Myopic Maculopathy and Optic Disc Changes in Highly Myopic Young Asian Eyes and Impact on Visual Acuity VICTOR KOH, COLIN TAN, PEI TING TAN, MARCUS TAN, VINAY BALLA, GERARD NAH, CHING-YU CHENG, KYOKO OHNO-MATSUI, MELLISA M.H. TAN, ADELINE YANG, PAUL ZHAO, TIEN YIN WONG, AND SEANG-MEI SAW PURPOSE:
To determine the prevalence and risk factors of myopic maculopathy and specific optic disc and macular changes in highly myopic eyes of young Asian adults and their impact on visual acuity. DESIGN: Prospective cross-sectional study. METHODS: In total, 593 highly myopic (spherical equivalent refraction [SER] less than L6.00 diopters [D]) and 156 emmetropic (SER between L1.00 and D1.00 D) male participants from a populationbased survey were included. All participants underwent standardized medical interviews, ophthalmic examination, and color fundus photographs. These photographs were graded systematically to determine the presence of optic disc and macular lesions. Myopic maculopathy was classified based on the International Classification of Myopic Maculopathy. RESULTS: The mean age was 21.1 ± 1.2 years. The mean SER for the highly myopic and emmetropic group was L8.87 ± 2.11 D and 0.40 ± 0.39 D, respectively (P < .001). Compared to emmetropic eyes, highly myopic eyes were significantly more likely to have optic disc tilt, peripapillary atrophy (PPA), posterior staphyloma, chorioretinal atrophy, and myopic maculopathy (all P < .001). The main findings included PPA (98.3%), disc tilt (22.0%), posterior staphyloma (32.0%), and chorioretinal atrophy (8.3%). Myopic maculopathy was present in 8.3% of highly myopic eyes
Supplemental Material available at AJO.com. Accepted for publication Jan 23, 2016. From the Vision Performance Centre, Military Medicine Institute, Singapore (V.K., M.T., G.N., P.Z.); Department of Ophthalmology, National University Health System, Singapore (V.K., M.T., V.B., C.C.-Y.); Department of Ophthalmology, Tan Tock Seng Hospital, Singapore (C.T.); Biostatistics Unit (P.T.T.) and Department of Ophthalmology (T.Y.W., S.S.-M.), Yong Loo Lin School of Medicine, National University of Singapore, Singapore; Singapore Eye Research Institute, Singapore National Eye Centre, Singapore (C.C.-Y., T.Y.W., S.S.-M.); Department of Ophthalmology and Visual Science, Tokyo Medical and Dental University Graduate School of Medicine, Tokyo, Japan (K.O.-M.); and Defence Medical & Environmental Research Institute, DSO National Laboratories, Singapore (M.M.H.T., A.Y.). Inquiries to Prof Seang-Mei Saw, Department of Epidemiology and Public Health, Yong Loo Lin School of Medicine, National University of Singapore, MD 3, Level 16 Medical Dr, Singapore 117597; e-mail: [email protected] 0002-9394/$36.00 http://dx.doi.org/10.1016/j.ajo.2016.01.005
Ó
2016 BY
and was associated with older age (odds ratio [OR] 1.66; 95% CI: 1.22, 2.26), reduced choroidal thickness (OR 0.99; 95% CI: 0.98, 0.99), and increased axial length (AL) (OR 1.52; 95% CI: 1.06, 2.19). The presence of disc tilt, posterior staphyloma, and chorioretinal atrophy were associated with reduced visual acuity. CONCLUSIONS: Our study showed that myopia-related changes of the optic disc and macula were common in highly myopic eyes even at a young age. The risk factors for myopic maculopathy include increased age, longer AL, and reduced choroidal thickness. Some of these changes were associated with reduced central visual function. (Am J Ophthalmol 2016;164:69–79. Ó 2016 by Elsevier Inc. All rights reserved.)
