This review article explores the relationship between hyperglycemia during pregnancy and the visual development of offspring, specifically focusing on refractive error. The authors conducted a comprehensive search for relevant articles in various databases and assessed the methodological quality of the included studies. The findings consistently indicate that hyperglycemia during pregnancy can have a detrimental impact on the structural and functional aspects of visual development in offspring. The intrauterine hyperglycemic environment appears to negatively affect the retina and lens, leading to refractive errors. In conclusion, there is likely an association between hyperglycemia during pregnancy and the development of refractive errors in offspring.
JiwaniAMarseilleELohseN, et al.Gestational diabetes mellitus: results from a survey of country prevalence and practices. J Matern Fetal Neonatal Med2012; 25: 600–610.
2.
FerraraA. Increasing prevalence of gestational diabetes mellitus: a public health perspective. Diabetes Care2007; 30: S141–S146.
3.
GuariguataLLinnenkampUBeagleyJ, et al.Global estimates of the prevalence of hyperglycaemia in pregnancy. Diabetes Res Clin Pract2014; 103: 176–185.
4.
HodMKapurASacksDA, et al.The International Federation of Gynecology and Obstetrics (FIGO) initiative on gestational diabetes mellitus: a pragmatic guide for diagnosis, management, and care. Int J Gynaecol Obstet2015; 131: S173–S211.
5.
Diagnostic criteria and classification of hyperglycaemia first detected in pregnancy: a World Health Organization Guideline. Diabetes Res Clin Pract2014; 103: 341–363.
6.
MaglianoDJBoykoEJ and committee IDFDAtes. Idf diabetes atlas. Brussels: International Diabetes Federation, 2021.
7.
Zhou T, Du S, Sun D, Li X, Heianza Y, Hu G, Sun L, Pei X, Shang X, Qi L. Prevalence and Trends in Gestational Diabetes Mellitus Among Women in the United States, 2006-2017: A Population-Based Study. Front Endocrinol (Lausanne). 2022 Jun 6;13:868094. doi: 10.3389/fendo.2022.868094. PMID: 35733768; PMCID: PMC9207520.
8.
HarbENWildsoetCF. Origins of refractive errors: environmental and genetic factors. Annu Rev Vis Sci2019; 5: 47–72.
9.
SankaridurgPTahhanNKandelH, et al.IMI Impact of myopia. Invest Ophthalmol Vis Sci2021; 62: 2.
10.
HoldenBAFrickeTRWilsonDA, et al.Global prevalence of myopia and high myopia and temporal trends from 2000 through 2050. Ophthalmology2016; 123: 1036–1042.
11.
WojciechowskiR. Nature and nurture: the complex genetics of myopia and refractive error. Clin Genet2011; 79: 301–320.
12.
BikbovMMKazakbaevaGMFakhretdinovaAA, et al.Prevalence and associated factors of myopia in children and adolescents in Russia: the Ural Children Eye Study. Br J Ophthalmol2023: 1–6. DOI: https://doi.org/10.1136/bjo-2022-322945.
13.
KamKWCheeASHZhangY, et al.Association of maternal and paternal astigmatism with child astigmatism in the Hong Kong Children Eye Study. JAMA Netw Open2022; 5: e2247795.
14.
HysiPGChoquetHKhawajaAP, et al.Meta-analysis of 542,934 subjects of European ancestry identifies new genes and mechanisms predisposing to refractive error and myopia. Nat Genet2020; 52: 401–407.
SaxenaRVashistPTandonR, et al.Prevalence of myopia and its risk factors in urban school children in Delhi: the North India Myopia Study (NIM Study). PLoS One2015; 10: e0117349.
17.
SeewoodharyM. An overview of diabetic retinopathy and other ocular complications of diabetes mellitus. Nurs Stand2021; 36: 71–76.
18.
RaniPKRamanRRachapalliSR, et al.Prevalence of refractive errors and associated risk factors in subjects with type 2 diabetes mellitus SN-DREAMS, report 18. Ophthalmology2010; 117: 1155–1162.
19.
