Evaluation of Shared Genetic Susceptibility to High and Low Myopia and Hyperopia

doi:10.1001/jamaophthalmol.2021.0497

. 2021 Jun 1;139(6):601-609.

doi: 10.1001/jamaophthalmol.2021.0497.

Evaluation of Shared Genetic Susceptibility to High and Low Myopia and Hyperopia

J Willem L Tideman^{1

2}, Olavi Pärssinen^{3

4}, Annechien E G Haarman^{1

2}, Anthony P Khawaja⁵, Juho Wedenoja^{6

7}, Katie M Williams^{8

9}, Ginevra Biino¹⁰, Xiaohu Ding¹¹, Mika Kähönen^{12

13}, Terho Lehtimäki^{12

14

15}, Olli T Raitakari^{16

17

18}, Ching-Yu Cheng^{19

20}, Jost B Jonas^{21

22}, Terri L Young²³, Joan E Bailey-Wilson²⁴, Jugnoo Rahi²⁵, Cathy Williams²⁶, Mingguang He^{11

27}, David A Mackey²⁸, Jeremy A Guggenheim²⁹; UK Biobank Eye and Vision Consortium and the Consortium for Refractive Error and Myopia (CREAM Consortium)

Collaborators, Affiliations

Collaborators

UK Biobank Eye and Vision Consortium and the Consortium for Refractive Error and Myopia (CREAM Consortium):
Adriana I Iglesias, Akira Meguro, Akitaka Tsujikawa, Alex W Hewitt, Veluchamy A Barathi, Andres Metspalu, Andrew D Paterson, Annechien E G Haarman, Anthony Musolf, Anthony P Khawaja, Barbara E Klein, Candace Middlebrooks, Caroline Hayward, Cathy Williams, Cécile Delcourt, Chi Pui Pang, Ching-Yu Cheng, Christopher J Hammond, Claire L Simpson, Cornelia M van Duijn, David A Mackey, Deyana Lewis, Dwight Stambolian, Emily Y Chew, E-Shyong Tai, Ginevra Biino, Harry Campbell, Igor Rudan, J Willem L Tideman, Jaakko Kaprio, James F Wilson, Jamie E Craig, Jason C S Yam, Jeremy A Guggenheim, Joan E Bailey-Wilson, Jonathan H Lass, Jost B Jonas, Jugnoo S Rahi, Juho Wedenoja, Kathryn P Burdon, Katie M Williams, Kenji Yamashiro, Konrad Oexle, Kris Lee, Leo-Pekka Lyytikäinen, Li Jia Chen, Margaret M Deangelis, Masahiro Miyake, Maurice K H Yap, Maurizio Fossarello, Mika Kähönen, Milly S Tedja, Mingguang He, Nicholas G Martin, Ningli Wang, Nobuhisa Mizuki, Norbert Pfeiffer, Olavi Pärssinen, Olli Raitakari, Ozren Polasek, Paul J Foster, Paul N Baird, Pirro G Hysi, Puya Gharahkhani, Qiao Fan, Qing Li, Quan Hoang, Robert P Igo Jr, Robert Wojciechowski, Seang-Mei Saw, Seyhan Yazar, Shea Ping Yip, Shi-Ming Li, Srujana Sahebjada, Stefan Nickels, Stuart MacGregor, Sudha K Iyengar, Terho Lehtimäki, Terri L Young, Toomas Haller, Veronique Vitart, Virginie J M Verhoeven, Wen Bin Wei, Xiangtian Zhou, Xiaobo Guo, Xiaohu Ding, Xikun Han, Ya Xing Wang, Naomi Allen, Tariq Aslam, Denize Atan, Sarah Barman, Jenny Barrett, Paul Bishop, Graeme Black, Catey Bunce, Roxana Carare, Usha Chakravarthy, Michelle Chan, Sharon Chua, Valentina Cipriani, Alexander Day, Parul Desai, Bal Dhillon, Andrew Dick, Alexander Doney, Cathy Egan, Sarah Ennis, Paul Foster, Marcus Fruttiger, John Gallacher, David Garway-Heath, Jane Gibson, Dan Gore, Jeremy Guggenheim, Chris Hammond, Alison Hardcastle, Simon Harding, Ruth Hogg, Pirro Hysi, Pearse A Keane, Peng Tee Khaw, Anthony Khawaja, Gerassimos Lascaratos, Thomas Littlejohns, Andrew Lotery, Phil Luthert, Tom Macgillivray, Sarah Mackie, Bernadette Mcguinness, Gareth Mckay, Martin Mckibbin, Danny Mitry, Tony Moore, James Morgan, Zaynah Muthy, Eoin O'sullivan, Chris Owen, Praveen Patel, Euan Paterson, Tunde Peto, Axel Petzold, Nikolas Pontikos, Jugnoo Rahi, Alicja Rudnicka, Jay Self, Panagiotis Sergouniotis, Sobha Sivaprasad, David Steel, Irene Stratton, Nicholas Strouthidis, Cathie Sudlow, Robyn Tapp, Caroline Thaung, Dhanes Thomas, Emanuele Trucco, Adnan Tufail, Stephen Vernon, Ananth Viswanathan, Katie Williams, Jayne Woodside, Max Yates, Jennifer Yip, Yalin Zheng

