Data quality in diffusion tensor imaging studies of the preterm brain: a systematic review

Pediatric Radiology

Volumn 45, Issue 9, 2015, Pages 1372-1381

  Pieterman, Kay ^a,b   Plaisier, Annemarie ^a,b   Govaert, Paul ^a,c   Leemans, Alexander ^d   Lequin, Maarten H ^b   Dudink, Jeroen ^a,b  

^a SOPHIA CHILDREN S HOSPITAL   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c Paola Childrens Hospital   (Belgium)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Diffusion tensor imaging; Image acquisition; Magnetic resonance imaging; Neonate; Prematurity; Systematic review

Indexed keywords

ALGORITHM; ARTICLE; ARTIFACT; COCHRANE LIBRARY; COMPUTER; DIFFUSION TENSOR IMAGING; EMBASE; HUMAN; IMAGE QUALITY; INFORMATION PROCESSING; MEDLINE; METHODOLOGY; NEUROIMAGING; PREMATURITY; PRIORITY JOURNAL; PUBLICATION; QUALITY CONTROL; SCREENING; SYSTEMATIC REVIEW; TRACTOGRAPHY; WEB OF SCIENCE; BRAIN; HEALTH CARE QUALITY; MEASUREMENT ACCURACY; META ANALYSIS; NEURODEVELOPMENTAL DISORDERS; NEWBORN; PATHOLOGY; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; STANDARDS; STATISTICS AND NUMERICAL DATA; UTILIZATION;

BRAIN; DATA ACCURACY; DIFFUSION TENSOR IMAGING; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; NEURODEVELOPMENTAL DISORDERS; NEUROIMAGING; QUALITY ASSURANCE, HEALTH CARE; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY;

EID: 84938738501     PISSN: 03010449     EISSN: 14321998     Source Type: Journal    
DOI: 10.1007/s00247-015-3307-y     Document Type: Article

References (101)

