
==== Front
Transl Vis Sci Technol
Transl Vis Sci Technol
TVST
Translational Vision Science & Technology
2164-2591
The Association for Research in Vision and Ophthalmology

39226063
10.1167/tvst.13.9.4
TVST-23-6002
Public Health
Public Health
Seeing in Color: Inclusion and Characterization of Hereditary Eye Disease in African Americans
Hereditary Eye Disease in African Americans
Owete Agnes C. 1 3
Ionin Raisa 2
Huryn Laryssa A. 1
Cukras Catherine A. 1
Blain Delphine 1
Agather Aime R. 1
Hufnagel Robert B. 1
Brooks Brian P. 1
Nwanyanwu Kristen 4
Zein Wadih M. 1
1 Ophthalmic Genetics and Visual Function Branch, National Eye Institute, National Institute of Health, Bethesda, MD, USA
2 National Institutes of Health Library, National Institutes of Health, Bethesda, MD, USA
3 Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
4 Department of Ophthalmology and Visual Science, Yale School of Medicine, New Haven, CT, USA
* Correspondence: Wadih M. Zein, Ophthalmic Genetics and Visual Function Branch, National Eye Institute, National Institutes of Health, 10 Center Drive, NIHBC 10 - Clinical Center BG RM 1L13D, Bethesda, MD 20892, USA. e-mail: zeinw@nei.nih.gov
03 9 2024
9 2024
13 9 415 10 2023
30 6 2023
Copyright 2024 The Authors
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Purpose

Hereditary eye diseases (HEDs) are individually rare but affect millions globally. The era of molecular genetics has ushered major advances in the study of these disorders; however, the inclusivity and population diversity of this research is unknown. Questions on the accuracy and applicability of these findings in diverse populations, especially African American patients, came up consistently during counselling sessions. This also raised the possibility of missed opportunities for broader understanding of these rare diseases. We conducted a literature review to measure the representation of African Americans in genomic research surrounding nine HEDs.

Methods

A detailed literature search using a predetermined set of search terms for each of nine HED categories was performed across PubMed, Embase, Web of Science, and Scopus focusing on studies published between Jan 1990 and July 2021. Predetermined inclusion criteria were applied to filter the sources.

Results

We identified 46 studies clearly reporting HED characterization in African Americans. Analysis of these inclusive studies revealed unique findings demonstrating the known usefulness of including diverse cohorts in genomics research.

Conclusions

HED characterization in diverse participants, specifically African Americans, is identified as a knowledge gap area. Genomic research is more applicable to patients when conducted in populations that share their ancestral background. Greater inclusion of African Americans in ophthalmic genetics research is a scientific imperative and a needed step in the pursuit of the best possible patient care for populations of all ancestries.

Translational Relevance

This work reveals gaps in genomic research in African Americans with HEDs.

hereditary eye diseases
african americans
inclusion
diversity
==== Body
pmcIntroduction

African Americans make up approximately 12% of the American population.1 However, genomic research in patients of African ancestry lags behind that in other populations of European or Asian descent. The 2018 NHGRI-EBI GWAS catalog only included 2.4% of individuals of African ancestry.2 Although race is a social construct and not a biological category, it can be a proxy for identifying shared ancestral backgrounds of individuals. It is well-understood that patients benefit most from genomic research conducted in populations that share their ancestral background.3 We performed a thorough search of the literature looking to identify work specifically reporting on the genotype, phenotype, and management of hereditary eye disease (HED) in the African American population. We specifically researched the following nine HEDs owing to their high prevalence and incidence: retinitis pigmentosa, Stargardt disease, corneal dystrophy, optic atrophy, congenital glaucoma, congenital cataracts, aniridia, oculocutaneous albinism, and retinoblastoma. We also selected these diseases to reflect the breadth of HEDs investigated by the field of ophthalmic genetics, with diseases affecting various ocular structures in different segments of the eye.

Of note, we defined African Americans as individuals who are a part of the diaspora of Black groups from Africa in the United States. As such, any publications studying populations of African origin residing in Africa or outside the United States were excluded.

