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Tractography of the corticospinal tracts in infants with focal perinatal injury: comparison with normal controls and to motor development

  • Paediatric Neuroradiology
  • Published:
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Abstract

Introduction

Our aims were to (1) assess the corticospinal tracts (CSTs) in infants with focal injury and healthy term controls using probabilistic tractography and (2) to correlate the conventional magnetic resonance imaging (MRI) and tractography findings in infants with focal injury with their later motor function.

Methods

We studied 20 infants with focal lesions and 23 controls using MRI and diffusion tensor imaging. Tract volume, fractional anisotropy (FA), apparent diffusion coefficient (ADC) values, axial diffusivity and radial diffusivity (RD) of the CSTs were determined. Asymmetry indices (AIs) were calculated by comparing ipsilateral to contralateral CSTs. Motor outcome was assessed using a standardized neurological examination.

Results

Conventional MRI was able to predict normal motor development (n = 9) or hemiplegia (n = 6). In children who developed a mild motor asymmetry (n = 5), conventional MRI predicted a hemiplegia in two and normal motor development in three infants. The AIs for tract volume, FA, ADC and RD showed a significant difference between controls and infants who developed a hemiplegia, and RD also showed a significant difference in AI between controls and infants who developed a mild asymmetry.

Conclusion

Conventional MRI was able to predict subsequent normal motor development or hemiplegia following focal injury in newborn infants. Measures of RD obtained from diffusion tractography may offer additional information for predicting a subsequent asymmetry in motor function.

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Abbreviations

AD:

Axial diffusivity

ADC:

Apparent diffusion coefficient

AI:

Asymmetry index

AIS:

Arterial ischemic stroke

CP:

Cerebral peduncle

CST:

Corticospinal tract

DTI:

Diffusion tensor imaging

DWI:

Diffusion weighted imaging

FA:

Fractional anisotropy

HPI:

Haemorrhagic parenchymal infarction

MCA:

Middle cerebral artery

MRI:

Magnetic resonance imaging

PLIC:

Posterior limb of the internal capsule

RD:

Radial diffusivity

SI:

Signal intensity

TE:

Echo time

TEA:

Term equivalent age

TR:

Repetition time

WM:

White matter

References

  1. Benders MJ, Groenendaal F, Uiterwaal CS, Nikkels PG, Bruinse HW, Nievelstein RA et al (2007) Maternal and infant characteristics associated with perinatal arterial stroke in the preterm infant. Stroke 38:1759–1765

    Article  PubMed  Google Scholar 

  2. Mercuri E, Rutherford M, Cowan F, Pennock J, Counsell S, Papadimitriou M et al (1999) Early prognostic indicators of outcome in infants with neonatal cerebral infarction: a clinical, electroencephalogram, and magnetic resonance imaging study. Pediatrics 103:39–46

    Article  PubMed  CAS  Google Scholar 

  3. deVeber GA, MacGregor D, Curtis R, Mayank S (2000) Neurologic outcome in survivors of childhood arterial ischemic stroke and sinovenous thrombosis. J Child Neurol 15:316–324

    Article  PubMed  CAS  Google Scholar 

  4. Sreenan C, Bhargava R, Robertson CM (2000) Cerebral infarction in the term newborn: clinical presentation and long-term outcome. J Pediatr 137:351–355

    Article  PubMed  CAS  Google Scholar 

  5. de Vries LS, Groenendaal F, van Haastert I, Eken P, Rademaker KJ, Meiners LC (1999) Asymmetrical myelination of the posterior limb of the internal capsule in infants with periventricular haemorrhagic infarction: an early predictor of hemiplegia. Neuropediatrics 30:314–319

    Article  PubMed  Google Scholar 

  6. Huppi PS, Maier SE, Peled S, Zientara GP, Barnes PD, Jolesz FA et al (1998) Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res 44:584–590

    Article  PubMed  CAS  Google Scholar 

  7. Neil JJ, Shiran SI, McKinstry RC, Schefft GL, Snyder AZ, Almli CR et al (1998) Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotropy measured by using diffusion tensor MR imaging. Radiology 209:57–66

    PubMed  CAS  Google Scholar 

  8. Seghier ML, Lazeyras F, Zimine S, Maier SE, Hanquinet S, Delavelle J et al (2004) Combination of event-related fMRI and diffusion tensor imaging in an infant with perinatal stroke. NeuroImage 21:463–472

