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Experimental and Computational Investigation of Guided Waves in a Human Skull

      Abstract

      We investigate guided (Lamb) waves in a human cadaver skull through experiments and computational simulations. Ultrasonic wedge transducers and scanning laser Doppler vibrometry are used respectively to excite and measure Lamb waves propagating in the cranial bone of a degassed skull. Measurements are performed over a section of the parietal bone and temporal bone spanning the squamous suture. The experimental data are analyzed for the identification of wave modes and the characterization of dispersion properties. In the parietal bone, for instance, the A0 wave mode is excited between 200 and 600 kHz, and higher-order Lamb waves are excited from 1 to 1.8 MHz. From the experimental dispersion curves and average thickness extracted from the skull computed tomography scan, we estimate average isotropic material properties that capture the essential dispersion characteristics using a semi-analytical finite-element model. We also explore the leaky and non-leaky wave behavior of the degassed skull with water loading in the cranial cavity. Successful excitation of leaky Lamb waves is confirmed (for higher-order wave modes with phase velocity faster than the speed of sound in water) from 500 kHz to 1.5 MHz, which may find applications in imaging and therapeutics at the brain periphery or skull–brain interface (e.g., for metastases). The non-leaky A0 Lamb wave mode propagates between 200 and 600 kHz, with or without fluid loading, for potential use in skull-related diagnostics and imaging (e.g., for sutures).

