Diffusion tensor imaging (DTI) can detect injury to specific white matter (WM) tracts
involved with sensorimotor processing and may provide sensitive measures for latent or
nascent motor skills. We hypothesized that DTI measures of WM fractional anisotropy (FA)
could predict early motor scores on a standardized assessment in a cohort of preterm
infants at risk for WM injury.
METHODS:
In this prospective study, preterm infants (n= 26, 11 female, 15 male, mean
gestational age 29.1 ± 2.5) underwent the Test of Infant Motor Performance (TIMP) at
term and at 12 weeks corrected age (CA) and underwent an non-sedated magnetic resonance
imaging (MRI) with DTI at a mean of 42 ± 1.5 weeks CA. Fractional anisotropy (FA) was
measured by Voxelwise statistical analysis using Tract-Based Spatial Statistics (TBSS)
in the specific regions of interest.
RESULTS:
Significant differences were found between infants with poor versus average
performance on motor assessments at 12-weeks and FA values in several left hemispheric
WM tracts (p< 0.05). High FA of the left anterior limb of the internal capsule (ALIC)
predicted mean increase in TIMP scores on specific items for head lift in prone and head
lift turn to sound (p= 0.045 and p= 0.002).
CONCLUSION:
Subtle WM injury, as indicated by low FA in left WM tracts, can predict outcomes of
early motor skills performance testing at 3 months. Early DTI may identify infants with
silent WM injury who need early intervention. Further studies may establish if
individual tract FA improve after targeted treatment.
KendallG, MelbourneA, JohnsonS, PriceD, BainbridgeA, GunnyR, Huertas-CeballosA, CadyEB, OurselinS, MarlowN, RobertsonNJ. White Matter NAA/Cho and Cho/Cr Ratios at MR Spectroscopy Are
Predictive of Motor Outcome in Preterm Infants.
Radiology. 2014; 271(1):
230-238. doi: 10.1148/radiol.13122679.
2.
RosenbaumP. Variation and abnormality: Recognizing the
differences. Journal of Pediatrics. 2006;
149: 593-94.
3.
SpittleA, LeeK, Spencer-SmithM, LoreficeL, AndersonP, DoyleL. Accuracy of Two Motor Assessments during the First Year of Life in
Preterm Infants for Predicting Motor Outcome at Preschool Age.
PLoS ONE. 2015; 10(5):
e0125854. doi: 10.1371/journal.pone.0125854.
4.
BarbosaVM, CampbellSK, SmithE, BerbaumM. Comparison of Test of Infant Motor Performance (TIMP) item
responses among children with cerebral palsy, developmental delay, and typical
development. American Journal of Occupational Therapy.
2005; 59: 446-456.
5.
HarmonH, TaylorH, MinichN, Wilson-CostelloD, HackM. Early school outcomes for extremely preterm infants with transient
neurological abnormalities. Dev Med Child Neurol.
2015; 57(9):
865-71. doi: 10.1111/dmcn.12811.
6.
HutchinsonEA, De LucaCR, DoyleLW, RobertsG, AndersonPJ. Victorian Infant Collaborative Study Group. School-age outcomes of
extremely preterm or extremely low birth weight children.
Pediatrics. 2013; 31:
e1053-61.
7.
Wilson-CostelloD, FriedmanH, MinichN, et al. Improved neurodevelopmental outcomes for extremely low
birth weight infants in 2000-2002. Pediatrics.
2007; 119: 37-45.
8.
DonohuePK, GrahamEM. Earlier markers for cerebral palsy and clinical research in
premature infants. Journal of Perinatology.
2007; (27): 259-261.
9.
MeadeVA, SweeneyJK, ChandlerLS, WoodwardBJ. Identifying 4-month old infants at risk in community
screenings. Pediatr Phys Ther. 2009;
21(2): 150-7.
10.
RydzD, SrourM, OskouiM, MargetN, ShillerM, BirnbaumR, MajnemerA, ShevellMI. Screening for developmental delay in the setting of a community
pediatric clinic: prospective assessment of parent-report
questionnaires. Pediatrics. 2006;
118(4): e1178-86.
11.
CardosoAC, CamposAC, SantosMM, SantosDC, RochasNA. Motor performance of children with down syndrome and typical
development at 2 to 4 and 26 months. Pediatr Phys Ther.
2013; 27(2):
135-41. doi: 10.1097/PEP.0000000000000120.
12.
CampbellSK, ZawackiL, RankinKM, YoderJC, ShapiroN, LiZ, White-TrautR. Concurrent validity of the TIMP and the Bayley III scales at 6
weeks corrected age. Pediatr Phys Ther.