1. Gulland A (2012) Fifteen million and rising — the number of premature births every year. BMJ 344:e3084
2. Bhutta AT, Cleves MA, Casey PH et al (2002) Cognitive and behavioral outcomes of school-aged children who were born preterm: a meta-analysis. JAMA 288:728–737
3. Marlow N, Hennessy EM, Bracewell MA et al (2007) Motor and executive function at 6 years of age after extremely preterm birth. Pediatrics 120:793–804
4. Rutherford MA, Supramaniam V, Ederies A et al (2010) Magnetic resonance imaging of white matter diseases of prematurity. Neuroradiology 52:505–521
5. Dyet LE, Kennea N, Counsell SJ et al (2006) Natural history of brain lesions in extremely preterm infants studied with serial magnetic resonance imaging from birth and neurodevelopmental assessment. Pediatrics 118:536–548
6. Volpe JJ (2009) Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 8:110–124
7. Counsell SJ, Allsop JM, Harrison MC et al (2003) Diffusion-weighted imaging of the brain in preterm infants with focal and diffuse white matter abnormality. Pediatrics 112:1–7
8. Dubois J, Dehaene-Lambertz G, Kulikova S et al (2014) The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience 276:48–71
9. Jones DK (2011) Diffusion MRI — theory, methods and applications. Oxford University Press USA, New York
10. Johansen-Berg H, Behrens TEJ (2014) Diffusion MRI — from quantitative measurement to in vivo neuroanatomy. Elsevier, London
11. Bassi L, Chew A, Merchant N (2011) Diffusion tensor imaging in preterm infants with punctate white matter lesions. Pediatr Res 69:561–566
12. Ment LR, Hirtz D, Huppi PS (2009) Imaging biomarkers of outcome in the developing preterm brain. Lancet Neurol 8:1042–1055
13. Tournier JD, Mori S, Leemans A (2011) Diffusion tensor imaging and beyond. Magn Reson Med 65:1532–1556
14. Ball G, Boardman JP, Aljabar P et al (2013) The influence of preterm birth on the developing thalamocortical connectome. Cortex 49:1711–1721
15. Bassi L, Ricci D, Volzone A et al (2008) Probabilistic diffusion tractography of the optic radiations and visual function in preterm infants at term equivalent age. Brain 131:573–582
16. de Bruine FT, van Wezel-Meijler G, Leijser LM et al (2011) Tractography of developing white matter of the internal capsule and corpus callosum in very preterm infants. Eur Radiol 21:538–547
17. van Kooij BJ, de Vries LS, Ball G et al (2012) Neonatal tract-based spatial statistics findings and outcome in preterm infants. AJNR Am J Neuroradiol 33:188–194
18. Dudink J, Kerr JL, Paterson K et al (2008) Connecting the developing preterm brain. Early Hum Dev 84:777–782
19. Pandit AS, Robinson E, Aljabar P et al (2014) Whole-brain mapping of structural connectivity in infants reveals altered connection strength associated with growth and preterm birth. Cereb Cortex 24:2324–2333
20. Collin G, van den Heuvel MP (2013) The ontogeny of the human connectome: development and dynamic changes of brain connectivity across the life span. Neuroscientist 19:616–628
21. Tymofiyeva O, Hess CP, Ziv E et al (2013) A DTI-based template-free cortical connectome study of brain maturation. PLoS One 8:e63310
22. Jones DK, Cercignani M (2010) Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed 23:803–820
23. Vos SB, Jones DK, Viergever MA et al (2011) Partial volume effect as a hidden covariate in DTI analyses. Neuroimage 55:1566–1576
24. Szczepankiewicz F, Latt J, Wirestam R et al (2013) Variability in diffusion kurtosis imaging: impact on study design, statistical power and interpretation. Neuroimage 76:145–154
25. Mathur AM, Neil JJ, McKinstry RC et al (2008) Transport, monitoring, and successful brain MR imaging in unsedated neonates. Pediatr Radiol 38:260–264
26. Kozak LR, David S, Rudas G et al (2013) Investigating the need of triggering the acquisition for infant diffusion MRI: a quantitative study including bootstrap statistics. Neuroimage 69:198–205
27. Plaisier A, Pieterman K, Lequin MH et al (2014) Choice of diffusion tensor estimation approach affects fiber tractography of the fornix in preterm brain. AJNR Am J Neuroradiol 35:1219–122528
28. Adams E, Chau V, Poskitt KJ et al (2010) Tractography-based quantitation of corticospinal tract development in premature newborns. J Pediatr 156:882–888
29. Aeby A, van Bogaert P, David P et al (2012) Nonlinear microstructural changes in the right superior temporal sulcus and lateral occipitotemporal gyrus between 35 and 43 weeks in the preterm brain. Neuroimage 63:104–110
