Advertisement

Translational Stroke Research

, Volume 9, Issue 4, pp 333–339 | Cite as

Clinical Importance of Temporal Bone Features for the Efficacy of Contrast-Enhanced Sonothrombolysis: a Retrospective Analysis of the NOR-SASS Trial

  • Vojtech Novotny
  • Aliona Nacu
  • Christopher E. Kvistad
  • Annette Fromm
  • Gesche F. Neckelmann
  • Andrej N. Khanevski
  • Haakon Tobro
  • Ulrike Waje-Andreassen
  • Halvor Naess
  • Lars Thomassen
  • Nicola Logallo
Original Article
  • 100 Downloads

Abstract

Contrast-enhanced sonothrombolysis (CEST) seems to be a safe and promising treatment in acute ischemic stroke. It remains unknown if temporal bone features may influence the efficacy of CEST. We investigated the association between different temporal bone features on admission computed tomography (CT) scan and the outcome in acute ischemic stroke patients included in the randomized Norwegian Sonothrombolysis in Acute Stroke Study (NOR-SASS). Patients diagnosed as stroke mimics and those with infratentorial stroke or with incorrect insonation were excluded. We retrospectively assessed temporal bone heterogeneity (presence of diploë), diploë ratio, thickness, and density on admission CT scans. National institute of Health Stroke Scale (NIHSS) at 24 h and modified Rankin Scale (mRS) at 3 months were correlated with CT findings both in CEST and sham CEST patients. A total of 99 patients were included of which 52 were assigned to CEST and 47 to sham CEST. Approximately 20% patients had a heterogeneous temporal bone in both the CEST and sham CEST group. All temporal bone CT features studied were associated with female sex. In the CEST group, temporal bone heterogeneity (p = 0.006) and higher temporal bone diploë ratio (p = 0.002) were associated with higher NIHSS at 24 h. There was no association between temporal bone features and mRS at 3 months. Approximately 20% of acute ischemic stroke patients have heterogeneous temporal bone and may be resistant to standard 2-MHz transcranial Doppler ultrasound treatment. Sonothrombolysis resistance may easily be predicted by admission CT for better selection.

Keywords

Sonothrombolysis Cerebral infarction Ultrasound CT scan Temporal bone Thrombolysis 

Notes

Acknowledgements

We gratefully acknowledge study nurses Leila Marie Frid, Linn Elin Rødal, and Maren Inselseth for study administration.

Sources of Funding

This study was supported by the University of Bergen and Bergen Stroke Research Group.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the regional local ethics committee (REK Vest) and with the 1964 Helsinki declaration and its later amendments.