2013; 25(4):
395-401. doi: 10.1097/PEP.0b013e31829db85b.
13.
NoritzG, MurphyN. Motor delays: Early identification and evaluation.
Journal of American Academy of Pediatrics. 2013;
131(6): 2015-2027.
14.
CounsellSJ, EdwardsAD, ChewATM, AnjariM, DyetLE, SrinivasanL, CowanFM. Specific relations between neurodevelopmental abilities and white
matter microstructure in children born preterm. Brain.
2008; 131(Pt 12):
3201-3208. http://dx.doi.org/10.1093/brain/awn268.
15.
RoseJ, VassarR, Cahill-RowleyK, GuzmanXS, StevensonDK, Barnea-GoralyN. Brain microstructural development at near-term age in
very-low-birth-weight preterm infants: An atlas-based diffusion imaging
study. Neuroimage. 2014;
86: 244-56. doi:
10.1016/j.neuroimage.2013.09.053.
LeydenKM, KucukboyaciNE, PuckettOK, LeeD, LoiRQ, PaulB, McDonaldCR. What does diffusion tensor imaging (DTI) tell us about cognitive
networks in temporal lobe epilepsy?Quant Imaging Med Surg. 2015;
5(2): 247-63. doi:
10.3978/j.issn.2223-4292.2015.02.01.
18.
QiuA, MoriS, MillerMI. Diffusion tensor imaging for understanding brain development in
early life. Annu Rev Psychol. 2015.
19.
van KooijBJ, de VriesLS, BallG, van HaastertIC, BendersMJ, GroenendaalF, CounsellSJ. Neonatal tract-based spatial statistics findings and outcome in
preterm infants. AJNR Am J Neuroradiol.
2012; 33(1):
188-94. doi: 10.3174/ajnr.A2723.
20.
ArzoumanianY, MirmiranM, BarnesPD, WoolleyK, AriagnoRL, MoseleyME, AtlasSW. Diffusion tensor brain imaging findings at term-equivalent age may
predict neurologic abnormalities in low birth weight preterm infants.
AJNR Am. J. Neuroradiol. 2003;
24(8): 1646-1653. [PubMed:
136 79287].
21.
van ZijlPC, ChangL. Multi-contrast human neonatal brain atlas: application to normal
neonate development analysis. Neuroimage.
2011; 56(1):
8-20.
22.
CampbellSK, LevyP, ZawackiL, LiaoPJ. Population-based age standards for interpreting results on the
test of motor infant performance. Pediatr Phys Ther.
2006; 18(2):
119-25.
23.
CampbellS. The test of infant motor performance test user's manual. Infant Motor Performance
Scales, LLC. Chicago, ILL.
24.
SmithS.M., JenkinsonM., WoolrichM.W., BeckmannC.F., BehrensT.E.J., Johansen-BergH., BannisterP.R., De LucaM., DrobnjakI., FlitneyD.E., NiazyR., SaundersJ., VickersJ., ZhangY., De StefanoN., BradyJ.M., and MatthewsP.M.. Advances in functional and structural MR image analysis and
implementation as FSL. NeuroImage. 2004;
23(S1): 208-219.
25.
OishiK, MoriS, DonohuePK, ErnstT, AndersonL, BuchthalS, FariaA, JiangH, LiX, MillerMI, van ZijlPC, ChangL. Multi-contrast human neonatal brain atlas: Application to normal
neonate development analysis. Neuroimage.
2011; 56(1):
8-20. doi: 10.1016/j.neuroimage.2011.01.051.
26.
Coker-BoltP, WoodburyM, PerkelJ, MoreauN, HopeH, RamakrishnanV, MulvihillD, JenkinsD. Identifying premature infant at high and low risk for motor delays
using motor performance testing and MRS. Journal of Pediatric
Rehabilitation Medicine. 2014; 7:
219-232. DOI: 10.3233/PRM-140291.
27.
GaoW, LinW, ChenY, GerigG, SmithJ, JewellsV, GilmoreJ. Temproal and spatial development of axonal maturation and
myelination of white matter in the developing brain. Am J
Neuroradiology. 2009; 30:
290-6.
28.
HuangH, ZhangJ, WakanaS, ZhangW, RenT, RichardsLJ, YarowskyP, DonohueP, GrahamE, van ZijlPC, MoriS. White and gray matter development in human fetal, newborn, and
pediatric brains. NEuroimage. 2006;
33: 27-38.
29.