    Article  PubMed  Google Scholar 

  9. Ward P, Counsell S, Allsop J, Cowan F, Shen Y, Edwards D et al (2006) Reduced fractional anisotropy on diffusion tensor magnetic resonance imaging after hypoxic–ischemic encephalopathy. Pediatrics 117:e619–e630

    Article  PubMed  Google Scholar 

  10. Behrens TE, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CA, Boulby PA et al (2003) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6:750–757

    Article  PubMed  CAS  Google Scholar 

  11. Counsell SJ, Dyet LE, Larkman DJ, Nunes RG, Boardman JP, Allsop JM et al (2007) Thalamo-cortical connectivity in children born preterm mapped using probabilistic magnetic resonance tractography. NeuroImage 34:896–904

    Article  PubMed  Google Scholar 

  12. Dudink J, Mercuri E, Al-Nakib L, Govaert P, Counsell SJ, Rutherford MA et al (2009) Evolution of unilateral perinatal arterial ischemic stroke on conventional and diffusion-weighted MR imaging. Am J Neuroradiol 30:998–1004

    Article  PubMed  CAS  Google Scholar 

  13. Krishnamoorthy KS, Soman TB, Takeoka M, Schaefer PW (2000) Diffusion-weighted imaging in neonatal cerebral infarction: clinical utility and follow-up. J Child Neurol 15:592–602

    Article  PubMed  CAS  Google Scholar 

  14. Kirton A, Shroff M, Visvanathan T, deVeber G (2007) Quantified corticospinal tract diffusion restriction predicts neonatal stroke outcome. Stroke 38:974–980

    Article  PubMed  Google Scholar 

  15. de Vries LS, Van der Grond J, van Haastert IC, Groenendaal F (2005) Prediction of outcome in new-born infants with arterial ischaemic stroke using diffusion-weighted magnetic resonance imaging. Neuropediatrics 36:12–20

    Article  PubMed  Google Scholar 

  16. Gilmore JH, Lin W, Corouge I, Vetsa YS, Smith JK, Kang C et al (2007) Early postnatal development of corpus callosum and corticospinal white matter assessed with quantitative tractography. Am J Neuroradiol 28:1789–1795

    Article  PubMed  CAS  Google Scholar 

  17. Aeby A, Liu Y, De Tiege X, Denolin V, David P, Baleriaux D et al (2009) Maturation of thalamic radiations between 34 and 41 weeks’ gestation: a combined voxel-based study and probabilistic tractography with diffusion tensor imaging. Am J Neuroradiol 30:1780–1786

    Article  PubMed  CAS  Google Scholar 

  18. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23:S208–S219

    Article  PubMed  Google Scholar 

  19. Bassi L, Chew A, Merchant N, Ball G, Ramenghi L, Boardman J et al (2011) Diffusion tensor imaging in preterm infants with punctate white matter lesions. Pediatr Res 69:561–566

    Article  PubMed  Google Scholar 

  20. Haataja L, Mercuri E, Regev R, Cowan F, Rutherford M, Dubowitz V et al (1999) Optimality score for the neurologic examination of the infant at 12 and 18 months of age. J Pediatr 135:153–161

    Article  PubMed  CAS  Google Scholar 

  21. Choi CH, Lee JM, Koo BB, Park JS, Kim DS, Kwon JS et al (2010) Sex differences in the temporal lobe white matter and the corpus callosum: a diffusion tensor tractography study. Neuroreport 21:73–77

    Article  PubMed  Google Scholar 

  22. Mercuri E, Barnett A, Rutherford M, Guzzetta A, Haataja L, Cioni G et al (2004) Neonatal cerebral infarction and neuromotor outcome at school age. Pediatrics 113:95–100

    Article  PubMed  Google Scholar 

  23. Puig J, Pedraza S, Blasco G, Daunis IE, Prats A, Prados F et al (2010) Wallerian degeneration in the corticospinal tract evaluated by diffusion tensor imaging correlates with motor deficit 30 days after middle cerebral artery ischemic stroke. Am J Neuroradiol 31:1324–1330

    Article  PubMed  Google Scholar 

  24. Pierpaoli C, Barnett A, Pajevic S, Chen R, Penix LR, Virta A et al (2001) Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. NeuroImage 13:1174–1185