Affiliations

¹ Department of Ophthalmology, Erasmus Medical Center, Rotterdam, the Netherlands.
² Department of Epidemiology, Erasmus Medical Center, Rotterdam, the Netherlands.
³ Gerontology Research Center and Faculty of Sport and Health Sciences, University of Jyväskylä, Jyväskylä, Finland.
⁴ Department of Ophthalmology, Central Hospital of Central Finland, Jyväskylä, Finland.
⁵ NIHR Biomedical Research Centre, Moorfields Eye Hospital National Health Service (NHS) Foundation Trust and UCL Institute of Ophthalmology, London, United Kingdom.
⁶ Department of Ophthalmology, University of Helsinki and Helsinki University Hospital, Helsinki, Finland.
⁷ Department of Public Health, University of Helsinki, Helsinki, Finland.
⁸ Section of Academic Ophthalmology, Faculty of Life Sciences and Medicine, King's College London School of Life Course Sciences, London, United Kingdom.
⁹ Moorfields Eye Hospital NHS Foundation Trust, London, United Kingdom.
¹⁰ Institute of Molecular Genetics, National Research Council of Italy, Pavia, Italy.
¹¹ State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, China.
¹² Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland.
¹³ Department of Clinical Physiology, Tampere University Hospital, Tampere, Finland.
¹⁴ Department of Clinical Chemistry, Fimlab Laboratories, Tampere, Finland.
¹⁵ Department of Clinical Chemistry, Finnish Cardiovascular Research Center, Tampere, Finland.
¹⁶ Centre for Population Health Research, University of Turku and Turku University Hospital, Finland.
¹⁷ Research Centre of Applied and Preventive Medicine, University of Turku, Turku, Finland.
¹⁸ Department of Clinical Physiology and Nuclear Medicine, Turku University Hospital, Turku, Finland.
¹⁹ Duke-NUS Medical School, Singapore, Singapore.
²⁰ Singapore Eye Research Institute, Singapore National Eye Centre, Singapore, Singapore.
²¹ Department of Ophthalmology, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
²² Beijing Institute of Ophthalmology, Beijing Key Laboratory of Ophthalmology and Visual Sciences, Beijing Tongren Eye Center, Beijing Tongren Hospital, Capital Medical University, Beijing, China.
²³ Department of Ophthalmology and Visual Sciences, University of Wisconsin, Madison.
²⁴ Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Baltimore, Maryland.
²⁵ UCL Great Ormond Street Institute of Child Health and Institute of Ophthalmology, University College London, London, United Kingdom.
²⁶ Centre for Academic Child Health, Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, United Kingdom.
²⁷ Centre for Eye Research Australia; Ophthalmology, Department of Surgery, University of Melbourne, Melbourne, Victoria, Australia.
²⁸ Centre for Ophthalmology and Visual Science, University of Western Australia, Perth, Western Australia, Australia.
²⁹ Cardiff University School of Optometry and Vision Sciences, Cardiff, United Kingdom.