Methods

A two-pronged approach was used with an initial search of the PubMed database of the National Library of Medicine followed by a review of the Embase, Web of Science, and Scopus databases to be as comprehensive as possible. Using the advanced search feature, we searched for mention of keywords (Table 1) related to the specific ocular dystrophies investigated in our study. These included names of syndromes, abbreviations, and known associated genes. With each of these keywords, we searched for the mention of “African-American” and “African American” in the title or abstract field to narrow our search to papers that specifically focused on our target research demographic. “African” was later used as a secondary check for literature focused on those of African ancestry in the United States. Use of the term “Black” to target our population of interest was found to be an ineffective search criterion as it was not specific to the racial or ethnic categorization and was often used as a qualitative descriptor of images or figures.

Table 1. Search Criteria Used for PubMed Search to Identify Relevant Works

Disease	Search Terms for Disease Names	Search Terms Mutation/Molecular Reference	
Retinitis pigmentosa	Retinitis Pigmentosa	RP	
Stargardt disease	Stargardt's	ABCA4	
	Stargardt		
	STGD		
	Stargardt's Disease		
Oculocutaneous albinism	Albinism	TYR, TYRP1, MATP	
	Oculocutaneous Albinism		
	OCA		
Corneal dystrophy	Corneal Dystrophy		
Congenital glaucoma	Congenital Glaucoma		
Optic atrophy	Optic Atrophy	OPA1	
Congenital cataracts	Congenital Cataracts		
	Congenital Cataract		
Aniridia	Aniridia	PAX6	
Retinoblastoma	Retinoblastoma	RB1	

All gathered sources were filtered through previously determined exclusion criteria listed here. Single patient or single family reports were excluded unless insight into the genetic basis of the associated disease was clear from the title or abstract. Sources were excluded if they were not specific to the diseases of interest or if they did not report findings specific to our target population in their results, discussion, figures, or tables. We also excluded studies from before 1990 to focus on the era of molecular medicine. Our review was finalized on July 1, 2021, so publications after this date were not included. Finally, we excluded all journal articles and relevant abstracts not published in peer-reviewed sources.

Results

We found 14 oculocutaneous albinism,4–18 9 retinitis pigmentosa,19–27 8 corneal dystrophy,28–35 6 optic atrophy,36–40 4 retinoblastoma,41–44 3 Stargardt disease,45–47 and 2 congenital glaucoma48,49 studies with specific characterization of disease in African American patients (Fig. 1). For two of our HEDs, congenital cataracts and aniridia, there were no studies found that characterized disease in African American patients based on our search criteria.

Figure 1. (A) Total number of 1990–2021 PubMed publications mentioning target disease in title/abstract as of July 27, 2021. (B) Number of HED studies with African American population-specific characterization of disease. (C) Comparison of the total number of HED studies published on PubMed with mention of target disease in title/abstract published vs. studies characterizing HED in African American patients between 1990 and July 2021. CC, congenital cataract; OCA, oculocutaneous albinism; PCG, primary congenital glaucoma.

Further analysis of studies that were inclusive of African American patients demonstrated the known usefulness of diverse genomics research by reporting novel disease-associated variants, challenging classifications of benign and pathogenic variants, proposing previously unreported genotype–phenotype correlations, and expanding documented manifestations of these diseases in more diverse populations (Fig. 2). Table 2 further highlights some of these findings.

Figure 2. Unique molecular findings from studies inclusive of disease characterization in African American patients that inform understanding and diagnosis of disease. OCA, oculocutaneous albinism; PCG, primary congenital glaucoma.

