Skip to main content
Erschienen in: European Radiology 3/2019

27.08.2018 | Paediatric

Proper timing for the evaluation of neonatal brain white matter development: a diffusion tensor imaging study

verfasst von: Chao Jin, Yanyan Li, Xianjun Li, Miaomiao Wang, Congcong Liu, Jie Gao, Qinli Sun, Deqiang Qiu, Lingxia Zeng, Xihui Zhou, Gailian Li, Jinni Zhang, Jie Zheng, Jian Yang

Erschienen in: European Radiology | Ausgabe 3/2019

Einloggen, um Zugang zu erhalten

Abstract

Objective

We aimed to determine the timing for assessing birth status of the developing brain (i.e. brain maturity at birth) by exploring the postnatal age-related changes in neonatal brain white matter (WM).

Methods

The institutional review board approved this study and all informed parental consents were obtained. 133 neonates (gestational age, 30–42 weeks) without abnormalities on MRI were studied with regard to WM development by diffusion tensor imaging-derived fractional anisotropy (FA). Tract-based spatial statistics (TBSS), locally-weighted scatterplot smoothing (LOESS) and piecewise linear-fitting were used to investigate the relationship between FA and postnatal age. FA along corticospinal tract (CST), optic radiation (OR), auditory radiation (AR) and thalamus-primary somatosensory cortex (thal-PSC) were extracted by automated fibre-tract quantification; their differences and associations with neonatal neurobehavioural scores at various postnatal age ranges were analysed by Wilcoxon’s rank-sum test and Pearson’s correlation.

Results

Using TBSS, postnatal age (days 1–28) positively correlated with FA in multiple WMs, including CST, OR, AR and thal-PSC (p<0.05). On the other hand, when narrowing the postnatal age window to days 1–14, no significant correlation was found, suggesting a biphasic WM development. LOESS and piecewise linear-fitting indicated that FA increased mildly before day 14 and its growth accelerated thereafter. Both FA and correlations with neurobehavioural scores in postnatal age range 2 (days 15–28) were significantly higher than in range 1 (days 1–14) (FA comparison: p<0.05; maximal correlation-coefficient: 0.693 vs. 0.169).

Conclusion

Brain WM development during the neonatal stage includes two phases, i.e. a close-to-birth period within the first 14 days and a following accelerated maturation period. Therefore, evaluations of birth status should preferably be performed during the first period.