    Article  PubMed  CAS  Google Scholar 

  25. Werring DJ, Toosy AT, Clark CA, Parker GJ, Barker GJ, Miller DH et al (2000) Diffusion tensor imaging can detect and quantify corticospinal tract degeneration after stroke. J Neurol Neurosurg Psychiatry 69:269–272

    Article  PubMed  CAS  Google Scholar 

  26. Bouza H, Dubowitz LM, Rutherford M, Pennock JM (1994) Prediction of outcome in children with congenital hemiplegia: a magnetic resonance imaging study. Neuropediatrics 25:60–66

    Article  PubMed  CAS  Google Scholar 

  27. Adams E, Chau V, Poskitt KJ, Grunau RE, Synnes A, Miller SP (2010) Tractography-based quantitation of corticospinal tract development in premature newborns. J Pediatr 156:882–888

    Article  PubMed  Google Scholar 

  28. Liu Y, Baleriaux D, Kavec M, Metens T, Absil J, Denolin V 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

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank the Medical Research Council (UK) and Imperial College Healthcare Comprehensive Biomedical Research Centre Funding Scheme.

Conflict of interest

We declare that we have no conflict of interest.

Author information

Authors and Affiliations

  1. Centre for the Developing Brain, Imperial College, Hammersmith Campus, London, W12 0NN, UK

    Elise Roze, Polly A. Harris, Gareth Ball, Leire Zubiaurre Elorza, Rodrigo M. Braga, Joanna M. Allsop, Nazakat Merchant, Tomoki Arichi, A. David Edwards, Mary A. Rutherford, Frances M. Cowan & Serena J. Counsell

  2. Robert Steiner MR Unit, MRC Clinical Sciences Centre, Hammersmith Hospital, Du Cane Road, London, W12 0HS, UK

    Elise Roze, Polly A. Harris, Gareth Ball, Leire Zubiaurre Elorza, Rodrigo M. Braga, Joanna M. Allsop, Nazakat Merchant, Tomoki Arichi, A. David Edwards, Frances M. Cowan & Serena J. Counsell

  3. Division of Neonatology, Imperial College Healthcare NHS Trust, London, W12 0HS, UK

    Nazakat Merchant, Emma Porter, Tomoki Arichi, A. David Edwards, Mary A. Rutherford & Frances M. Cowan

  4. Division of Neonatology, Beatrix Children’s Hospital, University Medical Center Groningen, Groningen, the Netherlands

    Elise Roze

  5. Department of Psychiatry and Clinical Psychobiology, Faculty of Medicine, University of Barcelona, Barcelona, 08036, Spain

    Leire Zubiaurre Elorza

Authors
  1. Elise Roze
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  2. Polly A. Harris
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  3. Gareth Ball
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  8. Emma Porter
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  9. Tomoki Arichi
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  10. A. David Edwards
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Corresponding author

Correspondence to Serena J. Counsell.

Electronic supplementary material

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Table S1

Patient characteristics. EmCS emergency caesarean section, SVD spontaneous vaginal delivery, PROM prolonged rupture of membranes, IUGR intrauterine growth restriction, HIE hypoxic–ischaemic encephalopathy, GA gestational age, M male, F female, BMI body mass index (DOCX 15 kb)

Table S2

Diffusion characteristics of the corticospinal tracts in infants with lesions and controls. #Indicates that connectivity distributions could not be generated (DOCX 15 kb)

Figure S1A

Asymmetry index for tract volume (a), FA (b), ADC values (c), axial diffusivity (d) and radial diffusivity (e) of the corticospinal tract in newborns with ischaemic lesions and controls. AI asymmetry index. Key: normal controls (diamond), cases with normal motor outcome (square), cases who developed an asymmetry (circle), cases who developed a hemiplegia (cross) (JPEG 7 kb)

High Resolution (TIFF 47 kb)

Figure S1B

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Figure S1C

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Figure S1D

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Figure S1E

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Roze, E., Harris, P.A., Ball, G. et al. Tractography of the corticospinal tracts in infants with focal perinatal injury: comparison with normal controls and to motor development. Neuroradiology 54, 507–516 (2012). https://doi.org/10.1007/s00234-011-0969-5

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  • DOI: https://doi.org/10.1007/s00234-011-0969-5

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