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Aberrant myelination in patients with Sturge-Weber syndrome analyzed using synthetic quantitative magnetic resonance imaging

  • Paediatric Neuroradiology
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Abstract

Purpose

Accelerated myelination in the affected hemisphere has been demonstrated previously in patients with Sturge-Weber syndrome (SWS). This prospective study investigated myelin-related changes in patients with unilateral SWS using synthetic quantitative magnetic resonance imaging (qMRI).

Methods

Fourteen children with unilateral SWS were categorized according to age, i.e., ≤ 2 years (group A, n = 5, mean age 1.1 years, 3 males) and > 2 years (group B, n = 9, mean age 3.9 years, 4 males). All children underwent two-dimensional synthetic qMRI. The myelin volume in the cerebral hemisphere and white matter (WM) myelin volume fraction (MVF), proton density (PD), R1 and R2 relaxation rates ipsilateral to the leptomeningeal enhancement, and/or a port-wine birthmark were compared with the corresponding values in the contralateral hemisphere.

Results

In group A, 3 patients had a higher myelin volume in the ipsilateral hemisphere and a higher MVF, R1, and R2 and lower PD in the ipsilateral WM than on the contralateral side; the findings were the opposite in the remaining two patients. All patients in group B had a significantly lower myelin volume in the ipsilateral hemisphere (P < 0.05) and a lower MVF and R1 and higher PD in the ipsilateral WM than on the contralateral side (P < 0.0125).

Conclusion

Higher estimated myelin was observed on the ipsilateral side in some patients aged ≤ 2 years and lower myelin on the ipsilateral side in all older patients. Synthetic qMRI might be useful for showing myelin-related abnormalities in SWS.

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References

  1. Lo W, Marchuk DA, Ball KL, Juhasz C, Jordan LC, Ewen JB, Comi A, Brain Vascular Malformation Consortium National Sturge-Weber Syndrome W (2012) Updates and future horizons on the understanding, diagnosis, and treatment of Sturge-Weber syndrome brain involvement. Dev Med Child Neurol 54(3):214–223. https://doi.org/10.1111/j.1469-8749.2011.04169.x

    Article  PubMed  Google Scholar 

  2. Sundaram SK, Michelhaugh SK, Klinger NV, Kupsky WJ, Sood S, Chugani HT, Mittal S, Juhasz C (2017) GNAQ mutation in the venous vascular malformation and underlying brain tissue in Sturge-Weber syndrome. Neuropediatrics 48(5):385–389. https://doi.org/10.1055/s-0037-1603515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Alkonyi B, Govindan RM, Chugani HT, Behen ME, Jeong JW, Juhasz C (2011) Focal white matter abnormalities related to neurocognitive dysfunction: an objective diffusion tensor imaging study of children with Sturge-Weber syndrome. Pediatr Res 69(1):74–79. https://doi.org/10.1203/PDR.0b013e3181fcb285

    Article  PubMed  PubMed Central  Google Scholar 

  4. Adamsbaum C, Pinton F, Rolland Y, Chiron C, Dulac O, Kalifa G (1996) Accelerated myelination in early Sturge-Weber syndrome: MRI-SPECT correlations. Pediatr Radiol 26(11):759–762

    Article  CAS  PubMed  Google Scholar 

  5. Andica C, Hagiwara A, Nakazawa M, Tsuruta K, Takano N, Hori M, Suzuki H, Sugano H, Arai H, Aoki S (2016) The advantage of synthetic MRI for the visualization of early white matter change in an infant with Sturge-Weber syndrome. Magn Reson Med Sci 15(4):347–348. https://doi.org/10.2463/mrms.ci.2015-0164

    Article  PubMed  PubMed Central  Google Scholar 

  6. George U, Rathore S, Nittala P (2010) MR demonstration of accelerated myelination in early Sturge Weber syndrome. Neurol India 58(2):336–337. https://doi.org/10.4103/0028-3886.63769

