Skip to main content

Advertisement

SpringerLink
Log in

Intraoperative transit-time ultrasonography combined with FLOW800 predicts the occurrence of cerebral hyperperfusion syndrome after direct revascularization of Moyamoya disease: a preliminary study

  • Original Article - Vascular Neurosurgery - Other
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

Cerebral hyperperfusion syndrome (CHS) is a common complication after direct bypass surgery in patients with Moyamoya disease (MMD). Since preventive measures may be inadequate, we assessed whether the blood flow difference between the superficial temporal artery (STA) and recipient vessels (△BF) and the direct perfusion range (DPR) are related to CHS.

Methods

We measured blood flow in the STA and recipient blood vessels before bypass surgery by transit-time probe to calculate △BF. Perfusion changes around the anastomosis before and after bypass were analyzed with FLOW800 to obtain DPR. Multiple factors, such as △BF, DPR, and postoperative CHS, were analyzed using binary logistic regression.

Results

Forty-one patients with MMD who underwent direct bypass surgery were included in the study. Postoperative CHS symptoms occurred in 13/41 patients. △BF and DPR significantly differed between the CHS and non-CHS groups. The optimal receiver operating characteristic (ROC) curve cut-off value was 31.4 ml/min for ΔBF, and the area under the ROC curve (AUC) was 0.695 (sensitivity 0.846, specificity 0.500). The optimal cut-off value was 3.5 cm for DPR, and the AUC was 0.702 (sensitivity 0.615, specificity 0.750).

Conclusion

Postoperative CHS is caused by multiple factors. △BF is a risk factor for CHS while DPR is a protective factor against CHS.

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

Similar content being viewed by others

References

  1. Alaraj A, Ashley WW Jr, Charbel FT, Amin-Hanjani S (2008) The superficial temporal artery trunk as a donor vessel in cerebral revascularization: benefits and pitfalls. Neurosurg Focus 24:E7

    Article  Google Scholar 

  2. Awano T, Sakatani K, Yokose N, Kondo Y, Igarashi T, Hoshino T, Nakamura S, Fujiwara N, Murata Y, Katayama Y, Shikayama T, Miwa M (2010) Intraoperative EC-IC bypass blood flow assessment with indocyanine green angiography in moyamoya and non-moyamoya ischemic stroke. World Neurosurg 73:668–674

    Article  Google Scholar 

  3. Czabanka M, Pena-Tapia P, Schubert GA, Woitzik J, Horn P, Schmiedek P, Vajkoczy P (2009) Clinical implications of cortical microvasculature in adult Moyamoya disease. J Cereb Blood Flow Metab 29:1383–1387

    Article  Google Scholar 

  4. Fujimura M, Mugikura S, Kaneta T, Shimizu H, Tominaga T (2009) Incidence and risk factors for symptomatic cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in patients with moyamoya disease. Surg Neurol 71:442–447

    Article  Google Scholar 

  5. Fujimura M, Niizuma K, Endo H, Sato K, Inoue T, Shimizu H, Tominaga T (2015) Quantitative analysis of early postoperative cerebral blood flow contributes to the prediction and diagnosis of cerebral hyperperfusion syndrome after revascularization surgery for moyamoya disease. Neurol Res 37:131–138

    Article  CAS  Google Scholar 

  6. Fujimura M, Shimizu H, Mugikura S, Tominaga T (2009) Delayed intracerebral hemorrhage after superficial temporal artery-middle cerebral artery anastomosis in a patient with moyamoya disease: possible involvement of cerebral hyperperfusion and increased vascular permeability. Surg Neurol 71:223–227 discussion 227

    Article  Google Scholar 

  7. Hamano E, Kataoka H, Morita N, Maruyama D, Satow T, Iihara K, Takahashi JC (2017) Clinical implications of the cortical hyperintensity belt sign in fluid-attenuated inversion recovery images after bypass surgery for moyamoya disease. J Neurosurg 126:1–7

    Article  Google Scholar 

  8. Hwang JW, Yang HM, Lee H, Lee HK, Jeon YT, Kim JE, Lim YJ, Park HP (2013) Predictive factors of symptomatic cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in adult patients with moyamoya disease. Br J Anaesth 110:773–779

