Exp Clin Endocrinol Diabetes 2024; 132(09): 522-530
DOI: 10.1055/a-2316-3903
Article

Optical Coherence Tomography Angiography Evaluation of Retinochoroidal Microvascular Circulation Differences in Pregnant Women with Pregestational and Gestational Diabetes Mellitus

1   The Department of Ophthalmology, Manavgat State Hospital, Antalya, Turkey
,
Mehmet E Doğan
2   The Department of Ophthalmology, Akdeniz University Faculty of Medicine, Antalya, Turkey
,
3   The Department of Obstetrics and Gynecology, Division of Perinatology, Akdeniz University Faculty of Medicine, Antalya, Turkey
,
3   The Department of Obstetrics and Gynecology, Division of Perinatology, Akdeniz University Faculty of Medicine, Antalya, Turkey
,
Ali Pota
4   The Department of Obstetrics and Gynecology, Antalya Ministry of Health Kepez State Hospital, Antalya, Turkey
› Author Affiliations

Funding The authors received no funding for the research, authorship, and/or publication of this article from any government or private institution.

Abstract

Purpose In this study, the changes in microvascular circulation caused by pregestational and gestational diabetes were observed, without focusing on retinal findings, to reveal the effect of diabetes regulation.

Methods A total of 135 subjects were included: 30 with gestational diabetes (GDM), 30 pregestational diabetes (PGDM), 30 healthy pregnant normoglycemic subjects, and 45 healthy non-pregnant subjects. All subjects were examined by optical coherence tomography (OCT) and angiography. The retina, retinal nerve fiber layer (RNFL), ganglion cell layer (GCL), choroidal thickness (CT), superficial capillary plexus (SCP), deep capillary plexus (DCP), choriocapillaris (CC), vascular density (VD), and foveal avascular zone (FAZ) areas were measured.

Results The foveal VD of SCP and DCP was significantly lower in the PGDM and GDM groups compared to the control groups (p:0.006 and p:0.001, respectively). CC VD was significantly higher in all pregnant groups compared to non-pregnant controls (p<0.001). The choroidal thickness values were highest in the healthy pregnant group and lowest in the PGDM group. There was no significant difference in FAZ area, retina, RNFL and GCL thickness between the groups. In the PGDM group, a negative correlation was observed between the FAZ area and the HbA1c level (r:− 0.417, p:0.043).

Conclusion There was a decrease in vascular density in pregnant women with diabetes compared to healthy pregnant women and controls. In the pregnant group with PGDM, a narrowing of the FAZ area was observed with increasing worsening of diabetes control. Diabetes type and glycemic control could influence the microvascular changes even in the absence of clinical or retinal findings.