M
YOPIA IS A MAJOR CAUSE OF VISUAL IMPAIRMENT
in the world1,2 and the prevalence is especially high in East Asia.3 In Asia, the prevalence of myopia (spherical equivalent refraction [SER] less than 0.50 diopters [D]) and high myopia (SER less than 6.00 D) in young adults (age range 18–24 years) are 81.6%–96.5% and 6.8%–21.6%, respectively.4–7 In addition, a study in Singapore comparing similar cohorts of young Asian men (aged 16–25 years) between 1996– 97 and 2009–10 showed that the prevalence of myopia and high myopia remained high in the latter group— 81.6% and 14.7%, respectively.4 This group of young myopic adults could pose a significant public health problem in the future. Complications associated with pathologic myopia can be irreversible and result in significant ocular morbidity. This includes myopic choroidal neovascularization, chorioretinal atrophy, and foveoschisis. These sightthreatening conditions result in reduced quality of life and increased socioeconomic burden, especially if they occur early in life.8 In the Singapore Cohort Study of Risk Factors for Myopia (SCORM) study (age range 12–16 years), the prevalence of optic disc tilt and peripapillary atrophy for children with SER less than 6.00 D (n ¼ 89) was 67.5% and 92.2%, respectively. Interestingly, compared to older myopic adults (aged more than 40 years), the prevalence of these myopic
ELSEVIER INC. ALL
RIGHTS RESERVED.
69
maculopathies was much lower in these highly myopic children (only 1 case each of posterior staphyloma and lacquer cracks).9–12 Electrophysiology studies have also shown that the myopic retinas of adolescents and young adults have diminished amplitudes and delayed latency despite a normal-looking retina.13 This evidence suggested that myopia-related structural changes in the retina could be age- and time-dependent. On the other hand, in population-based studies, among adults older than 40 years with high myopia (SER less than 5.00 D), only a relatively small proportion (0.9%–3.29%) develop structural changes.10,14,15 It is possible that apart from axial length (AL) and SER, there are other contributing risk factors leading to pathologic myopic changes. To date, there is little literature on the visual impact of pathologic myopia and when these myopiarelated changes affect highly myopic young adults. This is important in the assessment of visual potential because visual impairment at this young age group has significant impact on long-term visual prognosis and rehabilitation.14 We aim to describe the prevalence of myopic maculopathy and related structural abnormalities, including specific myopia-related optic disc and macular changes in a group of highly myopic (SER less than 6.00 D) young Asian men and compare them with emmetropic eyes of the same age group. We will also examine the risk factors for these myopia-related changes and their impact on visual acuity.
METHODS STUDY POPULATION:
INTERVIEW, VISUAL ACUITY MEASUREMENT, AND REFRACTION: All the participants who fulfill the inclu-
sion criteria and consented to the study underwent a standardized interview regarding their refraction status, including the age at which they started wearing glasses and the age at which their spherical refractive error first reached 6.00 D. Best-corrected visual acuity (BCVA) measurement and subjective cycloplegic refraction were conducted on the same day by a trained optometrist. The subjects’ monocular VA was measured using the logarithm of the minimal angle of resolution (logMAR) chart (Lighthouse International, New York, New York, USA) at 4 meters. If the largest number could not be identified at 4 meters, the chart was brought closer to the subject, then counting fingers, hand motion, or light perception vision was assessed. Cycloplegia was induced with 3 drops of cyclopentolate 1% 5 minutes apart. At least 30 minutes after the last drop, subjective cycloplegic refraction tests were performed by the same optometrist for all the participants. SER was calculated as the sum of the spherical power and half of the cylindrical power. OCULAR EXAMINATION AND IMAGING:
The current study was conducted between January 1, and December 31, 2012 and the methodology for subject recruitment was detailed elsewhere.16 Briefly, a total of 28 908 young male subjects aged 19–25 years underwent noncycloplegic autorefraction (Huvitz MRK-3100P, Republic of Korea) as part of a compulsory ophthalmic examination for pre-employment screening in Singapore. Out of 2584 persons identified to have high myopia (SER less than 6.00 D) based on noncycloplegic autorefraction, 719 subjects were selected based on refractive error–stratified random sampling strategy. They were invited to participate in the current study and underwent further examination and investigations at the Singapore Eye Research Institute as described below. For the control group, 168 emmetropic male subjects (SER between 1.00 and þ1.00 D) were recruited and underwent the same standardized examination and investigations as the highly myopic group. We further excluded participants with any history of anterior segment ocular diseases, trauma, or systemic condition that affects their visual performance; any form of refractive surgery or
70
ocular surgery that may alter the refractive status of the eye; and those who were unwilling or unable to take part in the study or unable to return for scheduled visits. Written informed consent were taken from the subjects and their parents/guardians (if they were below 21 years of age). The study was conducted in accordance with the tenets of the World Medical Association’s Declaration of Helsinki and had ethics approval from the Singhealth Centralized Institutional Review Board.