    Article  CAS  Google Scholar 

  9. Kim JE, Jeon JS (2014) An update on the diagnosis and treatment of adult Moyamoya disease taking into consideration controversial issues. Neurol Res 36:407–416

    Article  Google Scholar 

  10. Kim JE, Oh CW, Kwon OK, Park SQ, Kim SE, Kim YK (2008) Transient hyperperfusion after superficial temporal artery/middle cerebral artery bypass surgery as a possible cause of postoperative transient neurological deterioration. Cerebrovasc Dis 25:580–586

    Article  Google Scholar 

  11. Kim SJ, Son TO, Kim KH, Jeon P, Hyun SH, Lee KH, Yeon JY, Kim JS, Hong SC, Shin HJ, Bang OY (2014) Neovascularization precedes occlusion in moyamoya disease: angiographic findings in 172 pediatric patients. Eur Neurol 72:299–305

    Article  CAS  Google Scholar 

  12. Kim T, Oh CW, Bang JS, Kim JE, Cho WS (2016) Moyamoya disease: treatment and outcomes. J Stroke 18:21–30

    Article  Google Scholar 

  13. Lee M, Guzman R, Bell-Stephens T, Steinberg GK (2011) Intraoperative blood flow analysis of direct revascularization procedures in patients with moyamoya disease. J Cereb Blood Flow Metab 31:262–274

    Article  Google Scholar 

  14. Lundell A, Bergqvist D, Mattsson E, Nilsson B (1993) Volume blood flow measurements with a transit time flowmeter: an in vivo and in vitro variability and validation study. Clin Physiol 13:547–557

    Article  CAS  Google Scholar 

  15. Machida T, Nakano S, Ishige S, Ono J, Fujikawa A (2017) Subcortical low-intensity lesions on fluid-attenuated inversion recovery images after revascularization surgery for Moyamoya disease. World Neurosurg 98:512–519

    Article  Google Scholar 

  16. Miyamoto S, Yoshimoto T, Hashimoto N, Okada Y, Tsuji I, Tominaga T, Nakagawara J, Takahashi JC (2014) Investigators JAMT: effects of extracranial-intracranial bypass for patients with hemorrhagic moyamoya disease: results of the Japan Adult Moyamoya trial. Stroke 45:1415–1421

    Article  Google Scholar 

  17. Morisawa H, Kawamata T, Kawashima A, Hayashi M, Yamaguchi K, Yoneyama T, Okada Y (2013) Hemodynamics and changes after STA-MCA anastomosis in moyamoya disease and atherosclerotic cerebrovascular disease measured by micro-Doppler ultrasonography. Neurosurg Rev 36:411–419

    Article  Google Scholar 

  18. Nakagawa A, Fujimura M, Arafune T, Sakuma I, Tominaga T (2009) Clinical implications of intraoperative infrared brain surface monitoring during superficial temporal artery-middle cerebral artery anastomosis in patients with moyamoya disease. J Neurosurg 111:1158–1164

    Article  Google Scholar 

  19. Noguchi T, Kawashima M, Nishihara M, Egashira Y, Azama S, Irie H (2015) Noninvasive method for mapping CVR in moyamoya disease using ASL-MRI. Eur J Radiol 84:1137–1143

    Article  Google Scholar 

  20. Ogasawara K, Komoribayashi N, Kobayashi M, Fukuda T, Inoue T, Yamadate K, Ogawa A (2005) Neural damage caused by cerebral hyperperfusion after arterial bypass surgery in a patient with moyamoya disease: case report. Neurosurgery 56:E1380 discussion E1380

    Article  Google Scholar 

  21. Ohue S, Kumon Y, Kohno K, Watanabe H, Iwata S, Ohnishi T (2008) Postoperative temporary neurological deficits in adults with moyamoya disease. Surg Neurol 69:281–286 discussion 286-287

    Article  Google Scholar 

  22. Prinz V, Hecht N, Kato N, Vajkoczy P (2014) FLOW 800 allows visualization of hemodynamic changes after extracranial-to-intracranial bypass surgery but not assessment of quantitative perfusion or flow. Neurosurgery 10(Suppl 2):231–238 discussion 238-239