Informed Consent

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

References

  1. 1.
    Alexandrov AV, Molina CA, Grotta JC, Garami Z, Ford SR, et al. Ultrasound-enhanced systemic thrombolysis for acute ischemic stroke. N Engl J Med. 2004;351:2170–8.CrossRefPubMedGoogle Scholar
  2. 2.
    Eggers J, Konig IR, Koch B, Handler G, Seidel G. Sonothrombolysis with transcranial color-coded sonography and recombinant tissue-type plasminogen activator in acute middle cerebral artery main stem occlusion: results from a randomized study. Stroke. 2008;39:1470–5.CrossRefPubMedGoogle Scholar
  3. 3.
    Eggers J, Seidel G, Koch B, Konig IR. Sonothrombolysis in acute ischemic stroke for patients ineligible for rt-PA. Neurology. 2005;64:1052–4.CrossRefPubMedGoogle Scholar
  4. 4.
    Molina CA, Barreto AD, Tsivgoulis G, Sierzenski P, Malkoff MD, et al. Transcranial ultrasound in clinical sonothrombolysis (TUCSON) trial. Ann Neurol. 2009;66:28–38.CrossRefPubMedGoogle Scholar
  5. 5.
    Nedelmann M, Ritschel N, Doenges S, Langheinrich AC, Acker T, et al. Combined contrast-enhanced ultrasound and rt-PA treatment is safe and improves impaired microcirculation after reperfusion of middle cerebral artery occlusion. J Cereb Blood Flow Metab. 2010;30:1712–20.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Culp WC, Flores R, Brown AT, Lowery JD, Roberson PK, et al. Successful microbubble sonothrombolysis without tissue-type plasminogen activator in a rabbit model of acute ischemic stroke. Stroke. 2011;42:2280–5.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Nacu A, Kvistad CE, Naess H, Oygarden H, Logallo N, Assmus J, et al. Nor-sass (norwegian sonothrombolysis in acute stroke study): randomized controlled contrast-enhanced sonothrombolysis in an unselected acute ischemic stroke population. Stroke. 2017;48:335–41.Google Scholar
  8. 8.
    Jarquin-Valdivia AA, McCartney J, Palestrant D, Johnston SC, Gress D. The thickness of the temporal squama and its implication for transcranial sonography. J Neuroimaging. 2004;14:139–42.CrossRefPubMedGoogle Scholar
  9. 9.
    Wijnhoud AD, Franckena M, van der Lugt A, Koudstaal PJ, Dippel ED. Inadequate acoustical temporal bone window in patients with a transient ischemic attack or minor stroke: role of skull thickness and bone density. Ultrasound Med Biol. 2008;34:923–9.CrossRefPubMedGoogle Scholar
  10. 10.
    Nader JA, Andrade Mde L, Espinosa V, Zambrano M, Del Brutto OH. Technical difficulties due to poor acoustic insonation during transcranial Doppler recordings in Amerindians and individuals of European origin. A comparative study. Eur Neurol. 2015;73:230–2.CrossRefPubMedGoogle Scholar
  11. 11.
    Bazan R, Braga GP, Luvizutto GJ, Hueb JC, Hokama NK, et al. Evaluation of the temporal acoustic window for transcranial Doppler in a multi-ethnic population in Brazil. Ultrasound Med Biol. 2015;41:2131–4.CrossRefPubMedGoogle Scholar
  12. 12.
    Lin Y-P, M-H F, Tan T-Y. Factors associated with no or insufficient temporal bone window using transcranial color-coded sonography. J Med Ultrasound. 2015;23:129–32.CrossRefGoogle Scholar
  13. 13.
    Itoh T, Matsumoto M, Handa N, Maeda H, Hougaku H, et al. Rate of successful recording of blood flow signals in the middle cerebral artery using transcranial Doppler sonography. Stroke. 1993;24:1192–5.CrossRefPubMedGoogle Scholar
  14. 14.
    Tubbs RS, Bosmia AN, Cohen-Gadol AA. The human calvaria: a review of embryology, anatomy, pathology, and molecular development. Childs Nerv Syst. 2012;28:23–31.CrossRefPubMedGoogle Scholar
  15. 15.
    Kwon JH, Kim JS, Kang DW, Bae KS, Kwon SU. The thickness and texture of temporal bone in brain CT predict acoustic window failure of transcranial Doppler. J Neuroimaging. 2006;16:347–52.CrossRefPubMedGoogle Scholar
  16. 16.
    Del Brutto OH, Mera RM, de la Luz Andrade M, Espinosa V, Castillo PR, et al. Temporal bone thickness and texture are major determinants of the high rate of insonation failures of transcranial doppler in amerindians (the Atahualpa project). J Clin Ultrasound. 2016;44:55–60.CrossRefPubMedGoogle Scholar
  17. 17.
    Logallo N, Kvistad CE, Nacu A, Naess H, Waje-Andreassen U, et al. The Norwegian tenecteplase stroke trial (NOR-TEST): randomised controlled trial of tenecteplase vs. alteplase in acute ischaemic stroke. BMC Neurol. 2014;14:106.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Nacu A, Kvistad CE, Logallo N, Naess H, Waje-Andreassen U, et al. A pragmatic approach to sonothrombolysis in acute ischaemic stroke: the Norwegian randomised controlled sonothrombolysis in acute stroke study (NOR-SASS). BMC Neurol. 2015;15:110.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Rhoton AL Jr. The supratentorial arteries. Neurosurgery. 2002;51:S53–120.PubMedGoogle Scholar
  20. 20.
    Fry FJ, Barger JE. Acoustical properties of the human skull. J Acoust Soc Am. 1978;63:1576–90.CrossRefPubMedGoogle Scholar
  21. 21.
    Ammi AY, Mast TD, Huang IH, Abruzzo TA, Coussios CC, et al. Characterization of ultrasound propagation through ex-vivo human temporal bone. Ultrasound Med Biol. 2008;34:1578–89.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Wang Z, Komatsu T, Mitsumura H, Nakata N, Ogawa T, et al. An uncovered risk factor of sonothrombolysis: substantial fluctuation of ultrasound transmittance through the human skull. Ultrasonics. 2017;77:168–75.CrossRefPubMedGoogle Scholar
  23. 23.
    Vignon F, Shi WT, Erkamp R, Radulescu E, Shamdasani V, Powers JE. Mapping skull attenuation for optimal probe placement in transcranial ultrasound applications. Ultrasonics Symposium (IUS), 2009 IEEE International, Rome, Italy. 2009. pp. 2336–39.Google Scholar
  24. 24.
    Barlinn K, Barreto AD, Sisson A, Liebeskind DS, Schafer ME, et al. CLOTBUST-hands free: initial safety testing of a novel operator-independent ultrasound device in stroke-free volunteers. Stroke. 2013;44:1641–6.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Barreto AD, Alexandrov AV, Shen L, Sisson A, Bursaw AW, et al. CLOTBUST-hands free: pilot safety study of a novel operator-independent ultrasound device in patients with acute ischemic stroke. Stroke. 2013;44:3376–81.CrossRefPubMedGoogle Scholar
  26. 26.
    Saito O, Furuhata H. Improving uniformity of intensity distribution of ultrasound passing through a human-skull fragment by random modulation. Int J Clin Neurosci Mental Health. 2014;1:S23.Google Scholar
  27. 27.
    Furuhata H, Saito O. Comparative study of standing wave reduction methods using random modulation for transcranial ultrasonication. Ultrasound Med Biol. 2013;39:1440–50.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  • Vojtech Novotny
    • 1
    • 2
  • Aliona Nacu
    • 1
    • 2
  • Christopher E. Kvistad
    • 1
    • 2
  • Annette Fromm
    • 1
    • 2
  • Gesche F. Neckelmann
    • 3
  • Andrej N. Khanevski
    • 1
    • 4
  • Haakon Tobro
    • 5
  • Ulrike Waje-Andreassen
    • 1
    • 6
  • Halvor Naess
    • 1
    • 7
  • Lars Thomassen
    • 1
    • 2
  • Nicola Logallo
    • 1
    • 2
    • 8
  1. 1.Department of NeurologyHaukeland University HospitalBergenNorway
  2. 2.Department of Clinical MedicineUniversity of BergenBergenNorway
  3. 3.Department of RadiologyHaukeland University HospitalBergenNorway
  4. 4.The National Association for Public HealthOsloNorway
  5. 5.Department of NeurologyTelemark Central HospitalSkienNorway
  6. 6.Department of Biological and Medical PsychologyUniversity of BergenBergenNorway
  7. 7.Centre for Age-Related MedicineStavanger University HospitalStavangerNorway
  8. 8.Department of NeurosurgeryHaukeland University HospitalBergenNorway

Personalised recommendations