Ocular biometry was performed using the IOL Master (Carl Zeiss Meditec AG, Jena, Germany), which included AL measurements. The mean of 3 AL measurements was taken as the final AL. All the subjects underwent a standardized and detailed examination of the anterior segment at the Singapore Eye Research Institute by a trained ophthalmologist. Slit-lamp examination included assessment of cornea and lenticular pathology and anterior chamber depth. Goldmann applanation tonometry was used to measure the intraocular pressure in mm Hg. Retinal photography was performed by a trained ophthalmic technician using the Canon CR-DGI (Canon Inc, Tokyo, Japan) nonmydriatic retinal camera after pupil dilation. Seven retinal photographs were taken to obtain the view of the optic disc (disc-centered and rotated at 30 degrees to the right and 30 degrees to the left), macular view, and right and left upper and lower arcade peripheral views from both eyes. Spectral-domain optical coherence tomography (SD OCT; Spectralis OCT, Heidelberg Engineering, Heidelberg, Germany) of the macula was also performed after pupil dilation. The SD OCT scans were centered over the
AMERICAN JOURNAL OF OPHTHALMOLOGY
APRIL 2016
FIGURE 1. Examples of various myopia-related optic disc and macular changes including optic disc tilt (Top left), peripapillary atrophy (Top center), posterior staphyloma (Top right), chorioretinal atrophy (Bottom left), lacquer cracks (Bottom center; black arrow), and Fuchs spot (Bottom right; black arrow).
FIGURE 2. Examples of fundus photographs based on the International Classification of Myopic Maculopathy: (Top left) tessellated fundus only (category 1), (Top right) diffuse chorioretinal atrophy (category 2), (Bottom left) patchy chorioretinal atrophy (category 3), and (Bottom right) macular atrophy (category 4).
VOL. 164
MYOPIC MACULOPATHY, OPTIC DISC CHANGES IN HIGHLY MYOPIC EYES
71
TABLE 1. Myopia-related Optic Disc and Macular Changes in Myopic and Emmetropic Eyes and Their Relationship With Spherical Equivalent Refraction Optic Disc Tilt All Subjects (n ¼ 749)
N
Emmetropic (0.75D to þ1.00 D) With high myopia (23.50 to 6.13 D)
Peripapillary Atrophy
n (%)
P Value
N
151
2 (1.3)
To determine the prevalence and risk factors of myopic maculopathy and specific optic disc and macular changes in highly myopic eyes of young Asian adults and their impact on visual acuity. DESIGN: Prospective cross-sectional study. METHODS: In total, 593 highly myopic (spherical equivalent refraction [SER] less than L6.00 diopters [D]) and 156 emmetropic (SER between L1.00 and D1.00 D) male participants from a populationbased survey were included. All participants underwent standardized medical interviews, ophthalmic examination, and color fundus photographs. These photographs were graded systematically to determine the presence of optic disc and macular lesions. Myopic maculopathy was classified based on the International Classification of Myopic Maculopathy. RESULTS: The mean age was 21.1 ± 1.2 years. The mean SER for the highly myopic and emmetropic group was L8.87 ± 2.11 D and 0.40 ± 0.39 D, respectively (P < .001). Compared to emmetropic eyes, highly myopic eyes were significantly more likely to have optic disc tilt, peripapillary atrophy (PPA), posterior staphyloma, chorioretinal atrophy, and myopic maculopathy (all P < .001). The main findings included PPA (98.3%), disc tilt (22.0%), posterior staphyloma (32.0%), and chorioretinal atrophy (8.3%). Myopic maculopathy was present in 8.3% of highly myopic eyes
Supplemental Material available at AJO.com. Accepted for publication Jan 23, 2016. From the Vision Performance Centre, Military Medicine Institute, Singapore (V.K., M.T., G.N., P.Z.); Department of Ophthalmology, National University Health System, Singapore (V.K., M.T., V.B., C.C.-Y.); Department of Ophthalmology, Tan Tock Seng Hospital, Singapore (C.T.); Biostatistics Unit (P.T.T.) and Department of Ophthalmology (T.Y.W., S.S.-M.), Yong Loo Lin School of Medicine, National University of Singapore, Singapore; Singapore Eye Research Institute, Singapore National Eye Centre, Singapore (C.C.-Y., T.Y.W., S.S.-M.); Department of Ophthalmology and Visual Science, Tokyo Medical and Dental University Graduate School of Medicine, Tokyo, Japan (K.O.-M.); and Defence Medical & Environmental Research Institute, DSO National Laboratories, Singapore (M.M.H.T., A.Y.). Inquiries to Prof Seang-Mei Saw, Department of Epidemiology and Public Health, Yong Loo Lin School of Medicine, National University of Singapore, MD 3, Level 16 Medical Dr, Singapore 117597; e-mail: [email protected] 0002-9394/$36.00 http://dx.doi.org/10.1016/j.ajo.2016.01.005
