Share:
Share this content in WeChat
X
Clinical Article
A semi-quantitative MRI study on brain developmental abnormalities in infants of gestational diabetic mothers
SUN Fei  YU Jinhong  LUO Hedan  MIAO Yanwei 

Cite this article as: SUN F, YU J H, LUO H D, et al. A semi-quantitative MRI study on brain developmental abnormalities in infants of gestational diabetic mothers[J]. Chin J Magn Reson Imaging, 2024, 15(12): 87-93. DOI:10.12015/issn.1674-8034.2024.12.013.


[Abstract] Objective To investigate the value of semi-quantitative analysis based on T1WI, T2WI, T2 fluid attenuated inversion recovery (FLAIR), and diffusion-weighted imaging (DWI) sequences in exploring abnormal brain development changes in infants of gestational diabetic mothers (IDMs).Materials and Methods A total of 54 cases of DMs were retrospectively included as the observation group (IDMs group), while 70 infants born to mothers without high-risk perinatal factors during the same period served as the healthy control (HC) group. Based on whether the gestational age at birth was less than 37 weeks, the IDMs group and the HC group were further divided into preterm infants: 27 in the IDMs A group and 33 in the HC A group, and term infants: 27 in the IDMs B group and 37 in the HC B group. A 1.5 T MRI was performed using T1WI, T2WI, T2 FLAIR, and DWI sequences. Regions of interest (ROI) were manually drawn on the maximum slices of the cerebellar hemispheres, amygdala, hippocampus, temporal lobe white matter, globus pallidus, caudate nucleus, ventrolateral thalamic nucleus, posterior limb of the internal capsule, splenium of the corpus callosum, frontal white matter, occipital white matter, parietal white matter, centrum semiovale, and masseter muscles, measuring the signal intensity and apparent diffusion coefficient (ADC) values of each ROI. The mean signal intensity ratios (SIRT1, SIRT2, SIRT2 FLAIR) of each region/masseter muscle were calculated. Differences in these ratios and ADC values between groups were compared, and the diagnostic efficacy was evaluated using receiver operating characteristic (ROC) curves, with DeLong's test applied to compare the differences in the area under the curve (AUC). The relationship between MR intensity ratios and maternal 75 g oral glucose tolerance test (OGTT) blood glucose levels was also observed.Results Compared with the HC group, the IDMs group showed reduced SIRT1 in the occipital lobe, globus pallidus, caudate nucleus, posterior limb of the internal capsule, ventrolateral thalamic nucleus, parietal lobe, frontal lobe, and centrum semiovale, as well as lower SIRT2 in all regions, and lower SIRT2 FLAIR in all regions except for the occipital lobe and posterior limb of the internal capsule. The ADC values in the temporal lobe were also lower (P<0.05). After stratified analysis, it was found that SIRT1 in the cerebellar hemisphere, posterior limb of the internal capsule, ventrolateral thalamic nucleus, and centrum semiovale, as well as SIRT2 in all regions, and SIRT2 FLAIR in all areas except for the occipital lobe and splenium of the corpus callosum in the IDMs A group were lower than in the control group. In the IDMs B group, SIRT1 in the frontal and parietal lobes, SIRT2 in all regions, and ADC values in the cerebellar hemisphere and temporal lobe were lower than those in the HC B group (P<0.05). ROC curve analysis showed that the AUC values for SIRT2 in all regions in the IDMs group were the highest, with SIRT2 in the temporal lobe demonstrating good diagnostic efficacy (AUC=0.702). DeLong's test indicated statistically significant differences in AUC values between SIRT2 and SIRT1, SIRT2 FLAIR, or ADC in the cerebellar hemisphere, hippocampus, temporal lobe, occipital lobe, posterior limb of the internal capsule, and parietal lobe (P<0.05). SIRT2 in all regions of the IDMs group was negatively correlated with 1-hour blood glucose levels from the OGTT (P<0.05).Conclusions The relative signal intensity ratios of T1WI, T2WI, and T2 FLAIR, along with ADC values, are useful for the early detection of neurodevelopmental abnormalities in IDMs. Among these, SIRT2 demonstrates a higher diagnostic efficacy.
[Keywords] infant of gestational diabetic mothers;brain development;magnetic resonance imaging;diffusion-weighted imaging;signal intensity ratio

