Skip to main content

Advertisement

Log in

Structural network performance for early diagnosis of spastic cerebral palsy in periventricular white matter injury

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Periventricular white matter injury (PWMI) is a common cause of spastic cerebral palsy (SCP). Diffusion tensor imaging (DTI) shows high sensitivity but moderate specificity for predicting SCP. The limited specificity may be due to the diverse and extensive brain injuries seen in infants with PWMI. We enrolled 72 infants with corrected age from 6 to 18 months in 3 groups: PWMI with SCP (n = 20), non-CP PWMI (n = 19), and control (n = 33) groups. We compared DTI-based brain network properties among the three groups and evaluated the diagnostic performance of brain network properties for SCP in PWMI infants. Our results show abnormal global parameters (reduced global and local efficiency, and increased shortest path length), and local parameters (reduced node efficiency) in the PWMI with SCP group. On logistic regression, the combined node efficiency of the bilateral precentral gyrus and right middle frontal gyrus had a high sensitivity (90%) and specificity (95%) for differentiating PWMI with SCP from non-CP PWMI, and significantly correlated with the Gross Motor Function Classification System scores. This study confirms that DTI-based brain network has great diagnostic performance for SCP in PWMI infants, and the combined node efficiency improves the diagnostic accuracy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Arrigoni, F., Peruzzo, D., Gagliardi, C., Maghini, C., Colombo, P., Iammarrone, F. S., Pierpaoli, C., Triulzi, F., & Turconi, A. C. (2016). Whole-brain DTI assessment of white matter damage in children with bilateral cerebral palsy: Evidence of involvement beyond the primary target of the anoxic insult. AJNR. American Journal of Neuroradiology, 37(7), 1347–1353.

    Article  CAS  Google Scholar 

  • Azzopardi, D. V., Strohm, B., Edwards, A. D., Dyet, L., Halliday, H. L., Juszczak, E., ... TOBY Study Group. (2009). Moderate hypothermia to treat perinatal asphyxial encephalopathy. The New England Journal of Medicine, 361(14), 1349–1358.

  • Back, S. A., & Rivkees, S. A. (2004). Emerging concepts in periventricular white matter injury. Seminars in Perinatology, 28(6), 405–414.

    Article  Google Scholar 

  • Back, S. A., Riddle, A., & Mcclure, M. M. (2007). Maturation-dependent vulnerability of perinatal white matter in premature birth. Stroke, 38(2), 724–730.

    Article  Google Scholar 

  • Bai, F., Shu, N., Yuan, Y., Shi, Y., Yu, H., Wu, D., Wang, J., Xia, M., He, Y., & Zhang, Z. (2012). Topologically convergent and divergent structural connectivity patterns between patients with remitted geriatric depression and amnestic mild cognitive impairment. The Journal of Neuroscience, 32(12), 4307–4318.

    Article  CAS  Google Scholar 

  • Ballesterplane, J., Schmidt, R., Laportahoyos, O., Junque, C., Vazquez, E., Delgado, I., ... Toro, E. (2017). Whole-brain structural connectivity in dyskinetic cerebral palsy and its association with motor and cognitive function. Human Brain Mapping, 38(9), 4594–4612.

  • Bosanquet, M., Copeland, L., Ware, R. S., & Boyd, R. N. (2013). A systematic review of tests to predict cerebral palsy in young children. Developmental Medicine and Child Neurology, 55(5), 418–426.

    Article  Google Scholar 

  • Buchanan, C. R., Pernet, C., Gorgolewski, K. J., Storkey, A., & Bastin, M. E. (2014). Test–retest reliability of structural brain networks from diffusion MRI. Neuroimage, 86, 231–243.

    Article  Google Scholar 

  • Burton, H., Dixit, S., Litkowski, P., & Wingert, J. R. (2009). Functional connectivity for somatosensory and motor cortex in spastic diplegia. Somatosensory & Motor Research, 26(4), 90–104.

    Article  Google Scholar 

  • Cavaliere, C., Aiello, M., Perri, C. D., Fernandezespejo, D., Owen, A. M., & Soddu, A. (2015). Diffusion tensor imaging and white matter abnormalities in patients with disorders of consciousness. Frontiers in Human Neuroscience, 8, 1028–1028.

    Article  Google Scholar 

  • Ceschin, R., Lee, V. K., Schmithorst, V., & Panigrahy, A. (2015). Regional vulnerability of longitudinal cortical association connectivity: Associated with structural network topology alterations in preterm children with cerebral palsy. NeuroImage: Clinical, 9, 322–337.