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      References

        • Adams C
        • McLaughlan J
        • Nie L
        • Freear S.
        Excitation and acquisition of cranial guided waves using a concave array transducer.
        in: Proceedings of Meetings on Acoustics 173 EAA, Melville, NY30. Acoustical Society of America, 2017055003
        • Alleyne D
        • Cawley P.
        A two-dimensional Fourier transform method for the measurement of propagating multimode signals.
        J Acoust Soc Am. 1991; 89: 1159-1168
        • Aubry JF
        • Tanter M.
        MR-guided transcranial focused ultrasound.
        in: Escoffre JM Bouakaz A Therapeutic ultrasound. Springer, Cham2016: 97-111
        • Aubry JF
        • Tanter M
        • Pernot M
        • Thomas JL
        • Fink M.
        Experimental demonstration of noninvasive transskull adaptive focusing based on prior computed tomography scans.
        Journal Acoust Soc Am. 2003; 113: 84-93
        • Bochud N
        • Vallet Q
        • Minonzio JG
        • Laugier P.
        Predicting bone strength with ultrasonic guided waves.
        Sci Rep. 2017; 7: 43628
        • Boruah S
        • Subit DL
        • Paskoff GR
        • Shender BS
        • Crandall JR
        • Salzar RS.
        Influence of bone microstructure on the mechanical properties of skull cortical bone—A combined experimental and computational approach.
        J Mech Behav Biomed Mater. 2017; 65: 688-704
        • Clement GT
        • Hynynen K.
        A non-invasive method for focusing ultrasound through the human skull.
        Phys Med Biol. 2002; 47: 1219
        • Clement GT
        • Sun J
        • Giesecke T
        • Hynynen K.
        A hemisphere array for noninvasive ultrasound brain therapy and surgery.
        Phys Med Biol. 2000; 45: 3707
        • Datta SK
        • Shah AH
        • Bratton R
        • Chakraborty T.
        Wave propagation in laminated composite plates.
        J Acoust Soc Am. 1988; 83: 2020-2026
        • Dayal V
        • Kinra VK.
        Leaky lamb waves in an anisotropic plate: I. An exact solution and experiments.
        J Acoust Soc Am. 1989; 85: 2268-2276
        • Elias WJ
        • Huss D
        • Voss T
        • Loomba J
        • Khaled M
        • Zadicario E
        • Frysinger RC
        • Sperling SA
        • Wylie S
        • Monteith SJ
        • Druzgal J
        • Shah BB.
        A pilot study of focused ultrasound thalamotomy for essential tremor.
        N Engl J Med. 2013; 369: 640-648
        • Elias WJ
        • Lipsman N
        • Ondo WG
        • Ghanouni P
        • Kim YG
        • Lee W
        • Schwartz M
        • Hynynen K
        • Lozano AM
        • Shah BB
        • Huss D
        • Dallapiazza RF
        • Gwinn R
        • Witt J
        • Ro S
        • Eisenberg HM
        • Fishman PS
        • Gandhi D
        • Halpern CH
        • Chuang R
        • Butts Pauly K
        • Tierney TS
        • Hayes MT
        • Rees Cosgrove G
        • Yamaguchi T
        • Abe K
        • Taira T
        • Chang JW
        A randomized trial of focused ultrasound thalamotomy for essential tremor.
        N Engl J Med. 2016; 375: 730-739
        • Estrada H
        • Gottschalk S
        • Reiss M
        • Neuschmelting V
        • Goldbrunner R
        • Razansky D.
        Observation of guided acoustic waves in a human skull.
        Ultrasound Med Biol. 2018; 44: 2388-2392
        • Fearon JA
        • Singh DJ
        • Beals SP
        • Jack CY.
        The diagnosis and treatment of single-sutural synostoses: Are computed tomographic scans necessary?.
        Plast Reconstr Surg. 2007; 120: 1327-1331
        • Firouzi K
        • Ghanouni P
        • Khuri-Yakub BT.
        Efficient transcranial ultrasound delivery via excitation of lamb waves: Concept and preliminary results.
        in: 2017 IEEE International Ultrasonics Symposium (IUS), Washington, DC, Piscataway, NJ IEEE, 2017: 1-4
        • Foiret J
        • Minonzio JG
        • Chappard C
        • Talmant M
        • Laugier P.
        Combined estimation of thickness and velocities using ultrasound guided waves: A pioneering study on in vitro cortical bone samples.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2014; 61: 1478-1488
        • Fry FJ
        • Barger JE.
        Acoustical properties of the human skull.
        J Acoust Soc Am. 1978; 63: 1576-1590
        • Hubbard RP.
        Flexure of layered cranial bone.
        J Biomech. 1971; 4: 251-263
        • Hynynen K
        • Clement GT
        • McDannold N
        • Vykhodtseva N
        • King R
        • White PJ
        • Vitek S
        • Jolesz FA.
        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. 2004; 52: 100-107
        • Hynynen K
        • McDannold N
        • Sheikov NA
        • Jolesz FA
        • Vykhodtseva N.
        Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications.
        Neuroimage. 2005; 24: 12-20
        • Jaslow CR.
        Mechanical properties of cranial sutures.
        J Biomech. 1990; 23: 313-321
        • Kinoshita M
        • McDannold N
        • Jolesz FA
        • Hynynen K.
        Noninvasive localized delivery of herceptin to the mouse brain by MRI-guided focused ultrasound-induced blood-brain barrier disruption.
        Proc Natl Acad Sci USA. 2006; 103: 11719-11723
      1. Kohtanen E, Mazzotti M, Ruzzene M, Erturk A. Vibration-based elastic parameter identification of the diploë and cortical tables in dry cranial bones. In preparation.

        • Kyriakou A
        • Neufeld E
        • Werner B
        • Paulides MM
        • Szekely G
        • Kuster N.
        A review of numerical and experimental compensation techniques for skull-induced phase aberrations in transcranial focused ultrasound.
        Int J Hyperthermia. 2014; 30: 36-46
        • Lipsman N
        • Mainprize TG
        • Schwartz ML
        • Hynynen K
        • Lozano AM.
        Intracranial applications of magnetic resonance-guided focused ultrasound.
        Neurotherapeutics. 2014; 11: 593-605
        • Margulies SS
        • Thibault KL.
        Infant skull and suture properties: Measurements and implications for mechanisms of pediatric brain injury.
        J Biomech Eng. 2000; 122: 364-371
      2. Mazzotti M, Sugino C, Kohtanen E, Erturk A, Ruzzene M. Experimental identification of high order Lamb waves and estimation of the mechanical properties of a dry human skull. Under review.

