonioscopy was performed with a Goldmann-type one-mirror lens (Haag Streit, Bern, Switzerland) at x25 magnification with low ambient illumination by the same observer (MGH) whose work was standardized against that of an experienced gonioscopist (PJF). A weighted 
of 0.82 was achieved for assessment of occludable angle in 44 eyes (21 occludable and 23 not by PJF). A narrow vertical beam 1 mm in length was offset vertically for superior and inferior quadrants, horizontally for nasal and temporal quadrants. Care was taken to avoid light falling on the pupil. Small movements of the lens were allowed to visualize the drainage angle but large movement was avoided because of the possibility of indentation. Dynamic examination with Goldmann lens was performed after the static gonioscopy of four quadrants were completed. If a satisfactory examination could not be achieved with the Goldmann lens, a four-mirror lens was used. The Spaeth grading system was used to record the results.18
The optic disc was evaluated using a +78-D lens at x16 magnification without pupil dilation. The vertical cup-to-disc ratio (VCDR) was used as the key index of structural glaucomatous change. Measurement of VCDR excluded parapapillary atrophy and the scleral ring of Elschnig. The margins of the cup were defined by stereoscopic view as the point of maximum inflection of the vessels crossing the neuroretinal rim. Standard photographs for VCDR from 0.1 to 1.0 in 0.1 increments were used in the grading process. A measuring graticule was not used. Disc hemorrhage and notching were recorded. If the stereo view was not satisfactory, the pupil was dilated using 1% tropicamide (Mydriacyl; Alcon, Puurs, Belgium) plus 2.5% phenylephrine (Alcon), provided the participant did not have closed angles with raised intraocular pressure. If the optic disc was not visible despite pharmacological dilation, "fundus not seen" was recorded.
Those people with suspected glaucomatous disc damage (VCDR 
0.7 in either eye, VCDR asymmetry 0.2 or IOP 21 mm Hg) were asked to return for visual field (VF) testing on a subsequent day. White-on-white semiautomated perimetry (Humphrey 750; Carl Zeiss Meditec, Inc., Dublin, CA) was performed using near refractive correction. The SITA-Fast 24-2 mode was used throughout, followed by a SITA-standard if the first test result was abnormal. If the reliability of the field test was not satisfactory or there was a defect compatible with glaucoma, the participants were invited for a second field test on another day. A visual field compatible with glaucoma was defined as a glaucoma hemifield test result outside normal limits combined with a cluster of four or more contiguous points on the pattern deviation plot (P < 5% occurring in age-matched normal subjects) not crossing the horizontal meridian.2 12
The definitional criteria developed by ISGEO (International Society of Geographical and Epidemiological Ophthalmology) were used in the present study.15 Because definitive information on the presence of glaucomatous disc and field damage is not always available in field studies, the identification of glaucoma can be made on three levels of evidence. The highest level of evidence requires optic disc and visual field evidence (VCDR or asymmetry 97.5th percentile and reproducible glaucomatous field defect). In the second, if the visual field test could not be performed satisfactorily, a severely damaged disc (VCDR or asymmetry 99.5th percentile) is considered compatible with glaucoma. The third level of evidence specifies that if the optic discs cannot be examined due to severe media opacity, subjects who are blind (corrected visual acuity, <3/60) and have undergone previous glaucoma surgery, or have an IOP greater than the 99.5th percentile are classified as having glaucoma. The division of cases of glaucoma into primary angle-closure glaucoma (PACG) and POAG was based on the gonioscopic finding of a narrow angle (synonymous with the term occludable, where the posterior, usually pigmented, trabecular meshwork is not visible for 270° or more during a static examination). Established primary angle-closure (PAC) was diagnosed based on the combination of a narrow angle with an IOP 95th percentile of the normal population and/or primary peripheral anterior synechiae (PAS), or evidence of anterior segment ischemia after an increase in IOP (iris atrophy, distortion of radial muscle fibers, or "glaukomfleken" lens opacities), or a reliable medical history, if the angle status had been changed by previous treatment. Elevated IOP and PAS formation were not considered prerequisites for the diagnosis of PACG.
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Results |
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Among the 1864 eligible subjects, 1405 (75.3%) were successfully examined (19 subjects were examined in their own homes). Women in younger age groups were more likely to participate than men (P < 0.001). People at the extremes of the age distribution were less likely to participate (Table 1) .
