Transcranial MR-guided focused ultrasound sonothrombolysis in the treatment of intracerebral hemorrhage.

Intracerebral hemorrhage remains a significant cause of morbidity and mortality. Current surgical therapies aim to use a minimally invasive approach to remove as much of the clot as possible without causing undue disruption to surrounding neural structures. Transcranial MR-guided focused ultrasound (MRgFUS) surgery is an emerging technology that permits a highly concentrated focal point of ultrasound energy to be deposited to a target deep within the brain without an incision or craniotomy. With appropriate ultrasound parameters it has been shown that MRgFUS can effectively liquefy large-volume blood clots through the human calvaria. In this review the authors discuss the rationale for using MRgFUS to noninvasively liquefy intracerebral hemorrhage (ICH), thereby permitting minimally invasive aspiration of the liquefied clot via a small drainage tube. The mechanism of action of MRgFUS sonothrombolysis; current investigational work with in vitro, in vivo, and cadaveric models of ICH; and the potential clinical application of this disruptive technology for the treatment of ICH are discussed.

[1]  A. Rabinstein.  Early Surgery Versus Initial Conservative Treatment in Patients With Spontaneous Supratentorial Intracerebral Haematomas in the International Surgical Trial in Intracerebral Haemorrhage (STICH): A Randomised Trial , 2006 .

[2]  C. Francis,et al.  Ultrasound accelerates transport of recombinant tissue plasminogen activator into clots. , 1995, Ultrasound in medicine & biology.

[3]  C. Sudlow,et al.  Comparable studies of the incidence of stroke and its pathological types: results from an international collaboration. International Stroke Incidence Collaboration. , 1997, Stroke.

[4]  D. Hanley,et al.  Preliminary findings of the minimally-invasive surgery plus rtPA for intracerebral hemorrhage evacuation (MISTIE) clinical trial. , 2008, Acta neurochirurgica. Supplement.

[5]  S L Diamond,et al.  Inner clot diffusion and permeation during fibrinolysis. , 1993, Biophysical journal.

[6]  D. Hanley,et al.  Preliminary report of the clot lysis evaluating accelerated resolution of intraventricular hemorrhage (CLEAR-IVH) clinical trial. , 2008, Acta neurochirurgica. Supplement.

[7]  W. Hauser,et al.  The incidence of deep and lobar intracerebral hemorrhage in whites, blacks, and Hispanics , 2005, Neurology.

[8]  K. Ohno,et al.  Chronological changes of perihematomal edema of human intracerebral hematoma. , 2003, Acta neurochirurgica. Supplement.

[9]  Max Wintermark,et al.  Potential intracranial applications of magnetic resonance-guided focused ultrasound surgery. , 2013, Journal of neurosurgery.

[10]  J. Broderick,et al.  Relative Edema Volume Is a Predictor of Outcome in Patients With Hyperacute Spontaneous Intracerebral Hemorrhage , 2002, Stroke.

[11]  K. Hynynen.  MRI-guided focused ultrasound treatments. , 2010, Ultrasonics.

[12]  M. Wintermark,et al.  Optimal Imaging of In Vitro Clot Sonothrombolysis by MR‐Guided Focused Ultrasound , 2013, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[13]  J. Gilsbach,et al.  Fibrinolysis therapy achieved with tissue plasminogen activator and aspiration of the liquefied clot after experimental intracerebral hemorrhage: rapid reduction in hematoma volume but intensification of delayed edema formation. , 2002, Journal of neurosurgery.

[14]  John Muschelli,et al.  Minimally invasive evacuation of spontaneous intracerebral hemorrhage using sonothrombolysis. , 2011, Journal of neurosurgery.

[15]  S. Maier,et al.  MAGNETIC RESONANCE IMAGING‐GUIDED, HIGH‐INTENSITY FOCUSED ULTRASOUND FOR BRAIN TUMOR THERAPY , 2006, Neurosurgery.

[16]  Adnan I Qureshi,et al.  Intracerebral haemorrhage , 2011, Radiopaedia.org.

[17]  R. Hawes,et al.  High-intensity focused ultrasound. , 1994, Gastrointestinal endoscopy clinics of North America.

[18]  A. Morel,et al.  High‐intensity focused ultrasound for noninvasive functional neurosurgery , 2009, Annals of neurology.