Key Points

• Brain white matter development within the first two postnatal weeks resembles a close-to-birth maturation.
• Brain white matter development in the audio-visual, sensorimotor regions accelerates after two postnatal weeks.
• Postnatal age-related effects should be considered in comparing preterm and term neonates.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
2.
Zurück zum Zitat Buonocore G, Bracci R, Weindling M (2012) Neonatology. Springer, MilanoCrossRef Buonocore G, Bracci R, Weindling M (2012) Neonatology. Springer, MilanoCrossRef
3.
Zurück zum Zitat Dubois J, Dehaene-Lambertz G, Perrin M et al (2008) Asynchrony of the early maturation of white matter bundles in healthy infants: quantitative landmarks revealed noninvasively by diffusion tensor imaging. Hum Brain Mapp 29:14–27CrossRefPubMed Dubois J, Dehaene-Lambertz G, Perrin M et al (2008) Asynchrony of the early maturation of white matter bundles in healthy infants: quantitative landmarks revealed noninvasively by diffusion tensor imaging. Hum Brain Mapp 29:14–27CrossRefPubMed
4.
Zurück zum Zitat Huang H, Zhang J, Wakana S et al (2006) White and gray matter development in human fetal, newborn and pediatric brains. Neuroimage 33:27–38CrossRefPubMed Huang H, Zhang J, Wakana S et al (2006) White and gray matter development in human fetal, newborn and pediatric brains. Neuroimage 33:27–38CrossRefPubMed
5.
6.
Zurück zum Zitat Stoll BJ, Hansen NI, Bell EF et al (2015) Trends in care practices, morbidity, and mortality of extremely preterm neonates, 1993-2012. JAMA 314:1039–1051CrossRefPubMedPubMedCentral Stoll BJ, Hansen NI, Bell EF et al (2015) Trends in care practices, morbidity, and mortality of extremely preterm neonates, 1993-2012. JAMA 314:1039–1051CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat Patel RM, Kandefer S, Walsh MC et al (2015) Causes and timing of death in extremely premature infants from 2000 through 2011. N Engl J Med 372:331–340CrossRefPubMedPubMedCentral Patel RM, Kandefer S, Walsh MC et al (2015) Causes and timing of death in extremely premature infants from 2000 through 2011. N Engl J Med 372:331–340CrossRefPubMedPubMedCentral
8.
Zurück zum Zitat Plaisier A, Govaert P, Lequin MH, Dudink J (2014) Optimal timing of cerebral MRI in preterm infants to predict long-term neurodevelopmental outcome: a systematic review. AJNR Am J Neuroradiol 35:841–847 Plaisier A, Govaert P, Lequin MH, Dudink J (2014) Optimal timing of cerebral MRI in preterm infants to predict long-term neurodevelopmental outcome: a systematic review. AJNR Am J Neuroradiol 35:841–847
9.
Zurück zum Zitat Smyser CD, Kidokoro H, Inder TE (2012) MRI of the brain at term equivalent age in extremely premature neonates - to scan or not to scan? J Paediatr Child Health 48:794–800CrossRefPubMedPubMedCentral Smyser CD, Kidokoro H, Inder TE (2012) MRI of the brain at term equivalent age in extremely premature neonates - to scan or not to scan? J Paediatr Child Health 48:794–800CrossRefPubMedPubMedCentral
10.
Zurück zum Zitat de Bruïne FT, van den Berg-Huysmans AA, Leijser LM et al (2011) Clinical implications of MR imaging findings in the white matter in very preterm infants: a 2-year follow-up study. Radiology 261:899–906CrossRefPubMed de Bruïne FT, van den Berg-Huysmans AA, Leijser LM et al (2011) Clinical implications of MR imaging findings in the white matter in very preterm infants: a 2-year follow-up study. Radiology 261:899–906CrossRefPubMed
11.
Zurück zum Zitat Dubois J, Dehaene-Lambertz G, Kulikova S, Poupon C, Hüppi PS, Hertz-Pannier L (2014) The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience 276:48–71 Dubois J, Dehaene-Lambertz G, Kulikova S, Poupon C, Hüppi PS, Hertz-Pannier L (2014) The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience 276:48–71
12.
Zurück zum Zitat Tauber H, Waehneldt TV, Neuhoff V (1980) Myelination in rabbit optic nerves is accelerated by artificial eye opening. Neurosci Lett 16:235–238CrossRefPubMed Tauber H, Waehneldt TV, Neuhoff V (1980) Myelination in rabbit optic nerves is accelerated by artificial eye opening. Neurosci Lett 16:235–238CrossRefPubMed
13.
Zurück zum Zitat Berman JI, Glass HC, Miller SP et al (2009) Quantitative fiber tracking analysis of the optic radiation correlated with visual performance in premature newborns. AJNR Am J Neuroradiol 30:120–124CrossRefPubMedPubMedCentral Berman JI, Glass HC, Miller SP et al (2009) Quantitative fiber tracking analysis of the optic radiation correlated with visual performance in premature newborns. AJNR Am J Neuroradiol 30:120–124CrossRefPubMedPubMedCentral
14.
Zurück zum Zitat Broekman BF, Wang C, Li Y et al (2014) Gestational age and neonatal brain microstructure in term born infants: a birth cohort study. PLoS One 9:e115229CrossRefPubMedPubMedCentral Broekman BF, Wang C, Li Y et al (2014) Gestational age and neonatal brain microstructure in term born infants: a birth cohort study. PLoS One 9:e115229CrossRefPubMedPubMedCentral
15.