Table 2. Sample of a Few Notable Findings from HED Studies With African American Cohorts

HED	Type of Finding	Description	Citation	
RP	Phenotypic difference	African American patients with RP found to have twice the odds of having atrophic-appearing macular lesions	Fishman, 199424	
Congenital glaucoma	Phenotypic difference	Statistically significant higher C/D ratio seen in African American cohort	Kooner, 201448	
Oculocutaneous albinism	Molecular marker difference	A 2.7-kb deletion of the P gene found in unrelated African Americans with OCA2 but not in African American controls or Caucasians with OCA2	Durham-Pierre, 19944; Stevens, 19946; Lee, 19955	
Stargardt disease	Reclassification of variant/molecular marker difference	ABCA4 variants c.3602T>G and c.3899G>A believed to be nonpathogenic based on high prevalence in nondiseased African Americans 	Utz, 201345	
Corneal dystrophy	Difference in treatment	Keratoplasty 1.9 times more likely in Caucasian patients than African Americans	Mahr, 201633	
RP, retinitis pigmentosa.

Discussion and Future Directions

Patients benefit most from genetic research conducted in populations that share their ancestral background.3 Yet, few studies document the presentations and characterization of HEDs in African American patients. We show that studies investigating diverse populations report unique and interesting findings (Table 2). Of note, we see results with diagnostic implications including the identification of potentially pathogenic molecular markers,4,6–8,20,26,32,34,35,45 reclassification of proposed pathogenic markers as benign,20,48 and greater phenotypic variation to be added to illness scripts of disease.20,24 With regard to treatment, identification of disease-causing genetic variants has therapeutic implications as genome modifying tools are being developed to treat these conditions. Additionally, we see that race is correlated with differential treatments and outcomes of treatment being offered to patients highlighting a health disparity that can be addressed by clinicians.33,42

These findings should not be interpreted to mean that these HEDs present in unique and different ways in African American patients, because we know that race alone is not a corollary of genetic divergence. However, by including patients of different races and ethnicities, we increase the pool of genomic data. This finding emphasizes the need for genomics research to be conducted in intentionally heterogeneous populations. By diversifying the ancestries of the populations included in our ophthalmic genetics studies, we allow for increased accuracy, novel discoveries, and better diagnostic and prognostic tools, and pave the path for more equitable generalizability of findings and access to treatments. Although race is not a biological category, diversity in ancestry provides a richer scientific sample from which conclusions of greater power and accuracy can be drawn and treatments with wider usefulness can be developed.

Some limitations of this work include the possibility that some studies were missed in our search owing to methodological limitations including term selection and exclusion criteria. It is also possible that additional work conducted by contributors in the field did not include information on the demographic criterion central to this study in the title or abstract, namely, African American race. Despite these possible limitations, this work demonstrates a lack of inclusion of African American patients when sampling a large body of ophthalmic genetics literature.

With this knowledge gap identified, we are left with the question of what can be done and turn our attention to future directions. Much work has already been done to bring needed attention to disparities in vision health and informing strategies for steps forward.50–52 Other recent efforts have focused on providing guidance on the use and reporting of race and ethnicity in health research and medical journals.53,54 Practical steps to increase inclusion and diversity specifically in genetics research have been identified by researchers outside of the field of ophthalmology, including Bentley et al. in 2017.3 We adapted some of these steps in Table 3 to be specifically pertinent to the field of ophthalmic genetics. These recommendations provide a path forward for individual researchers and the field of ophthalmic genetics as a whole as we continue to build a more equitable research future.

Table 3. Challenges and Recommendations for Increasing Diversity in Research, Derived From Bentley, 20173

Challenge	Recommendation	
Lags in diversity within body of eye researchers	Encourage and foster greater diversity in the body of career Ophthalmic Genetics researchers (e.g., DIVRO internship at NEI)	
Preference for well-characterized and	Incentivize research with diverse ophthalmic cohorts	
powered, predominantly European ancestry ocular disease cohorts	Encourage inclusion of diverse populations for funding and publication of ophthalmic genetics studies	
Limited engagement of diverse ophthalmic patients	Involve study participants in the process of developing and structuring research methods for ophthalmic studies	
	Foster greater understanding of ophthalmic patient perspectives and patient definitions of engagement	
Publication and funding difficulties of ocular studies with small size diverse cohorts	Attribute greater value to the usefulness and advanced knowledge found in the research conducted in diverse populations, using trusted bodies of vision research	
Analytical challenges of diversity	Develop new strategies to capture and manage expanded genomic diversity in analyses	
DIVRO, Diversity in Vision Research and Ophthalmology; NEI, National Eye Institute.

