Skip to main content

Advertisement

SpringerLink
Log in

Assessment of cerebral perfusion in moyamoya disease with dynamic pseudo-continuous arterial spin labeling using a variable repetition time scheme with optimized background suppression

  • Diagnostic Neuroradiology
  • Published:
Neuroradiology Aims and scope Submit manuscript

Abstract

Purpose

Accurate assessment of cerebral perfusion in moyamoya disease is necessary to determine the indication for treatment. We aimed to investigate the usefulness of dynamic PCASL using a variable TR scheme with optimized background suppression in the evaluation of cerebral perfusion in moyamoya disease.

Methods

We retrospectively analyzed the images of 24 patients (6 men and 18 women, mean age 31.4 ± 18.2 years) with moyamoya disease; each of whom was imaged with both dynamic PCASL using the variable-TR scheme and 123IMP SPECT with acetazolamide challenge. ASL dynamic data at 10 phases are acquired by changing the LD and PLD. The background suppression timing was optimized for each phase. CBF and ATT were measured with ASL, and CBF and CVR to an acetazolamide challenge were measured with SPECT.

Results

A significant moderate correlation was found between the CBF measured by dynamic PCASL and that by SPECT (r = 0.53, P < 0.001). The CBF measured by dynamic PCASL (52.5 ± 13.3 ml/100 mg/min) was significantly higher than that measured by SPECT (43.0 ± 12.6 ml/100 mg/min, P < 0.001). The ATT measured by dynamic PCASL showed a significant correlation with the CVR measured by SPECT (r = 0.44, P < 0.001). ATT was significantly longer in areas where the CVR was impaired (CVR < 18.4%, ATT = 1812 ± 353 ms) than in areas where it was preserved (CVR > 18.4%, ATT = 1301 ± 437 ms, P < 0.001). The ROC analysis showed a moderate accuracy (AUC = 0.807, sensitivity = 87.7%, specificity = 70.4%) when the cutoff value of ATT was set at 1518 ms.

Conclusion

Dynamic PCASL using this scheme was found to be useful for assessing cerebral perfusion in moyamoya disease.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The data will be made available by the corresponding author upon reasonable request. Anonymized data will be shared by request from qualified investigators.

Abbreviations

ASL:

Arterial spin labeling

AUC:

Area under the curve

ATT:

Arterial transit time

CBF:

Cerebral blood flow

CVR:

Cerebrovascular reactivity

123I-IMP:

Iodine-123-N-isopropyl-p-iodoamphetamine

LD:

Label duration

PCASL:

Pseudo-continuous arterial spin labeling

PLD:

Post-labeling delay

SPECT:

Single photon emission computed tomography

TR:

Repetition time

References

  1. Ikezaki K, Matsushima T, Kuwabara Y, Suzuki SO, Nomura T, Fukui M (1994) Cerebral circulation and oxygen metabolism in childhood moyamoya disease: a perioperative positron emission tomography study. J Neurosurg 81(6):843–850. https://doi.org/10.3171/jns.1994.81.6.0843

    Article  CAS  Google Scholar 

  2. Kuwabara Y, Ichiya Y, Sasaki M, Yoshida T, Masuda K, Ikezaki K, Matsushima T, Fukui M (1997) Cerebral hemodynamics and metabolism in moyamoya disease–a positron emission tomography study. Clin Neurol Neurosurg 99(Suppl 2):S74-78. https://doi.org/10.1016/s0303-8467(97)00061-9

    Article  Google Scholar 

  3. Tominaga T, Suzuki N, Miyamoto S, Koizumi A, Kuroda S, Takahashi J, Fujimura M, Houkin K (2018) Recommendations for the management of moyamoya disease: a statement from research committee on spontaneous occlusion of the circle of Willis (moyamoya disease) [2nd edition]. Surg Cerebral Stroke 46(1):1–24. https://doi.org/10.2335/scs.46.1

    Article  Google Scholar 

  4. Alsop DC, Detre JA, Golay X, Gunther M, Hendrikse J, Hernandez-Garcia L, Lu H, MacIntosh BJ, Parkes LM, Smits M, van Osch MJ, Wang DJ, Wong EC, Zaharchuk G (2015) Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: a consensus of the ISMRM perfusion study group and the European consortium for ASL in dementia. Magn Reson Med 73(1):102–116. https://doi.org/10.1002/mrm.25197

    Article  Google Scholar 

  5. Setta K, Matsuda T, Sasaki M, Chiba T, Fujiwara S, Kobayashi M, Yoshida K, Kubo Y, Suzuki M, Yoshioka K, Ogasawara K (2021) Diagnostic accuracy of screening arterial spin-labeling MRI using Hadamard encoding for the detection of reduced CBF in adult patients with ischemic moyamoya disease. AJNR Am J Neuroradiol 42(8):1403–1409. https://doi.org/10.3174/ajnr.A7167

    Article  CAS  Google Scholar 

  6. Obara M, Togao O, Wada T, Tokunaga C, Mikayama R, Hamano H, van de Ven K, Yoneyama M, Ogino T, Akamine Y, Ueda Y, Kwon J, Van Cauteren M (2021) Pseudo-continuous arterial spin labeling using multiple label- and post-label duration with dynamically optimized background suppression. Proc Int Soc Magn Reson Med 870

