Validation of a brain MRI relaxometry protocol to measure effects of preterm birth at a flexible postnatal age

BMC Pediatrics

Adam W Anderson⁴  Judy L Aschner¹  Ann R Stark²  James C Slaughter³  Nathalie L Maitre⁵ 

[1]Department of Pediatrics, Albert Einstein College of Medicine, Bronx, NY, USA

[2]Department of Pediatrics, Vanderbilt University, Nashville, TN, USA

[3]Department of Biostatistics, Vanderbilt University, Nashville, TN, USA

[4]Departments of Biomedical Engineering and of Radiology and Radiological Sciences, Vanderbilt University, Nashville, TN, USA

[5]Division of Neonatology, The Monroe Carell Jr. Children’s Hospital at Vanderbilt 11111 Doctor’s Office Tower, 2200 Children’s Way, Nashville, TN 37232-9544, USA

关键词: Neonate;    Prematurity;    Maturation;    Globus pallidus;    Basal ganglia;    Relaxometry;    MRI;   

Others  :  1232745
DOI  :  10.1186/1471-2431-14-84

 received in 2013-12-11, accepted in 2014-03-25,  发布年份 2014

【 摘 要 】

Background

Magnetic resonance imaging (MRI) is a useful tool to study brain growth and organization in preterm neonates for clinical and research purposes, but its practicality can be limited by time and medical constraints. The aim of this study was to determine if MRI relaxometry of the deep nuclei, as opposed to white matter, would reflect the influence of gestational age at birth on structures essential to motor development, regardless of postnatal age at the time of imaging.

Results

This was a prospective observational study of infants without brain injury on conventional neuroimaging who were cared for in the neonatal intensive care unit (NICU) at Vanderbilt. Infants were studied using MRI relaxometry within a 2-month window of postmenstrual term age. In 45 infants, white matter MRI T1 relaxation times were influenced by both gestational age and postnatal age at imaging time (R² = 0.19 for gestational age vs. R² = 0.34 adjusting for both gestational age and age at imaging; all p < 0.01). Similar results were obtained with T2 relaxation times. In contrast, globus pallidus T1 reflected gestational age but was minimally affected by postnatal age (R² = 0.50 vs. 0.57, p < 0.001).

Conclusions

The results obtained using this imaging protocol are consistent with the slow maturation of the globus pallidus, essential to normal development of complex motor programs into adulthood. Globus pallidus MRI relaxometry measures the impact of gestational age at birth on brain development independent of postnatal age in preterm infants and should prove useful for predictive modeling in a flexible time-window around postmenstrual term age.