Ó
2016 BY
and was associated with older age (odds ratio [OR] 1.66; 95% CI: 1.22, 2.26), reduced choroidal thickness (OR 0.99; 95% CI: 0.98, 0.99), and increased axial length (AL) (OR 1.52; 95% CI: 1.06, 2.19). The presence of disc tilt, posterior staphyloma, and chorioretinal atrophy were associated with reduced visual acuity. CONCLUSIONS: Our study showed that myopia-related changes of the optic disc and macula were common in highly myopic eyes even at a young age. The risk factors for myopic maculopathy include increased age, longer AL, and reduced choroidal thickness. Some of these changes were associated with reduced central visual function. (Am J Ophthalmol 2016;164:69–79. Ó 2016 by Elsevier Inc. All rights reserved.)
M
YOPIA IS A MAJOR CAUSE OF VISUAL IMPAIRMENT
in the world1,2 and the prevalence is especially high in East Asia.3 In Asia, the prevalence of myopia (spherical equivalent refraction [SER] less than 0.50 diopters [D]) and high myopia (SER less than 6.00 D) in young adults (age range 18–24 years) are 81.6%–96.5% and 6.8%–21.6%, respectively.4–7 In addition, a study in Singapore comparing similar cohorts of young Asian men (aged 16–25 years) between 1996– 97 and 2009–10 showed that the prevalence of myopia and high myopia remained high in the latter group— 81.6% and 14.7%, respectively.4 This group of young myopic adults could pose a significant public health problem in the future. Complications associated with pathologic myopia can be irreversible and result in significant ocular morbidity. This includes myopic choroidal neovascularization, chorioretinal atrophy, and foveoschisis. These sightthreatening conditions result in reduced quality of life and increased socioeconomic burden, especially if they occur early in life.8 In the Singapore Cohort Study of Risk Factors for Myopia (SCORM) study (age range 12–16 years), the prevalence of optic disc tilt and peripapillary atrophy for children with SER less than 6.00 D (n ¼ 89) was 67.5% and 92.2%, respectively. Interestingly, compared to older myopic adults (aged more than 40 years), the prevalence of these myopic
ELSEVIER INC. ALL
RIGHTS RESERVED.
69
maculopathies was much lower in these highly myopic children (only 1 case each of posterior staphyloma and lacquer cracks).9–12 Electrophysiology studies have also shown that the myopic retinas of adolescents and young adults have diminished amplitudes and delayed latency despite a normal-looking retina.13 This evidence suggested that myopia-related structural changes in the retina could be age- and time-dependent. On the other hand, in population-based studies, among adults older than 40 years with high myopia (SER less than 5.00 D), only a relatively small proportion (0.9%–3.29%) develop structural changes.10,14,15 It is possible that apart from axial length (AL) and SER, there are other contributing risk factors leading to pathologic myopic changes. To date, there is little literature on the visual impact of pathologic myopia and when these myopiarelated changes affect highly myopic young adults. This is important in the assessment of visual potential because visual impairment at this young age group has significant impact on long-term visual prognosis and rehabilitation.14 We aim to describe the prevalence of myopic maculopathy and related structural abnormalities, including specific myopia-related optic disc and macular changes in a group of highly myopic (SER less than 6.00 D) young Asian men and compare them with emmetropic eyes of the same age group. We will also examine the risk factors for these myopia-related changes and their impact on visual acuity.
