Brain Development in Fetuses of Mothers with Diabetes: A Case-Control MR Imaging Study

REFERENCES

1. 1.↵
   2. Mitanchez D,
   3. Yzydorczyk C,
   4. Siddeek B, et al

   . The offspring of the diabetic mother: short- and long-term implications. Best Pract Res Clin Obstet Gynaecol 2015;29:256–69 doi:10.1016/j.bpobgyn.2014.08.004 pmid:25267399

   CrossRefPubMed
2. 2.↵
   2. Bolaños L,
   3. Matute E,
   4. Ramírez-Dueñas Mde L, et al

   . Neuropsychological impairment in school-aged children born to mothers with gestational diabetes. J Child Neurol 2015;30:1616–24 doi:10.1177/0883073815575574 pmid:25814475

   CrossRefPubMed
3. 3.↵
   2. Stehbens JA,
   3. Baker GL,
   4. Kitchell M

   . Outcome at ages 1, 3, and 5 years of children born to diabetic women. Am J Obstet Gynecol 1977;127:408–13 doi:10.1016/0002-9378(77)90499-9 pmid:835641

   CrossRefPubMedWeb of Science
4. 4.↵
   2. Nomura Y,
   3. Marks DJ,
   4. Grossman B, et al

   . Exposure to gestational diabetes mellitus and low socioeconomic status: effects on neurocognitive development and risk of attention-deficit/hyperactivity disorder in offspring. Arch Pediatr Adolesc Med 2012;166:337–43 doi:10.1001/archpediatrics.2011.784 pmid:22213602

   CrossRefPubMedWeb of Science
5. 5.↵
   2. Temple RC,
   3. Hardiman M,
   4. Pellegrini M, et al

   . Cognitive function in 6- to 12-year-old offspring of women with Type 1 diabetes. Diabet Med 2011;28:845–48 doi:10.1111/j.1464-5491.2011.03285.x pmid:21395676

   CrossRefPubMed
6. 6.↵
   2. Dionne G,
   3. Boivin M,
   4. Séguin JR, et al

   . Gestational diabetes hinders language development in offspring. Pediatrics 2008;122:e1073–79 doi:10.1542/peds.2007-3028 pmid:18977957

   Abstract/FREE Full Text
7. 7.↵
   2. Kalhan S,
   3. Parimi P

   . Gluconeogenesis in the fetus and neonate. Semin Perinatol 2000;24:94–106 doi:10.1053/sp.2000.6360 pmid:10805165

   CrossRefPubMedWeb of Science
8. 8.↵
   2. Pagán A,
   3. Prieto-Sánchez MT,
   4. Blanco-Carnero JE, et al

   . Materno-fetal transfer of docosahexaenoic acid is impaired by gestational diabetes mellitus. Am J Physiol Endocrinol Metab 2013;305:E826–33 doi:10.1152/ajpendo.00291.2013 pmid:23921142

   Abstract/FREE Full Text
9. 9.↵
   2. Larqué E,
   3. Demmelmair H,
   4. Gil-Sánchez A, et al

   . Placental transfer of fatty acids and fetal implications. Am J Clin Nutr 2011;94(6 suppl):1908S–13S doi:10.3945/ajcn.110.001230 pmid:21562082

   Abstract/FREE Full Text
10. 10.↵
    2. Limperopoulos C,
    3. Tworetzky W,
    4. McElhinney DB, et al

    . Brain volume and metabolism in fetuses with congenital heart disease: evaluation with quantitative magnetic resonance imaging and spectroscopy. Circulation 2010;121:26–33 doi:10.1161/CIRCULATIONAHA.109.865568 pmid:20026783

    Abstract/FREE Full Text
11. 11.↵
    2. Hoffmann C,
    3. Grossman R,
    4. Bokov I, et al

    . Effect of cytomegalovirus infection on temporal lobe development in utero: quantitative MRI studies. Eur Neuropsychopharmacol 2010;20:848–54 doi:10.1016/j.euroneuro.2010.08.006 pmid:20833515

    CrossRefPubMed
12. 12.↵
    2. Erdem G,
    3. Celik O,
    4. Hascalik S, et al

    . Diffusion-weighted imaging evaluation of subtle cerebral microstructural changes in intrauterine fetal hydrocephalus. Magn Reson Imaging 2007;25:1417–22 doi:10.1016/j.mri.2007.03.028 pmid:17513078

    CrossRefPubMed
13. 13.↵
    2. Pier DB,
    3. Levine D,
    4. Kataoka ML, et al