    Article  PubMed  Google Scholar 

  7. Hagiwara A, Andica C, Hori M, Aoki S (2017) Synthetic MRI showed increased myelin partial volume in the white matter of a patient with Sturge-Weber syndrome. Neuroradiology 59(11):1065–1066. https://doi.org/10.1007/s00234-017-1908-x

    Article  PubMed  Google Scholar 

  8. Jacoby CG, Yuh WT, Afifi AK, Bell WE, Schelper RL, Sato Y (1987) Accelerated myelination in early Sturge-Weber syndrome demonstrated by MR imaging. J Comput Assist Tomogr 11(2):226–231

    Article  CAS  PubMed  Google Scholar 

  9. Moritani T, Kim J, Sato Y, Bonthius D, Smoker WR (2008) Abnormal hypermyelination in a neonate with Sturge-Weber syndrome demonstrated on diffusion-tensor imaging. J Magn Reson Imaging 27(3):617–620. https://doi.org/10.1002/jmri.21248

    Article  PubMed  Google Scholar 

  10. Pfund Z, Kagawa K, Juhasz C, Shen C, Lee JS, Chugani DC, Muzik O, Chugani HT (2003) Quantitative analysis of gray- and white-matter volumes and glucose metabolism in Sturge-Weber syndrome. J Child Neurol 18(2):119–126. https://doi.org/10.1177/08830738030180021501

    Article  PubMed  Google Scholar 

  11. Porto L, Kieslich M, Yan B, Zanella FE, Lanfermann H (2006) Accelerated myelination associated with venous congestion. Eur Radiol 16(4):922–926. https://doi.org/10.1007/s00330-005-0044-x

    Article  CAS  PubMed  Google Scholar 

  12. Adams ME, Aylett SE, Squier W, Chong W (2009) A spectrum of unusual neuroimaging findings in patients with suspected Sturge-Weber syndrome. AJNR Am J Neuroradiol 30(2):276–281. https://doi.org/10.3174/ajnr.A1350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Comi AM, Sahin M, Hammill A, Kaplan EH, Juhasz C, North P, Ball KL, Levin AV, Cohen B, Morris J, Lo W, Roach ES, Sturge-Weber Syndrome Research W (2016) Leveraging a Sturge-Weber gene discovery: an agenda for future research. Pediatr Neurol 58:12–24. https://doi.org/10.1016/j.pediatrneurol.2015.11.009

    Article  PubMed  PubMed Central  Google Scholar 

  14. Sled JG, Nossin-Manor R (2013) Quantitative MRI for studying neonatal brain development. Neuroradiology 55(Suppl 2):97–104. https://doi.org/10.1007/s00234-013-1235-9

    Article  PubMed  Google Scholar 

  15. Hagiwara A, Warntjes M, Hori M, Andica C, Nakazawa M, Kumamaru KK, Abe O, Aoki S (2017) SyMRI of the brain: rapid quantification of relaxation rates and proton density, with synthetic MRI, automatic brain segmentation, and myelin measurement. Investig Radiol 52(10):647–657. https://doi.org/10.1097/RLI.0000000000000365

    Article  Google Scholar 

  16. Hagiwara A, Hori M, Cohen-Adad J, Nakazawa M, Suzuki Y, Kasahara A, Horita M, Haruyama T, Andica C, Maekawa T, Kamagata K, Kumamaru KK, Abe O, Aoki S (2019) Linearity, bias, intrascanner repeatability, and interscanner reproducibility of quantitative multidynamic multiecho sequence for rapid simultaneous relaxometry at 3 T: a validation study with a standardized phantom and healthy controls. Investig Radiol 54:39–47. https://doi.org/10.1097/RLI.0000000000000510

    Article  Google Scholar 

  17. Andica C, Hagiwara A, Hori M, Nakazawa M, Goto M, Koshino S, Kamagata K, Kumamaru KK, Aoki S (2018) Automated brain tissue and myelin volumetry based on quantitative MR imaging with various in-plane resolutions. J Neuroradiol 45(3):164–168. https://doi.org/10.1016/j.neurad.2017.10.002