FledeliusHCFuchsJReckA. Refraction in diabetics during metabolic dysregulation, acute or chronic. With special reference to the diabetic myopia concept. Acta Ophthalmol (Copenh)1990; 68: 275–280.
20.
GwinupGVillarrealA. Relationship of serum glucose concentration to changes in refraction. Diabetes1976; 25: 29–31.
21.
ChenSJTungTHLiuJH, et al.Prevalence and associated factors of refractive errors among type 2 diabetics in Kinmen, Taiwan. Ophthalmic Epidemiol2008; 15: 2–9.
22.
MuttiDOMitchellGLMoeschbergerML, et al.Parental myopia, near work, school achievement, and children's refractive error. Invest Ophthalmol Vis Sci2002; 43: 3633–3640.
23.
ZhangSJLiYFTanRR, et al.A new gestational diabetes mellitus model: hyperglycemia-induced eye malformation via inhibition of Pax6 in the chick embryo. Dis Model Mech2016; 9: 177–186.
24.
SinghACastilloHABrownJ, et al.High glucose levels affect retinal patterning during zebrafish embryogenesis. Sci Rep2019; 9: 4121.
25.
WallPBTraboulsiEI. Congenital abnormalities of the optic nerve: from gene mutation to clinical expression. Curr Neurol Neurosci Rep2013; 13: 363.
26.
ChenCAYinJLewisRA, et al.Genetic causes of optic nerve hypoplasia. J Med Genet2017; 54: 441–449.
27.
DimasiDPBurdonKPCraigJE. The genetics of central corneal thickness. Br J Ophthalmol2010; 94: 971–976.
28.
SuDHWongTYWongWL, et al.Diabetes, hyperglycemia, and central corneal thickness: the Singapore Malay Eye Study. Ophthalmology2008; 115: 964–968.e961.
29.
BezDMegreliJBezM, et al.Association between type of educational system and prevalence and severity of myopia among male adolescents in Israel. JAMA Ophthalmol2019; 137: 887–893.
30.
HeMZhengYXiangF. Prevalence of myopia in urban and rural children in mainland China. Optom Vis Sci2009; 86: 40–44.
31.
WongTYFosterPJJohnsonGJ, et al.Education, socioeconomic status, and ocular dimensions in Chinese adults: the Tanjong Pagar Survey. Br J Ophthalmol2002; 86: 963–968.
32.
HuangHMChangDSWuPC. The association between near work activities and myopia in children-a systematic review and meta-analysis. PLoS One2015; 10: e0140419.
33.
RoseKAMorganIGIpJ, et al.Outdoor activity reduces the prevalence of myopia in children. Ophthalmology2008; 115: 1279–1285.
34.
GuggenheimJANorthstoneKMcMahonG, et al.Time outdoors and physical activity as predictors of incident myopia in childhood: a prospective cohort study. Invest Ophthalmol Vis Sci2012; 53: 2856–2865.
35.
JiangXTarczy-HornochKStramD, et al.Prevalence, characteristics, and risk factors of moderate or high hyperopia among multiethnic children 6 to 72 months of age: a pooled analysis of individual participant data. Ophthalmology2019; 126: 989–999.
36.
SawSMChiaKSLindstromJM, et al.Childhood myopia and parental smoking. Br J Ophthalmol2004; 88: 934–937.
37.
ZhangYZhangXJYuanN, et al.Analysis of secondhand smoke exposure and myopia among children aged 6 to 8 years in Hong Kong. JAMA Netw Open2023; 6: e2313006.
38.
FledeliusHC. Is myopia getting more frequent? A cross-sectional study of 1416 Danes aged 16 years +. Acta Ophthalmol (Copenh)1983; 61: 545–559.
39.
SaitoYOhmiGKinoshitaS, et al.Transient hyperopia with lens swelling at initial therapy in diabetes. Br J Ophthalmol1993; 77: 145–148.
40.
LøgstrupNSjølieAKKyvikKO, et al.Long-term influence of insulin dependent diabetes mellitus on refraction and its components: a population based twin study. Br J Ophthalmol1997; 81: 343–349.
41.