    . Magnetic resonance volumetric assessments of brains in fetuses with ventriculomegaly correlated to outcomes. J Ultrasound Med 2011;30:595–603 doi:10.7863/jum.2011.30.5.595 pmid:21527607

    Abstract/FREE Full Text
14. 14.↵
    2. Egaña-Ugrinovic G,
    3. Sanz-Cortes M,
    4. Figueras F, et al

    . Fetal MRI insular cortical morphometry and its association with neurobehavior in late-onset small-for-gestational-age fetuses. Ultrasound Obstet Gynecol 2014;44:322–29 doi:10.1002/uog.13360 pmid:24616027

    CrossRefPubMed
15. 15.↵
    2. Masoller N,
    3. Sanz-Cortés M,
    4. Crispi F, et al

    . Severity of fetal brain abnormalities in congenital heart disease in relation to the main expected pattern of in utero brain blood supply. Fetal Diagn Ther 2016;39:269–78 doi:10.1159/000439527 pmid:26613580

    CrossRefPubMed
16. 16.↵
    2. Sanz Cortes M,
    3. Bargallo N,
    4. Arranz A, et al

    . Feasibility and success rate of a fetal MRI and MR spectroscopy research protocol performed at term using a 3.0-Tesla scanner. Fetal Diagn Ther 2016 May 27. [Epub ahead of print] doi:10.1159/000445947 pmid:27230519

    CrossRefPubMed
17. 17.↵
    2. Sanz-Cortes M,
    3. Egaña-Ugrinovic G,
    4. Simoes RV, et al

    . Association of brain metabolism with sulcation and corpus callosum development assessed by MRI in late-onset small fetuses. Am J Obstet Gynecol 2015;212:804 e1–8 doi:10.1016/j.ajog.2015.01.041 pmid:25640049

    CrossRefPubMed
18. 18.↵
    2. Sanz-Cortes M,
    3. Simoes RV,
    4. Bargallo N, et al

    . Proton magnetic resonance spectroscopy assessment of fetal brain metabolism in late-onset ‘small for gestational age’ versus ‘intrauterine growth restriction’ fetuses. Fetal Diagn Ther 2015;37:108–16 doi:10.1159/000365102 pmid:25115414

    CrossRefPubMed
19. 19.↵
    2. Simões RV,
    3. Sanz-Cortes M,
    4. Muñoz-Moreno E, et al

    . Feasibility and technical features of fetal brain magnetic resonance spectroscopy in 1.5 T scanners. Am J Obstet Gynecol 2015;213:741–42 doi:10.1016/j.ajog.2015.06.033 pmid:26116100

    CrossRefPubMed
20. 20.↵
    2. Taylor-Clarke M

    . Re: mid-gestation brain Doppler and head biometry in fetuses with congenital heart disease predict abnormal brain development at birth. N. Masoller, M. Sanz-Cortés, F. Crispi, O. Gómez, M. Bennasar, G. Egaña-Ugrinovic, N. Bargalló, J. M. Martínez and E. Gratacós. Ultrasound Obstet Gynecol 2016; 47: 65–73. Ultrasound Obstet Gynecol 2016;47:15 doi:10.1002/uog.15825 pmid:26731037

    CrossRefPubMed
21. 21.↵
    2. Victoria T,
    3. Johnson AM,
    4. Edgar JC, et al

    . Comparison between 1.5-T and 3-T MRI for fetal imaging: is there an advantage to imaging with a higher field strength? AJR Am J Roentgenol 2016;206:195–201 doi:10.2214/AJR.14.14205 pmid:26700352

    CrossRefPubMed
22. 22.↵
    2. Van Kooij BJ,
    3. Benders MJ,
    4. Anbeek P, et al

    . Cerebellar volume and proton magnetic resonance spectroscopy at term, and neurodevelopment at 2 years of age in preterm infants. Dev Med Child Neurol 2012;54:260–66 doi:10.1111/j.1469-8749.2011.04168.x pmid:22211363

    CrossRefPubMed
23. 23.↵
    2. Hanrahan JD,
    3. Cox IJ,
    4. Azzopardi D, et al

    . Relation between proton magnetic resonance spectroscopy within 18 hours of birth asphyxia and neurodevelopment at 1 year of age. Dev Med Child Neurol 1999;41:76–82 doi:10.1017/S0012162299000171 pmid:10075092

    CrossRefPubMedWeb of Science
24. 24.↵
    2. Amess PN,
    3. Penrice J,
    4. Wylezinska M, et al