METHODS STUDY POPULATION:
INTERVIEW, VISUAL ACUITY MEASUREMENT, AND REFRACTION: All the participants who fulfill the inclu-
sion criteria and consented to the study underwent a standardized interview regarding their refraction status, including the age at which they started wearing glasses and the age at which their spherical refractive error first reached 6.00 D. Best-corrected visual acuity (BCVA) measurement and subjective cycloplegic refraction were conducted on the same day by a trained optometrist. The subjects’ monocular VA was measured using the logarithm of the minimal angle of resolution (logMAR) chart (Lighthouse International, New York, New York, USA) at 4 meters. If the largest number could not be identified at 4 meters, the chart was brought closer to the subject, then counting fingers, hand motion, or light perception vision was assessed. Cycloplegia was induced with 3 drops of cyclopentolate 1% 5 minutes apart. At least 30 minutes after the last drop, subjective cycloplegic refraction tests were performed by the same optometrist for all the participants. SER was calculated as the sum of the spherical power and half of the cylindrical power. OCULAR EXAMINATION AND IMAGING:
The current study was conducted between January 1, and December 31, 2012 and the methodology for subject recruitment was detailed elsewhere.16 Briefly, a total of 28 908 young male subjects aged 19–25 years underwent noncycloplegic autorefraction (Huvitz MRK-3100P, Republic of Korea) as part of a compulsory ophthalmic examination for pre-employment screening in Singapore. Out of 2584 persons identified to have high myopia (SER less than 6.00 D) based on noncycloplegic autorefraction, 719 subjects were selected based on refractive error–stratified random sampling strategy. They were invited to participate in the current study and underwent further examination and investigations at the Singapore Eye Research Institute as described below. For the control group, 168 emmetropic male subjects (SER between 1.00 and þ1.00 D) were recruited and underwent the same standardized examination and investigations as the highly myopic group. We further excluded participants with any history of anterior segment ocular diseases, trauma, or systemic condition that affects their visual performance; any form of refractive surgery or
70
ocular surgery that may alter the refractive status of the eye; and those who were unwilling or unable to take part in the study or unable to return for scheduled visits. Written informed consent were taken from the subjects and their parents/guardians (if they were below 21 years of age). The study was conducted in accordance with the tenets of the World Medical Association’s Declaration of Helsinki and had ethics approval from the Singhealth Centralized Institutional Review Board.
Ocular biometry was performed using the IOL Master (Carl Zeiss Meditec AG, Jena, Germany), which included AL measurements. The mean of 3 AL measurements was taken as the final AL. All the subjects underwent a standardized and detailed examination of the anterior segment at the Singapore Eye Research Institute by a trained ophthalmologist. Slit-lamp examination included assessment of cornea and lenticular pathology and anterior chamber depth. Goldmann applanation tonometry was used to measure the intraocular pressure in mm Hg. Retinal photography was performed by a trained ophthalmic technician using the Canon CR-DGI (Canon Inc, Tokyo, Japan) nonmydriatic retinal camera after pupil dilation. Seven retinal photographs were taken to obtain the view of the optic disc (disc-centered and rotated at 30 degrees to the right and 30 degrees to the left), macular view, and right and left upper and lower arcade peripheral views from both eyes. Spectral-domain optical coherence tomography (SD OCT; Spectralis OCT, Heidelberg Engineering, Heidelberg, Germany) of the macula was also performed after pupil dilation. The SD OCT scans were centered over the
AMERICAN JOURNAL OF OPHTHALMOLOGY
APRIL 2016
FIGURE 1. Examples of various myopia-related optic disc and macular changes including optic disc tilt (Top left), peripapillary atrophy (Top center), posterior staphyloma (Top right), chorioretinal atrophy (Bottom left), lacquer cracks (Bottom center; black arrow), and Fuchs spot (Bottom right; black arrow).
FIGURE 2. Examples of fundus photographs based on the International Classification of Myopic Maculopathy: (Top left) tessellated fundus only (category 1), (Top right) diffuse chorioretinal atrophy (category 2), (Bottom left) patchy chorioretinal atrophy (category 3), and (Bottom right) macular atrophy (category 4).
VOL. 164
MYOPIC MACULOPATHY, OPTIC DISC CHANGES IN HIGHLY MYOPIC EYES
71
TABLE 1. Myopia-related Optic Disc and Macular Changes in Myopic and Emmetropic Eyes and Their Relationship With Spherical Equivalent Refraction Optic Disc Tilt All Subjects (n ¼ 749)
N
Emmetropic (0.75D to þ1.00 D) With high myopia (23.50 to 6.13 D)
Peripapillary Atrophy
n (%)
P Value
N
151
2 (1.3)