[19]  Max Wintermark,et al.  Magnetic resonance-guided focused ultrasound surgery: Part 2: A review of current and future applications. , 2012, Neurosurgery.

[20]  K. Butcher,et al.  Perihematomal Edema in Primary Intracerebral Hemorrhage Is Plasma Derived , 2004, Stroke.

[21]  A. Unterberg,et al.  Surgical treatment of intracerebral haemorrhage. , 2007, Current opinion in critical care.

[22]  J. Bernheim,et al.  Ultrasound imaging-guided noninvasive ultrasound thrombolysis: preclinical results. , 2000, Circulation.

[23]  Natalia Vykhodtseva,et al.  Improved anti-tumor effect of liposomal doxorubicin after targeted blood-brain barrier disruption by MRI-guided focused ultrasound in rat glioma. , 2012, Ultrasound in medicine & biology.

[24]  A. Kleindienst,et al.  Spontaneous intracerebral hemorrhage , 1997 .

[25]  J. Broderick,et al.  Volume of Intracerebral Hemorrhage: A Powerful and Easy‐to‐Use Predictor of 30‐Day Mortality , 1993, Stroke.

[26]  R. B. Roemer,et al.  Treatment of malignant brain tumors with focused ultrasound hyperthermia and radiation: results of a phase I trial , 1991, Journal of Neuro-Oncology.

[27]  Takenoriyamaguchi,et al.  Enlargement of Spontaneous Intracerebral Hemorrhage , 1996 .

[28]  D. Rijken,et al.  Acceleration of fibrinolysis by high-frequency ultrasound: the contribution of acoustic streaming and temperature rise. , 2000, Thrombosis research.

[29]  Max Wintermark,et al.  Minimally invasive treatment of intracerebral hemorrhage with magnetic resonance-guided focused ultrasound. , 2013, Journal of neurosurgery.

[30]  ThomasBrott,et al.  Early Hemorrhage Growth in Patients With Intracerebral Hemorrhage , 1997 .

[31]  Joseph P Broderick,et al.  Natural History of Perihematomal Edema in Patients With Hyperacute Spontaneous Intracerebral Hemorrhage , 2002, Stroke.

[32]  Daniel Jeanmonod,et al.  Measurement of targeting accuracy in focused ultrasound functional neurosurgery. , 2012, Neurosurgical focus.

[33]  K. Hynynen,et al.  Focusing of therapeutic ultrasound through a human skull: a numerical study. , 1998, The Journal of the Acoustical Society of America.

[34]  Andreas Unterberg,et al.  Surgical treatment of intracerebral haemorrhage , 2007, British medical bulletin.

[35]  Lars Michels,et al.  Transcranial magnetic resonance imaging-guided focused ultrasound: noninvasive central lateral thalamotomy for chronic neuropathic pain. , 2012, Neurosurgical focus.

[36]  Jay Jagannathan,et al.  HIGH‐INTENSITY FOCUSED ULTRASOUND SURGERY OF THE BRAIN: PART 1—A HISTORICAL PERSPECTIVE WITH MODERN APPLICATIONS , 2009, Neurosurgery.

[37]  Natalia Vykhodtseva,et al.  Temporary disruption of the blood-brain barrier by use of ultrasound and microbubbles: safety and efficacy evaluation in rhesus macaques. , 2012, Cancer research.

[38]  Haruko Yamamoto,et al.  Enlargement of spontaneous intracerebral hemorrhage. Incidence and time course. , 1996, Stroke.

[39]  F A Jolesz,et al.  Demonstration of potential noninvasive ultrasound brain therapy through an intact skull. , 1998, Ultrasound in medicine & biology.

[40]  L. Mayfrank,et al.  CT-guided stereotactic fibrinolysis of spontaneous and hypertensive cerebellar hemorrhage: long-term results. , 1990, Journal of neurosurgery.

[41]  Issam A Awad,et al.  Thrombolytic Evacuation of Intracerebral and Intraventricular Hemorrhage , 2012, Current Cardiology Reports.

[42]  M. Hennerici,et al.  Brain Temperature During 340-kHz Pulsed Ultrasound Insonation: A Safety Study for Sonothrombolysis , 2006, Stroke.