Publication History

Received: 10 January 2024
Received: 19 April 2024

Accepted: 22 April 2024

Article published online:
06 June 2024

© 2024. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Committee on Practice B-O. ACOG Practice Bulletin No. 190: Gestational Diabetes Mellitus. Obstet Gynecol 2018; 131: e49-e64
  • 2 Butte NF. Carbohydrate and lipid metabolism in pregnancy: Normal compared with gestational diabetes mellitus. Am J Clin Nutr 2000; 71: 1256S-1261S
  • 3 International Association of Diabetes and Pregnancy Study Groups Consensus Panel. Metzger BE, Gabbe SG. et al. International association of diabetes and pregnancy study groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy. Diabetes Care 2010; 33: 676-682
  • 4 American Diabetes Association. 2. Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes-2018. Diabetes Care 2018; 41: S13-S27
  • 5 Jensen DM, Damm P, Sørensen B. et al. Proposed diagnostic thresholds for gestational diabetes mellitus according to a 75-g oral glucose tolerance test. Maternal and perinatal outcomes in 3260 Danish women. Diabet Med 2003; 20: 51-57
  • 6 Mackensen F, Paulus WE, Max R. et al Ocular changes during pregnancy. Dtsch Arztebl Int 2014; 111: 567-575 quiz 76
  • 7 Kubicka-Trzaska A, Karska-Basta I, Kobylarz J. et al. Pregnancy and the eye. Klin Ocz 2008; 110: 401-404
  • 8 Roglic G. WHO Global report on diabetes: A summary. Int J Noncommun Dis 2016; 1: 3-8
  • 9 Lamar ME, Kuehl TJ, Cooney AT. et al. Jelly beans as an alternative to a fifty-gram glucose beverage for gestational diabetes screening. Am J Obstet Gynecol 1999; 181: 1154-1157
  • 10 Samples JR, Meyer SM. Use of ophthalmic medications in pregnant and nursing women. Am J Ophthalmol 1988; 106: 616-623
  • 11 Chong YS, Cai S, Lin H. Ethnic differences translate to inadequacy of high-risk screening for gestational diabetes mellitus in an Asian population: A cohort study. BMC Pregnancy Childbirth 2014; 14: 345
  • 12 Alberti KG, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med 1998; 15: 539-553
  • 13 Quintanilla Rodriguez BS, Mahdy H. Gestational Diabetes. In: StatPearls. Treasure Island (FL): . StatPearls Publishing; August 8 2023
  • 14 Spaide RF, Klancnik JM, Cooney MJ. Retinal vascular layers imaged by fluorescein angiography and optical coherence tomography angiography. JAMA Ophthalmol 2015; 133: 45-50
  • 15 Little RR, Rohlfing C, Sacks DB. The National Glycohemoglobin Standardization Program: Over 20 years of improving hemoglobin A1c measurement. Clin Chem 2019; 65: 839-848
  • 16 Liu G, Wang F. Macular vascular changes in pregnant women with gestational diabetes mellitus by optical coherence tomography angiography. BMC Ophthalmol 2021; 21: 170
  • 17 Chen HC, Newsom RS, Patel V. et al. Retinal blood flow changes during pregnancy in women with diabetes. Invest Ophthalmol Vis Sci 1994; 35: 3199-3208
  • 18 Larinkari J, Laatikainen L, Ranta T. et al. Metabolic control and serum hormone levels in relation to retinopathy in diabetic pregnancy. Diabetologia 1982; 22: 327-332
  • 19 Liu YJ, Tsushima T, Onoda N. et al. Expression of messenger RNA of insulin-like growth factors (IGFs) and IGF binding proteins (IGFBP1-6) in placenta of normal and diabetic pregnancy. Endocr J 1996; 43: S89-S91
  • 20 Lauszus FF, Klebe JG, Bek T. et al. Increased serum IGF-I during pregnancy is associated with progression of diabetic retinopathy. Diabetes 2003; 52: 852-856
  • 21 Li LJ, Tan KH, Aris IM. et al. Gestational retinal microvasculature and the risk of 5 year postpartum abnormal glucose metabolism. Diabetologia 2017; 60: 2368-2376
  • 22 Inanc M, Tekin K, Kiziltoprak H. et al. Changes in retinal microcirculation precede the clinical onset of diabetic retinopathy in children with type 1 diabetes mellitus. Am J Ophthalmol 2019; 207: 37-44
  • 23 Cao D, Yang D, Huang Z. et al. Optical coherence tomography angiography discerns preclinical diabetic retinopathy in eyes of patients with type 2 diabetes without clinical diabetic retinopathy. Acta Diabetol 2018; 55: 469-477
  • 24 Evliyaoglu F, Kurt MM, Yilmaz M. et al. Evaluation of microvascular density and retinal vessel diameter in gestational and type 2 diabetes using swept-source OCT-A technology. J Fr Ophtalmol 2022; 45: 430-437
  • 25 Pomytkina NV, Sorokin EL. Features of retinal blood flow in pregnant women with carbohydrate metabolism disorders. Vestn Oftalmol 2022; 138: 16-23
  • 26 Chanwimol K, Balasubramanian S, Nassisi M. et al. Retinal vascular changes during pregnancy detected with optical coherence tomography angiography. Invest Ophthalmol Vis Sci 2019; 60: 2726-2732
  • 27 Durbin MK, An L, Shemonski ND. et al. Quantification of retinal microvascular density in optical coherence tomographic angiography images in diabetic retinopathy. JAMA Ophthalmol 2017; 135: 370-376
  • 28 Nesper PL, Roberts PK, Onishi AC. et al. Quantifying microvascular abnormalities with increasing severity of diabetic retinopathy using optical coherence tomography angiography. Invest Ophthalmol Vis Sci 2017; 58: BIO307-BIO315
  • 29 Taylor E, Dobree JH. Proliferative diabetic retinopathy. Site and size of initial lesions. Br J Ophthalmol 1970; 54: 11-18
  • 30 Jung JJ, Lim SY, Chan X. et al. Correlation of diabetic disease severity to degree of quadrant asymmetry in En Face OCTA metrics. Invest Ophthalmol Vis Sci 2022; 63: 12
  • 31 Sugimoto M, Wakamatsu Y, Miyata R. et al. Relationship between size of the foveal avascular zone and carbohydrate metabolic disorders during pregnancy. Biomed Res Int 2019; 2019: 3261279
  • 32 Tokayer J, Jia Y, Dhalla AH. et al. Blood flow velocity quantification using split-spectrum amplitude-decorrelation angiography with optical coherence tomography. Biomed Opt Express 2013; 4: 1909-1924
  • 33 Chai Q, Yao Y, Guo C. et al. Structural and functional retinal changes in patients with type 2 diabetes without diabetic retinopathy. Ann Med 2022; 54: 1816-1825