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. 2023 Jan 18;13(1):e062098. doi: 10.1136/bmjopen-2022-062098

Table 1.

Total of 11 studies included

Title, lead author Year Study design Population: n=sample size, age; mean±SD or median (range), (F/M) Control group: n=sample size, age; mean±SD or median (range), (F/M) Results: RHI reported. if RHI not specified, we reported p/r values Outcomes
Adolescents and young adults with type 1 diabetes display a high prevalence of endothelial dysfunction. Scaramuzza et al17 2015 Cohort prospective observational study. Results at baseline and after a 1-year follow-up n=73 T1D adolescents, diagnosed>1 year, 16.2±3.5 years,(F/M 25/48) No controls. 56 (76.7%) had ED, with lower mean RHI scores (1.26±0.22 vs 2.24±0.48, p<0.0001). More with ED had abnormal cardiac autonomic tests (p=0.02) and were more sedentary. After 1-year follow-up in 64/73 patients, 81.8% had ED, despite some improvement in HbA1c. T1D adolescents had evidence of ED. Good metabolic control (HbA1c ≤7.5%) and regular physical activity might be protective. ED progression despite some improvement to HbA1c.
Alpha-lipoic acid and antioxidant diet help to improve endothelial dysfunction in adolescents with type 1 diabetes: a pilot trial. Scaramuzza et al19 2015 Double- blind, randomised controlled trial—snow balling. Results at baseline and after follow-up n=71 T1D patients, followed for at least 1 year, age 16.3±3.4 years,(F/M 29/42). (a) antioxidant diet 10.000 ORAC+alpha-lipoic acid; (b) antioxidant diet 10.000 ORAC+placebo; (c)controls Three double-blind study arms: (a) antioxidant diet 10 000 ORAC+lipoic acid: RHI 1.40±0.68 vs 1.72±0.66 (p<0.05) (baseline vs after 6 months). (b) Antioxidant diet 10 000 ORAC+placebo: RHI 1.39±0.41 vs 1.58±0.40 (p>0.05). (c) Controls: RHI 1.58±0.64 vs 1.54±0.42 (p>0.05). Improved RHI with alpha-lipoic acid in T1D patients.
Effect of metformin on endothelial function in overweight adolescents with type 1 diabetes (T1D). Nadeau et al20 2016 Conference abstract. Endo-PAT scores at baseline and 13 weeks. Total n=70 overweight T1D patients. n=41 on metformin (up to 2000 mg/day), 12–19 years (mean 15.8) n=29 placebo group. Mean baseline RHI 1.8±0.6 in metformin group and 1.7±0.6 placebo group. At 13 weeks, no significant change from baseline RHI (+0.1 in metformin vs −0.0 in placebo, p=0.08). Some improvement in endothelial function in men. No significant RHI change with metformin overall but some improvement in overweight T1D males.
Assessment of biomarkers of inflammation and premature atherosclerosis in adolescents with type-1 diabetes mellitus. Babar et al18 2019 Cross-sectional study T1D adolescents≥12 years. Two groups based on different HbA1c ranges. (a) HbA1c ≥9.5% (n=25) (b) HbA1c ≤8.5% (n=27). PAT results were not significantly different between the groups. Pearson correlation showed a significant direct relationship between rising HbA1c and PAT (p=0.03, r=0.31). Suboptimal glycaemic control (rising HbA1c) causes early atherosclerosis.
Improvements in peripheral vascular function with vitamin D treatment in deficient adolescents with type 1 diabetes. Deda et al21 2018 Research article—snow balling. Tested at two different time points. n=21 T1D patients followed for~2 years. 25-OH-Vit. D levels<37.5 nmol/L. Age 15.7±1.4 years,(F/M 19/12) Controls: matched age, sex and T1D. After 4.8±1.3 months of Vit. D supplementation RHI improved: 1.83±0.42 vs 2.02±0.68 (p<0.05). Vit. D supplementation associated with improvement to endothelial function and reduced urinary inflammatory markers.
Non-alcoholic fatty liver disease in hispanic youth with dysglycemia: risk for subclinical atherosclerosis? Bacha et al23 2017 Cross-sectional study n=23 overweight/ obese with NAFLD, age 15.2±0.5 years.
