Genome-wide association analyses identify distinct genetic architectures for age-related macular degeneration across ancestries

Bryan R Gorman^#^{1

2}, Georgios Voloudakis^#^{3

4}, Robert P Igo Jr^#^{5

6}, Tyler Kinzy^{5

6}, Christopher W Halladay⁷, Tim B Bigdeli^{8

9}, Biao Zeng³, Sanan Venkatesh^{3

4}, Jessica N Cooke Bailey^{5

6

10

11}, Dana C Crawford^{5

6

10

11}, Kyriacos Markianos¹, Frederick Dong^{1

2}, Patrick A Schreiner^{1

2}, Wen Zhang³; VA Million Veteran Program; International AMD Genomics Consortium (IAMDGC); Tamer Hadi^{12

13}, Matthew D Anger^{14

15}, Amy Stockwell¹⁶, Ronald B Melles¹⁷, Jie Yin¹⁸, Hélène Choquet¹⁸, Rebecca Kaye^{19

20}, Karina Patasova^{21

22}, Praveen J Patel^{23

24}, Brian L Yaspan¹⁶, Eric Jorgenson²⁵, Pirro G Hysi^{21

22

26

27}, Andrew J Lotery^{19

20}, J Michael Gaziano^{28

29}, Philip S Tsao^{30

31

32}, Steven J Fliesler^{15

33

34

35}, Jack M Sullivan^{15

33

35}, Paul B Greenberg^{36

37}, Wen-Chih Wu^{38

39}, Themistocles L Assimes^{30

31}, Saiju Pyarajan^{1

40}, Panos Roussos^{41

42}, Neal S Peachey^{43

44

45}, Sudha K Iyengar^{46

47

48

49

50}

Collaborators, Affiliations

Collaborators

Lars G Fritsche, Wilmar Igl, Jessica N Cooke Bailey, Felix Grassman, Sebanti Sengupta, Jennifer L Bragg-Gresham, Kathryn P Burdon, Scott J Hebring, Cindy Wen, Mathias Gorski, Ivana K Kim, David Cho, Donald Zack, Eric Souied, Hendrik P N Scholl, Elisa Bala, Kristine E Lee, David J Hunter, Rebecca J Sardell, Paul Mitchell, Joanna E Merriam, Valentina Cipriani, Joshua D Hoffman, Tina Schick, Yara T E Lechanteur, Robyn H Guymer, Matthew P Johnson, Yingda Jiang, Chloe M Stanton, Gabriëlle H S Buitendijk, Xiaowei Zhan, Alan M Kwong, Alexis Boleda, Matthew Brooks, Linn Gieser, Rinki Ratnapriya, Kari E Branham, Johanna R Foerster, John R Heckenlively, Mohammad I Othman, Brendan J Vote, Helena Hai Liang, Emmanuelle Souzeau, Ian L McAllister, Timothy Isaacs, Janette Hall, Stewart Lake, David A Mackey, Ian J Constable, Jamie E Craig, Terrie Kitchner, Zhenglin Yang, Zhiquang Su, Hongrong Luo, Daniel Chen, Ouyang Ouyang, Ken Flagg, Daniel Lin, Guanping Mao, Henry Ferreyra, Klaus Stark, Claudia Nvon Strachwitz, Armin Wolf, Caroline Brandl, Guenther Rudolph, Matthias Olden, Margaux A Morrison, Deniste J Morgan, Matthew Schu, Jeeyun Ahn, Giuliana Silvestri, Evangelia E Tsironi, Kyu Hyung Park, Lindsay A Farrer, Anton Orlin, Alexander Brucker, Mingyao Li, Christine A Curcio, Saddek Mohand-Saïd, José-Alain Sahel, Isabelle Audo, Mustapha Benchaboune, Angela J Cree, Christina A Rennie, Srinivas V Goverdhan, Michelle Grunin, Shira Hagbi-Levi, Peter Campochiaro, Nicholas Katsanis, Frank G Holz, Frédéric Blond, Hélène Blanché, Jean-François Deleuze, Robert P Igo Jr, Barbara Truitt, Stacy M Meuer, Chelsea E Myers, Emily L Moore, Ronald Klein, Michael A Hauser, Eric A Postel, Monique D Courtenay, Stephen G Schwartz, Jaclyn L Kovach, William K Scott, Gerald Liew, Ava G Tan, Bamini Gopinath, John C Merriam, R Theodore Smith, Jane C Khan, Humma Shahidi, Anthony T Moore, J Allie McGrath, Reneé Laux, Milam A Brantley Jr, Anita Agarwal, Lebriz Ersoy, Albert Caramoy, Thomas Langmann, Nicole T M Saksens, Eiko K deJohn, Carel B Hoyng, Melinda S Cain, Andrea J Richardson, Tammy M Martin, John Blangero, Daniel E Weeks, Bal Dhillon, Cornelia M van Duijn, Kimberly F Doheny, Jane Romm, Caroline C W Klaver, Caroline Hayward, Michael B Gorin, Michael L Klein, Paul N Baird, Anneke I den Hollander, Sascha Fauser, John R W Yates, Rando Allikmets, Jie Jin Wang, Debra A Schaumberg, Barbara E K Klein, Stephanie A Hagstrom, Itay Chowers, Andrew J Lotery, Thierry Léveillard, Kang Zhang, Murray H Brilliant, Alex W Hewitt, Anand Swaroop, Emily Y Chew, Margaret A Pericak-Vance, Margaret DeAngelis, Dwight Stambolian, Jonathan L Haines, Sudha K Iyengar, Bernhard H F Weber, Gonçalo R Abecasis, Iris M Heid