Conclusions

Genomic research conducted in populations of shared ancestral background is more likely to be applicable to patients in that population.3 HED characterization in diverse participants, specifically African Americans, is identified as a knowledge gap area; addressing this gap will lead to a better understanding of HEDs in broader populations. Greater inclusion of African Americans in ophthalmic genetics research is a scientific imperative and is a needed step in the pursuit of the best possible patient care.

Acknowledgments

The authors are grateful to the DIVRO Program for their support of this research. This work was supported by the Intramural Research Program of the National Eye Institute, part of the National Institutes of Health (NIH).

Funding provided by the NEI Intramural Research Fund and Diversity In Vision Research and Ophthalmology (DIVRO) Program, NIH.

Disclosure: A.C. Owete, None; R. Ionin, None; L.A. Huryn, None; C.A. Cukras, None; D. Blain, None; A.R. Agather, None; R.B. Hufnagel, None; B.P. Brooks, None; K. Nwanyanwu, None; W.M. Zein, None
==== Refs
References

1. Office of Minority Heath. Profile: Black/African Americans. Washington, DC: US Department of Health and Human Services Office of Minority Heath; 2023.
2. Morales J, Welter D, Bowler EH, et al . A standardized framework for representation of ancestry data in genomics studies, with application to the NHGRI-EBI GWAS Catalog. Genome Biol . 2018; 19 : 21. Published 2018 Feb 15, doi:10.1186/s13059-018-1396-2.29448949
3. Bentley AR, Callier S, Rotimi CN. Diversity and inclusion in genomic research: why the uneven progress? J Community Genet. 2017; 8 : 255–266, doi:10.1007/s12687-017-0316-6.28770442
4. Durham-Pierre D, Gardner JM, Nakatsu Y, et al . African origin of an intragenic deletion of the human P gene in tyrosinase positive oculocutaneous albinism. Nat Genet. 1994; 7 : 176–179, doi:10.1038/ng0694-176.7920637
5. Lee ST, Nicholls RD, Schnur RE, et al . Diverse mutations of the P gene among African-Americans with type II (tyrosinase-positive) oculocutaneous albinism (OCA2). Hum Mol Genet. 1994; 3 : 2047–2051.7874125
6. Stevens G, van Beukering J, Jenkins T, Ramsay M. An intragenic deletion of the P gene is the common mutation causing tyrosinase-positive oculocutaneous albinism in southern African Negroids. Am J Hum Genet. 1995; 56 : 586–591.7887411
7. Morrone K, Wang Y, Huizing M, et al . Two novel mutations identified in an African American child with Chediak-Higashi syndrome. Case Rep Med. 2010; 2010 : 967535, doi:10.1155/2010/967535.20368792
8. Merideth MA, Vincent LM, Sparks SE, et al . Hermansky-Pudlak syndrome in two African-American brothers. Am J Med Genet A. 2009; 149A : 987–992, doi:10.1002/ajmg.a.32757.19334085
9. Boissy RE, Zhao H, Oetting WS, et al . Mutation in and lack of expression of tyrosinase-related protein-1 (TRP-1) in melanocytes from an individual with brown oculocutaneous albinism: a new subtype of albinism classified as “OCA3”. Am J Hum Genet. 1996; 58 : 1145–1156.8651291
10. Kheterpal S, Shields JA, Shields CL, De Potter P, Ehya H, Eng KY. Choroidal melanoma in an African-American albino. Am J Ophthalmol. 1996; 122 : 901–903, doi:10.1016/s0002-9394(14)70396-4.8956654