  7. Nishizawa S, Iida H, Tsuchida T, Ito H, Konishi J, Yonekura Y (2003) Validation of the dual-table autoradiographic method to quantify two sequential rCBFs in a single SPET session with N-isopropyl-[123I] p-iodoamphetamine. Eur J Nucl Med Mol Imaging 30(7):943–950. https://doi.org/10.1007/s00259-003-1180-7

    Article  CAS  Google Scholar 

  8. Buxton RB, Frank LR, Wong EC, Siewert B, Warach S, Edelman RR (1998) A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magn Reson Med 40(3):383–396. https://doi.org/10.1002/mrm.1910400308

    Article  CAS  Google Scholar 

  9. Inokuchi Y, Koya S, Uematsu M, Takashina T (2019) Usefulness of the frontal lobe bottom and cerebellum tuber vermis line as an alternative clue to set the axial angle parallel to the AC-PC line in I-123 IMP SPECT imaging: a retrospective study. Radiol Phys Technol 12(4):388–392. https://doi.org/10.1007/s12194-019-00535-5

    Article  Google Scholar 

  10. Koo TK, Li MY (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 15(2):155–163. https://doi.org/10.1016/j.jcm.2016.02.012

    Article  Google Scholar 

  11. Ogasawara K, Ito H, Sasoh M, Okuguchi T, Kobayashi M, Yukawa H, Terasaki K, Ogawa A (2003) Quantitative measurement of regional cerebrovascular reactivity to acetazolamide using 123I-N-isopropyl-p-iodoamphetamine autoradiography with SPECT: validation study using H2 15O with PET. J Nucl Med 44(4):520–525

    CAS  Google Scholar 

  12. Yun TJ, Sohn CH, Han MH, Kang HS, Kim JE, Yoon BW, Paeng JC, Choi SH, Kim JH, Song IC, Chang KH (2013) Effect of delayed transit time on arterial spin labeling: correlation with dynamic susceptibility contrast perfusion magnetic resonance in moyamoya disease. Invest Radiol 48(11):795–802. https://doi.org/10.1097/RLI.0b013e3182981137

    Article  Google Scholar 

  13. Ha JY, Choi YH, Lee S, Cho YJ, Cheon JE, Kim IO, Kim WS (2019) Arterial spin labeling MRI for quantitative assessment of cerebral perfusion before and after cerebral revascularization in children with moyamoya disease. Korean J Radiol : Off J Korean Radiol Soc 20(6):985–996. https://doi.org/10.3348/kjr.2018.0651

    Article  Google Scholar 

  14. Lee S, Yun TJ, Yoo RE, Yoon BW, Kang KM, Choi SH, Kim JH, Kim JE, Sohn CH, Han MH (2018) Monitoring cerebral perfusion changes after revascularization in patients with moyamoya disease by using arterial spin-labeling MR imaging. Radiol 288(2):565–572. https://doi.org/10.1148/radiol.2018170509

    Article  Google Scholar 

  15. Tortora D, Scavetta C, Rebella G, Bertamino M, Scala M, Giacomini T, Morana G, Pavanello M, Rossi A, Severino M (2020) Spatial coefficient of variation applied to arterial spin labeling MRI may contribute to predict surgical revascularization outcomes in pediatric moyamoya vasculopathy. Neuroradiol 62(8):1003–1015. https://doi.org/10.1007/s00234-020-02446-4

    Article  Google Scholar 

  16. Hara S, Tanaka Y, Ueda Y, Hayashi S, Inaji M, Ishiwata K, Ishii K, Maehara T, Nariai T (2017) Noninvasive evaluation of CBF and perfusion delay of moyamoya disease using arterial spin-labeling MRI with multiple postlabeling delays: comparison with (15)O-gas PET and DSC-MRI. AJNR Am J Neuroradiol 38(4):696–702. https://doi.org/10.3174/ajnr.A5068

    Article  CAS  Google Scholar 

  17. Kim JH, Lee SJ, Shin T, Kang KH, Choi PY, Kim JH, Gong JC, Choi NC, Lim BH (2000) Correlative assessment of hemodynamic parameters obtained with T2*-weighted perfusion MR imaging and SPECT in symptomatic carotid artery occlusion. AJNR Am J Neuroradiol 21(8):1450–1456

    CAS  Google Scholar 

  18. Kikuchi K, Murase K, Miki H, Yasuhara Y, Sugawara Y, Mochizuki T, Ikezoe J, Ohue S (2002) Quantitative evaluation of mean transit times obtained with dynamic susceptibility contrast-enhanced MR imaging and with (133)Xe SPECT in occlusive cerebrovascular disease. AJR Am J Roentgenol 179(1):229–235. https://doi.org/10.2214/ajr.179.1.1790229

    Article  Google Scholar 

  19. Gibbs JM, Wise RJ, Leenders KL, Jones T (1984) Evaluation of cerebral perfusion reserve in patients with carotid-artery occlusion. Lancet 1(8372):310–314. https://doi.org/10.1016/s0140-6736(84)90361-1