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0.7 or asymmetry, 0.2) did not complete a satisfactory visual field test. Among these, seven individuals had poor vision, mainly from cataract, the nine individuals were very frail and were unable to complete the visual field test due to physical or cognitive limitations. Of these 42 individuals with large VCDR who lacked visual field testing, nine were ultimately diagnosed as having glaucoma based on the category - (six individuals) or -3 (three individuals) definitions. Fifty-three people were found to have glaucoma, 29 (54.7%) with POAG, 21 (39.6%) with PACG, and 2 (3.8%) with secondary glaucoma (one neovascular, one traumatic; Table 4 ). It was not possible to classify the mechanism in one case because both eyes had undergone cataract surgery, and broad PAS were seen. Consequently, objective classification of angle width was not possible. Ocular hypertension in this cohort was defined by the 95th percentile of IOP in people who did not have a reproducible visual field defect (i.e., 21 mm Hg). There were 30 people (3.0%) in the cohort who had statistically elevated IOP but were not classified as having glaucoma. In 29 people classified as having POAG, four had IOP higher than 21 mm Hg in the affected eye, one had normal IOP on medication, and another one had normal pressure after surgical trabeculectomy. Therefore 85% of untreated open-angle glaucoma could be classified as "normal-tension" disease.
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21 mm Hg) at screening and 10 had normal IOP after laser or surgical iridectomy or trabeculectomy. The remaining two cases with normal IOP on the screening examination had not received glaucoma treatment. These two cases were diagnosed on the basis of glaucomatous field and disc damage, combined with gonioscopically occludable angles; one had PAS, the other did not. The prevalence of PACG increased with age and was higher in the women (13 cases, 1.6%) than the men (eight cases, 1.3%) although this difference between the sexes was not statistically significant (
2, P > 0.05). In the 21 PACG cases, 13 were unilateral and 8 bilateral. Eight (38%) had a history and consistent clinical signs of an acute, symptomatic attack, among which, seven had been diagnosed and treated. Five cases without symptomatic onset had been diagnosed previously (three had had surgery). Among all PACG cases, nine (42.9%) patients were blind in at least one eye, but none were bilaterally blind. In contrast to PACG, among 29 cases of POAG, only 2 (6.9%) had been diagnosed and surgically treated previously. Five of the persons were unilaterally blind (17%), 1 because of highly myopic eyes (spherical equivalent: –20 D). In 13 unilateral cases of PACG, the fellow eyes were classified as PAC,5 PACS,5 and wide angles after cataract surgery.3 |
Discussion |
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2 test, P < 0.001), a common finding in population-based research studies. Lower response rates were also encountered among elderly people (aged 80 years), possibly reflecting their limited mobility and poorer physical health. Although incomplete response in these age groups probably affected the crude prevalence estimates, the adjusted (standardized) prevalence should be affected less. It is possible that the healthier younger people (those who thought that their vision was normal) did not come, and that we therefore have overestimated the prevalence of glaucoma in this age range. It also is possible that the frailest elderly did not attend, and these individuals may have had higher rates of eye disease than those who attended. Nevertheless, given the high response rates, we believe the estimates we have obtained are probably an accurate reflection of the true rates in this population. Liwan District is an "old district" of Guangzhou, with limited recent urban development. The Resident Registry was used as the sampling frame to identify eligible subjects. Registration is a legal requirement and is maintained by the local police, detailing all permanent residents in the city. This dataset is updated on a yearly basis, assimilating information on migration, death, and new births. By using this information to identify households with eligible subjects, the need to perform door-to-door enumeration of all households in the area was avoided. Although we found that the sample was similar to the larger Liwan District population, it is possible that more transient populations and illegal populations living in the area were missed. Such individuals are likely to be poorer than permanent residents and may not have similar access to healthcare services. If they were missed, we suspect that the overall estimate of vision loss may be somewhat lower than we would have found had we performed a complete enumeration.
Defining glaucoma in population-based research continues to pose challenges, particularly in patients with missing data. Using the ISGEO classification scheme requires an assessment of VCDR, and the VCDR cutoffs for glaucoma are assessed based on population norms. A recent publication by Crowston et al.19 using Blue Mountains data indicate that the VCDR cutoffs vary depending on disc size. We did not record disc size in this study, and therefore applied a uniform cutoff to the entire cohort which may have resulted in some persons with small discs being classified as "normal," even though they had glaucomatous optic neuropathy and visual field loss. Conversely, some with large discs may have had physiological large VCDRs. In general, such people would be expected to have normal visual fields and therefore would not have been identified as having glaucoma. Furthermore, the identification of the disc and cup margins can be difficult, particularly in myopic eyes or discs with a flat contour.13 This feature is common in Chinese eyes. All these factors may compromise the accuracy of the estimates of prevalence of glaucoma.