PMID: 33830181
PMCID: PMC8033508
DOI: 10.1001/jamaophthalmol.2021.0497

Free PMC article

Evaluation of Shared Genetic Susceptibility to High and Low Myopia and Hyperopia

J Willem L Tideman et al. JAMA Ophthalmol. 2021.

Free PMC article

. 2021 Jun 1;139(6):601-609.

doi: 10.1001/jamaophthalmol.2021.0497.

Authors

Collaborators

UK Biobank Eye and Vision Consortium and the Consortium for Refractive Error and Myopia (CREAM Consortium):
Adriana I Iglesias, Akira Meguro, Akitaka Tsujikawa, Alex W Hewitt, Veluchamy A Barathi, Andres Metspalu, Andrew D Paterson, Annechien E G Haarman, Anthony Musolf, Anthony P Khawaja, Barbara E Klein, Candace Middlebrooks, Caroline Hayward, Cathy Williams, Cécile Delcourt, Chi Pui Pang, Ching-Yu Cheng, Christopher J Hammond, Claire L Simpson, Cornelia M van Duijn, David A Mackey, Deyana Lewis, Dwight Stambolian, Emily Y Chew, E-Shyong Tai, Ginevra Biino, Harry Campbell, Igor Rudan, J Willem L Tideman, Jaakko Kaprio, James F Wilson, Jamie E Craig, Jason C S Yam, Jeremy A Guggenheim, Joan E Bailey-Wilson, Jonathan H Lass, Jost B Jonas, Jugnoo S Rahi, Juho Wedenoja, Kathryn P Burdon, Katie M Williams, Kenji Yamashiro, Konrad Oexle, Kris Lee, Leo-Pekka Lyytikäinen, Li Jia Chen, Margaret M Deangelis, Masahiro Miyake, Maurice K H Yap, Maurizio Fossarello, Mika Kähönen, Milly S Tedja, Mingguang He, Nicholas G Martin, Ningli Wang, Nobuhisa Mizuki, Norbert Pfeiffer, Olavi Pärssinen, Olli Raitakari, Ozren Polasek, Paul J Foster, Paul N Baird, Pirro G Hysi, Puya Gharahkhani, Qiao Fan, Qing Li, Quan Hoang, Robert P Igo Jr, Robert Wojciechowski, Seang-Mei Saw, Seyhan Yazar, Shea Ping Yip, Shi-Ming Li, Srujana Sahebjada, Stefan Nickels, Stuart MacGregor, Sudha K Iyengar, Terho Lehtimäki, Terri L Young, Toomas Haller, Veronique Vitart, Virginie J M Verhoeven, Wen Bin Wei, Xiangtian Zhou, Xiaobo Guo, Xiaohu Ding, Xikun Han, Ya Xing Wang, Naomi Allen, Tariq Aslam, Denize Atan, Sarah Barman, Jenny Barrett, Paul Bishop, Graeme Black, Catey Bunce, Roxana Carare, Usha Chakravarthy, Michelle Chan, Sharon Chua, Valentina Cipriani, Alexander Day, Parul Desai, Bal Dhillon, Andrew Dick, Alexander Doney, Cathy Egan, Sarah Ennis, Paul Foster, Marcus Fruttiger, John Gallacher, David Garway-Heath, Jane Gibson, Dan Gore, Jeremy Guggenheim, Chris Hammond, Alison Hardcastle, Simon Harding, Ruth Hogg, Pirro Hysi, Pearse A Keane, Peng Tee Khaw, Anthony Khawaja, Gerassimos Lascaratos, Thomas Littlejohns, Andrew Lotery, Phil Luthert, Tom Macgillivray, Sarah Mackie, Bernadette Mcguinness, Gareth Mckay, Martin Mckibbin, Danny Mitry, Tony Moore, James Morgan, Zaynah Muthy, Eoin O'sullivan, Chris Owen, Praveen Patel, Euan Paterson, Tunde Peto, Axel Petzold, Nikolas Pontikos, Jugnoo Rahi, Alicja Rudnicka, Jay Self, Panagiotis Sergouniotis, Sobha Sivaprasad, David Steel, Irene Stratton, Nicholas Strouthidis, Cathie Sudlow, Robyn Tapp, Caroline Thaung, Dhanes Thomas, Emanuele Trucco, Adnan Tufail, Stephen Vernon, Ananth Viswanathan, Katie Williams, Jayne Woodside, Max Yates, Jennifer Yip, Yalin Zheng