        • McElhaney JH
        • Fogle JL
        • Melvin JW
        • Haynes RR
        • Roberts VL
        • Alem NM.
        Mechanical properties of cranial bone.
        J Biomech. 1970; 3: 495-511
        • Mesiwala AH
        • Farrell L
        • Wenzel HJ
        • Silbergeld DL
        • Crum LA
        • Winn HR
        • Mourad PD.
        High-intensity focused ultrasound selectively disrupts the blood-brain barrier in vivo.
        Ultrasound Med Biol. 2002; 28: 389-400
        • Michaels TE
        • Michaels JE
        • Ruzzene M.
        Frequency-wavenumber domain analysis of guided wavefields.
        Ultrasonics. 2011; 51: 452-466
        • Miller GW
        • Eames M
        • Snell J
        • Aubry JF.
        Ultrashort echo-time MRI versus CT for skull aberration correction in MR-guided transcranial focused ultrasound: In vitro comparison on human calvaria.
        Med Phys. 2015; 42: 2223-2233
        • Moilanen P.
        Ultrasonic guided waves in bone.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2008; 55: 1277-1286
        • Moilanen P
        • Nicholson PH
        • Kilappa V
        • Cheng S
        • Timonen J.
        Assessment of the cortical bone thickness using ultrasonic guided waves: Modelling and in vitro study.
        Ultrasound Med Biol. 2007; 33: 254-262
        • Nicholson PH
        • Moilanen P
        • Karkkainen T
        • Timonen J
        • Cheng S.
        Guided ultrasonic waves in long bones: Modelling, experiment and in vivo application.
        Physiol Meas. 2002; 23: 755-768
        • Niethammer M
        • Jacobs LJ
        • Qu J
        • Jarzynski J.
        Time–frequency representations of Lamb waves.
        J Acoust Soc Am. 2001; 109: 1841-1847
        • Odeen H
        • de Bever J
        • Almquist S
        • Farrer A
        • Todd N
        • Payne A
        • Snell JW
        • Christensen DA
        • Parker DL.
        Treatment envelope evaluation in transcranial magnetic resonance-guided focused ultrasound utilizing 3 D MR thermometry.
        J Ther Ultrasound. 2014; 2: 19
        • Peterson J
        • Dechow PC.
        Material properties of the human cranial vault and zygoma.
        Anat Rec A Discov Mol Cell Evol Biol. 2003; 274: 785-797
        • Protopappas VC
        • Fotiadis DI
        • Malizos KN.
        Guided ultrasound wave propagation in intact and healing long bones.
        Ultrasound Med Biol. 2006; 32: 693-708
        • Rabiner JE
        • Friedman LM
        • Khine H
        • Avner JR
        • Tsung JW.
        Accuracy of point-of-care ultrasound for diagnosis of skull fractures in children.
        Pediatrics. 2013; 131: e1757-e1764
        • Regelsberger J
        • Delling G
        • Helmke K
        • Tsokos M
        • Kammler G
        • Kranzlein H
        • Westphal M.
        Ultrasound in the diagnosis of craniosynostosis.
        J Craniofac Surg. 2006; 17: 623-625
        • Ruzzene M.
        Frequency-wavenumber domain filtering for improved damage visualization.
        Smart Mater Struct. 2007; 16: 2116
        • Tian Z
        • Yu L.
        Lamb wave frequency-wavenumber analysis and decomposition.
        J Intell Mater Syst Struct. 2014; 25: 1107-1123
        • Vavva MG
        • Protopappas VC
        • Gergidis LN
        • Charalambopoulos A
        • Fotiadis DI
        • Polyzos D.
        The effect of boundary conditions on guided wave propagation in two-dimensional models of healing bone.
        Ultrasonics. 2008; 48: 598-606
        • Weinberg ER
        • Tunik MG
        • Tsung JW.
        Accuracy of clinician-performed point-of-care ultrasound for the diagnosis of fractures in children and young adults.
        Injury. 2010; 41: 862-868
        • Wood JL.
        Dynamic response of human cranial bone.
        J Biomech. 1971; 4: 1-12
        • Yoganandan N
        • Pintar FA
        • Sances Jr, A
        • Walsh PR
        • Ewing CL
        • Thomas DJ
        • Snyder RG.
        Biomechanics of skull fracture.
        J Neurotrauma. 1995; 12: 659-668
        • Zhang X
        • Fincke JR
        • Wynn CM
        • Johnson MR
        • Haupt RW
        • Anthony BW.
        Full noncontact laser ultrasound: First human data.
        Light Sci Appl. 2019; 8: 1-11