11. Tsai AL, Agustines D. The coexistence of oculocutaneous albinism with schizophrenia. Cureus. 2020; 12 : e6617. Published 2020 Jan 9, doi:10.7759/cureus.6617.32064197
12. Endo LM, Rowe SM, Romp RL, Buckmaster MA, Atkinson TP. Pulmonary aneurysms and intracardiac thrombi due to Behçet's disease in an African-American adolescent with oculocutaneous albinism. Clin Rheumatol. 2007; 26 : 1537–1539, doi:10.1007/s10067-006-0426-8.17047893
13. Spritz RA, Fukai K, Holmes SA, Luande J. Frequent intragenic deletion of the P gene in Tanzanian patients with type II oculocutaneous albinism (OCA2). Am J Hum Genet. 1995; 56 : 1320–1323.7762554
14. Gurney JG, Ross JA, Wall DA, Bleyer WA, Severson RK, Robison LL. Infant cancer in the U.S.: histology-specific incidence and trends, 1973 to 1992. J Pediatr Hematol Oncol. 1997; 19 : 428–432, doi:10.1097/00043426-199709000-00004.9329464
15. Fridman C, Hosomi N, Varela MC, Souza AH, Fukai K, Koiffmann CP. Angelman syndrome associated with oculocutaneous albinism due to an intragenic deletion of the P gene. Am J Med Genet A. 2003; 119A : 180–183, doi:10.1002/ajmg.a.20105.12749060
16. Gold M. The effects of the physical features associated with albinism on the self-esteem of African American youths. Journal of Visual Impairment & Blindness . 2002; 96 : 133–142.
17. Graf J, Voisey J, Hughes I, van Daal A. Promoter polymorphisms in the MATP (SLC45A2) gene are associated with normal human skin color variation. Hum Mutat. 2007; 28 : 710–717, doi:10.1002/humu.20504.17358008
18. Graf J, Hodgson R, van Daal A. Single nucleotide polymorphisms in the MATP gene are associated with normal human pigmentation variation. Hum Mutat. 2005; 25 : 278–284, doi:10.1002/humu.20143.15714523
19. Thiel B, Sharma A, Shaikh S. Retinitis pigmentosa associated with glucose-6-phosphate dehydrogenase deficiency. Cureus. 2017; 9 e1506, doi:10.7759/cureus.1506.28948126
20. Walia S, Fishman GA, Zernant-Rajang J, Raime K, Allikmets R. Phenotypic expression of a PRPF8 gene mutation in a Large African American family. Arch Ophthalmol. 2008; 126 : 1127–1132, doi:10.1001/archopht.126.8.1127.18695108
21. Lagarde WH, Underwood LE, Moats-Staats BM, Calikoglu AS. Novel mutation in the SLC19A2 gene in an African-American female with thiamine-responsive megaloblastic anemia syndrome. Am J Med Genet A. 2004; 125A : 299–305, doi:10.1002/ajmg.a.20506.14994241
22. Kilgore DA, Kilgore TA, Sukpraprut-Braaten S, Schaefer GB, Uwaydat SH. Multimodal imaging of an RPGR carrier female. Ophthalmic Genet. 2021; 42 : 312–316, doi:10.1080/13816810.2021.1881981.33620278
23. Toma HS, Tan PL, McKusick VA, Katsanis N, Adams NA. Bardet-Biedl syndrome in an African-American patient: should the diagnostic criteria be expanded to include hydrometrocolpos? Ophthalmic Genet. 2007; 28 : 95–99, doi:10.1080/13816810701209545.17558852
24. Fishman GA, Lam BL, Anderson RJ. Racial differences in the prevalence of atrophic-appearing macular lesions between black and white patients with retinitis pigmentosa. Am J Ophthalmol. 1994; 118 : 33–38, doi:10.1016/s0002-9394(14)72839-9.8023873