    Article  Google Scholar 

  • Cao, Q., Shu, N., An, L., Wang, P., Sun, L., Xia, M.R.,... He, Y. (2013). Probabilistic diffusion tractography and graph theory analysis reveal abnormal white matter structural connectivity networks in drug-naive boys with attention deficit/hyperactivity disorder. Journal of Neuroscience, 33(26),10676–10687. https://doi.org/10.1523/JNEUROSCI.4793-12.2013.

  • Coté, C. J., Wilson, S., & American Academy of Pediatrics., & American Academy of Pediatric Dentistry. (2016). Guidelines for monitoring and management of pediatric patients before, during, and after sedation for diagnostic and therapeutic procedures: Update 2016. Pediatrics, 138(1), e20161212.

    Article  Google Scholar 

  • Cui, Z., Zhong, S., Xu, P., He, Y., & Gong, G. (2013). PANDA: A pipeline toolbox for analyzing brain diffusion images. Frontiers in Human Neuroscience, 7, 42.

    PubMed  PubMed Central  Google Scholar 

  • Englander, Z. A., Pizoli, C. E., Batrachenko, A., Sun, J., Worley, G., Mikati, M. A., Kurtzberg, J., & Song, A. W. (2013). Diffuse reduction of white matter connectivity in cerebral palsy with specific vulnerability of long range fiber tracts. NeuroImage: Clinical, 2, 440–447.

    Article  Google Scholar 

  • Engle, W. A. (2006). A recommendation for the definition of “late preterm” (near-term) and the birth weight–gestational age classification system. Seminars in Perinatology, 30(1), 2–7.

    Article  Google Scholar 

  • Hagmann, P., Cammoun, L., Gigandet, X., Meuli, R., Honey, C. J., Wedeen, V. J., & Sporns, O. (2008). Mapping the structural Core of human cerebral cortex. PLoS Biology, 6(7), 1479–1493.

    Article  CAS  Google Scholar 

  • Hodge, J., Goodyear, B., Carlson, H., Wei, X. C., & Kirton, A. (2017). Segmental diffusion properties of the corticospinal tract and motor outcome in hemiparetic children with perinatal stroke. Journal of Child Neurology, 32(6), 550–559.

    Article  Google Scholar 

  • Holmström, L., Lennartsson, F., Eliasson, A. C., Flodmark, O., Clark, C., Tedroff, K., Forssberg, H., & Vollmer, B. (2011). Diffusion MRI in corticofugal fibers correlates with hand function in unilateral cerebral palsy. Neurology, 77(8), 775–783.

    Article  Google Scholar 

  • Hoon, A. H., Jr., Stashinko, E. E., Nagae, L. M., Lin, D. D., Keller, J., Bastian, A.,... Johnston, M. V. (2009). Sensory and motor deficits in children with cerebral palsy born preterm correlate with diffusion tensor imaging abnormalities in thalamocortical pathways. Developmental Medicine and Child Neurology, 51(9), 697–704.

  • Imamura, T., Ariga, H., Kaneko, M., Watanabe, M., Shibukawa, Y., Fukuda, Y.,... Fujiki, T. (2013). Neurodevelopmental outcomes of children with periventricular leukomalacia. Pediatrics and Neonatology, 54(6), 367–372.

  • Jiang, H., Li, X., Jin, C., Wang, M., Liu, C., Chan, K. C., & Yang, J. (2019). Early diagnosis of spastic cerebral palsy in infants with periventricular white matter injury using diffusion tensor imaging. AJNR. American Journal of Neuroradiology, 40(1), 162–168.

    Article  CAS  Google Scholar 

  • Jiang, H., Liu, H., He, H., Yang, J., Liu, Z., Huang, T., ... Li, X. (2020). Specific white matter lesions related to motor dysfunction in spastic cerebral palsy: A meta-analysis of diffusion tensor imaging studies. Journal of Child Neurology, 35(2), 146–154.

  • Knezevic, S., Stojanovic, N., Oros, A., Savic, D., Simovic, A., & Knezevic, J. (2011). Analysis of risk factors in the development of retinopathy of prematurity. Srpski Arhiv za Celokupno Lekarstvo, 139, 433–438.

