Journal of Korean Neurosurgical Society

The Korean Neurosurgical Society (대한신경외과학회)
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Factors Related to Successful Energy Transmission of Focused Ultrasound through a Skull : A Study in Human Cadavers and Its Comparison with Clinical Experiences

  • Received : 2018.12.08
  • Accepted : 2019.03.09
  • Published : 2019.11.01
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Abstract

Objective : Although magnetic resonance guided focused ultrasound (MRgFUS) has been used as minimally invasive and effective neurosurgical treatment, it exhibits some limitations, mainly related to acoustic properties of the skull barrier. This study was undertaken to identify skull characteristics that contribute to optimal ultrasonic energy transmission for MRgFUS procedures. Methods : For ex vivo skull experiments, various acoustic fields were measured under different conditions, using five non-embalmed cadaver skulls. For clinical skull analyses, brain computed tomography data of 46 patients who underwent MRgFUS ablations (18 unilateral thalamotomy, nine unilateral pallidotomy, and 19 bilateral capsulotomy) were retrospectively reviewed. Patients' skull factors and sonication parameters were comparatively analyzed with respect to the cadaveric skulls. Results : Skull experiments identified three important factors related skull penetration of ultrasound, including skull density ratio (SDR), skull volume, and incidence angle of the acoustic rays against the skull surface. In clinical results, SDR and skull volume correlated with maximal temperature (Tmax) and energy requirement to achieve Tmax (p<0.05). In addition, considering the incidence angle determined by brain target location, less energy was required to reach Tmax in the central, rather than lateral targets particularly when compared between thalamotomy and capsulotomy (p<0.05). Conclusion : This study reconfirmed previously identified skull factors, including SDR and skull volume, for successful MRgFUS; it identified an additional factor, incidence angle of acoustic rays against the skull surface. To guarantee successful transcranial MRgFUS treatment without suffering these various skull issues, further technical improvements are required.