25. Daiger SP, Churchill JD, Bowne SJ, et al . A novel locus for autosomal dominant retinitis pigmentosa (adRP) on chromosome 19q13. Invest Ophthalmol Vis Sci. 2014; 55 : 3267.
26. Perreault-Micale C, Frieden A, Kennedy CJ, et al . Truncating variants in the majority of the cytoplasmic domain of PCDH15 are unlikely to cause Usher syndrome 1F. J Mol Diagn. 2014; 16 : 673–678, doi:10.1016/j.jmoldx.2014.07.001.25307757
27. Vezinaw CM, Fishman GA, Chiang J. Unanticipated prognosis for a patient with type 2 Usher syndrome. Doc Ophthalmol. 2019; 138 : 161–166, doi:10.1007/s10633-019-09677-8.30796641
28. Ali ZK, Whitson JT, Mootha VV, et al . Glaucoma in patients with corneal endothelial dystrophy. Eye Contact Lens. 2011; 37 : 332–336, doi:10.1097/ICL.0b013e31822d0fa6.21912260
29. Afshari NA, Bahadur RP, Eifrig DE Jr, Thogersen IB, Enghild JJ, Klintworth GK. Atypical asymmetric lattice corneal dystrophy associated with a novel homozygous mutation (Val624Met) in the TGFBI gene. Mol Vis. 2008; 14 : 495–499.18385782
30. Eghrari AO, Vahedi S, Afshari NA, Riazuddin SA, Gottsch JD. CTG18.1 expansion in TCF4 among African Americans with Fuchs' corneal dystrophy. Invest Ophthalmol Vis Sci. 2017; 58 : 6046–6049, doi:10.1167/iovs.17-21661.29196769
31. Meallet MA, Affeldt JA, McFarland TJ, et al . An unusual clinical phenotype of Avellino corneal dystrophy associated with an Arg124His beta iG-H3 mutation in an African-American woman. Am J Ophthalmol. 2004; 137 : 765–767, doi:10.1016/j.ajo.2003.09.062.15059726
32. Minear MA, Li YJ, Rimmler J, et al . Genetic screen of African Americans with Fuchs endothelial corneal dystrophy. Mol Vis. 2013; 19 : 2508–2516.24348007
33. Mahr MA, Baratz KH, Hodge DO, Erie JC. Racial/ethnic differences in rates of penetrating or endothelial keratoplasty for Fuchs endothelial corneal dystrophy among US Medicare beneficiaries. JAMA Ophthalmol. 2016; 134 : 1178–1180, doi:10.1001/jamaophthalmol.2016.2735.27533017
34. Patel DA, Harocopos GJ, Chang SH, Vora SC, Lubniewski AJ, Huang AJ. Novel CHST6 gene mutations in 2 unrelated cases of macular corneal dystrophy. Cornea. 2011; 30 : 664–669, doi:10.1097/ICO.0b013e3182012888.21242781
35. Weiss JS, Kruth HS. Kuivaniemi H, et al . Genetic analysis of 14 families with Schnyder crystalline corneal dystrophy reveals clues to UBIAD1 protein function. Am J Med Genet A. 2008; 146A : 271–283, doi:10.1002/ajmg.a.32201.18176953
36. Chen X, Kuehlewein L, Pineles SL, et al . En face optical coherence tomography of macular microcysts due to optic neuropathy from neuromyelitis optica. Retin Cases Brief Rep. 2015; 9 : 302–306, doi:10.1097/ICB.0000000000000197.26296052
37. Shahid K, Kolomeyer AM, Nayak NV, et al . Ocular telehealth screenings in an urban community. Telemed J E health. 2012; 18 : 95–100, doi:10.1089/tmj.2011.0067.22283358
38. Liu Y, Schmidt S, Qin X, et al . No association between OPA1 polymorphisms and primary open-angle glaucoma in three different populations. Mol Vis. 2007; 13 : 2137–2141.18079692
39. McClelland CM, Van Stavern GP, Tselis AC. Leber hereditary optic neuropathy mimicking neuromyelitis optica. J Neuroophthalmol. 2011; 31 : 265–268, doi:10.1097/WNO.0b013e318225247b.21734595