SUN Fei1, 2   YU Jinhong2   LUO Hedan2, 3   MIAO Yanwei2*  

1 Department of Radiology, Dalian Women and Children Medical Group, Dalian116001, China

2 Department of Radiology, First Affiliated Hospital of Dalian Medical University, Dalian116011, China

3 Department of Radiology, Dalian Public Health Clinical Center, Dalian116031, China

Corresponding author: MIAO Y W, E-mail: ywmiao716@163.com

Conflicts of interest   None.

Received  2024-04-29
Accepted  2024-12-16
DOI: 10.12015/issn.1674-8034.2024.12.013
Cite this article as: SUN F, YU J H, LUO H D, et al. A semi-quantitative MRI study on brain developmental abnormalities in infants of gestational diabetic mothers[J]. Chin J Magn Reson Imaging, 2024, 15(12): 87-93. DOI:10.12015/issn.1674-8034.2024.12.013.

[1]
Obstetrics Science Group of Obstetrics and Gynecology Branch of Chinese Medical Association, Perinatal Medicine Branch of Chinese Medical Association, Pregnancy Combined with Diabetes Professional Committee of China Maternal and Child Health Care Association. Guideline of diagnosis and treatment of hyperglycemia in pregnancy (2022) [Part one][J]. Chinese Journal of Obstetrics and Gynecology, 2022, 57(1): 3-12. DOI: 10.3760/cma.j.cn112141-20210917-00528.
[2]
ELSAYED N A, ALEPPO G, BANNURU R R, et al. American Diabetes Association Professional Practice Committee. 2. Diagnosis and Classification of Diabetes: Standards of Care in Diabetes—2024[J]. Diabetes Care, 2024, 47(Supplement_1): S20-S42. DOI: 10.2337/dc24-S002.
[3]
SUN H, SAEEDI P, KARURANGA S, et al. IDF Diabetes Atlas: Global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045[J/OL]. Diabetes Res Clin Pract, 2022, 183: 109119 [2024-04-29]. https://pmc.ncbi.nlm.nih.gov/articles/PMC11057359/. DOI: 10.1016/j.diabres.2021.109119.
[4]
Chinese Diabetes Society. Guideline for the prevention and treatment of type 2 diabetes mellitus in China (2020 edition)[J]. Chinese Journal of Diabetes Mellitus, 2021, 13(4): 315-409. DOI: 10.3760/cma.j.cn115791-20210221-00095.
[5]
ELSAYED N A, ALEPPO G, BANNURU R R, et al. American Diabetes Association Professional Practice Committee. 15. Management of Diabetes in Pregnancy: Standards of Care in Diabetes—2024[J]. Diabetes Care, 2024, 47(Supplement_1): S282-S294. DOI: 10.2337/dc24-S015.
[6]
PREDA A, PĂDUREANU V, MOȚA M, et al. Analysis of maternal and neonatal complications in a group of patients with gestational diabetes mellitus[J/OL]. Medicina (Kaunas), 2021, 57(11): 1170 [2024-04-29]. https://doi.org/10.3390/medicina57111170. DOI: 10.3390/medicina57111170.
[7]
YE W, LUO C, HUANG J, et al. Gestational diabetes mellitus and adverse pregnancy outcomes: systematic review and meta-analysis[J/OL]. BMJ, 2022, 377: e067946 [2024-04-29]. https://pmc.ncbi.nlm.nih.gov/articles/PMC9131781/. DOI: 10.1136/bmj-2021-067946.
[8]
OLMOS-ORTIZ A, FLORES-ESPINOSA P, DIAZ L, et al. Immunoendocrine dysregulation during gestational diabetes mellitus: The central role of the placenta[J/OL]. Int J Mol Sci, 2021, 22(15): 8087 [2024-04-29]. https://doi.org/10.3390/ijms22158087. DOI: 10.3390/ijms22158087.