In this study, we did not perform visual field testing on all subjects because the glaucoma grading scheme required an enlarged VCDR for a person to be classified as having glaucoma. This streamlined the logistics of examining the cohort, but it is possible that some subjects with subtle optic nerve changes were missed because visual fields would not have been performed in these individuals. The estimate of glaucoma prevalence therefore may be biased downward somewhat. Assessment of the VCDR in the present study was performed during a slit lamp examination with a +78-D lens. In most cases, this allows a stereoscopic view of the disc and may make the assessment of the margin of cup and disc easier. However, the disc assessment was not routinely performed with pupil dilation. The pupil was dilated only when the disc could not be seen satisfactorily. The VCDR assessment may therefore have been inaccurate in eyes with small, undilated pupils. Kirwan et al.14 have described that pharmacological mydriasis of the pupil improves the interobserver agreement in the calculation of the VCDR. To improve the objectivity of the VCDR assessment, a set of standard photographs of VCDR grades was used.
Among the 53 glaucoma cases identified, 
50% were diagnosed on the basis of abnormal VCDR combined with a reproducible field defect (category 1, 28 cases), 33% of the cases by significant enlargement of the VCDR when visual field testing was not possible (category 2, 17 cases), and 15% on the basis of previous history of glaucoma surgery (usually trabeculectomy) or significantly elevated IOP and severe visual impairment (category 3, 8 cases). Incomplete field testing would bias the results toward an underestimation of the prevalence of glaucoma, because more severe glaucomatous optic nerve damage is needed to satisfy category 2 than category 1. In our study, nearly 70% of the glaucoma cases were confirmed with a reproducible field defect and VCDR damage. Forty-two subjects met the optic nerve criteria for possible glaucoma but did not have reproducible field results. Among them, 20% (9/42 cases) had glaucoma diagnosed based on category 2 or 3 criteria. Approximately 33% of the persons in the 42 cases were very elderly and frequently had significant media opacities limiting our ability to complete visual field testing. Some glaucoma cases may have been missed in this group of patients.
Table 7 compares the age-specific prevalence of all glaucoma in African and European-derived Americans (Baltimore),7 the population of Barbados10 and the data derived from East Asians populations in Japan,9 Singapore,2 Mongolia,1 and the present study in urban Guangzhou. The census data from the year 2000 in Liwan District, Guangzhou, is used as the standard population. The age and sex standardized prevalence in Guangzhou is lower than in all East Asian populations and the African populations, but higher than that in people of European origin. The age-standardized prevalence in men is approximately 1.5 to 2 times higher than in women. This has been a consistent finding in Mongolia, Singapore, and Barbados, and in blacks in Baltimore. A higher prevalence in women was found only in Thailand, Japan, and the white population of Baltimore. Examining the age-specific prevalence rates, an increase with age was observed in almost all studies. The prevalence figures in the 50 to 59 and 60 to 69 years in Guangzhou are similar to what has been found in other East Asian population. However, the prevalence in the seventh decade is lower, and this may in part account for the lower standardized prevalence in Guangzhou.
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In summary, our data suggest that glaucoma is highly prevalent in older urban Chinese and that is a major cause of blindness. Most cases of glaucomatous optic neuropathy were classified as open-angle glaucoma, with rates similar to those seen in European-derived populations. The prevalence of angle-closure glaucoma was greater than that recognized in European people and is typically asymptomatic. These data represent a unique insight into the burden of glaucoma in the world’s most populous nation and, we hope, will promote efforts to prevent glaucoma blindness in the densely populated countries of Asia.
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Footnotes |
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Supported by Grant G0401527 from The Medical Research Council, The Wellcome Trust (075110) and The Richard Desmond Charitable Foundation (via Fight for Sight) (PJF); Medical Research Council Grant G9330070, Moorfields Special Trustees, and the Michael and Isle Katz Foundation (PTK); and Helen Keller International, which provided logistic support and some of equipment used. MH is recipient of a UCL Graduate School Research Scholarship and UCL Overseas Research Scholarship 2001061054.
Submitted for publication January 18, 2006; revised February 16, 2006; accepted April 26, 2006.
Disclosure: M. He, None; P.J. Foster, None; J. Ge, None; W. Huang, None; Y. Zheng, None; D.S. Friedman, None; P.S. Lee, None; P.T. Khaw, None
The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked "advertisement" in accordance with 18 U.S.C. 
1734 solely to indicate this fact.
Corresponding author: Mingguang He, Department of Preventive Ophthalmology, Zhongshan Ophthalmic Center, Guangzhou 510060, People’s Republic of China; mingguang_he{at}yahoo.com.
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