WeinsteinM, MaromR, BergerI, Ben BashatD, Gross-TsurV, Ben-SiraL, ArtziM, UlielS, LeitnerY, GevaR. Neonatal Neuropsychology: Emerging relations of neonatal
sensory-motor responses to white matter integrity.
Neuropsychologia. 2014; 62:
209-219.
30.
OrtibusE, VerhoevenJ, SunaertS, CasteelsI, de CockP, LagaeL. Integrity of the inferior longitudinal fasciculus and impaired
object recognition in children: A diffusion tensor imaging study.
Dev Med Child Neurol. 2012;
54(1): 38-43. doi:
10.1111/j.1469-8749.2011.04147.x.
31.
BritoAR, VasconcelosMM, DominguesRC, Hygino da Cruz Jr.LC, Rodrigues LdeS, GasparettoEL, CalcadaCA. Diffusion tensor imaging findings in schoolaged autistic
children. Journal of Neuroimaging. 2009;
19: 337-343.
32.
JouRJ, JackowskiAP, PapademetrisX, RajeevanN, StaibLH, VolkmarFR. Diffusion tensor imaging in Autism Spectrum Disorders: preliminary
evidence of abnormal neural connectivity. The Australian and New
Zealand Journal of Psychiatry. 2010; 45:
153-162.
33.
JouRJ, MateljevicN, KaiserMD, SugrueDR, VolkmarFR, PelphreyKA. Structural neural phenotype of autism: Preliminary evidence from a
diffusion tensor imaging study using tract-based spatial statistics.
AJNR. American Journal of Neuroradiology. 2011;
32: 1607-1613.
34.
ShuklaDK, KeehnB, MullerRA. Tract-specific analyses of diffusion tensor imaging show
widespread white matter compromise in autism spectrum disorder.
Journal of Child Psychology and Psychiatry. 2011a;
52: 286-295.
35.
PuglieseL, CataniM, AmeisS, Dell'AcquaF, Thiebaut de SchottenM, MurphyC, RobertsonD, DeeleyQ, DalyE, MurphyDG. The anatomy of extended limbic pathways in Asperger syndrome: A
preliminary diffusion tensor imaging tractography study.
NeuroImage. 2009; 47:
427-434.18.
36.
TraversBG, et al. Diffusion tensor imaging in autism spectrum disorder: A
review. Autism Res. 2012;
5(5): 289-313.
37.
RoseJ, Cahill-RowleyK, VassarR, YeornK, StecherX, StevensonD, HintzS, Barnea-GoralyN. Neonatal brain microstructure correlates of neurodevelopment and
gait in preterm children 18-22 mo of age: MRI and DTI study.
Pediatric Research. 2015;
78(6): 700-708.
38.
SkranesJ, VangbergTR, KulsengS, et al. Clinical findings and white matter abnormalities seen on
diffusion tensor imaging in adolescents with very low birth weight.
Brain. 2007; 130:
654-66.
39.
DuerdenEG, CardD, LaxI, DonnerE, TaylorM. Alterations in frontostriatal pathways in children born very
preterm. Developmental Medicine and Child Neurology.
2013; 55: 952-958.
40.
DuerdenEG, FoongJ, ChauV, BransonH, PoskittKJ, GrunauRE, SynnesA, ZwickerJG, MillerSP. Tract-based spatial statistics in preterm-born neonates predicts
cognitive and motor outcomes at 18 months. American Journal of
Neuroradiology. 2015; 36(8):
1565-71. doi: 10.3174/ajnr.A4312.
41.
PavaineJ, YoungJM, MorganBR, ShroffM, RaybaudC, TaylorM. Diffusion tensor imaging-based assessment of white matter tracts
and visual-motor outcomes in very preterm neonates.
Neuroradiology. 2015 Dec. 21.
42.
de VriesAM, de GrootL. Transient dystonias revisited: A comparative study of preterm and
term children at 2 1/2 years of age. Developmental Medicine and
Child Neurology. 2002; 44:
415-421.
43.
SamsomJF, de GrootL. The influence of postural control on motility and hand function in
a group of ``high risk'' preterm infants at 1 year of age. Early
Human Development. 2000; 60:
101-113.
44.
BlyL. Components of Typical and Atypical Motor Development 2011, Neuro-Developmental
Treatment Association. http://www.ndta.org/marketplace.php.
45.
FlanaganJE, LandaR, BhatA, BaumanM. Head lag in infants at risk for autism: A preliminary
study. American Journal of Occupational Therapy.
2012; 66: 577-585. http://
dx.doi.org/10.5014/ajot.2012.004192.