    . Early brain proton magnetic resonance spectroscopy and neonatal neurology related to neurodevelopmental outcome at 1 year in term infants after presumed hypoxic-ischaemic brain injury. Dev Med Child Neurol 1999;41:436–45 pmid:10454226

    CrossRefPubMedWeb of Science
25. 25.↵
    2. Filippi CG,
    3. Uluğ AM,
    4. Deck MD, et al

    . Developmental delay in children: assessment with proton MR spectroscopy. AJNR Am J Neuroradiol 2002;23:882–88 pmid:12006297

    Abstract/FREE Full Text
26. 26.↵
    2. Counsell SJ,
    3. Allsop JM,
    4. Harrison MC, et al

    . Diffusion-weighted imaging of the brain in preterm infants with focal and diffuse white matter abnormality. Pediatrics 2003;112(1 pt 1):1–7 doi:10.1542/peds.112.1.1 pmid:12837859

    Abstract/FREE Full Text
27. 27.↵
    2. Cavalleri F,
    3. Lugli L,
    4. Pugliese M, et al

    . Prognostic value of diffusion-weighted imaging summation scores or apparent diffusion coefficient maps in newborns with hypoxic-ischemic encephalopathy. Pediatr Radiol 2014;44:1141–54 doi:10.1007/s00247-014-2945-9 pmid:24715056

    CrossRefPubMed
28. 28.↵
    2. Rutherford M,
    3. Biarge MM,
    4. Allsop , et al

    . MRI of perinatal brain injury. Pediatr Radiol 2010;40:819–33 doi:10.1007/s00247-010-1620-z pmid:20432000

    CrossRefPubMed
29. 29.↵
    2. Boardman JP,
    3. Counsell SJ,
    4. Rueckert D, et al

    . Early growth in brain volume is preserved in the majority of preterm infants. Ann Neurol 2007;62:185–92 doi:10.1002/ana.21171 pmid:17696128

    CrossRefPubMedWeb of Science
30. 30.↵
    2. Inder TE,
    3. Warfield SK,
    4. Wang H, et al

    . Abnormal cerebral structure is present at term in premature infants. Pediatrics 2005;115:286–94 doi:10.1542/peds.2004-0326 pmid:15687434

    Abstract/FREE Full Text
31. 31.↵
    2. Boardman JP,
    3. Craven C,
    4. Valappil S, et al

    . A common neonatal image phenotype predicts adverse neurodevelopmental outcome in children born preterm. Neuroimage 2010;52:409–14 doi:10.1016/j.neuroimage.2010.04.261 pmid:20451627

    CrossRefPubMedWeb of Science
32. 32.↵
    2. Ullman H,
    3. Spencer-Smith M,
    4. Thompson DK, et al

    . Neonatal MRI is associated with future cognition and academic achievement in preterm children. Brain 2015;138(pt 11):3251–62 doi:10.1093/brain/awv244 pmid:26329284

    Abstract/FREE Full Text
33. 33.↵
    Scottish Intercollegiate Guidelines Network. Management of diabetes: a national clinical guideline, 2014. Edinburgh. http://www.sign.ac.uk/pdf/sign116.pdf. Accessed May 30, 2016.
34. 34.↵
    2. Macnaught G,
    3. Gray C,
    4. Walker J, et al

    . (1)H MRS: a potential biomarker of in utero placental function. NMR Biomed 2015;28:1275–82 doi:10.1002/nbm.3370 pmid:26313636

    CrossRefPubMed
35. 35.↵
    2. Ratiney H,
    3. Sdika M,
    4. Coenradie Y, et al

    . Time-domain semi-parametric estimation based on a metabolite basis set. NMR Biomed 2005;18:1–13 doi:10.1002/nbm.895 pmid:15660450

    CrossRefPubMedWeb of Science
36. 36.↵
    2. Horton MK,
    3. Margolis AE,
    4. Tang C, et al

    . Neuroimaging is a novel tool to understand the impact of environmental chemicals on neurodevelopment. Curr Opin Pediatr 2014;26:230–36 doi:10.1097/MOP.0000000000000074 pmid:24535497

    CrossRefPubMed
37. 37.↵
    2. Spader HS,
    3. Ellermeier A,
    4. O'Muircheartaigh J, et al

    . Advances in myelin imaging with potential clinical application to pediatric imaging. Neurosurg Focus 2013;34:E9 doi:10.3171/2013.1.FOCUS12426 pmid:23544415

    CrossRefPubMed
38. 38.↵
    2. Boardman JP,
    3. Counsell SJ,
    4. Rueckert D, et al