40. Moran R, Blace N, Haddad N, Eleff T. Diagnostic yield of laboratory testing and imaging studies in patients with optic atrophy in an inner city population. Invest Ophthalmol Vis Sci. 2018; 59 : 616.
41. Gurney JG, Ross JA, Wall DA, Bleyer WA, Severson RK, Robison LL. Infant cancer in the U.S.: histology-specific incidence and trends, 1973 to 1992. J Pediatr Hematol Oncol. 1997; 19 : 428–432, doi:10.1097/00043426-199709000-00004.9329464
42. Orman A, Koru-Sengul T, Miao F, Markoe A, Panoff JE. The modern role of radiation therapy in treating advanced-stage retinoblastoma: long-term outcomes and racial differences. Int J Radiat Oncol Biol Phys. 2014; 90 : 1037–1043, doi:10.1016/j.ijrobp.2014.08.336.25442037
43. Shields CL, Lally SE, Manjandavia FP, Leahey A, Shields JA. Diffuse anterior retinoblastoma with globe salvage and visual preservation in 3 consecutive cases. Ophthalmology. 2016; 123 : 378–384, doi:10.1016/j.ophtha.2015.09.040.26522706
44. Fitzpatrick SG, Woodworth BA, Monteiro C, Makary R. Nasal sinus leiomyosarcoma in a patient with history of non-hereditary unilateral treated retinoblastoma. Head Neck Pathol. 2011; 5 : 57–62, doi:10.1007/s12105-010-0207-1.20803265
45. Utz VM, Chappelow AV, Marino MJ, et al . Identification of three ABCA4 sequence variations exclusive to African American patients in a cohort of patients with Stargardt disease. Am J Ophthalmol. 2013; 156 : 1220–1227.e2, doi:10.1016/j.ajo.2013.07.008.24011517
46. Zernant J, Xie YA, Ayuso C, et al . Analysis of the ABCA4 genomic locus in Stargardt disease. Hum Mol Genet. 2014; 23 : 6797–806, doi:10.1093/hmg/ddu396.25082829
47. Zernant J, Collison FT, Lee W, et al . Genetic and clinical analysis of ABCA4-associated disease in African American patients. Hum Mutat. 2014; 35 : 1187–1194, doi:10.1002/humu.22626.25066811
48. Kooner K, Harrison M, Prasla Z, Albdour M, Adams-Huet B. Pediatric glaucoma suspects. Clin Ophthalmol. 2014; 8 : 1139–1145, doi:10.2147/OPTH.S61682.24966666
49. Fung DS, Roensch MA, Kooner KS, Cavanagh HD, Whitson JT. Epidemiology and characteristics of childhood glaucoma: results from the Dallas Glaucoma Registry. Clin Ophthalmol. 2013; 7 : 1739–1746, doi:10.2147/OPTH.S45480.24039394
50. Andoh JE, Ezekwesili AC, Nwanyanwu K, Elam A. Disparities in eye care access and utilization: a narrative review. Annu Rev Vis Sci. 2023; 9 : 15–37, doi:10.1146/annurev-vision-112122-020934.37254050
51. Randolph JD, Zebardast N, Pérez-González CE. Improving ophthalmic workforce diversity: a call to action. Ophthalmology. 2022; 129 : 1081–1082, doi:10.1016/j.ophtha.2022.06.030.36058732
52. Elam AR, Tseng VL, Rodriguez TM, et al . Disparities in vision health and eye care. Ophthalmology. 2022; 129 : e89–e113, doi:10.1016/j.ophtha.2022.07.010.36058735
53. Flanagin A, Frey T, Christiansen SL, AMA Manual of Style Committee. Updated guidance on the reporting of race and ethnicity in medical and science journals. JAMA. 2021; 326 : 621–627, doi:10.1001/jama.2021.13304.34402850
54. Lu C, Ahmed R, Lamri A, Anand SS. Use of race, ethnicity, and ancestry data in health research. PLOS Glob Public Health. 2022; 2 : e0001060, doi:10.1371/journal.pgph.0001060.36962630