30. Aeby A, de Tiege X, Creuzil M et al (2013) Language development at 2 years is correlated to brain microstructure in the left superior temporal gyrus at term equivalent age: a diffusion tensor imaging study. Neuroimage 78:145–151
31. Als H, Duffy FH, McAnulty GB et al (2004) Early experience alters brain function and structure. Pediatrics 113:846–857
32. Anjari M, Srinivasan L, Allsop JM et al (2007) Diffusion tensor imaging with tract-based spatial statistics reveals local white matter abnormalities in preterm infants. Neuroimage 35:1021–1027
33. Anjari M, Counsell SJ, Srinivasan L et al (2009) The association of lung disease with cerebral white matter abnormalities in preterm infants. Pediatrics 124:268–276
34. Arichi T, Moraux A, Melendez A et al (2010) Somatosensory cortical activation identified by functional MRI in preterm and term infants. Neuroimage 49:2063–2071
35. Arzoumanian Y, Mirmiran M, Barnes PD et al (2003) Diffusion tensor brain imaging findings at term-equivalent age may predict neurologic abnormalities in low birth weight preterm infants. AJNR Am J Neuroradiol 24:1646–1653
36. Ball G, Boardman JP, Arichi T et al (2013) Testing the sensitivity of tract-based spatial statistics to simulated treatment effects in preterm neonates. PLoS One 8:e67706
37. Ball G, Counsell SJ, Anjari M et al (2010) An optimised tract-based spatial statistics protocol for neonates: applications to prematurity and chronic lung disease. Neuroimage 53:94–102
38. Ball G, Boardman JP, Rueckert D et al (2012) The effect of preterm birth on thalamic and cortical development. Cereb Cortex 22:1016–1024
39. Berman JI, Mukherjee P, Partridge SC et al (2005) Quantitative diffusion tensor MRI fiber tractography of sensorimotor white matter development in premature infants. Neuroimage 27:862–871
40. 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 30:120–124
41. Bonifacio SL, Glass HC, Chau V et al (2010) Extreme premature birth is not associated with impaired development of brain microstructure. J Pediatr 157:726–732
42. Brummelte S, Grunau RE, Chau V et al (2012) Procedural pain and brain development in premature newborns. Ann Neurol 71:385–396
43. Chau V, Poskitt KJ, McFadden DE et al (2009) Effect of chorioamnionitis on brain development and injury in premature newborns. Ann Neurol 66:155–164
44. Chau V, Brant R, Poskitt KJ et al (2012) Postnatal infection is associated with widespread abnormalities of brain development in premature newborns. Pediatr Res 71:274–279
45. Cheong JLY, Thompson DK, Wang HX et al (2009) Abnormal white matter signal on MR imaging is related to abnormal tissue microstructure. AJNR Am J Neuroradiol 30:623–628
46. Counsell SJ, Shen Y, Boardman JP et al (2006) Axial and radial diffusivity in preterm infants who have diffuse white matter changes on magnetic resonance imaging at term-equivalent age. Pediatrics 117:376–386
47. de Bruine FT, van Wezel-Meijler G, Leijser LM et al (2013) Tractography of white-matter tracts in very preterm infants: a 2-year follow-up study. Dev Med Child Neurol 55:427–433
48. DeIpolyi AR, Mukherjee P, Gill K et al (2005) Comparing microstructural and macrostructural development of the cerebral cortex in premature newborns: diffusion tensor imaging versus cortical gyration. Neuroimage 27:579–586
49. Drobyshevsky A, Bregman J, Storey P et al (2007) Serial diffusion tensor imaging detects white matter changes that correlate with motor outcome in premature infants. Dev Neurosci 29:289–301
50. Dudink J, Lequin M, van Pul C et al (2007) Fractional anisotropy in white matter tracts of very-low-birth-weight infants. Pediatr Radiol 37:1216–1223
51. Dudink J, Larkman DJ, Kapellou O et al (2008) High b-value diffusion tensor imaging of the neonatal brain at 3T. AJNR Am J Neuroradiol 29:1966–1972
52. Dudink J, Buijs J, Govaert P et al (2010) Diffusion tensor imaging of the cortical plate and subplate in very-low-birth-weight infants. Pediatr Radiol 40:1397–1404
53. Gimenez M, Miranda MJ, Born AP et al (2008) Accelerated cerebral white matter development in preterm infants: a voxel-based morphometry study with diffusion tensor MR imaging. Neuroimage 41:728–734