    Article  CAS  Google Scholar 

  20. Schumann P, Touzani O, Young AR, Morello R, Baron JC, MacKenzie ET (1998) Evaluation of the ratio of cerebral blood flow to cerebral blood volume as an index of local cerebral perfusion pressure. Brain 121(Pt 7):1369–1379. https://doi.org/10.1093/brain/121.7.1369

    Article  Google Scholar 

  21. Vagal AS, Leach JL, Fernandez-Ulloa M, Zuccarello M (2009) The acetazolamide challenge: techniques and applications in the evaluation of chronic cerebral ischemia. AJNR Am J Neuroradiol 30(5):876–884. https://doi.org/10.3174/ajnr.A1538

    Article  CAS  Google Scholar 

  22. Kawano T, Ohmori Y, Kaku Y, Muta D, Uekawa K, Nakagawa T, Amadatsu T, Kasamo D, Shiraishi S, Kitajima M, Kuratsu J (2016) Prolonged mean transit time detected by dynamic susceptibility contrast magnetic resonance imaging predicts cerebrovascular reserve impairment in patients with woyamoya disease. Cerebrovasc Dis 42(1–2):131–138. https://doi.org/10.1159/000445696

    Article  CAS  Google Scholar 

  23. Wang R, Yu S, Alger JR, Zuo Z, Chen J, Wang R, An J, Wang B, Zhao J, Xue R, Wang DJ (2014) Multi-delay arterial spin labeling perfusion MRI in moyamoya disease–comparison with CT perfusion imaging. Eur Radiol 24(5):1135–1144. https://doi.org/10.1007/s00330-014-3098-9

    Article  Google Scholar 

  24. Choi HJ, Sohn CH, You SH, Yoo RE, Kang KM, Yun TJ, Choi SH, Kim JH, Cho WS, Kim JE (2018) Can arterial spin-labeling with multiple postlabeling delays predict cerebrovascular reserve? AJNR Am J Neuroradiol 39(1):84–90. https://doi.org/10.3174/ajnr.A5439

    Article  CAS  Google Scholar 

  25. Inugami A, Kanno I, Uemura K, Shishido F, Murakami M, Tomura N, Fujita H, Higano S (1988) Linearization correction of 99mTc-labeled hexamethyl-propylene amine oxime (HM-PAO) image in terms of regional CBF distribution: comparison to C15O2 inhalation steady-state method measured by positron emission tomography. J Cerebral Blood Flow Metab : Off J Int Soc Cerebr Blood Flow Metab 8(6):S52-60. https://doi.org/10.1038/jcbfm.1988.33

    Article  CAS  Google Scholar 

Download references

Funding

This study was supported by JSPS KAKENHI Grant Number JP20K08111.

Author information

Authors and Affiliations

  1. Department of Molecular Imaging & Diagnosis, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi Higashi-Ku, Fukuoka, 812-8582, Japan

    Osamu Togao

  2. Philips Japan, 13-37, Kohnan 2-Chome, Minato-Ku, Tokyo, 108-8507, Japan

    Makoto Obara, Hiroshi Hamano & Marc Van Cauteren

  3. Department of Radiology Informatics and Network, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi Higashi-Ku, Fukuoka, 812-8582, Japan

    Koji Yamashita

  4. Department of Clinical Radiology, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi Higashi-Ku, Fukuoka, 812-8582, Japan

    Kazufumi Kikuchi, Kousei Ishigami & Shingo Baba

  5. Department of Neurosurgery, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi Higashi-Ku, Fukuoka, 812-8582, Japan

    Koichi Arimura, Ataru Nishimura & Akira Nakamizo

  6. Division of Radiology, Department of Medical Technology, Kyushu University Hospital, Fukuoka, 812-8582, Japan

    Tatsuhiro Wada, Chiaki Tokunaga, Ryoji Mikayama & Yasuo Yamashita

Authors
  1. Osamu Togao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Makoto Obara
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Koji Yamashita
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kazufumi Kikuchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Koichi Arimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ataru Nishimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Akira Nakamizo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Tatsuhiro Wada
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Chiaki Tokunaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ryoji Mikayama
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yasuo Yamashita
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Hiroshi Hamano
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Marc Van Cauteren
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Kousei Ishigami
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Shingo Baba
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Osamu Togao.

Ethics declarations

Conflict of interest

Drs. Makoto Obara, Hiroshi Hamano, and Marc van Cauteren are employees of Philips Japan. The other authors declare no competing interests.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. This retrospective investigation was approved by the Institutional Review Board of Kyushu University Hospital (No. 22049–00). The informed consent requirement was waived based on the retrospective study design.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Togao, O., Obara, M., Yamashita, K. et al. Assessment of cerebral perfusion in moyamoya disease with dynamic pseudo-continuous arterial spin labeling using a variable repetition time scheme with optimized background suppression. Neuroradiology 65, 529–538 (2023). https://doi.org/10.1007/s00234-022-03095-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-022-03095-5

Keywords

Search

Navigation