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References

  1. Bond AE, Shah BB, Huss DS, Dallapiazza RF, Warren A, Harrison MB, et al. : Safety and efficacy of focused ultrasound thalamotomy for patients with medication-refractory, tremor-dominant parkinson disease: a randomized clinical trial. JAMA Neurol 74 : 1412-1418, 2017 https://doi.org/10.1001/jamaneurol.2017.3098
  2. Chang WS, Jung HH, Kweon EJ, Zadicario E, Rachmilevitch I, Chang JW : Unilateral magnetic resonance guided focused ultrasound thalamotomy for essential tremor: practices and clinicoradiological outcomes. J Neurol Neurosurg Psychiatry 86 : 257-264, 2015 https://doi.org/10.1136/jnnp-2014-307642
  3. Chang WS, Jung HH, Zadicario E, Rachmilevitch I, Tlusty T, Vitek S, et al. : Factors associated with successful magnetic resonance-guided focused ultrasound treatment: efficiency of acoustic energy delivery through the skull. J Neurosurg 124 : 411-416, 2016 https://doi.org/10.3171/2015.3.JNS142592
  4. Chazen JL, Sarva H, Stieg PE, Min RJ, Ballon DJ, Pryor KO, et al. : Clinical improvement associated with targeted interruption of the cerebellothalamic tract following MR-guided focused ultrasound for essential tremor. J Neurosurg 129 : 315-323, 2018 https://doi.org/10.3171/2017.4.JNS162803
  5. Chen PY, Hsieh HY, Huang CY, Lin CY, Wei KC, Liu HL : Focused ultrasound- induced blood-brain barrier opening to enhance interleukin-12 delivery for brain tumor immunotherapy: a preclinical feasibility study. J Transl Med 13 : 93, 2015 https://doi.org/10.1186/s12967-015-0451-y
  6. Choi JJ, Wang S, Brown TR, Small SA, Duff KE, Konofagou EE : Noninvasive and transient blood-brain barrier opening in the hippocampus of alzheimer's double transgenic mice using focused ultrasound. Ultrason Imaging 30 : 189-200, 2008 https://doi.org/10.1177/016173460803000304
  7. Chu PC, Liu HL, Lai HY, Lin CY, Tsai HC, Pei YC : Neuromodulation accompanying focused ultrasound-induced blood-brain barrier opening. Sci Rep 5 : 15477, 2015 https://doi.org/10.1038/srep15477
  8. Clement GT, White J, Hynynen K : Investigation of a large-area phased array for focused ultrasound surgery through the skull. Phys Med Biol 45 : 1071-1083, 2000 https://doi.org/10.1088/0031-9155/45/4/319
  9. Clement GT, Hynynen K : A non-invasive method for focusing ultrasound through the human skull. Phys Med Biol 47 : 1219-1236, 2002 https://doi.org/10.1088/0031-9155/47/8/301
  10. Dobrakowski PP, Machowska-Majchrzak AK, Labuz-Roszak B, Majchrzak KG, Kluczewska E, Pierzchala KB : Mr-guided focused ultrasound: a new generation treatment of parkinson's disease, essential tremor and neuropathic pain. Interv Neuroradiol 20 : 275-282, 2014 https://doi.org/10.15274/INR-2014-10033
  11. Elias WJ, Lipsman N, Ondo WG, Ghanouni P, Kim YG, Lee W, et al. : A randomized trial of focused ultrasound thalamotomy for essential tremor. N Engl J Med 375 : 730-739, 2016 https://doi.org/10.1056/NEJMoa1600159
  12. Fry FJ, Ades HW, Fry WJ : Production of reversible changes in the central nervous system by ultrasound. Science 127 : 83-84, 1958 https://doi.org/10.1126/science.127.3289.83
  13. Fry WJ, Mosberg WH Jr, Barnard JW, Fry FJ : Production of focal destructive lesions in the central nervous system with ultrasound. J Neurosurg 11 : 471-478, 1954 https://doi.org/10.3171/jns.1954.11.5.0471
  14. Fry WJ, Barnard JW, Fry EJ, Krumins RF, Brennan JF : Ultrasonic lesions in the mammalian central nervous system. Science 122 : 517-518, 1955 https://doi.org/10.1126/science.122.3168.517
  15. Gallay MN, Moser D, Rossi F, Pourtehrani P, Magara AE, Kowalski M, et al. : Incisionless transcranial mr-guided focused ultrasound in essential tremor: cerebellothalamic tractotomy. J Ther Ultrasound 4 : 5, 2016 https://doi.org/10.1186/s40349-016-0049-8
  16. Hynynen K, Clement GT, McDannold N, Vykhodtseva N, King R, White PJ, et al. : 500-element ultrasound phased array system for noninvasive focal surgery of the brain: a preliminary rabbit study with ex vivo human skulls. Magn Reson Med 52 : 100-107, 2004 https://doi.org/10.1002/mrm.20118