【 授权许可】

   
2014 Maitre et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 2.

【 参考文献 】

• [1]de Kieviet JF, Piek JP, Aarnoudse-Moens CS, Oosterlaan J: Motor development in very preterm and very low-birth-weight children from birth to adolescence: a meta-analysis. JAMA 2009, 302:2235-2242.
• [2]Saigal S, Doyle LW: An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet 2008, 371:261-269.
• [3]Schmidt B, Anderson PJ, Doyle LW, Dewey D, Grunau RE, Asztalos EV, Davis PG, Tin W, Moddemann D, Solimano A, Ohlsson A, Barrington KJ, Roberts RS, Caffeine for Apnea of Prematurity (CAP) Trial Investigators: Survival without disability to age 5 years after neonatal caffeine therapy for apnea of prematurity. JAMA: J Am Med Assoc 2012, 307:275-282.
• [4]Marlow N, Wolke D, Bracewell MA, Samara M: Neurologic and developmental disability at six years of age after extremely preterm birth. N Engl J Med 2005, 352:9-19.
• [5]Luciana M: Cognitive development in children born preterm: implications for theories of brain plasticity following early injury. Dev Psychopathol 2003, 15:1017-1047.
• [6]Stephens BE, Vohr BR: Neurodevelopmental outcome of the premature infant. Pediatr Clin North Am 2009, 56:631-646.
• [7]Volpe JJ: Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurology 2009, 8:110-124.
• [8]Kuban KC, Allred EN, O’Shea TM, Paneth N, Pagano M, Dammann O, Leviton A, Du Plessis A, Westra SJ, Miller CR, Bassan H, Krishnamoorthy K, Junewick J, Olomu N, Romano E, Seibert J, Engelke S, Karna P, Batton D, O’Connor SE, Keller CE: Cranial ultrasound lesions in the NICU predict cerebral palsy at age 2 years in children born at extremely low gestational age. J Child Neurol 2009, 24:63-72.
• [9]O’Shea TM, Kuban KC, Allred EN, Paneth N, Pagano M, Dammann O, Bostic L, Brooklier K, Butler S, Goldstein DJ, Hounshell G, Keller C, McQuiston S, Miller A, Pasternak S, Plesha-Troyke S, Price J, Romano E, Solomon KM, Jacobson A, Westra S, Leviton A: Neonatal cranial ultrasound lesions and developmental delays at 2 years of age among extremely low gestational age children. Pediatrics 2008, 122:e662-e669.
• [10]Woodward LJ, Anderson PJ, Austin NC, Howard K, Inder TE: Neonatal MRI to predict neurodevelopmental outcomes in preterm infants. N Engl J Med 2006, 355:685-694.
• [11]Hintz SR, O’Shea M: Neuroimaging and neurodevelopmental outcomes in preterm infants. Semin Perinatol 2008, 32:11-19.
• [12]de Vries LS, Rademaker KJ, Groenendaal F, Eken P, van Haastert IC, Vandertop WP, Gooskens R, Meiners LC: Correlation between neonatal cranial ultrasound, MRI in infancy and neurodevelopmental outcome in infants with a large intraventricular haemorrhage with or without unilateral parenchymal involvement. Neuropediatrics 1998, 29:180-188.
• [13]Woodward LJ, Clark CAC, Bora S, Inder TE: Neonatal white matter abnormalities an important predictor of neurocognitive outcome for very preterm children. PLoS ONE 2012, 7:e51879.
• [14]Spittle AJ, Cheong J, Doyle LW, Roberts G, Lee KJ, Lim J, Hunt RW, Inder TE, Anderson PJ: Neonatal white matter abnormality predicts childhood motor impairment in very preterm children. Dev Med Child Neurol 2011, 53:1000-1006.
• [15]Iwata S, Nakamura T, Hizume E, Kihara H, Takashima S, Matsuishi T, Iwata O: Qualitative brain MRI at term and cognitive outcomes at 9 years after very preterm birth. Pediatrics 2012, 129:e1138-e1147.
• [16]McConnell J: The Theory of Nuclear Magnetic Relaxation in Liquids. 1st edition. New York, NY: Cambridge University Press; 2009.
• [17]Ferrie JC, Barantin L, Saliba E, Akoka S, Tranquart F, Sirinelli D, Pourcelot L: MR assessment of the brain maturation during the perinatal period: quantitative T2 MR study in premature newborns. Magn Reson Imag 1999, 17:1275-1288.
• [18]Groenewegen HJ: The basal ganglia and motor control. Neural Plast 2003, 10(1-2):107-120.
• [19]Andersen HF, Johnson TR, Flora JD, Barclay ML: Gestational age assessment. II. Prediction from combined clinical observations. YMOB 1981, 140:770-774.
• [20]Mathur AM, Neil JJ, McKinstry RC, Inder TE: Transport, monitoring, and successful brain MR imaging in unsedated neonates. Pediatr Radiol 2008, 38:260-264.
• [21]Dixon RL: The physics of proton NMR. Med Phys 1982, 9:807.
• [22]Maes F, Collignon A, Vandermeulen D, Marchal G, Suetens P: Multimodality image registration by maximization of mutual information. IEEE Trans Med Imag 1997, 16:187-198.