Affiliations

¹ Department of Ophthalmology, Erasmus Medical Center, Rotterdam, the Netherlands.
² Department of Epidemiology, Erasmus Medical Center, Rotterdam, the Netherlands.
³ Gerontology Research Center and Faculty of Sport and Health Sciences, University of Jyväskylä, Jyväskylä, Finland.
⁴ Department of Ophthalmology, Central Hospital of Central Finland, Jyväskylä, Finland.
⁵ NIHR Biomedical Research Centre, Moorfields Eye Hospital National Health Service (NHS) Foundation Trust and UCL Institute of Ophthalmology, London, United Kingdom.
⁶ Department of Ophthalmology, University of Helsinki and Helsinki University Hospital, Helsinki, Finland.
⁷ Department of Public Health, University of Helsinki, Helsinki, Finland.
⁸ Section of Academic Ophthalmology, Faculty of Life Sciences and Medicine, King's College London School of Life Course Sciences, London, United Kingdom.
⁹ Moorfields Eye Hospital NHS Foundation Trust, London, United Kingdom.
¹⁰ Institute of Molecular Genetics, National Research Council of Italy, Pavia, Italy.
¹¹ State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, China.
¹² Faculty of Medicine and Health Technology, Tampere University, Tampere, Finland.
¹³ Department of Clinical Physiology, Tampere University Hospital, Tampere, Finland.
¹⁴ Department of Clinical Chemistry, Fimlab Laboratories, Tampere, Finland.
¹⁵ Department of Clinical Chemistry, Finnish Cardiovascular Research Center, Tampere, Finland.
¹⁶ Centre for Population Health Research, University of Turku and Turku University Hospital, Finland.
¹⁷ Research Centre of Applied and Preventive Medicine, University of Turku, Turku, Finland.
¹⁸ Department of Clinical Physiology and Nuclear Medicine, Turku University Hospital, Turku, Finland.
¹⁹ Duke-NUS Medical School, Singapore, Singapore.
²⁰ Singapore Eye Research Institute, Singapore National Eye Centre, Singapore, Singapore.
²¹ Department of Ophthalmology, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
²² Beijing Institute of Ophthalmology, Beijing Key Laboratory of Ophthalmology and Visual Sciences, Beijing Tongren Eye Center, Beijing Tongren Hospital, Capital Medical University, Beijing, China.
²³ Department of Ophthalmology and Visual Sciences, University of Wisconsin, Madison.
²⁴ Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Baltimore, Maryland.
²⁵ UCL Great Ormond Street Institute of Child Health and Institute of Ophthalmology, University College London, London, United Kingdom.
²⁶ Centre for Academic Child Health, Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, United Kingdom.
²⁷ Centre for Eye Research Australia; Ophthalmology, Department of Surgery, University of Melbourne, Melbourne, Victoria, Australia.
²⁸ Centre for Ophthalmology and Visual Science, University of Western Australia, Perth, Western Australia, Australia.
²⁹ Cardiff University School of Optometry and Vision Sciences, Cardiff, United Kingdom.

PMID: 33830181
PMCID: PMC8033508
DOI: 10.1001/jamaophthalmol.2021.0497

Abstract

Importance: Uncertainty currently exists about whether the same genetic variants are associated with susceptibility to low myopia (LM) and high myopia (HM) and to myopia and hyperopia. Addressing this question is fundamental to understanding the genetics of refractive error and has clinical relevance for genotype-based prediction of children at risk for HM and for identification of new therapeutic targets.

Objective: To assess whether a common set of genetic variants are associated with susceptibility to HM, LM, and hyperopia.

Design, setting, and participants: This genetic association study assessed unrelated UK Biobank participants 40 to 69 years of age of European and Asian ancestry. Participants 40 to 69 years of age living in the United Kingdom were recruited from January 1, 2006, to October 31, 2010. Of the total sample of 502 682 participants, 117 279 (23.3%) underwent an ophthalmic assessment. Data analysis was performed from December 12, 2019, to June 23, 2020.

