Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
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Monitoring Cerebral Perfusion Changes Using Arterial Spin-Labeling Perfusion MRI after Indirect Revascularization in Children with Moyamoya Disease

  • Seul Bi Lee (Department of Radiology, Seoul National University Hospital) ;
  • Seunghyun Lee (Department of Radiology, Seoul National University Hospital) ;
  • Yeon Jin Cho (Department of Radiology, Seoul National University Hospital) ;
  • Young Hun Choi (Department of Radiology, Seoul National University Hospital) ;
  • Jung-Eun Cheon (Department of Radiology, Seoul National University Hospital) ;
  • Woo Sun Kim (Department of Radiology, Seoul National University Hospital)
  • Received : 2020.09.28
  • Accepted : 2021.03.12
  • Published : 2021.09.01
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Abstract

Objective: To assess the role of arterial spin-labeling (ASL) perfusion MRI in identifying cerebral perfusion changes after indirect revascularization in children with moyamoya disease. Materials and Methods: We included pre- and postoperative perfusion MRI data of 30 children with moyamoya disease (13 boys and 17 girls; mean age ± standard deviation, 6.3± 3.0 years) who underwent indirect revascularization between June 2016 and August 2017. Relative cerebral blood flow (rCBF) and qualitative perfusion scores for arterial transit time (ATT) effects were evaluated in the middle cerebral artery (MCA) territory on ASL perfusion MRI. The rCBF and relative time-to-peak (rTTP) values were also measured using dynamic susceptibility contrast (DSC) perfusion MRI. Each perfusion change on ASL and DSC perfusion MRI was analyzed using the paired t test. We analyzed the correlation between perfusion changes on ASL and DSC images using Spearman's correlation coefficient. Results: The ASL rCBF values improved at both the ganglionic and supraganglionic levels of the MCA territory after surgery (p = 0.040 and p = 0.003, respectively). The ATT perfusion scores also improved at both levels (p < 0.001 and p < 0.001, respectively). The rCBF and rTTP values on DSC MRI showed significant improvement at both levels of the MCA territory of the operated side (all p < 0.05). There was no significant correlation between the improvements in rCBF values on the two perfusion images (r = 0.195, p = 0.303); however, there was a correlation between the change in perfusion scores on ASL and rTTP on DSC MRI (r = 0.701, p < 0.001). Conclusion: Recognizing the effects of ATT on ASL perfusion MRI may help monitor cerebral perfusion changes and complement quantitative rCBF assessment using ASL perfusion MRI in patients with moyamoya disease after indirect revascularization.

Keywords

Acknowledgement

Six patients in this study overlapped with a previous report (Ha JY et al. Korean J Radiol 2019;20:985-996) [9].