[9]
VUONG B, ODERO G, ROZBACHER S, et al. Exposure to gestational diabetes mellitus induces neuroinflammation, derangement of hippocampal neurons, and cognitive changes in rat offspring[J/OL]. J Neuroinflammation, 2017, 14(1): 80 [2024-04-29]. https://pubmed.ncbi.nlm.nih.gov/28388927/. DOI: 10.1186/s12974-017-0859-9.
[10]
ORNOY A, BECKER M, WEINSTEIN-FUDIM L, et al. Diabetes during pregnancy: A maternal disease complicating the course of pregnancy with long-term deleterious effects on the offspring. A clinical review[J/OL]. Int J Mol Sci, 2021, 22(6): 2965 [2024-04-29]. https://pmc.ncbi.nlm.nih.gov/articles/PMC5384149/. DOI: 10.3390/ijms22062965.
[11]
VALLE-BAUTISTA R, MARQUEZ-VALADEZ B, FRAGOSO-CABRERA A D, et al. Impaired cortical cytoarchitecture and reduced excitability of deep-layer neurons in the offspring of diabetic rats[J/OL]. Front Cell Dev Biol, 2020, 8: 564561 [2024-04-29]. https://pmc.ncbi.nlm.nih.gov/articles/PMC7527606/. DOI: 10.3389/fcell.2020.564561.
[12]
ROWLAND J, WILSON C A. The association between gestational diabetes and ASD and ADHD: a systematic review and meta-analysis[J/OL]. Sci Rep, 2021, 11(1): 5136 [2024-04-29]. https://pubmed.ncbi.nlm.nih.gov/33664319/. DOI: 10.1038/s41598-021-84573-3.
[13]
ZHANG D, ZHAO X, XING Q N, et al. Synthetic MRI in evaluation on abnormal brain development in offspring of pregnant women with gestational hypertension[J]. Chin J Med Imaging Technol, 2022, 38(11): 1601-1605. DOI: 10.13929/j.issn.1003-3289.2022.11.001.
[14]
YILDIZ ATAR H, BAATZ J E, RYAN R M. Molecular mechanisms of maternal diabetes effects on fetal and neonatal surfactant[J/OL]. Children (Basel), 2021, 8(4): 281 [2024-04-29]. https://pmc.ncbi.nlm.nih.gov/articles/PMC8067463/. DOI: 10.3390/children8040281.
[15]
SALMASO N, JABLONSKA B, SCAFIDI J, et al. Neurobiology of premature brain injury[J]. Nat Neurosci, 2014, 17(3): 341-346. DOI: 10.1038/nn.3604.
[16]
RAY G W, ZENG Q, KUSI P, et al. Genetic and inflammatory factors underlying gestational diabetes mellitus: a review[J/OL]. Front Endocrinol (Lausanne), 2024, 15: 1399694 [2024-04-29]. https://pmc.ncbi.nlm.nih.gov/articles/PMC11061502/. DOI: 10.3389/fendo.2024.1399694.
[17]
VERNER A M, MANDERSON J, LAPPIN T R, et al. Influence of maternal diabetes mellitus on fetal iron status[J/OL]. Arch Dis Child Fetal Neonatal Ed, 2007, 92(5): F399-401 [2024-04-29]. https://pubmed.ncbi.nlm.nih.gov/17095546/. DOI: 10.1136/adc.2006.097279.
[18]
KRUSE M S, BARUTTA J, VEGA M C, et al. Down regulation of the proliferation and apoptotic pathways in the embryonic brain of diabetic rats[J]. Cell Mol Neurobiol, 2012, 32(6): 1031-1037. DOI: 10.1007/s10571-012-9820-8.
[19]
RODOLAKI K, PERGIALIOTIS V, IAKOVIDOU N, et al. The impact of maternal diabetes on the future health and neurodevelopment of the offspring: a review of the evidence[J/OL]. Front Endocrinol (Lausanne), 2023, 14: 1125628 [2024-04-29]. https://pmc.ncbi.nlm.nih.gov/articles/PMC10352101/. DOI: 10.3389/fendo.2023.1125628.