54. Glass HC, Berman JI, Norcia AM et al (2010) Quantitative fiber tracking of the optic radiation is correlated with visual-evoked potential amplitude in preterm infants. AJNR Am J Neuroradiol 31:1424–1429
55. Groppo M, Ricci D, Bassi L et al (2014) Development of the optic radiations and visual function after premature birth. Cortex 56:30–37
56. Hasegawa T, Yamada K, Morimoto M et al (2011) Development of corpus callosum in preterm infants is affected by the prematurity: in vivo assessment of diffusion tensor imaging at term-equivalent age. Pediatr Res 69:249–254
57. Hemels MA, Nijman J, Leemans A et al (2012) Cerebral white matter and neurodevelopment of preterm infants after coagulase-negative staphylococcal sepsis. Pediatr Crit Care Med 13:678–684
58. Jo HM, Cho HK, Jang SH et al (2012) A comparison of microstructural maturational changes of the corpus callosum in preterm and full-term children: a diffusion tensor imaging study. Neuroradiology 54:997–1005
59. Lee AY, Jang SH, Lee E et al (2013) Radiologic differences in white matter maturation between preterm and full-term infants: TBSS study. Pediatr Radiol 43:612–619
60. Lee EC, Kwatra NS, Vezina G et al (2013) White matter integrity on fractional anisotropy maps in encephalopathic neonates post hypothermia therapy with normal-appearing MR imaging. Pediatr Radiol 43:709–715
61. Lepomaki V, Paavilainen T, Matomaki J et al (2012) Effect of antenatal growth and prematurity on brain white matter: diffusion tensor study. Pediatr Radiol 42:692–698
62. Lepomaki V, Leppanen M, Matomaki J et al (2013) Preterm infants’ early growth and brain white matter maturation at term age. Pediatr Radiol 43:1357–1364
63. Lepomaki VK, Paavilainen TP, Hurme SAM et al (2012) Fractional anisotropy and mean diffusivity parameters of the brain white matter tracts in preterm infants: reproducibility of region-of-interest measurements. Pediatr Radiol 42:175–182
64. Lepomaki V, Matomaki J, Lapinleimu H et al (2013) Effect of antenatal growth on brain white matter maturation in preterm infants at term using tract-based spatial statistics. Pediatr Radiol 43:80–85
65. Ling X, Tang W, Liu G et al (2013) Assessment of brain maturation in the preterm infants using diffusion tensor imaging (DTI) and enhanced T2 star weighted angiography (ESWAN). Eur J Radiol 82:e476–483
66. Liu Y, Baleriaux D, Kavec M et al (2010) Structural asymmetries in motor and language networks in a population of healthy preterm neonates at term equivalent age: a diffusion tensor imaging and probabilistic tractography study. Neuroimage 51:783–788
67. Liu Y, Metens T, Absil J et al (2011) Gender differences in language and motor-related fibers in a population of healthy preterm neonates at term-equivalent age: a diffusion tensor and probabilistic tractography study. AJNR Am J Neuroradiol 32:2011–2016
68. Liu Y, Aeby A, Baleriaux D et al (2012) White matter abnormalities are related to microstructural changes in preterm neonates at term-equivalent age: a diffusion tensor imaging and probabilistic tractography study. AJNR Am J Neuroradiol 33:839–845
69. Maas LC, Mukherjee P, Carballido-Gamio J et al (2004) Early laminar organization of the human cerebrum demonstrated with diffusion tensor imaging in extremely premature infants. Neuroimage 22:1134–1140
70. Mathew P, Pannek K, Snow P et al (2013) Maturation of corpus callosum anterior midbody is associated with neonatal motor function in eight preterm-born infants. Neural Plast 2013:359532
71. Melbourne A, Kendall GS, Cardoso MJ et al (2012) Radial structure in the preterm cortex: persistence of the preterm phenotype at term equivalent age? Med Image Comput Comput Assist Interv 15:256–263
72. Milgrom J, Newnham C, Anderson PJ et al (2010) Early sensitivity training for parents of preterm infants: impact on the developing brain. Pediatr Res 67:330–335
73. Nijman J, Gunkel J, de Vries LS et al (2013) Reduced occipital fractional anisotropy on cerebral diffusion tensor imaging in preterm infants with postnatally acquired cytomegalovirus infection. Neonatology 104:143–150
74. 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 64:505–516
75. Paquette LB, Wisnowski JL, Ceschin R et al (2013) Abnormal cerebral microstructure in premature neonates with congenital heart disease. AJNR Am J Neuroradiol 34:2026–2033
76. Partridge SC, Mukherjee P, Henry RG et al (2004) Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns. Neuroimage 22:1302–1314