AraújoJRKeatingEMartelF. Impact of gestational diabetes mellitus in the maternal-to-fetal transport of nutrients. Curr Diab Rep2015; 15: 569.
42.
PedersenJ. Weight and length at birth of infants of diabetic mothers. Acta Endocrinol (Copenh)1954; 16: 330–342.
43.
DuJLiJLiuX, et al.Association of maternal diabetes during pregnancy with high refractive error in offspring: a nationwide population-based cohort study. Diabetologia2021; 64: 2466–2477.
44.
ChungYWChoiMYKimJS, et al.The association between macular thickness and axial length in myopic eyes. Biomed Res Int2019; 2019: 8913582.
45.
FledeliusHC. Refractive change in diabetes mellitus around onset or when poorly controlled. A clinical study. Acta Ophthalmol (Copenh)1987; 65: 53–57.
46.
GabbayKH. The sorbitol pathway and the complications of diabetes. N Engl J Med1973; 288: 831–836.
47.
BerglundSKGarcía-ValdésLTorres-EspinolaFJ, et al.Maternal, fetal and perinatal alterations associated with obesity, overweight and gestational diabetes: an observational cohort study (PREOBE). BMC Public Health2016; 16: 207.
48.
Camprubi RoblesMCampoyCGarcia FernandezL, et al.Maternal diabetes and cognitive performance in the offspring: a systematic review and meta-analysis. PLoS One2015; 10: e0142583.
49.
Torres-EspínolaFJBerglundSKGarcíaS, et al.Visual evoked potentials in offspring born to mothers with overweight, obesity and gestational diabetes. PLoS One2018; 13: e0203754.
50.
ShiYVanhouttePM. Macro- and microvascular endothelial dysfunction in diabetes. J Diabetes2017; 9: 434–449.
51.
Cunha-VazJG. The blood-ocular barriers: past, present, and future. Doc Ophthalmol1997; 93: 149–157.
52.
FraserANelsonSMMacdonald-WallisC, et al.Associations of existing diabetes, gestational diabetes, and glycosuria with offspring IQ and educational attainment: the avon longitudinal study of parents and children. Exp Diabetes Res2012; 2012: 963735.
53.
DionneGBoivinMSéguinJR, et al.Gestational diabetes hinders language development in offspring. Pediatrics2008; 122: e1073–e1079.
54.
EidelmanAISamueloffA. The pathophysiology of the fetus of the diabetic mother. Semin Perinatol2002; 26: 232–236.
55.
LinQJiaYLiT, et al.Optic disc morphology and peripapillary atrophic changes in diabetic children and adults without diabetic retinopathy or visual impairment. Acta Ophthalmol2022; 100: e157–e166.
56.
WeissAHRossEA. Axial myopia in eyes with optic nerve hypoplasia. Graefes Arch Clin Exp Ophthalmol1992; 230: 372–377.
57.
TariqYMSamarawickramaCLiH, et al.Retinal thickness in the offspring of diabetic pregnancies. Am J Ophthalmol2010; 150: 883–887.
58.
van DijkHWKokPHGarvinM, et al.Selective loss of inner retinal layer thickness in type 1 diabetic patients with minimal diabetic retinopathy. Invest Ophthalmol Vis Sci2009; 50: 3404–3409.
59.
MonnierVMSellDRAbdul-KarimFW, et al.Collagen browning and cross-linking are increased in chronic experimental hyperglycemia. Relevance to diabetes and aging. Diabetes1988; 37: 867–872.
60.
MimouniMFloresVShapiraY, et al.Correlation between central corneal thickness and myopia. Int Ophthalmol2018; 38: 2547–2551.
61.
Bueno-GimenoIEspaña-GregoriEGene-SampedroA, et al.Relationship among corneal biomechanics, refractive error, and axial length. Optom Vis Sci2014; 91: 507–513.
62.
SrivannaboonS. Relationship between corneal thickness and level of myopia. J Med Assoc Thai2002; 85: 162–166.
63.