    Article  CAS  PubMed  Google Scholar 

  18. Warntjes JBM, Persson A, Berge J, Zech W (2017) Myelin detection using rapid quantitative MR imaging correlated to macroscopically registered Luxol fast blue-stained brain specimens. AJNR Am J Neuroradiol 38(6):1096–1102. https://doi.org/10.3174/ajnr.A5168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Hagiwara A, Hori M, Kamagata K, Warntjes M, Matsuyoshi D, Nakazawa M, Ueda R, Andica C, Koshino S, Maekawa T, Irie R, Takamura T, Kumamaru KK, Abe O, Aoki S (2018) Myelin measurement: comparison between simultaneous tissue relaxometry, magnetization transfer saturation index, and T1w/T2w ratio methods. Sci Rep 8(1):10554. https://doi.org/10.1038/s41598-018-28852-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Hagiwara A, Hori M, Yokoyama K, Nakazawa M, Ueda R, Horita M, Andica C, Abe O, Aoki S (2017) Analysis of white matter damage in patients with multiple sclerosis via a novel in vivo magnetic resonance method for measuring myelin, axons, and G-ratio. AJNR Am J Neuroradiol 38:1934–1940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Wallaert L, Hagiwara A, Andica C, Hori M, Yamashiro K, Koshino S, Maekawa T, Kamagata K, Aoki S (2017) The advantage of synthetic MRI for the visualization of anterior temporal pole lesions on double inversion recovery (DIR), phase-sensitive inversion recovery (PSIR), and myelin images in a patient with CADASIL. Magn Reson Med Sci 17:275–276. https://doi.org/10.2463/mrms.ci.2017-0110

    Article  PubMed  PubMed Central  Google Scholar 

  22. Tanenbaum LN, Tsiouris AJ, Johnson AN, Naidich TP, DeLano MC, Melhem ER, Quarterman P, Parameswaran SX, Shankaranarayanan A, Goyen M, Field AS (2017) Synthetic MRI for clinical neuroimaging: results of the MAGnetic resonance image Compilation (MAGiC) prospective, multicenter, multireader trial. AJNR Am J Neuroradiol 38(6):1103–1110. https://doi.org/10.3174/ajnr.A5227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. West H, Leach JL, Jones BV, Care M, Radhakrishnan R, Merrow AC, Alvarado E, Serai SD (2017) Clinical validation of synthetic brain MRI in children: initial experience. Neuroradiology 59(1):43–50. https://doi.org/10.1007/s00234-016-1765-z

    Article  PubMed  Google Scholar 

  24. Kim HG, Moon WJ, Han J, Choi JW (2017) Quantification of myelin in children using multiparametric quantitative MRI: a pilot study. Neuroradiology 59:1043–1051. https://doi.org/10.1007/s00234-017-1889-9

    Article  PubMed  Google Scholar 

  25. Lee SM, Choi YH, You SK, Lee WK, Kim WH, Kim HJ, Lee SY, Cheon H (2018) Age-related changes in tissue value properties in children: simultaneous quantification of relaxation times and proton density using synthetic magnetic resonance imaging. Investig Radiol 53(4):236–245. https://doi.org/10.1097/RLI.0000000000000435

    Article  Google Scholar 

  26. McAllister A, Leach J, West H, Jones B, Zhang B, Serai S (2017) Quantitative synthetic MRI in children: normative intracranial tissue segmentation values during development. AJNR Am J Neuroradiol 38(12):2364–2372. https://doi.org/10.3174/ajnr.A5398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Serai S, Dudley J, Leach J (2019) Comparison of whole brain segmentation and volume estimation in children and young adults using SPM and SyMRI. Clin Imaging 57:77–82. https://doi.org/10.1016/j.clinimag.2019.05.008

    Article  PubMed  Google Scholar 

  28. Andica C, Hagiwara A, Hori M, Kamagata K, Koshino S, Maekawa T, Suzuki M, Fujiwara H, Ikeno M, Shimizu T, Suzuki H, Sugano H, Arai H, Aoki S (2019) Review of synthetic MRI in pediatric brains: basic principle of MR quantification, its features, clinical applications, and limitations. J Neuroradiol 46:268–275. https://doi.org/10.1016/j.neurad.2019.02.005