Affiliations

¹ Center for Data and Computational Sciences (C-DACS), VA Cooperative Studies Program, VA Boston Healthcare System, Boston, MA, USA.
² Booz Allen Hamilton, McLean, VA, USA.
³ Center for Disease Neurogenomics, Department of Psychiatry; Friedman Brain Institute; Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
⁴ Center for Precision Medicine and Translational Therapeutics, VISN 2 Mental Illness Research, Education, and Clinical Center (MIRECC), James J. Peters Veterans Affairs Medical Center, New York/New Jersey VA Health Care Network, Bronx, NY, USA.
⁵ Research Service, VA Northeast Ohio Healthcare System, Cleveland, OH, USA.
⁶ Department of Population and Quantitative Health Sciences, Case Western Reserve University, Cleveland, OH, USA.
⁷ Center of Innovation in Long Term Services and Supports, VA Providence Healthcare System, Providence, RI, USA.
⁸ Research Service, VA New York Harbor Healthcare System, Brooklyn, NY, USA.
⁹ Department of Psychiatry and Behavioral Sciences, SUNY Downstate Health Sciences University, Brooklyn, NY, USA.
¹⁰ Cleveland Institute for Computational Biology, Case Western Reserve University, Cleveland, OH, USA.
¹¹ Department of Genetics & Genome Sciences, Case Western Reserve University, Cleveland, OH, USA.
¹² Eye Clinic, VA Northeast Ohio Healthcare System, Cleveland, OH, USA.
¹³ Department of Ophthalmology and Visual Sciences, University Hospitals Eye Institute, Cleveland, OH, USA.
¹⁴ Eye Clinic, VA Western NY Healthcare System, Buffalo, NY, USA.
¹⁵ Ophthalmology, Jacobs School of Medicine and Biomedical Sciences, SUNY-University at Buffalo, Buffalo, NY, USA.
¹⁶ Department of Human Genetics, Genentech, South San Francisco, CA, USA.
¹⁷ Department of Ophthalmology, Kaiser Permanente Northern California, Redwood City, CA, USA.
¹⁸ Division of Research, Kaiser Permanente Northern California, Oakland, CA, USA.
¹⁹ Southampton Eye Unit, University Hospital Southampton National Health Service Foundation Trust, Southampton, UK.
²⁰ Clinical and Experimental Sciences, Faculty of Medicine, University of Southampton, Southampton, UK.
²¹ Section of Ophthalmology, School of Life Course Sciences, King's College London, London, UK.
²² Department of Twin Research and Genetic Epidemiology, King's College London, London, UK.
²³ National Institute for Health and Care Research Biomedical Research Centre, Moorfields Eye Hospital National Health Service Foundation Trust, London, UK.
²⁴ Institute of Ophthalmology, University College London, London, UK.
²⁵ Regeneron Genetics Center, Tarrytown, NY, USA.
²⁶ UCL Great Ormond Street Institute of Child Health, King's College London, London, UK.
²⁷ Sørlandet Sykehus Arendal, Arendal Hospital, Arendal, Norway.
²⁸ Million Veteran Program Coordinating Center, VA Boston Healthcare System, Boston, MA, USA.