Zurück zum Zitat Partridge SC, Mukherjee P, Henry RG et al (2004) Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns. Neuroimage 22:1302–1314CrossRefPubMed Partridge SC, Mukherjee P, Henry RG et al (2004) Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns. Neuroimage 22:1302–1314CrossRefPubMed
16.
Zurück zum Zitat Mukherjee P, McKinstry RC (2006) Diffusion tensor imaging and tractography of human brain development. Neuroimaging Clin N Am 16:19–43CrossRefPubMed Mukherjee P, McKinstry RC (2006) Diffusion tensor imaging and tractography of human brain development. Neuroimaging Clin N Am 16:19–43CrossRefPubMed
17.
Zurück zum Zitat Hüppi PS, Dubois J (2006) Diffusion tensor imaging of brain development. Semin Fetal Neonatal Med 11:489–497CrossRefPubMed Hüppi PS, Dubois J (2006) Diffusion tensor imaging of brain development. Semin Fetal Neonatal Med 11:489–497CrossRefPubMed
18.
Zurück zum Zitat [No authors listed] (1992) American Academy of Pediatrics Committee on Drugs: Guidelines for monitoring and management of pediatric patients during and after sedation for diagnostic and therapeutic procedures. Pediatrics 89:1110–1115 [No authors listed] (1992) American Academy of Pediatrics Committee on Drugs: Guidelines for monitoring and management of pediatric patients during and after sedation for diagnostic and therapeutic procedures. Pediatrics 89:1110–1115
19.
Zurück zum Zitat Bao XL, Yu RJ, Li ZS, Zhang BL (1991) Twenty-item behavioral neurological assessment for normal newborns in 12 cities of China. Chin Med J (Eng) 104:742–746 Bao XL, Yu RJ, Li ZS, Zhang BL (1991) Twenty-item behavioral neurological assessment for normal newborns in 12 cities of China. Chin Med J (Eng) 104:742–746
20.
Zurück zum Zitat Dubowitz LMS, Dubowitz V, Mercuri E (1999) The neurological assessment of the preterm and full-term newborn infant, 2nd edn. Mac Keith Press, London Dubowitz LMS, Dubowitz V, Mercuri E (1999) The neurological assessment of the preterm and full-term newborn infant, 2nd edn. Mac Keith Press, London
21.
Zurück zum Zitat Fortin JP, Parker D, Tunç B et al (2017) Harmonization of multi-site diffusion tensor imaging data. Neuroimage 161:149–170CrossRefPubMed Fortin JP, Parker D, Tunç B et al (2017) Harmonization of multi-site diffusion tensor imaging data. Neuroimage 161:149–170CrossRefPubMed
22.
Zurück zum Zitat Li X, Gao J, Wang M, Wan M, Yang J (2016) Rapid and reliable tract-based spatial statistics pipeline for diffusion tensor imaging in the neonatal brain: applications to the white matter development and lesions. Magn Reson Imaging 34:1314–1321 Li X, Gao J, Wang M, Wan M, Yang J (2016) Rapid and reliable tract-based spatial statistics pipeline for diffusion tensor imaging in the neonatal brain: applications to the white matter development and lesions. Magn Reson Imaging 34:1314–1321
23.
Zurück zum Zitat Fjell AM, Walhovd KB, Westlye LT et al (2010) When does brain aging accelerate? Dangers of quadratic fits in cross-sectional studies. Neuroimage 50:1376–1383CrossRefPubMed Fjell AM, Walhovd KB, Westlye LT et al (2010) When does brain aging accelerate? Dangers of quadratic fits in cross-sectional studies. Neuroimage 50:1376–1383CrossRefPubMed
24.
Zurück zum Zitat Tanaka-Arakawa MM, Matsui M, Tanaka C et al (2015) Developmental changes in the corpus callosum from infancy to early adulthood: a structural magnetic resonance imaging study. PLoS One 10:e0118760CrossRefPubMedPubMedCentral Tanaka-Arakawa MM, Matsui M, Tanaka C et al (2015) Developmental changes in the corpus callosum from infancy to early adulthood: a structural magnetic resonance imaging study. PLoS One 10:e0118760CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Chen H, Zhao B, Cao G et al (2016) Statistical approaches for the study of cognitive and brain aging. Front Aging Neurosci 8:176PubMedPubMedCentral Chen H, Zhao B, Cao G et al (2016) Statistical approaches for the study of cognitive and brain aging. Front Aging Neurosci 8:176PubMedPubMedCentral
26.
Zurück zum Zitat Yeatman JD, Dougherty RF, Myall NJ, Wandell BA, Feldman HM (2012) Tract profiles of white matter properties: automating fiber-tract quantification. PLoS One 7:e49790 Yeatman JD, Dougherty RF, Myall NJ, Wandell BA, Feldman HM (2012) Tract profiles of white matter properties: automating fiber-tract quantification. PLoS One 7:e49790
27.
Zurück zum Zitat Oishi K, Mori S, Donohue PK et al (2011) Multi-contrast human neonatal brain atlas: application to normal neonate development analysis. Neuroimage 56:8–20CrossRefPubMed Oishi K, Mori S, Donohue PK et al (2011) Multi-contrast human neonatal brain atlas: application to normal neonate development analysis. Neuroimage 56:8–20CrossRefPubMed
28.