Exposures: Four refractive error groups were defined: HM, -6.00 diopters (D) or less; LM, -3.00 to -1.00 D; hyperopia, +2.00 D or greater; and emmetropia, 0.00 to +1.00 D. Four genome-wide association study (GWAS) analyses were performed in participants of European ancestry: (1) HM vs emmetropia, (2) LM vs emmetropia, (3) hyperopia vs emmetropia, and (4) LM vs hyperopia. Polygenic risk scores were generated from GWAS summary statistics, yielding 4 sets of polygenic risk scores. Performance was assessed in independent replication samples of European and Asian ancestry.

Main outcomes and measures: Odds ratios (ORs) of polygenic risk scores in replication samples.

Results: A total of 51 841 unrelated individuals of European ancestry and 2165 unrelated individuals of Asian ancestry were assigned to a specific refractive error group and included in our analyses. Polygenic risk scores derived from all 4 GWAS analyses were predictive of all categories of refractive error in both European and Asian replication samples. For example, the polygenic risk score derived from the HM vs emmetropia GWAS was predictive in the European sample of HM vs emmetropia (OR, 1.58; 95% CI, 1.41-1.77; P = 1.54 × 10-15) as well as LM vs emmetropia (OR, 1.15; 95% CI, 1.07-1.23; P = 8.14 × 10-5), hyperopia vs emmetropia (OR, 0.83; 95% CI, 0.77-0.89; P = 4.18 × 10-7), and LM vs hyperopia (OR, 1.45; 95% CI, 1.33-1.59; P = 1.43 × 10-16).

Conclusions and relevance: Genetic risk variants were shared across HM, LM, and hyperopia and across European and Asian samples. Individuals with HM inherited a higher number of variants from among the same set of myopia-predisposing alleles and not different risk alleles compared with individuals with LM. These findings suggest that treatment interventions targeting common genetic risk variants associated with refractive error could be effective against both LM and HM.

PubMed Disclaimer

Conflict of interest statement

Conflict of Interest Disclosures: Dr Khawaja reported receiving personal fees from Allergan, Novartis, Santen, Google Health, and Aerie outside the submitted work. Dr Jonas reported having a pending patent for use in the therapeutic or prophylactic treatment of myopia or hyperopia. Dr Young reported receiving grants from Research to Prevent Blindness Inc, University of Wisconsin Centennial Scholars Fund, and Research to Prevent Blindness Inc and consulting fees from Aerpio Pharmaceuticals Consultant outside the submitted work. Dr Guggenheim reported being an unpaid consultant for CooperVision Inc (consultancy fee paid directly by company to a charity selected by the company). No other disclosures were reported.

Figures

**Figure 1.. Refractive Groups of European Ancestry Samples**
Relative frequency distribution of refractive groups (n = 94 914). Genome-wide association studies (GWASs) were as follows: GWAS 1, high myopia (HM) vs emmetropia; GWAS 2, low myopia (LM) vs emmetropia; GWAS 3, hyperopia vs emmetropia; and GWAS 4, LM vs hyperopia.

**Figure 2.. Prediction of Refractive Error Categories Using Polygenic Risk Scores**
Polygenic risk scores derived from specific case-control genome-wide association study (GWAS) analyses in individuals of European ancestry were used to predict all categories of refractive error in European ancestry and Asian ancestry replication samples. Error bars represent 95% CI. HM indicates high myopia; LM, low myopia.

**Figure 3.. Association Between Odds Ratio for Prediction and Difference in Refractive Error Between Groups**
Results are presented for polygenic risk scores (PRSs) selected using a P value threshold of P < 1 × 10⁻⁵ in the clumping and thresholding step. Prediction was assessed in the European ancestry replication samples. Error bars represent 95% CIs. GWAS indicates genome-wide association study; HM, high myopia; LM, low myopia.