    Article  Google Scholar 

  • Lasry, O., Shevell, M. I., Dagenais, L., & REPACQ Consortium. (2010). Cross-sectional comparison of periventricular leukomalacia in preterm and term children. Neurology, 74(17), 1386–1391.

    Article  Google Scholar 

  • Lee, J. D., Park, H. J., Park, E. S., Oh, M. K., Park, B., Rha, D. W., Cho, S. R., Kim, E. Y., Park, J. Y., Kim, C. H., Kim, D. G., & Park, C. I. (2011). Motor pathway injury in patients with periventricular leucomalacia and spastic diplegia. Brain, 134(Pt 4), 1199–1210.

    Article  Google Scholar 

  • Leech, R., & Sharp, D. J. (2014). The role of the posterior cingulate cortex in cognition and disease. Brain, 137(1), 12–32.

    Article  Google Scholar 

  • Li, X., Yang, J., Gao, J., Luo, X., Zhou, Z., Hu, Y., Wu, E. X., & Wan, M. (2014). A robust post-processing workflow for datasets with motion artifacts in diffusion kurtosis imaging. PLoS One, 9(4), e94592.

    Article  Google Scholar 

  • 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. Magnetic Resonance Imaging, 34(9), 1314–1321.

    Article  Google Scholar 

  • Löbel, U., Sedlacik, J., Güllmar, D., Kaiser, W. A., Reichenbach, J. R., & Mentzel, H. J. (2009). Diffusion tensor imaging: The normal evolution of ADC, RA, FA, and eigenvalues studied in multiple anatomical regions of the brain. Neuroradiology, 51(4), 253–263.

    Article  Google Scholar 

  • Mu, X., Wang, Z., Nie, B., Duan, S., Ma, Q., Dai, G., Wu, C., Dong, Y., Shan, B., & Ma, L. (2018). Altered regional and circuit resting-state activity in patients with occult spastic diplegic cerebral palsy. Pediatrics and Neonatology, 59(4), 345–351.

    Article  Google Scholar 

  • Murakami, A., Morimoto, M., Yamada, K., Kizu, O., Nishimura, A., Nishimura, T., & Sugimoto, T. (2008). Fiber-tracking techniques can predict the degree of neurologic impairment for periventricular leukomalacia. Pediatrics, 122(3), 500–506.

    Article  Google Scholar 

  • Novak, I., Morgan, C., Adde, L., Blackman, J. A., Boyd, R. N., Brunstrom-Hernandez, J.,... Badawi, N. (2017). Early, accurate diagnosis and early intervention in cerebral palsy: Advances in diagnosis and treatment. JAMA Pediatrics, 171(9), 897–907.

  • Qi, S., Meesters, S., Nicolay, K., Romeny, B. M. T. H., & Ossenblok, P. (2016). Structural brain network: What is the effect of LiFE optimization of whole brain Tractography? Frontiers in Computational Neuroscience, 10, 12–12.

    Article  Google Scholar 

  • Qin, Y., Li, Y., Sun, B., He, H., Peng, R., Zhang, T.,... Yao, D. (2018). Functional connectivity alterations in children with spastic and dyskinetic cerebral palsy. Neural Plasticity, 2018, 7058953.

  • Reid, L. B., Cunnington, R., Boyd, R. N., & Rose, S. E. (2016). Surface-based fMRI-driven diffusion tractography in the presence of significant brain pathology: A study linking structure and function in cerebral palsy. PLoS One, 11(8), e0162271.

    Article  Google Scholar 

  • Rosenbaum, P., Paneth, N., Leviton, A., Goldstein, M., Bax, M., Damiano, D., Dan, B., & Jacobsson, B. (2007). A report : The definition and classification of cerebral palsy April 2006. Developmental Medicine and Child Neurology. Supplement, 109, 8–14.

    PubMed  Google Scholar 

  • Rubinov, M., & Sporns, O. (2010). Complex network measures of brain connectivity: Uses and interpretations. Neuroimage, 52(3), 1059–1069.

    Article  Google Scholar 

  • Scheck, S. M., Boyd, R. N., & Rose, S. E. (2012). New insights into the pathology of white matter tracts in cerebral palsy from diffusion magnetic resonance imaging: A systematic review. Developmental Medicine and Child Neurology, 54(8), 684–696.

    Article  Google Scholar 

  • Shu, N., Wang, X., Bi, Q., Zhao, T., & Han, Y. (2018). Disrupted topologic efficiency of white matter structural connectome in individuals with subjective cognitive decline. Radiology, 286(1), 229–238.