    . Abnormal deep grey matter development following preterm birth detected using deformation-based morphometry. Neuroimage 2006;32:70–78 doi:10.1016/j.neuroimage.2006.03.029 pmid:16675269

    CrossRefPubMedWeb of Science
39. 39.↵
    2. Rousseau F,
    3. Oubel E,
    4. Pontabry J, et al

    . BTK: an open-source toolkit for fetal brain MR image processing. Comput Methods Programs Biomed 2013;109:65–73 doi:10.1016/j.cmpb.2012.08.007 pmid:23036854

    CrossRefPubMed
40. 40.↵
    2. Serag A,
    3. Aljabar P,
    4. Ball G, et al

    . Construction of a consistent high-definition spatio-temporal atlas of the developing brain using adaptive kernel regression. Neuroimage 2012;59:2255–65 doi:10.1016/j.neuroimage.2011.09.062 pmid:21985910

    CrossRefPubMedWeb of Science
41. 41.↵
    2. Serag A,
    3. Kyriakopoulou V,
    4. Rutherford MA, et al

    . A multi-channel 4D probabilistic atlas of the developing brain: application to fetuses and neonates. Ann BMVA 2012;2012:1–14. http://www.bmva.org/annals/2012/2012-0003.pdf.
42. 42.↵
    2. Billingham SA,
    3. Whitehead AL,
    4. Julious SA

    . An audit of sample sizes for pilot and feasibility trials being undertaken in the United Kingdom registered in the United Kingdom Clinical Research Network database. BMC Med Res Methodol 2013;13:104 doi:10.1186/1471-2288-13-104 pmid:23961782

    CrossRefPubMed
43. 43.↵
    2. Whitehead AL,
    3. Julious SA,
    4. Cooper CL, et al

    . Estimating the sample size for a pilot randomised trial to minimise the overall trial sample size for the external pilot and main trial for a continuous outcome variable. Stat Methods Med Res 2016;25:1057–73 doi:10.1177/0962280215588241 pmid:26092476

    CrossRefPubMed
44. 44.↵
    2. Santhakumari R,
    3. Reddy IY,
    4. Archana R

    . Effect of type 2 diabetes mellitus on brain metabolites by using proton magnetic resonance spectroscopy: a systematic review. Int J Pharma Bio Sci 2014;5:1118–23 pmid:25568610

    PubMed
45. 45.↵
    2. Cannie M,
    3. De Keyzer F,
    4. Meersschaert J, et al

    . A diffusion-weighted template for gestational age-related apparent diffusion coefficient values in the developing fetal brain. Ultrasound Obstet Gynecol 2007;30:318–24 doi:10.1002/uog.4078 pmid:17688307

    CrossRefPubMed
46. 46.↵
    2. Kok RD,
    3. van den Berg PP,
    4. van den Bergh AJ, et al

    . Maturation of the human fetal brain as observed by 1H MR spectroscopy. Magn Reson Med 2002;48:611–16 doi:10.1002/mrm.10264 pmid:12353277

    CrossRefPubMedWeb of Science
47. 47.↵
    2. Righini A,
    3. Bianchini E,
    4. Parazzini C, et al

    . Apparent diffusion coefficient determination in normal fetal brain: a prenatal MR imaging study. AJNR Am J Neuroradiol 2003;24:799–804 pmid:12748074

    Abstract/FREE Full Text
48. 48.↵
    2. Wardlaw JM,
    3. Brindle W,
    4. Casado AM, et al

    ; SINAPSE Collaborative Group. A systematic review of the utility of 1.5 versus 3 Tesla magnetic resonance brain imaging in clinical practice and research. Eur Radiol 2012;22:2295–303 doi:10.1007/s00330-012-2500-8 pmid:22684343

    CrossRefPubMed
49. 49.↵
    2. Alvarez-Linera J

    . 3T MRI: advances in brain imaging. Eur J Radiol 2008;67:415–26 doi:10.1016/j.ejrad.2008.02.045 pmid:18455895

    CrossRefPubMedWeb of Science
50. 50.↵
    2. Azzopardi D,
    3. Robertson NJ,
    4. Bainbridge A, et al

    . Moderate hypothermia within 6 h of birth plus inhaled xenon versus moderate hypothermia alone after birth asphyxia (TOBY-Xe): a proof-of-concept, open-label, randomised controlled trial. Lancet Neurol 2015 Dec 18. [Epub ahead of print] doi:10.1016/S1474-4422(15)00347-6 pmid:26708675

    CrossRefPubMed