    Article  PubMed  Google Scholar 

  29. Barkovich AJ (2000) Concepts of myelin and myelination in neuroradiology. AJNR Am J Neuroradiol 21(6):1099–1109

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Alkonyi B, Chugani HT, Juhasz C (2011) Transient focal cortical increase of interictal glucose metabolism in Sturge-Weber syndrome: implications for epileptogenesis. Epilepsia 52(7):1265–1272. https://doi.org/10.1111/j.1528-1167.2011.03066.x

    Article  PubMed  PubMed Central  Google Scholar 

  31. Cheepsunthorn P, Palmer C, Menzies S, Roberts RL, Connor JR (2001) Hypoxic/ischemic insult alters ferritin expression and myelination in neonatal rat brains. J Comp Neurol 431(4):382–396

    Article  CAS  PubMed  Google Scholar 

  32. Hamilton SP, Rome LH (1994) Stimulation of in vitro myelin synthesis by microglia. Glia 11(4):326–335. https://doi.org/10.1002/glia.440110405

    Article  CAS  PubMed  Google Scholar 

  33. Rischke R, Krieglstein J (1991) Postischemic neuronal damage causes astroglial activation and increase in local cerebral glucose utilization of rat hippocampus. J Cereb Blood Flow Metab 11(1):106–113. https://doi.org/10.1038/jcbfm.1991.12

    Article  CAS  PubMed  Google Scholar 

  34. John F, Maqbool M, Jeong JW, Agarwal R, Behen ME, Juhasz C (2018) Deep cerebral vein expansion with metabolic and neurocognitive recovery in Sturge-Weber syndrome. Ann Clin Transl Neurol 5(4):502–506. https://doi.org/10.1002/acn3.546

    Article  PubMed  PubMed Central  Google Scholar 

  35. Roach ES (1992) Neurocutaneous syndromes. Pediatr Clin N Am 39(4):591–620

    Article  CAS  Google Scholar 

  36. Waelchli R, Aylett SE, Robinson K, Chong WK, Martinez AE, Kinsler VA (2014) New vascular classification of port-wine stains: improving prediction of Sturge-Weber risk. Br J Dermatol 171(4):861–867. https://doi.org/10.1111/bjd.13203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Plateroti AM, Plateroti R, Mollo R, Librando A, Contestabile MT, Fenicia V (2017) Sturge-Weber syndrome associated with monolateral ocular melanocytosis, iris mammillations, and diffuse choroidal haemangioma. Case Rep Ophthalmol 8(2):375–384. https://doi.org/10.1159/000477612

    Article  PubMed  PubMed Central  Google Scholar 

  38. Yamaguchi K, Lonic D, Chen C, Lo LJ (2016) Correction of facial deformity in Sturge-Weber syndrome. Plast Reconstr Surg Glob Open 4(8):e843. https://doi.org/10.1097/GOX.0000000000000843

    Article  PubMed  PubMed Central  Google Scholar 

  39. Warne RR, Carney OM, Wang G, Bhattacharya D, Chong WK, Aylett SE, Mankad K (2018) The bone does not predict the brain in Sturge-Weber syndrome. AJNR Am J Neuroradiol. https://doi.org/10.3174/ajnr.A5722

  40. Sujansky E, Conradi S (1995) Sturge-Weber syndrome: age of onset of seizures and glaucoma and the prognosis for affected children. J Child Neurol 10(1):49–58. https://doi.org/10.1177/088307389501000113

    Article  CAS  PubMed  Google Scholar 

  41. Lee JS, Asano E, Muzik O, Chugani DC, Juhasz C, Pfund Z, Philip S, Behen M, Chugani HT (2001) Sturge-Weber syndrome: correlation between clinical course and FDG PET findings. Neurology 57(2):189–195

    Article  CAS  PubMed  Google Scholar 

  42. Jagtap SA, Srinivas G, Radhakrishnan A, Harsha KJ (2013) A clinician’s dilemma: Sturge-Weber syndrome ‘without facial nevus’!! Ann Indian Acad Neurol 16(1):118–120. https://doi.org/10.4103/0972-2327.107725