77. Partridge SC, Mukherjee P, Berman JI et al (2005) Tractography-based quantitation of diffusion tensor imaging parameters in white matter tracts of preterm newborns. J Magn Reson Imaging 22:467–474
78. Pogribna U, Yu X, Burson K et al (2013) Perinatal clinical antecedents of white matter microstructural abnormalities on diffusion tensor imaging in extremely preterm infants. PLoS One 8:e72974
79. Pogribna U, Burson K, Lasky RE et al (2014) Role of diffusion tensor imaging as an independent predictor of cognitive and language development in extremely low-birth-weight infants. AJNR Am J Neuroradiol 35:790–796
80. Ratnarajah N, Rifkin-Graboi A, Fortier MV et al (2013) Structural connectivity asymmetry in the neonatal brain. Neuroimage 75:187–194
81. Reiman M, Parkkola R, Johansson R et al (2009) Diffusion tensor imaging of the inferior colliculus and brainstem auditory-evoked potentials in preterm infants. Pediatr Radiol 39:804–809
82. Rogers CE, Anderson PJ, Thompson DK et al (2012) Regional cerebral development at term relates to school-age social-emotional development in very preterm children. J Am Acad Child Adolesc Psychiatry 51:181–191
83. Rose SE, Hatzigeorgiou X, Strudwick MW et al (2008) Altered white matter diffusion anisotropy in normal and preterm infants at term-equivalent age. Magn Reson Med 60:761–767
84. Rose J, Butler EE, Lamont LE et al (2009) Neonatal brain structure on MRI and diffusion tensor imaging, sex, and neurodevelopment in very-low-birthweight preterm children. Dev Med Child Neurol 51:526–535
85. Shim SY, Jeong HJ, Son DW et al (2012) Altered microstructure of white matter except the corpus callosum is independent of prematurity. Neonatology 102:309–315
86. Skiold B, Horsch S, Hallberg B et al (2010) White matter changes in extremely preterm infants, a population-based diffusion tensor imaging study. Acta Paediatr Int J Paediatr 99:842–849
87. Tam EWY, Ferriero DM, Xu D et al (2009) Cerebellar development in the preterm neonate: effect of supratentorial brain injury. Pediatr Res 66:102–106
88. Thompson DK, Inder TE, Faggian N et al (2011) Characterization of the corpus callosum in very preterm and full-term infants utilizing MRI. Neuroimage 55:479–490
89. Thompson DK, Inder TE, Faggian N et al (2012) Corpus callosum alterations in very preterm infants: perinatal correlates and 2 year neurodevelopmental outcomes. Neuroimage 59:3571–3581
90. van Kooij BJ, van Pul C, Benders MJ et al (2011) Fiber tracking at term displays gender differences regarding cognitive and motor outcome at 2 years of age in preterm infants. Pediatr Res 70:626–632
91. van Pul C, van Kooij BJ, de Vries LS et al (2012) Quantitative fiber tracking in the corpus callosum and internal capsule reveals microstructural abnormalities in preterm infants at term-equivalent age. AJNR Am J Neuroradiol 33:678–684
92. Vinall J, Grunau RE, Brant R et al. (2013) Slower postnatal growth is associated with delayed cerebral cortical maturation in preterm newborns. Sci Transl Med 5:168ra168
93. Yoo SS, Park HJ, Soul JS et al (2005) In vivo visualization of white matter fiber tracts of preterm- and term-infant brains with diffusion tensor magnetic resonance imaging. Invest Radiol 40:110–115
94. Zwicker JG, Grunau RE, Adams E et al (2013) Score for neonatal acute physiology-II and neonatal pain predict corticospinal tract development in premature newborns. Pediatr Neurol 48:123–129
95. Keil B, Alagappan V, Mareyam A et al (2011) Size-optimized 32-channel brain arrays for 3 T pediatric imaging. Magn Reson Med 66:1777–1787
96. Pannek K, Guzzetta A, Colditz PB et al (2012) Diffusion MRI of the neonate brain: acquisition, processing and analysis techniques. Pediatr Radiol 42:1169–1182
97. Jones DK, Leemans A (2011) Diffusion tensor imaging. Methods Mol Biol 711:127–144
98. Veraart J, Rajan J, Peeters RR et al (2013) Comprehensive framework for accurate diffusion MRI parameter estimation. Magn Reson Med 70:972–984
99. Chang LC, Jones DK, Pierpaoli C (2005) RESTORE: robust estimation of tensors by outlier rejection. Magn Reson Med 53:1088–1095
100. Plaisier A, Govaert P, Lequin MH et al (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
101. Pannek K, Scheck SM, Colditz PB et al (2014) Magnetic resonance diffusion tractography of the preterm infant brain: a systematic review. Dev Med Child Neurol 56:113–124