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References

1. Chua SYL, Foster PJ. The Economic and Societal Impact of Myopia and High Myopia. In: Ang M, Wong TY, eds. Updates on Myopia: A Clinical Perspective. Springer Singapore; 2020:53-63. doi:10.1007/978-981-13-8491-2_3 - DOI
1. Flitcroft DI. The complex interactions of retinal, optical and environmental factors in myopia aetiology. Prog Retin Eye Res. 2012;31(6):622-660. doi:10.1016/j.preteyeres.2012.06.004 - DOI - PubMed
1. Ip JM, Robaei D, Kifley A, Wang JJ, Rose KA, Mitchell P. Prevalence of hyperopia and associations with eye findings in 6- and 12-year-olds. Ophthalmology. 2008;115(4):678-685.e1. doi:10.1016/j.ophtha.2007.04.061 - DOI - PubMed
1. Morgan IG, French AN, Ashby RS, et al. . The epidemics of myopia: aetiology and prevention. Prog Retin Eye Res. 2018;62:134-149. doi:10.1016/j.preteyeres.2017.09.004 - DOI - PubMed
1. He M, Xiang F, Zeng Y, et al. . Effect of time spent outdoors at school on the development of myopia among children in China: a randomized clinical trial. JAMA. 2015;314(11):1142-1148. doi:10.1001/jama.2015.10803 - DOI - PubMed

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[1] Chua SYL, Foster PJ. The Economic and Societal Impact of Myopia and High Myopia. In: Ang M, Wong TY, eds. Updates on Myopia: A Clinical Perspective. Springer Singapore; 2020:53-63. doi:10.1007/978-981-13-8491-2_3 - DOI

[2] Chua SYL, Foster PJ. The Economic and Societal Impact of Myopia and High Myopia. In: Ang M, Wong TY, eds. Updates on Myopia: A Clinical Perspective. Springer Singapore; 2020:53-63. doi:10.1007/978-981-13-8491-2_3 - DOI

[3] Flitcroft DI. The complex interactions of retinal, optical and environmental factors in myopia aetiology. Prog Retin Eye Res. 2012;31(6):622-660. doi:10.1016/j.preteyeres.2012.06.004 - DOI - PubMed

[4] Flitcroft DI. The complex interactions of retinal, optical and environmental factors in myopia aetiology. Prog Retin Eye Res. 2012;31(6):622-660. doi:10.1016/j.preteyeres.2012.06.004 - DOI - PubMed

[5] Ip JM, Robaei D, Kifley A, Wang JJ, Rose KA, Mitchell P. Prevalence of hyperopia and associations with eye findings in 6- and 12-year-olds. Ophthalmology. 2008;115(4):678-685.e1. doi:10.1016/j.ophtha.2007.04.061 - DOI - PubMed

[6] Ip JM, Robaei D, Kifley A, Wang JJ, Rose KA, Mitchell P. Prevalence of hyperopia and associations with eye findings in 6- and 12-year-olds. Ophthalmology. 2008;115(4):678-685.e1. doi:10.1016/j.ophtha.2007.04.061 - DOI - PubMed

[7] Morgan IG, French AN, Ashby RS, et al. . The epidemics of myopia: aetiology and prevention. Prog Retin Eye Res. 2018;62:134-149. doi:10.1016/j.preteyeres.2017.09.004 - DOI - PubMed

[8] Morgan IG, French AN, Ashby RS, et al. . The epidemics of myopia: aetiology and prevention. Prog Retin Eye Res. 2018;62:134-149. doi:10.1016/j.preteyeres.2017.09.004 - DOI - PubMed

[9] He M, Xiang F, Zeng Y, et al. . Effect of time spent outdoors at school on the development of myopia among children in China: a randomized clinical trial. JAMA. 2015;314(11):1142-1148. doi:10.1001/jama.2015.10803 - DOI - PubMed

[10] He M, Xiang F, Zeng Y, et al. . Effect of time spent outdoors at school on the development of myopia among children in China: a randomized clinical trial. JAMA. 2015;314(11):1142-1148. doi:10.1001/jama.2015.10803 - DOI - PubMed

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Evaluation of Shared Genetic Susceptibility to High and Low Myopia and Hyperopia

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Evaluation of Shared Genetic Susceptibility to High and Low Myopia and Hyperopia

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