²⁹ Division of Aging, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
³⁰ VA Palo Alto Epidemiology Research and Information Center for Genomics, VA Palo Alto Health Care System, Palo Alto, CA, USA.
³¹ Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA.
³² Stanford Cardiovascular Institute, Stanford University School of Medicine, Stanford, CA, USA.
³³ Research Service, VA Western NY Healthcare System, Buffalo, NY, USA.
³⁴ Biochemistry, Jacobs School of Medicine and Biomedical Sciences, SUNY-University at Buffalo, Buffalo, NY, USA.
³⁵ Graduate Program in Neurosciences, Jacobs School of Medicine and Biomedical Sciences, SUNY-University at Buffalo, Buffalo, NY, USA.
³⁶ Section of Ophthalmology, VA Providence Healthcare System, Providence, RI, USA.
³⁷ Division of Ophthalmology, Alpert Medical School, Brown University, Providence, RI, USA.
³⁸ Section of Cardiology, Medical Service, VA Providence Healthcare System, Providence, RI, USA.
³⁹ Division of Cardiology, Department of Medicine, Alpert Medical School, Brown University, Providence, RI, USA.
⁴⁰ Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
⁴¹ Center for Disease Neurogenomics, Department of Psychiatry; Friedman Brain Institute; Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA. panagiotis.roussos@mssm.edu.
⁴² Center for Precision Medicine and Translational Therapeutics, VISN 2 Mental Illness Research, Education, and Clinical Center (MIRECC), James J. Peters Veterans Affairs Medical Center, New York/New Jersey VA Health Care Network, Bronx, NY, USA. panagiotis.roussos@mssm.edu.
⁴³ Research Service, VA Northeast Ohio Healthcare System, Cleveland, OH, USA. neal.peachey@va.gov.
⁴⁴ Cole Eye Institute, Cleveland Clinic, Cleveland, OH, USA. neal.peachey@va.gov.
⁴⁵ Department of Ophthalmology, Cleveland Clinic Lerner College of Medicine of Case Western Reserve University, Cleveland, OH, USA. neal.peachey@va.gov.
⁴⁶ Research Service, VA Northeast Ohio Healthcare System, Cleveland, OH, USA. ski@case.edu.
⁴⁷ Department of Population and Quantitative Health Sciences, Case Western Reserve University, Cleveland, OH, USA. ski@case.edu.
⁴⁸ Cleveland Institute for Computational Biology, Case Western Reserve University, Cleveland, OH, USA. ski@case.edu.
⁴⁹ Department of Genetics & Genome Sciences, Case Western Reserve University, Cleveland, OH, USA. ski@case.edu.
⁵⁰ Department of Ophthalmology and Visual Sciences, University Hospitals Eye Institute, Cleveland, OH, USA. ski@case.edu.

^# Contributed equally.

PMID: 39623103
DOI: 10.1038/s41588-024-01764-0

Genome-wide association analyses identify distinct genetic architectures for age-related macular degeneration across ancestries

Bryan R Gorman et al. Nat Genet. 2024 Dec.

. 2024 Dec;56(12):2659-2671.

doi: 10.1038/s41588-024-01764-0. Epub 2024 Dec 2.