References

  1. Fung LW, Thompson D, Ganesan V. Revascularisation surgery for paediatric moyamoya: a review of the literature. Childs Nerv Syst 2005;21:358-364 
  2. Zeifert PD, Karzmark P, Bell-Stephens TE, Steinberg GK, Dorfman LJ. Neurocognitive performance after cerebral revascularization in adult moyamoya disease. Stroke 2017;48:1514-1517 
  3. Zaharchuk G, Bammer R, Straka M, Shankaranarayan A, Alsop DC, Fischbein NJ, et al. Arterial spin-label imaging in patients with normal bolus perfusion-weighted MR imaging findings: pilot identification of the borderzone sign. Radiology 2009;252:797-807 
  4. Goetti R, O'Gorman R, Khan N, Kellenberger CJ, Scheer I. Arterial spin labelling MRI for assessment of cerebral perfusion in children with moyamoya disease: comparison with dynamic susceptibility contrast MRI. Neuroradiology 2013;55:639-647 
  5. Essig M, Shiroishi MS, Nguyen TB, Saake M, Provenzale JM, Enterline D, et al. Perfusion MRI: the five most frequently asked technical questions. AJR Am J Roentgenol 2013;200:24-34 
  6. Nezamzadeh M, Matson GB, Young K, Weiner MW, Schuff N. Improved pseudo-continuous arterial spin labeling for mapping brain perfusion. J Magn Reson Imaging 2010;31:1419-1427 
  7. Wang R, Yu S, Alger JR, Zuo Z, Chen J, Wang R, et al. Multi-delay arterial spin labeling perfusion MRI in moyamoya disease--comparison with CT perfusion imaging. Eur Radiol 2014;24:1135-1144 
  8. Lee S, Yun TJ, Yoo RE, Yoon BW, Kang KM, Choi SH, et al. Monitoring cerebral perfusion changes after revascularization in patients with moyamoya disease by using arterial spin-labeling MR imaging. Radiology 2018;288:565-572 
  9. Ha JY, Choi YH, Lee S, Cho YJ, Cheon JE, Kim IO, et al. Arterial spin labeling MRI for quantitative assessment of cerebral perfusion before and after cerebral revascularization in children with moyamoya disease. Korean J Radiol 2019;20:985-996 
  10. Quon JL, Kim LH, Lober RM, Maleki M, Steinberg GK, Yeom KW. Arterial spin-labeling cerebral perfusion changes after revascularization surgery in pediatric moyamoya disease and syndrome. J Neurosurg Pediatr 2019;23:486-492 
  11. Fahlstrom M, Lewen A, Enblad P, Larsson EM, Wikstrom J. High intravascular signal arterial transit time artifacts have negligible effects on cerebral blood flow and cerebrovascular reserve capacity measurement using single postlabel delay arterial spin-labeling in patients with moyamoya disease. AJNR Am J Neuroradiol 2020;41:430-436 
  12. Tortora D, Scavetta C, Rebella G, Bertamino M, Scala M, Giacomini T, et al. Spatial coefficient of variation applied to arterial spin labeling MRI may contribute to predict surgical revascularization outcomes in pediatric moyamoya vasculopathy. Neuroradiology 2020;62:1003-1015 
  13. Zaharchuk G, Do HM, Marks MP, Rosenberg J, Moseley ME, Steinberg GK. Arterial spin-labeling MRI can identify the presence and intensity of collateral perfusion in patients with moyamoya disease. Stroke 2011;42:2485-2491 
  14. Suzuki J, Kodama N. Moyamoya disease--a review. Stroke 1983;14:104-109 
  15. Helton KJ, Glass JO, Reddick WE, Paydar A, Zandieh AR, Dave R, et al. Comparing segmented ASL perfusion of vascular territories using manual versus semiautomated techniques in children with sickle cell anemia. J Magn Reson Imaging 2015;41:439-446 
  16. Lou X, Yu S, Scalzo F, Starkman S, Ali LK, Kim D, et al. Multi-delay ASL can identify leptomeningeal collateral perfusion in endovascular therapy of ischemic stroke. Oncotarget 2017;8:2437-2443 
  17. Bolar DS, Gagoski B, Orbach DB, Smith E, Adalsteinsson E, Rosen BR, et al. Comparison of CBF measured with combined velocity-selective arterial spin-labeling and pulsed arterial spin-labeling to blood flow patterns assessed by conventional angiography in pediatric moyamoya. AJNR Am J Neuroradiol 2019;40:1842-1849 
  18. Ukai R, Mikami T, Nagahama H, Wanibuchi M, Akiyama Y, Miyata K, et al. Arterial transit artifacts observed by arterial spin labeling in Moyamoya disease. J Stroke Cerebrovasc Dis 2020;29:105058 
  19. Potreck A, Seker F, Hoffmann A, Pfaff J, Nagel S, Bendszus M, et al. A novel method to assess pial collateralization from stroke perfusion MRI: subdividing Tmax into anatomical compartments. Eur Radiol 2017;27:618-626 
  20. Schmidt MA, Knott M, Hoelter P, Engelhorn T, Larsson EM, Nguyen T, et al. Standardized acquisition and post-processing of dynamic susceptibility contrast perfusion in patients with brain tumors, cerebrovascular disease and dementia: comparability of post-processing software. Br J Radiol 2020;93:20190543 
  21. Yun TJ, Cheon JE, Na DG, Kim WS, Kim IO, Chang KH, et al. Childhood moyamoya disease: quantitative evaluation of perfusion MR imaging--correlation with clinical outcome after revascularization surgery. Radiology 2009;251:216-223 
  22. Lee SK, Kim DI, Jeong EK, Kim SY, Kim SH, In YK, et al. Postoperative evaluation of moyamoya disease with perfusion-weighted MR imaging: initial experience. AJNR Am J Neuroradiol 2003;24:741-747 
  23. Acker G, Fekonja L, Vajkoczy P. Surgical management of moyamoya disease. Stroke 2018;49:476-482 
  24. Kim HG, Lee SK, Lee JD. Characteristics of infarction after encephaloduroarteriosynangiosis in young patients with moyamoya disease. J Neurosurg Pediatr 2017;19:1-7 
  25. Kuwabara Y, Ichiya Y, Sasaki M, Yoshida T, Masuda K, Ikezaki K, et al. Cerebral hemodynamics and metabolism in moyamoya disease--a positron emission tomography study. Clin Neurol Neurosurg 1997;99 Suppl 2:S74-S78 
  26. Noguchi T, Kawashima M, Irie H, Ootsuka T, Nishihara M, Matsushima T, et al. Arterial spin-labeling MR imaging in moyamoya disease compared with SPECT imaging. Eur J Radiol 2011;80:e557-e562 
  27. Gaudino S, Martucci M, Botto A, Ruberto E, Leone E, Infante A, et al. Brain DSC MR perfusion in children: a clinical feasibility study using different technical standards of contrast administration. AJNR Am J Neuroradiol 2019;40:359-365 
  28. Calamante F, Gadian DG, Connelly A. Delay and dispersion effects in dynamic susceptibility contrast MRI: simulations using singular value decomposition. Magn Reson Med 2000;44:466-473 
  29. Tortora D, Severino M, Pacetti M, Morana G, Mancardi MM, Capra V, et al. Noninvasive assessment of hemodynamic stress distribution after indirect revascularization for pediatric moyamoya vasculopathy. AJNR Am J Neuroradiol 2018;39:1157-1163 
  30. Nael K, Meshksar A, Liebeskind DS, Coull BM, Krupinski EA, Villablanca JP. Quantitative analysis of hypoperfusion in acute stroke: arterial spin labeling versus dynamic susceptibility contrast. Stroke 2013;44:3090-3096 
  31. Donahue MJ, Achten E, Cogswell PM, De Leeuw FE, Derdeyn CP, Dijkhuizen RM, et al. Consensus statement on current and emerging methods for the diagnosis and evaluation of cerebrovascular disease. J Cereb Blood Flow Metab 2018;38:1391-1417