n=12 pre-diabetes,
n=11 T2D,(F/M 13/10)
n=13 overweight/ obese without NAFLD, age 15.7±0.4 years. n=8 pre-diabetes, n=5 T2D,(F/M 3/10) NAFLD group had lower RHI (1.4±0.05 vs 1.7±0.09, p=0.002). Hepatic fat is inversely related to RHI (r=−0.49, p=0.002). Hepatic fat and AST/ALT levels inversely related to RHI. If dysglycemia, NAFLD is associated with worse ED.
Endothelial function in youth: A Biomarker modulated by adiposity-related insulin resistance. Tomsa et al22 2016 Cross-sectional study Total n=60.
n=25 obese without DM, n=19 obese with impaired glucose tolerance,
n=16 obese T2D but HB1Ac <8%.
Age 15.5 (0.2),(F/M 37/23)
n=21 normal weight, age 15.5 (0.2),(F/M 9/12) RHI inversely related to % body fat (r = −0.29, p = 0.008), total (r = −0.37, p = 0.004), subcutaneous (r = −0.39, p = 0.003), and visceral abdominal fat (r = −0.26, p = 0.04). Childhood obesity is associated with ED (lower RHI). RHI lower in obese and T2D. RHI negatively related with percentage body fat, WC, Leptin, TNF-alpha, blood glucose.
Circulating fibroblast growth factor-21 (FGF-21): A biomarker of subclinical atherosclerosis in obese youth with non-alcoholic fatty liver disease (NAFLD)? Bacha et al24 2017 Conference abstract Obese adolescents with NAFLD, 15.4±0.3 years. n=13 normal glucose tolerance, n=19 pre-diabetes, n=16 T2D patients Control group: no NAFLD.
No difference in age/gender between groups.
Lower RHI in NAFLD group. High FGF-21 concentrations related to RHI (r=−0.33, p=0.03). Increased FGF-21 in obese adolescents with NAFLD associated with insulin sensitivity and ED. FGF-21 may constitute a biomarker ED.
Assessment of Microvascular Function in Children and Adolescents with Diabetes and Obesity. Kochummen et al26 2019 Cross-sectional study DM group.
n=33 T1D with normal weight.
n=8 obese T2D, age 12.7 (3.8) years,(F/M 25/16)
n=17 obese, non-DM children (normal BGL, BP and lipid profile), 12.8 (2.7) years,(F/M 9/8) For every 1% increase in HbA1C, RHI decreased by 0.097 (p=0.01). RHI of DM group with HbA1C<10% (1.70±0.58) vs those with≥10% (1.21±0.19) (p=0.02). Poorly-controlled DM (HbA1C ≥10%) had lower RHI. RHI negatively related with HbA1C. RHI similar between obese and normal weight with T1D. Similar between T1D and T2D.
Free Vitamin D: Relationship to Insulin Sensitivity and Vascular Health in Youth. Bacha et al27 2019 Cross-sectional study. Comparison across tertiles of free 25(OH)D concentrations n=79, age 15.4±0.2 years,(F/M 45/34). n=30 overweight.
n=31 overweight with pre-diabetes
n=18 normal weight and normal glucose tolerance. The lowest tertile group had lower RHI (1.42±0.06, 1.54±0.06, and 1.77±0.09, p=0.002), compared with the second and third tertiles. Youth with low free 25(OH)D or BioD concentrations have lower insulin sensitivity and worse endothelial function.
Urine Albumin-to-Creatinine Ratio (UACR): A Marker of Early Endothelial Dysfunction in Youth. Bartz et al25 2015 Control study. Fasting UACR analysed. n=25 overweight (OW) with normal glucose tolerance, 15.6±0.2 years,(F/M 17/8).
n=20 OW with pre-diabetes,(F/M 11/9).
n=13 normal weight, 16.3±0.4,(F/M 7/6). Normal weight group RHI 1.84±0.1. OW with normal glucose tolerance 1.56±0.1. OW with pre-diabetes 1.56±0.1 (p=0.04). UACR was related to RHI (r=−0.33, p=0.01). UACR is an early marker of endothelial dysfunction in youth, independent of glycaemia.

Endo-PAT 2000 in paediatric type 1 diabetes mellitus (T1D) patients (five studies), type 2 diabetes and pre-diabetes (six studies).

ED, endothelial dysfunction; NAFLD, non-alcoholic fatty liver disease; ORAC, oxygen radical absorbance capacity units; OW, overweight; RHI, reactive hyperemia index; T1D, type 1 diabetes mellitus; T2D, type 2 diabetes mellitus; UACR, urine albumin-to-creatinine ratio.