    Article  Google Scholar 

  • Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T.E., Johansen-Berg, H.,... Matthews, P. M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage, 23(Suppl 1), S208-S219.

  • Trivedi, R., Agarwal, S., Rathore, R. K. S., Saksena, S., Tripathi, R. P., Malik, G. K., ... Gupta, R. K. (2009). Understanding development and lateralization of major cerebral Fiber bundles in pediatric population through quantitative diffusion tensor Tractography. Pediatric Research, 66(6), 636–641.

  • Trivedi, R., Agarwal, S., Shah, V., Goyel, P., Paliwal, V. K., Rathore, R. K., & Gupta, R. K. (2010). Correlation of quantitative sensorimotor tractography with clinical grade of cerebral palsy. Neuroradiology, 52(8), 759–765.

    Article  Google Scholar 

  • Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B., & Joliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage, 15(1), 273–289.

    Article  CAS  Google Scholar 

  • Van’t Hooft, J., van der Lee, J. H., Opmeer, B. C., Aarnoudse-Moens, C. S., Leenders, A. G., Mol, B. W., & de Haan, T. R. (2015). Predicting developmental outcomes in premature infants by term equivalent MRI: Systematic review and meta-analysis. Systematic Reviews, 4, 71.

    Article  Google Scholar 

  • Wang, S., Wu, E. X., Cai, K., Lau, H. F., Cheung, P. T., & Khong, P. L. (2009). Mild hypoxic-ischemic injury in the neonatal rat brain: Longitudinal evaluation of white matter using diffusion tensor MR imaging. AJNR. American Journal of Neuroradiology, 30(10), 1907–1913.

    Article  CAS  Google Scholar 

  • Wang, J., Wang, X., Xia, M., Liao, X., Evans, A., & He, Y. (2015). GRETNA: A graph theoretical network analysis toolbox for imaging connectomics. Frontiers in Human Neuroscience, 9, 386.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Woodward, K. E., Carlson, H. L., Kuczynski, A. M., Saunders, J., Hodge, J., & Kirton, A. (2019). Sensory-motor network functional connectivity in children with unilateral cerebral palsy secondary to perinatal stroke. NeuroImage: Clinical, 21, 101670.

    Article  CAS  Google Scholar 

  • Xia, M., Wang, J., & He, Y. (2013). BrainNet biewer: A network visualization tool for human brain connectomics. PLoS One, 8(7), e68910.

    Article  CAS  Google Scholar 

  • Yuan, K., Yu, D., Zhao, M., Li, M., Wang, R., Li, Y., Manza, P., Shokri-Kojori, E., Wiers, C. E., Wang, G. J., & Tian, J. (2018). Abnormal frontostriatal tracts in young male tobacco smokers. Neuroimage, 183, 346–355.

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by the National Natural Science Foundation of China (81971581, 81771810, 81901823, 81901732 and 81760309), the Innovation Team Project of Natural Science Fund of Shaanxi Province (2019TD-018), the National Key Research and Development Program of China (2016YFC0100300), the Project Funded by China Postdoctoral Science Foundation (No. 2019 M653659), and the Natural Science Basic Research Plan in Shaanxi Province of China (No.2019JQ-198).The authors are grateful to Dr. Liming Liu and Dr. Jie Yue at the Department of Child Health Care for the diagnosis of CP.

Author information

Authors and Affiliations

Authors

Contributions

Guarantors of integrity of entire study, HJ, HL, TH, JY, XL; study design, HJ, JY; Data acquisition, HJ, HL, LW, FW, CL, MW; data analysis, HJ, XL, CJ; manuscript drafting, HJ, HL, TH, XL; manuscript revision, all authors.

Corresponding authors

Correspondence to Jian Yang or Xianjun Li.

Ethics declarations

This retrospective cohort study was approved by the institutional review board of the First Affiliated Hospital of Xi’an Jiaotong University. Written informed consent was obtained from parents of the enrolled infants.

Declaration of interest

The authors have stated that they had no interests which might be perceived as posing a conflict or bias

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 23 kb)

ESM 2

(PDF 1186 kb)

ESM 3

(DOCX 34 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, H., Liu, H., Huang, T. et al. Structural network performance for early diagnosis of spastic cerebral palsy in periventricular white matter injury. Brain Imaging and Behavior 15, 855–864 (2021). https://doi.org/10.1007/s11682-020-00295-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-020-00295-6

Keywords

Navigation