[20]
KONAR A S, PAUDYAL R, SHAH A D, et al. Qualitative and quantitative performance of magnetic resonance image compilation (MAGiC) method: An exploratory analysis for head and neck imaging[J/OL]. Cancers (Basel), 2022, 14(15): 3624 [2024-04-29]. https://pmc.ncbi.nlm.nih.gov/articles/PMC9331960/. DOI: 10.3390/cancers14153624.
[21]
ZH C W, ZHAO X, LIU Y C, et al. Initial application of synthetic MRI in evaluating brain maturation of preterm infants[J]. Chin J Magn Reson Imaging, 2021, 12(12): 1-5. DOI: 10.12015/issn.1674-8034.2021.12.001.
[22]
MILOS R I, SCHMIDBAUER V, WATZENBOECK M L, et al. T1-weighted fast fluid-attenuated inversion-recovery sequence (T1-FFLAIR) enables the visualization and quantification of fetal brain myelination in utero[J]. Eur Radiol, 2024, 34(7): 4573-4584. DOI: 10.1007/s00330-023-10401-z.
[23]
CACCIATORE M, GRASSO E A, TRIPODI R, et al. Impact of glucose metabolism on the developing brain[J/OL]. Front Endocrinol (Lausanne), 2022, 13: 1047545 [2024-04-29]. https://pmc.ncbi.nlm.nih.gov/articles/PMC9816389/. DOI: 10.3389/fendo.2022.1047545.
[24]
PAREDES M F, JAMES D, GIL-PEROTIN S, et al. Extensive migration of young neurons into the infant human frontal lobe[J/OL]. Science, 2016, 354(6308): aaf7073 [2024-04-29]. https://pmc.ncbi.nlm.nih.gov/articles/PMC5436574/. DOI: 10.1126/science.aaf7073.
[25]
MAURAS N, MAZAIKA P, BUCKINGHAM B, et al. Longitudinal assessment of neuroanatomical and cognitive differences in young children with type 1 diabetes: association with hyperglycemia[J]. Diabetes, 2015, 64(5): 1770-1779. DOI: 10.2337/db14-1445.
[26]
LINDSAY K L, BUSS C, WADHWA P D, et al. The interplay between nutrition and stress in pregnancy: Implications for fetal programming of brain development[J]. Biol Psychiatry, 2019, 85(2): 135-149. DOI: 10.1016/j.biopsych.2018.06.021.
[27]
LETISSIER C, CROMBE A, CHERIER L, et al. Brain fetal magnetic resonance imaging to evaluate maturation of normal white matter during the third trimester of pregnancy[J]. Pediatr Radiol, 2021, 51(10): 1826-1838. DOI: 10.1007/s00247-021-05064-1.
[28]
HASEGAWA Y, FORMATO J E, LATOUR L L, et al. Severe transient hypoglycemia causes reversible change in the apparent diffusion coefficient of water[J]. Stroke, 1996, 27(9): 1648-1655; discussion 1655-1656. DOI: 10.1161/01.str.27.9.1648.
[29]
LUO S, HSU E, LAWRENCE K E, et al. Associations among prenatal exposure to gestational diabetes mellitus, brain structure, and child adiposity markers[J]. Obesity (Silver Spring), 2023, 31(11): 2699-2708. DOI: 10.1002/oby.23901.
[30]
DENISON F C, MACNAUGHT G, SEMPLE S I K, et al. Brain development in fetuses of mothers with diabetes: A case-control MR imaging study[J]. AJNR Am J Neuroradiol, 2017, 38(5): 1037-1044. DOI: 10.3174/ajnr.A5118.
[31]
TAM E W, WIDJAJA E, BLASER S I, et al. Occipital lobe injury and cortical visual outcomes after neonatal hypoglycemia[J]. Pediatrics, 2008, 122(3): 507-512. DOI: 10.1542/peds.2007-2002.
[32]