Authors

Collaborators

Lars G Fritsche, Wilmar Igl, Jessica N Cooke Bailey, Felix Grassman, Sebanti Sengupta, Jennifer L Bragg-Gresham, Kathryn P Burdon, Scott J Hebring, Cindy Wen, Mathias Gorski, Ivana K Kim, David Cho, Donald Zack, Eric Souied, Hendrik P N Scholl, Elisa Bala, Kristine E Lee, David J Hunter, Rebecca J Sardell, Paul Mitchell, Joanna E Merriam, Valentina Cipriani, Joshua D Hoffman, Tina Schick, Yara T E Lechanteur, Robyn H Guymer, Matthew P Johnson, Yingda Jiang, Chloe M Stanton, Gabriëlle H S Buitendijk, Xiaowei Zhan, Alan M Kwong, Alexis Boleda, Matthew Brooks, Linn Gieser, Rinki Ratnapriya, Kari E Branham, Johanna R Foerster, John R Heckenlively, Mohammad I Othman, Brendan J Vote, Helena Hai Liang, Emmanuelle Souzeau, Ian L McAllister, Timothy Isaacs, Janette Hall, Stewart Lake, David A Mackey, Ian J Constable, Jamie E Craig, Terrie Kitchner, Zhenglin Yang, Zhiquang Su, Hongrong Luo, Daniel Chen, Ouyang Ouyang, Ken Flagg, Daniel Lin, Guanping Mao, Henry Ferreyra, Klaus Stark, Claudia Nvon Strachwitz, Armin Wolf, Caroline Brandl, Guenther Rudolph, Matthias Olden, Margaux A Morrison, Deniste J Morgan, Matthew Schu, Jeeyun Ahn, Giuliana Silvestri, Evangelia E Tsironi, Kyu Hyung Park, Lindsay A Farrer, Anton Orlin, Alexander Brucker, Mingyao Li, Christine A Curcio, Saddek Mohand-Saïd, José-Alain Sahel, Isabelle Audo, Mustapha Benchaboune, Angela J Cree, Christina A Rennie, Srinivas V Goverdhan, Michelle Grunin, Shira Hagbi-Levi, Peter Campochiaro, Nicholas Katsanis, Frank G Holz, Frédéric Blond, Hélène Blanché, Jean-François Deleuze, Robert P Igo Jr, Barbara Truitt, Stacy M Meuer, Chelsea E Myers, Emily L Moore, Ronald Klein, Michael A Hauser, Eric A Postel, Monique D Courtenay, Stephen G Schwartz, Jaclyn L Kovach, William K Scott, Gerald Liew, Ava G Tan, Bamini Gopinath, John C Merriam, R Theodore Smith, Jane C Khan, Humma Shahidi, Anthony T Moore, J Allie McGrath, Reneé Laux, Milam A Brantley Jr, Anita Agarwal, Lebriz Ersoy, Albert Caramoy, Thomas Langmann, Nicole T M Saksens, Eiko K deJohn, Carel B Hoyng, Melinda S Cain, Andrea J Richardson, Tammy M Martin, John Blangero, Daniel E Weeks, Bal Dhillon, Cornelia M van Duijn, Kimberly F Doheny, Jane Romm, Caroline C W Klaver, Caroline Hayward, Michael B Gorin, Michael L Klein, Paul N Baird, Anneke I den Hollander, Sascha Fauser, John R W Yates, Rando Allikmets, Jie Jin Wang, Debra A Schaumberg, Barbara E K Klein, Stephanie A Hagstrom, Itay Chowers, Andrew J Lotery, Thierry Léveillard, Kang Zhang, Murray H Brilliant, Alex W Hewitt, Anand Swaroop, Emily Y Chew, Margaret A Pericak-Vance, Margaret DeAngelis, Dwight Stambolian, Jonathan L Haines, Sudha K Iyengar, Bernhard H F Weber, Gonçalo R Abecasis, Iris M Heid