RoszkowskaAMLicitraCTumminelloG, et al.Corneal nerves in diabetes-the role of the in vivo corneal confocal microscopy of the subbasal nerve plexus in the assessment of peripheral small fiber neuropathy. Surv Ophthalmol2021; 66: 493–513.
64.
AzmiSFerdousiMPetropoulosIN, et al.Corneal confocal microscopy identifies small-fiber neuropathy in subjects with impaired glucose tolerance who develop type 2 diabetes. Diabetes Care2015; 38: 1502–1508.
65.
BoucekP. ‘Observing’ diabetic neuropathy with corneal confocal microscopy: the effect of improvement of risk factors. Expert Rev Endocrinol Metab2011; 6: 773–775.
66.
dell'OmoRCifarielloFDe TurrisS, et al. Confocal microscopy of corneal nerve plexus as an early marker of eye involvement in patients with type 2 diabetes. Diabetes Res Clin Pract2018; 142: 393–400.
67.
De ClerckEEBSchoutenJBerendschotT, et al.Reduced corneal nerve fibre length in prediabetes and type 2 diabetes: the Maastricht Study. Acta Ophthalmol2020; 98: 485–491.
68.
FerdousiMRomanchukKMahJK, et al.Early corneal nerve fibre damage and increased Langerhans cell density in children with type 1 diabetes mellitus. Sci Rep2019; 9: 8758.
69.
GöncüTÇakmakAAkalA, et al.Comparison of refractive error and central corneal thickness in neonates of diabetic and healthy mothers. Eur J Ophthalmol2015; 25: 396–399.
70.
Alvarez-BulnesOMonés-LlivinaACavero-RoigL, et al.Ophthalmic pathology in the offspring of pregnant women with gestational diabetes mellitus. Matern Child Health J2020; 24: 524–529.
71.
WalterETsumiEWainstockT, et al.Maternal gestational diabetes mellitus: is it associated with long-term pediatric ophthalmic morbidity of the offspring?J Matern Fetal Neonatal Med2019; 32: 2529–2538.
72.
YounanCMitchellPCummingRG, et al.Myopia and incident cataract and cataract surgery: the blue mountains eye study. Invest Ophthalmol Vis Sci2002; 43: 3625–3632.
73.
MitchellPHourihanFSandbachJ, et al.The relationship between glaucoma and myopia: the Blue Mountains Eye Study. Ophthalmology1999; 106: 2010–2015.
74.
ChiharaEChiharaK. Covariation of optic disc measurements and ocular parameters in the healthy eye. Graefes Arch Clin Exp Ophthalmol1994; 232: 265–271.
75.
YuraT. The relationship between the types of axial elongation and the prevalence of lattice degeneration of the retina. Acta Ophthalmol Scand1998; 76: 90–95.
76.
XuQZhangFLiJ, et al.Association of maternal diabetes during pregnancy with visual acuity development in offspring: a prospective cohort study. Acta Diabetol2022; 59: 1461–1468.
77.
PhoswaWNKhaliqOP. The role of oxidative stress in hypertensive disorders of pregnancy (Preeclampsia, Gestational Hypertension) and metabolic disorder of pregnancy (Gestational diabetes Mellitus). Oxid Med Cell Longev2021; 2021: 5581570.
78.
El-SayyadHIEl-SherbinyMASobhMA, et al.Protective effects of Morus alba leaves extract on ocular functions of pups from diabetic and hypercholesterolemic mother rats. Int J Biol Sci2011; 7: 715–728.
79.
HamWTJr.MuellerHARuffoloJJJr., et al.Basic mechanisms underlying the production of photochemical lesions in the mammalian retina. Curr Eye Res1984; 3: 165–174.
80.
Titialii-TorresKFMorrisAC. Embryonic hyperglycemia perturbs the development of specific retinal cell types, including photoreceptors. J Cell Sci2022; 135. DOI: https://doi.org/10.1242/jcs.259187.
81.
SunWHuangLXuY, et al.Exome sequencing on 298 probands with early-onset high myopia: approximately one-fourth show potential pathogenic mutations in RetNet genes. Invest Ophthalmol Vis Sci2015; 56: 8365–8372.
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