  17. Ishihara Y, Calderon A, Watanabe H, Okamoto K, Suzuki Y, Kuroda K, et al. : A precise and fast temperature mapping using water proton chemical shift. Magn Reson Med 34 : 814-823, 1995 https://doi.org/10.1002/mrm.1910340606
  18. Jeanmonod D, Werner B, Morel A, Michels L, Zadicario E, Schiff G, et al. : Transcranial magnetic resonance imaging-guided focused ultrasound: noninvasive central lateral thalamotomy for chronic neuropathic pain. Neurosurg Focus 32 : E1, 2012
  19. Jung HH, Kim SJ, Roh D, Chang JG, Chang WS, Kweon EJ, et al. : Bilateral thermal capsulotomy with MR-guided focused ultrasound for patients with treatment-refractory obsessive-compulsive disorder: a proof-ofconcept study. Mol Psychiatry 20 : 1205-1211, 2015 https://doi.org/10.1038/mp.2014.154
  20. Kim M, Kim CH, Jung HH, Kim SJ, Chang JW : Treatment of major depressive disorder via magnetic resonance-guided focused ultrasound surgery. Biol Psychiatry 83 : e17-e18, 2018 https://doi.org/10.1016/j.biopsych.2017.05.008
  21. Kim SJ, Noh DY, Jung HH, Chang WS, Chang JW, Kim H : PT620. A pilot study of bilateral thermal capsulotomy with focused ultrasound for treatment-refractory (MRgFUS) obsessive-compulsive disorder. Int J Neuropsychopharmacol 19(Suppl 1) : 27-28, 2016
  22. Kuroda K, Oshio K, Chung AH, Hynynen K, Jolesz FA : Temperature mapping using the water proton chemical shift: a chemical shift selective phase mapping method. Magn Reson Med 38 : 845-851, 1997 https://doi.org/10.1002/mrm.1910380523
  23. Martinez-Fernandez R, Rodriguez-Rojas R, Del Alamo M, Hernandez-Fernandez F, Pineda-Pardo JA, Dileone M, et al. : Focused ultrasound subthalamotomy in patients with asymmetric parkinson's disease: a pilot study. Lancet Neurol 17 : 54-63, 2018 https://doi.org/10.1016/S1474-4422(17)30403-9
  24. Mueller JK, Ai L, Bansal P, Legon W : Numerical evaluation of the skull for human neuromodulation with transcranial focused ultrasound. J Neural Eng 14 : 066012, 2017 https://doi.org/10.1088/1741-2552/aa843e
  25. Na YC, Chang WS, Jung HH, Kweon EJ, Chang JW : Unilateral magnetic resonance-guided focused ultrasound pallidotomy for parkinson disease. Neurology 85 : 549-551, 2015 https://doi.org/10.1212/WNL.0000000000001826
  26. Sun J, Hynynen K : The potential of transskull ultrasound therapy and surgery using the maximum available skull surface area. J Acoust Soc Am 105 : 2519-2527, 1999 https://doi.org/10.1121/1.426863
  27. Tsai SJ : Transcranial focused ultrasound as a possible treatment for major depression. Med Hypotheses 84 : 381-383, 2015 https://doi.org/10.1016/j.mehy.2015.01.030
  28. Tung YS, Marquet F, Teichert T, Ferrera V, Konofagou EE : Feasibility of noninvasive cavitation-guided blood-brain barrier opening using focused ultrasound and microbubbles in nonhuman primates. Appl Phys Lett 98 : 163704, 2011 https://doi.org/10.1063/1.3580763
  29. Wegener N, Kaegi G, Bauer R, Werner B, Martin E, Schreglmann SR, et al. : MR-guided high intensity focused ultrasound in Parkinson's disease: a series of 5 cases. Mov Disord 31 : S2, 2016
  30. Wei KC, Chu PC, Wang HY, Huang CY, Chen PY, Tsai HC, et al. : Focused ultrasound-induced blood-brain barrier opening to enhance temozolomide delivery for glioblastoma treatment: a preclinical study. PLoS One 8 : e58995, 2013 https://doi.org/10.1371/journal.pone.0058995
  31. Weintraub D, Elias WJ : The emerging role of transcranial magnetic resonance imaging-guided focused ultrasound in functional neurosurgery. Mov Disord 32 : 20-27, 2017 https://doi.org/10.1002/mds.26599
  32. Wu SK, Chu PC, Chai WY, Kang ST, Tsai CH, Fan CH, et al. : Characterization of different microbubbles in assisting focused ultrasound-induced blood-brain barrier opening. Sci Rep 7 : 46689, 2017 https://doi.org/10.1038/srep46689
  33. Zaaroor M, Sinai A, Goldsher D, Eran A, Nassar M, Schlesinger I : Magnetic resonance-guided focused ultrasound thalamotomy for tremor: a report of 30 parkinson's disease and essential tremor cases. J Neurosurg 128 : 202-210, 2018 https://doi.org/10.3171/2016.10.JNS16758

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