Affiliations

¹ Center for Data and Computational Sciences (C-DACS), VA Cooperative Studies Program, VA Boston Healthcare System, Boston, MA, USA.
² Booz Allen Hamilton, McLean, VA, USA.
³ Center for Disease Neurogenomics, Department of Psychiatry; Friedman Brain Institute; Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
⁴ Center for Precision Medicine and Translational Therapeutics, VISN 2 Mental Illness Research, Education, and Clinical Center (MIRECC), James J. Peters Veterans Affairs Medical Center, New York/New Jersey VA Health Care Network, Bronx, NY, USA.
⁵ Research Service, VA Northeast Ohio Healthcare System, Cleveland, OH, USA.
⁶ Department of Population and Quantitative Health Sciences, Case Western Reserve University, Cleveland, OH, USA.
⁷ Center of Innovation in Long Term Services and Supports, VA Providence Healthcare System, Providence, RI, USA.
⁸ Research Service, VA New York Harbor Healthcare System, Brooklyn, NY, USA.
⁹ Department of Psychiatry and Behavioral Sciences, SUNY Downstate Health Sciences University, Brooklyn, NY, USA.
¹⁰ Cleveland Institute for Computational Biology, Case Western Reserve University, Cleveland, OH, USA.
¹¹ Department of Genetics & Genome Sciences, Case Western Reserve University, Cleveland, OH, USA.
¹² Eye Clinic, VA Northeast Ohio Healthcare System, Cleveland, OH, USA.
¹³ Department of Ophthalmology and Visual Sciences, University Hospitals Eye Institute, Cleveland, OH, USA.
¹⁴ Eye Clinic, VA Western NY Healthcare System, Buffalo, NY, USA.
¹⁵ Ophthalmology, Jacobs School of Medicine and Biomedical Sciences, SUNY-University at Buffalo, Buffalo, NY, USA.
¹⁶ Department of Human Genetics, Genentech, South San Francisco, CA, USA.
¹⁷ Department of Ophthalmology, Kaiser Permanente Northern California, Redwood City, CA, USA.
¹⁸ Division of Research, Kaiser Permanente Northern California, Oakland, CA, USA.
¹⁹ Southampton Eye Unit, University Hospital Southampton National Health Service Foundation Trust, Southampton, UK.
²⁰ Clinical and Experimental Sciences, Faculty of Medicine, University of Southampton, Southampton, UK.
²¹ Section of Ophthalmology, School of Life Course Sciences, King's College London, London, UK.
²² Department of Twin Research and Genetic Epidemiology, King's College London, London, UK.
²³ National Institute for Health and Care Research Biomedical Research Centre, Moorfields Eye Hospital National Health Service Foundation Trust, London, UK.
²⁴ Institute of Ophthalmology, University College London, London, UK.
²⁵ Regeneron Genetics Center, Tarrytown, NY, USA.
²⁶ UCL Great Ormond Street Institute of Child Health, King's College London, London, UK.
²⁷ Sørlandet Sykehus Arendal, Arendal Hospital, Arendal, Norway.
²⁸ Million Veteran Program Coordinating Center, VA Boston Healthcare System, Boston, MA, USA.
²⁹ Division of Aging, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
³⁰ VA Palo Alto Epidemiology Research and Information Center for Genomics, VA Palo Alto Health Care System, Palo Alto, CA, USA.
³¹ Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA.
³² Stanford Cardiovascular Institute, Stanford University School of Medicine, Stanford, CA, USA.
³³ Research Service, VA Western NY Healthcare System, Buffalo, NY, USA.
³⁴ Biochemistry, Jacobs School of Medicine and Biomedical Sciences, SUNY-University at Buffalo, Buffalo, NY, USA.
³⁵ Graduate Program in Neurosciences, Jacobs School of Medicine and Biomedical Sciences, SUNY-University at Buffalo, Buffalo, NY, USA.
³⁶ Section of Ophthalmology, VA Providence Healthcare System, Providence, RI, USA.
³⁷ Division of Ophthalmology, Alpert Medical School, Brown University, Providence, RI, USA.
³⁸ Section of Cardiology, Medical Service, VA Providence Healthcare System, Providence, RI, USA.
³⁹ Division of Cardiology, Department of Medicine, Alpert Medical School, Brown University, Providence, RI, USA.
⁴⁰ Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
⁴¹ Center for Disease Neurogenomics, Department of Psychiatry; Friedman Brain Institute; Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA. panagiotis.roussos@mssm.edu.
⁴² Center for Precision Medicine and Translational Therapeutics, VISN 2 Mental Illness Research, Education, and Clinical Center (MIRECC), James J. Peters Veterans Affairs Medical Center, New York/New Jersey VA Health Care Network, Bronx, NY, USA. panagiotis.roussos@mssm.edu.
⁴³ Research Service, VA Northeast Ohio Healthcare System, Cleveland, OH, USA. neal.peachey@va.gov.
⁴⁴ Cole Eye Institute, Cleveland Clinic, Cleveland, OH, USA. neal.peachey@va.gov.
⁴⁵ Department of Ophthalmology, Cleveland Clinic Lerner College of Medicine of Case Western Reserve University, Cleveland, OH, USA. neal.peachey@va.gov.
⁴⁶ Research Service, VA Northeast Ohio Healthcare System, Cleveland, OH, USA. ski@case.edu.
⁴⁷ Department of Population and Quantitative Health Sciences, Case Western Reserve University, Cleveland, OH, USA. ski@case.edu.
⁴⁸ Cleveland Institute for Computational Biology, Case Western Reserve University, Cleveland, OH, USA. ski@case.edu.
⁴⁹ Department of Genetics & Genome Sciences, Case Western Reserve University, Cleveland, OH, USA. ski@case.edu.
⁵⁰ Department of Ophthalmology and Visual Sciences, University Hospitals Eye Institute, Cleveland, OH, USA. ski@case.edu.