    Article  PubMed  PubMed Central  Google Scholar 

  43. Arulrajah S, Ertan G, A MC, Tekes A, Lin DL, Huisman TA (2010) MRI with diffusion-weighted imaging in children and young adults with simultaneous supra- and infratentorial manifestations of Sturge-Weber syndrome. J Neuroradiol 37(1):51–59. https://doi.org/10.1016/j.neurad.2009.05.001

    Article  CAS  PubMed  Google Scholar 

  44. Guseo A (1975) Ultrastructure of calcification in Sturge-Weber disease. Virchows Arch A Pathol Anat Histol 366(4):353–356

    Article  CAS  PubMed  Google Scholar 

  45. Wu J, Tarabishy B, Hu J, Miao Y, Cai Z, Xuan Y, Behen M, Li M, Ye Y, Shoskey R, Haacke EM, Juhasz C (2011) Cortical calcification in Sturge-Weber syndrome on MRI-SWI: relation to brain perfusion status and seizure severity. J Magn Reson Imaging 34(4):791–798. https://doi.org/10.1002/jmri.22687

    Article  PubMed  PubMed Central  Google Scholar 

  46. Alkonyi B, Chugani HT, Behen M, Halverson S, Helder E, Makki MI, Juhasz C (2010) The role of the thalamus in neuro-cognitive dysfunction in early unilateral hemispheric injury: a multimodality imaging study of children with Sturge-Weber syndrome. Eur J Paediatr Neurol 14(5):425–433. https://doi.org/10.1016/j.ejpn.2010.03.012

    Article  PubMed  PubMed Central  Google Scholar 

  47. Deoni SC, Mercure E, Blasi A, Gasston D, Thomson A, Johnson M, Williams SC, Murphy DG (2011) Mapping infant brain myelination with magnetic resonance imaging. J Neurosci 31(2):784–791. https://doi.org/10.1523/JNEUROSCI.2106-10.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank all parents and patients who participated in this study.

Funding

This work was supported by the Japan Society for the Promotion of Science (JSPS) KAKENHI (Grant numbers 16K19852 and 16K10327); by a JSPS Grant-in-Aid for Scientific Research on Innovative Areas, resource and technical support platforms for promoting research “Advanced Bioimaging Support” (Grant number JP16H06280); by the Japanese Society for Magnetic Resonance in Medicine; by the program for Brain Mapping by Integrated Neurotechnologies for Disease Studies (Brain/MINDS) from the Japan Agency for Medical Research and Development (AMED); by the AMED under Grant number JP18lk1010025; and by the Impulsing Paradigm Change through Disruptive Technologies (ImPACT) Program of the Council for Science, Technology and Innovation (Cabinet Office, Government of Japan).

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Authors and Affiliations

  1. Department of Radiology, Juntendo University Graduate School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo, 113-8421, Japan

    Christina Andica, Akifumi Hagiwara, Masaaki Hori, Takuya Haruyama, Shohei Fujita, Tomoko Maekawa, Koji Kamagata, Mariko Takemura Yoshida, Michimasa Suzuki & Shigeki Aoki

  2. Department of Radiology, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan

    Akifumi Hagiwara & Tomoko Maekawa

  3. Department of Radiological Sciences, Graduate School of Human Health Sciences, Tokyo Metropolitan University, 7-2-10 Higashi-Ogu, Arakawa-ku, Tokyo, 116-8551, Japan

    Takuya Haruyama

  4. Department of Neurosurgery, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo, 113-8421, Japan

    Hidenori Sugano & Hajime Arai

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  1. Christina Andica
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  2. Akifumi Hagiwara
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Correspondence to Akifumi Hagiwara.

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Andica, C., Hagiwara, A., Hori, M. et al. Aberrant myelination in patients with Sturge-Weber syndrome analyzed using synthetic quantitative magnetic resonance imaging. Neuroradiology 61, 1055–1066 (2019). https://doi.org/10.1007/s00234-019-02250-9

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