Zurück zum Zitat Gilmore JH, Lin W, Corouge I et al (2007) Early postnatal development of corpus callosum and corticospinal white matter assessed with quantitative tractography. AJNR Am J Neuroradiol 28:1789–1795CrossRefPubMedPubMedCentral Gilmore JH, Lin W, Corouge I et al (2007) Early postnatal development of corpus callosum and corticospinal white matter assessed with quantitative tractography. AJNR Am J Neuroradiol 28:1789–1795CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat Kollias S (2012) Insights into the connectivity of the human brain using DTI. NJR 1:78–91 Kollias S (2012) Insights into the connectivity of the human brain using DTI. NJR 1:78–91
30.
Zurück zum Zitat Hinkley LBN, Marco EJ, Findlay AM et al (2012) The role of corpus callosum development in functional connectivity and cognitive processing. PLoS One 7:e39804CrossRefPubMedPubMedCentral Hinkley LBN, Marco EJ, Findlay AM et al (2012) The role of corpus callosum development in functional connectivity and cognitive processing. PLoS One 7:e39804CrossRefPubMedPubMedCentral
31.
Zurück zum Zitat Dean DC 3rd, Planalp EM, Wooten W et al (2017) Mapping white matter microstructure in the one month human brain. Sci Rep 7:9759 Dean DC 3rd, Planalp EM, Wooten W et al (2017) Mapping white matter microstructure in the one month human brain. Sci Rep 7:9759
32.
Zurück zum Zitat Nossin-Manor R, Card D, Morris D et al (2013) Quantitative MRI in the very preterm brain: assessing tissue organization and myelination using magnetization transfer, diffusion tensor and T1 imaging. Neuroimage 64:505–516CrossRefPubMed Nossin-Manor R, Card D, Morris D et al (2013) Quantitative MRI in the very preterm brain: assessing tissue organization and myelination using magnetization transfer, diffusion tensor and T1 imaging. Neuroimage 64:505–516CrossRefPubMed
33.
Zurück zum Zitat Rose J, Vassar R, Cahill-Rowley K, Guzman XS, Stevenson DK, Barnea-Goraly N (2014) Brain microstructural development at near-term age in very-low-birth-weight preterm infants: an atlas-based diffusion imaging study. Neuroimage 86:244–256 Rose J, Vassar R, Cahill-Rowley K, Guzman XS, Stevenson DK, Barnea-Goraly N (2014) Brain microstructural development at near-term age in very-low-birth-weight preterm infants: an atlas-based diffusion imaging study. Neuroimage 86:244–256
34.
Zurück zum Zitat Nelson CA, Luciana M (2008) Handbook of developmental cognitive neuroscience, 2nd edn. MIT Press, CambridgeCrossRef Nelson CA, Luciana M (2008) Handbook of developmental cognitive neuroscience, 2nd edn. MIT Press, CambridgeCrossRef
35.
Zurück zum Zitat Gotts SJ, Jo HJ, Wallace GL, Saad ZS, Cox RW, Martin A (2013) Two distinct forms of functional lateralization in the human brain. Proc Natl Acad Sci U S A 110:3435–3444 Gotts SJ, Jo HJ, Wallace GL, Saad ZS, Cox RW, Martin A (2013) Two distinct forms of functional lateralization in the human brain. Proc Natl Acad Sci U S A 110:3435–3444
36.
Zurück zum Zitat Provenzale JM, Liang L, DeLong D, White LE (2007) Diffusion tensor imaging assessment of brain white matter maturation during the first postnatal year. AJR Am J Roentgenol 189:476–486 Provenzale JM, Liang L, DeLong D, White LE (2007) Diffusion tensor imaging assessment of brain white matter maturation during the first postnatal year. AJR Am J Roentgenol 189:476–486
37.
Zurück zum Zitat Erberich SG, Panigrahy A, Friedlich P, Seri I, Nelson MD, Gilles F (2006) Somatosensory lateralization in the newborn brain. Neuroimage 29:155–161 Erberich SG, Panigrahy A, Friedlich P, Seri I, Nelson MD, Gilles F (2006) Somatosensory lateralization in the newborn brain. Neuroimage 29:155–161
38.
Zurück zum Zitat Gilmore JH, Lin W, Prastawa MW et al (2007) Regional gray matter growth, sexual dimorphism, and cerebral asymmetry in the neonatal brain. J Neurosci 27:1255–1260CrossRefPubMedPubMedCentral Gilmore JH, Lin W, Prastawa MW et al (2007) Regional gray matter growth, sexual dimorphism, and cerebral asymmetry in the neonatal brain. J Neurosci 27:1255–1260CrossRefPubMedPubMedCentral
39.
Zurück zum Zitat Hüppi PS, Maier SE, Peled S et al (1998) Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res 44:584–590CrossRefPubMed Hüppi PS, Maier SE, Peled S et al (1998) Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res 44:584–590CrossRefPubMed
40.
Zurück zum Zitat Inder TE, Warfield SK, Wang H, Hüppi PS, Volpe JJ (2005) Abnormal cerebral structure is present at term in premature infants. Pediatrics 115:286–294 Inder TE, Warfield SK, Wang H, Hüppi PS, Volpe JJ (2005) Abnormal cerebral structure is present at term in premature infants. Pediatrics 115:286–294
Metadaten
Titel
Proper timing for the evaluation of neonatal brain white matter development: a diffusion tensor imaging study
verfasst von
Chao Jin
Yanyan Li
Xianjun Li
Miaomiao Wang
Congcong Liu
Jie Gao
Qinli Sun
Deqiang Qiu
Lingxia Zeng
Xihui Zhou
Gailian Li
Jinni Zhang
Jie Zheng
Jian Yang
Publikationsdatum
27.08.2018
Verlag
Springer Berlin Heidelberg
Erschienen in
European Radiology / Ausgabe 3/2019
Print ISSN: 0938-7994
Elektronische ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-018-5665-y

Weitere Artikel der Ausgabe 3/2019

European Radiology 3/2019 Zur Ausgabe

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.