^# Contributed equally.

PMID: 39623103
DOI: 10.1038/s41588-024-01764-0

Abstract

To effectively reduce vision loss due to age-related macular generation (AMD) on a global scale, knowledge of its genetic architecture in diverse populations is necessary. A critical element, AMD risk profiles in African and Hispanic/Latino ancestries, remains largely unknown. We combined data in the Million Veteran Program with five other cohorts to conduct the first multi-ancestry genome-wide association study of AMD and discovered 63 loci (30 novel). We observe marked cross-ancestry heterogeneity at major risk loci, especially in African-ancestry populations which demonstrate a primary signal in a major histocompatibility complex class II haplotype and reduced risk at the established CFH and ARMS2/HTRA1 loci. Dissecting local ancestry in admixed individuals, we find significantly smaller marginal effect sizes for CFH risk alleles in African ancestry haplotypes. Broadening efforts to include ancestrally distinct populations helped uncover genes and pathways that boost risk in an ancestry-dependent manner and are potential targets for corrective therapies.

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Conflict of interest statement

Competing interests: A.S. and B.L.Y. are employees of Genentech/Roche and hold stock and stock options in Roche. E.J. is an employee and a stockholder of Regeneron Genetics Center. The other authors declare no competing interests.

References

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1. Vanderbeek, B. L. et al. Racial differences in age-related macular degeneration rates in the United States: a longitudinal analysis of a managed care network. Am. J. Ophthalmol. 152, 273–282.e3 (2011). - PubMed - PMC - DOI
1. Mahr, M. A., Hodge, D. O. & Erie, J. C. Racial differences in age-related macular degeneration and associated anti-vascular endothelial growth factor intravitreal injections among Medicare beneficiaries. Ophthalmol. Retina 2, 1188–1195 (2018). - PubMed - DOI
1. Wang, D., Jiang, Y., He, M., Scheetz, J. & Wang, W. Disparities in the global burden of age-related macular degeneration: An analysis of trends from 1990 to 2015. Curr. Eye Res. 44, 657–663 (2019). - PubMed - DOI
1. Haines, J. L. et al. Complement factor H variant increases the risk of age-related macular degeneration. Science 308, 419–421 (2005). - PubMed - DOI

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Genome-wide association analyses identify distinct genetic architectures for age-related macular degeneration across ancestries

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Affiliations

Genome-wide association analyses identify distinct genetic architectures for age-related macular degeneration across ancestries

Authors

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Abstract

Conflict of interest statement

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