    PubMed  Google Scholar 

  23. Research Committee on the Pathology, Treatment of Spontaneous Occlusion of the Circle of Willis, Health Labour Sciences Research Grant for Research on Measures for Infractable Diseases (2012) Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo) 52:245–266

    Article  Google Scholar 

  24. Saito M, Saga T, Hayashi H, Noro S, Wada H, Kamada K (2018) Quantitative blood flow assessment by multiparameter analysis of indocyanine green video angiography. World Neurosurg 116:e187–e193

    Article  Google Scholar 

  25. Suzuki J, Kodama N (1983) Moyamoya disease--a review. Stroke 14:104–109

    Article  CAS  Google Scholar 

  26. Uda K, Araki Y, Muraoka S, Ota S, Wada K, Yokoyama K, Nishihori M, Izumi T, Okamoto S, Wakabayashi T (2018) Intraoperative evaluation of local cerebral hemodynamic change by indocyanine green videoangiography: prediction of incidence and duration of postoperative transient neurological events in patients with moyamoya disease. J Neurosurg 1:1–9

    Article  Google Scholar 

  27. Yamaguchi K, Kawamata T, Kawashima A, Hori T, Okada Y (2010) Incidence and predictive factors of cerebral hyperperfusion after extracranial-intracranial bypass for occlusive cerebrovascular diseases. Neurosurgery 67:1548–1554 discussion 1554

    Article  Google Scholar 

  28. Yang T, Higashino Y, Kataoka H, Hamano E, Maruyama D, Iihara K, Takahashi JC (2018) Correlation between reduction in microvascular transit time after superficial temporal artery-middle cerebral artery bypass surgery for moyamoya disease and the development of postoperative hyperperfusion syndrome. J Neurosurg 128:1304–1310

    Article  Google Scholar 

  29. Ye X, Liu XJ, Ma L, Liu LT, Wang WL, Wang S, Cao Y, Zhang D, Wang R, Zhao JZ, Zhao YL (2013) Clinical values of intraoperative indocyanine green fluorescence video angiography with Flow 800 software in cerebrovascular surgery. Chin Med J 126:4232–4237

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

    Dongxu Yang, Zhiguang Han, Yutao Su, Junshi Shao, Penghui Cao, Shihao He & Rong Wang

  2. Department of Neurosurgery, Affiliated Hospital of Jining Medical University, Jining Medical University, Jining, Shandong, China

    Dongxu Yang

  3. Department of Laboratory Medicine, Affiliated Hospital of Jining Medical University, Jining Medical University, Jining, Shandong, China

    Xiaohong Zhang

  4. Department of Neurosurgery, Peking University International Hospital, Beijing, China

    Cunxin Tan, Ran Duan, Guangchao Shi & Rong Wang

Authors
  1. Dongxu Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaohong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cunxin Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhiguang Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yutao Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ran Duan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Guangchao Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Junshi Shao
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Penghui Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Shihao He
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Rong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Rong Wang and Dongxu Yang conceived and designed the research; Dongxu Yang, Rong Wang, Xiaohong Zhang, Cunxin Tan, Zhiguang Han, Yutao Su, Ran Duan, Guangchao Shi, Junshi Shao, Penghui Cao, and Shihao He performed the research, analyzed the data, and carried out the statistics. Dongxu Yang and Xiaohong Zhang wrote the manuscript, and Rong Wang revised the manuscript.

Corresponding author

Correspondence to Rong Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This is a retrospective study and for this type of study formal consent is not required.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Comments

The authors perform a retrospective review of 41 patients with MMD who underwent STA-MCA bypass to evaluate for a relationship between changes in pre and post anastomosis blood flow in the donor and recipient vessels as well as FLOW800 are associated with cerebral hyperperfusion syndrome.

The authors do a great job of quantifying a difficult to predict problem.

Fady Charbel

Illinois, USA

Publisher’s note

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

This article is part of the Topical Collection on Vascular Neurosurgery

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, D., Zhang, X., Tan, C. et al. Intraoperative transit-time ultrasonography combined with FLOW800 predicts the occurrence of cerebral hyperperfusion syndrome after direct revascularization of Moyamoya disease: a preliminary study. Acta Neurochir 163, 563–571 (2021). https://doi.org/10.1007/s00701-020-04599-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-020-04599-w

Keywords

Search

Navigation