ZHANG Y, CHEN D, JI Y, et al. Dynamic magnetic resonance imaging findings in the early stages of neonatal hypoglycemic brain injury[J]. Eur J Pediatr, 2022, 181(12): 4167-4174. DOI: 10.1007/s00431-022-04637-y.
[33]
DE WAEL R VOS, ROYER J, TAVAKOL S, etal. Structural connectivity gradients of the temporal lobe serve as multiscale axes of brain organization and cortical evolution[J]. Cereb Cortex, 2021, 31(11): 5151-5164. DOI: 10.1093/cercor/bhab149.
[34]
BURNS C M, RUTHERFORD M A, BOARDMAN J P, et al. Patterns of cerebral injury and neurodevelopmental outcomes after symptomatic neonatal hypoglycemia[J]. Pediatrics, 2008, 122(1): 65-74. DOI: 10.1542/peds.2007-2822.
[35]
YALCIN E U, GENC H M, BAYHAN A, et al. Neurodevelopmental outcome in patients with typical imaging features of injury as a result of neonatal hypoglycemia[J]. Noro Psikiyatr Ars, 2022, 59(4): 296-302. DOI: 10.29399/npa.27997.
[36]
YU M, GAO X, NIU X, et al. Meta-analysis of structural and functional alterations of brain in patients with attention-deficit/hyperactivity disorder[J/OL]. Front Psychiatry, 2022, 13: 1070142 [2024-04-29]. https://pmc.ncbi.nlm.nih.gov/articles/PMC9853532/. DOI: 10.3389/fpsyt.2022.1070142.
[37]
UNTERBERGER I, BAUER R, WALSER G, et al. Corpus callosum and epilepsies[J]. Seizure, 2016, 37: 55-60. DOI: 10.1016/j.seizure.2016.02.012.
[38]
MONTASSIR H, MAEGAKI Y, OHNO K, et al. Long term prognosis of symptomatic occipital lobe epilepsy secondary to neonatal hypoglycemia[J]. Epilepsy Res, 2010, 88(2-3): 93-99. DOI: 10.1016/j.eplepsyres.2009.10.001
[39]
MUDD A T, FIL J E, KNIGHT L C, et al. Early-life iron deficiency reduces brain iron content and alters brain tissue composition despite iron repletion: A neuroimaging assessment[J/OL]. Nutrients, 2018, 10(2): 135 [2024-04-29]. https://pmc.ncbi.nlm.nih.gov/articles/PMC5852711/. DOI: 10.3390/nu10020135.
[40]
LIU Y, ZHU Z J, CAO M M, et al. Early brain overgrowth in children with autism spectrum disorders based on structural magnetic resonance imaging[J]. Chin J Magn Reson Imaging, 2020, 11(4): 264-269. DOI: 10.12015/issn.1674-8034.2020.04.005.
[41]
COURCHESNE E, PRESS G A, YEUNG-COURCHESNE R. Parietal lobe abnormalities detected with MR in patients with infantile autism[J]. AJR Am J Roentgenol, 1993, 160(2): 387-393. DOI: 10.2214/ajr.160.2.8424359.
[42]
SCHOLTENS D M, KUANG A, LOWE L P, et al. Hyperglycemia and adverse pregnancy outcome follow-up study (HAPO FUS): Maternal glycemia and childhood glucose metabolism[J]. Diabetes Care, 2019, 42(3): 381-392. DOI: 10.2337/dc18-2021.
[43]
TOMLINSON D R, GARDINER N J. Glucose neurotoxicity[J]. Nat Rev Neurosci, 2008, 9(1): 36-45. DOI: 10.1038/nrn2294.

PREV Preliminary study on different stages of Parkinson,s Disease combined with amide proton transfer imaging and quantitative susceptibility mapping
NEXT Combined analysis based on the characteristics of intracranial atherosclerotic plaque and apparent diffusion coefficient histogram in predicting the recurrence of ischemic stroke
  



Tel & Fax: +8610-67113815    E-mail: editor@cjmri.cn