• [23]Fischer HW, Ketonen L: Radiographic Neuroanatomy: a Working Atlas. 2nd edition. Texas: Mcgraw-Hill; 1998.
• [24]Bullmore ET, Suckling J, Overmeyer S, Rabe-Hesketh S, Taylor E, Brammer MJ: Global, Voxel, and Cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans Med Imag 1999, 18:32.
• [25]Wuttikul C, Taoka T, Akashi T, Nakagawa H, Miyasaka T, Sakamoto M, Takayama K, Wada T, Kitano S, Takahama J, Marugami N, Kichikawa K: Prominent signal intensity of T1/T2 prolongation in subcortical white matter of the anterior temporal region on conventional screening MRI of late preterm infants with normal development. Magn Reson Imag 2008, 26:1374-1380.
• [26]Nossin-Manor R, Card D, Morris D, Noormohamed S, Shroff MM, Whyte HE, Taylor MJ, Sled JG: Quantitative MRI in the very preterm brain: Assessing tissue organization and myelination using magnetization transfer, diffusion tensor and T1 imaging. NeuroImage 2012, 64:1-12.
• [27]Boardman JP, Craven C, Valappil S, Counsell SJ, Dyet LE, Rueckert D, Aljabar P, Rutherford MA, Chew ATM, Allsop JM, Cowan F, Edwards AD: A common neonatal image phenotype predicts adverse neurodevelopmental outcome in children born preterm. NeuroImage 2010, 52:409-414.
• [28]Peterson BS, Anderson AW, Ehrenkranz R, Staib LH, Tageldin M, Colson E, Gore JC, Duncan CC, Makuch R, Ment LR: Regional brain volumes and their later neurodevelopmental correlates in term and preterm infants. Pediatrics 2003, 111:939-948.
• [29]Deoni SCL, Dean DC, O’Muircheartaigh J, Dirks H, Jerskey BA: Investigating white matter development in infancy and early childhood using myelin water faction and relaxation time mapping. NeuroImage 2012, 63:1038-1053.
• [30]Sarnat HB, Auer RN, Flores-Sarnat L: Synaptogenesis in the fetal corpus striatum, globus pallidus, and substantia nigra: correlations with striosomes of Graybiel and dyskinesias in premature infants. J Child Neurol 2013, 28:60-69.
• [31]Dexter DT, Carayon A, Javoy-Agid F, Agid Y, Wells FR, Daniel SE, Lees A, Jenner P, Marsden CD: Alterations in the levels of iron, ferritin and other trace metals in Parkinson’s disease and other neurodegenerative diseases affecting the basal ganglia. Brain 1991, 114(4):1953-1975.
• [32]Zhang N, Fitsanakis VA, Erikson KM, Aschner M, Avison MJ, Gore JC: A model for the analysis of competitive relaxation effects of manganese and iron in vivo. NMR Biomed 2009, 22:391-404.
• [33]Aschner JL, Aschner M: Nutritional aspects of manganese homeostasis. Mol Aspects Med 2005, 26:353-362.
• [34]Erikson KM, Thompson K, Aschner J, Aschner M: Manganese neurotoxicity: A focus on the neonate. Pharmacol Therapeut 2007, 113:369-377.
• [35]Lee AY, Jang SH, Lee E, Ahn SH, Cho HK, Jo HM, Son SM: Radiologic differences in white matter maturation between preterm and full-term infants: TBSS study. Pediatr Radiol 2013, 43:612-619.
• [36]Volpe JJ: The encephalopathy of prematurity–brain injury and impaired brain development inextricably intertwined. Semin Pediatr Neurol 2009, 16:167-178.
• [37]Seo JP, Chang P-H, Jang SH: Anatomical location of the corticospinal tract according to somatotopies in the centrum semiovale. Neurosci Lett 2012, 523:111-114.
• [38]Skranes J, Vik T, Nilsen G, Smevik O, Andersson HW, Brubakk AM: Can cerebral MRI at age 1 year predict motor and intellectual outcomes in very-low-birth weight children? Dev Med Child Neurol 1998, 40:256-262.
• [39]Tusor N, Wusthoff C, Smee N, Merchant N, Arichi T, Allsop JM, Cowan FM, Azzopardi D, Edwards AD, Counsell SJ: Prediction of neurodevelopmental outcome after hypoxic-ischemic encephalopathy treated with hypothermia by diffusion tensor imaging analyzed using tract-based spatial statistics. Pediatr Res 2012, 72:63-69.
• [40]Murakami A, Morimoto M, Yamada K, Kizu O, Nishimura A, Nishimura T, Sugimoto T: Fiber-tracking techniques can predict the degree of neurologic impairment for periventricular leukomalacia. Pediatrics 2008, 122:500-506.
• [41]Roze E, Harris PA, Ball G, Elorza LZ, Braga RM, Allsop JM, Merchant N, Porter E, Arichi T, Edwards AD, Rutherford MA, Cowan FM, Counsell SJ: Tractography of the corticospinal tracts in infants with focal perinatal injury: comparison with normal controls and to motor development. Neuroradiology 2012, 54:507-516.
• [42]Deoni SCL: Quantitative relaxometry of the brain. Top Magn Reson Imag 2010, 21:101-113.