Advertisement

Fast, Low-Frequency Plane-Wave Imaging for Ultrasound Contrast Imaging

  • Jiro Kusunose
    Affiliations
    Vanderbilt University Institute of Imaging Science, Vanderbilt University Medical Center, Nashville, Tennessee, USA
    Search for articles by this author
  • Charles F. Caskey
    Correspondence
    Address correspondence to: Charles F. Caskey, Vanderbilt University, Medical Center North, 1161 21st Avenue South, R-0103, Nashville, TN 37232, USA.
    Affiliations
    Vanderbilt University Institute of Imaging Science, Vanderbilt University Medical Center, Nashville, Tennessee, USA

    Department of Radiology and Radiologic Sciences, Vanderbilt University Medical Center, Nashville, Tennessee, USA

    Department of Biomedical Engineering, Vanderbilt University, Nashville, Tennessee, USA
    Search for articles by this author

      Abstract

      Plane-wave ultrasound contrast imaging offers a faster, less destructive means for imaging microbubbles compared with traditional ultrasound imaging. Even though many of the most acoustically responsive microbubbles have resonant frequencies in the lower-megahertz range, higher frequencies (>3 MHz) have typically been employed to achieve high spatial resolution. In this work we implement and optimize low-frequency (1.5-4 MHz) plane-wave pulse inversion imaging on a commercial, phased-array imaging transducer in vitro and illustrate its use in vivo by imaging a mouse xenograft model. We found that the 1.8-MHz contrast signal was about four times that acquired at 3.1 MHz on matched probes and nine times greater than echoes received on a higher-frequency probe. Low-frequency imaging was also much more resilient to motion. In vivo, we could identify sub-millimeter vasculature inside a xenograft tumor model and easily assess microbubble half-life. Our results indicate that low-frequency imaging can provide better signal-to-noise because it generates stronger non-linear responses. Combined with high-speed plane-wave imaging, this method could open the door to super-resolution imaging at depth, while high power pulses could be used for image-guided therapeutics.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Ultrasound in Medicine and Biology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Bez M
        • Sheyn D
        • Tawackoli W
        • Avalos P
        • Shapiro G
        • Giaconi J
        • Da X
        • David SB
        • Gavrity J
        • Awad HA
        • Bae HW
        • Ley EJ
        • Kremen TJ
        • Gazit Z
        • Ferrara KW
        • Pelled G
        • Gazit D
        In situ bone tissue engineering via ultrasound-mediated gene delivery to endogenous progenitor cells in mini-pigs.
        Sci Transl Med. 2017; 9: 6
        • Borden MA
        • Kruse DE
        • Caskey CF
        • Zhao S
        • Dayton PA
        • Ferrara KW
        Influence of lipid shell physicochemical properties on ultrasound-induced microbubble destruction.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2005; 52: 1992-2002
        • Bottenus NB
        • Long W
        • Morgan M
        • Trahey GE
        Evaluation of large aperture imaging through the ex vivo human abdominal wall.
        Ultrasound Med Biol. 2018; 44: 687-701
        • Choi JW
        • Lee JY
        • Hwang EJ
        • Hwang I
        • Woo S
        • Lee CJ
        • Park EJ
        • Choi BI
        Portable high-intensity focused ultrasound system with 3D electronic steering, real-time cavitation monitoring, and 3D image reconstruction algorithms: A preclinical study in pigs.
        Ultrasonography. 2014; 33: 191-199
        • Couture O
        • Bannouf S
        • Montaldo G
        • Aubry JF
        • Fink M
        • Tanter M
        Ultrafast imaging of ultrasound contrast agents.
        Ultrasound Med Biol. 2009; 35: 1908-1916
        • Couture O
        • Fink M
        • Tanter M
        Ultrasound contrast plane wave imaging.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2012; 59: 1
        • Crouse LJ
        • Cheirif J
        • Hanly DE
        • Kisslo JA
        • Labovitz AJ
        • Raichlen JS
        • Schutz RW
        • Shah PM
        • Smith MD
        Opacification and border delineation improvement in patients with suboptimal endocardial border definition in routine echocardiography: Results of the phase III Albunex Multicenter Trial.
        J Am Coll Cardiol. 1993; 22: 1494-1500
        • De Jong N
        • Bouakaz A
        • Frinking P
        Basic acoustic properties of microbubbles.
        Echocardiography . 2002; 19: 229-240
        • De Jong N
        • Bouakaz A
        • Ten Cate FJ
        Contrast harmonic imaging.
        Ultrasonics . 2002; 40: 567-573
        • De Jong N
        • Cornet R
        • Lancee CT
        Higher harmonics of vibrating gas-filled microspheres: Part One. Simulations.
        Ultrasonics. 1994; 32: 447-453
        • Ebbini ES
        • Ter Haar G
        Ultrasound-guided therapeutic focused ultrasound: Current status and future directions.
        Int J Hyperthermia. 2015; 31: 77-89
        • Ebbini ES
        • Yao H
        • Shrestha A
        Dual-mode ultrasound phased arrays for image-guided surgery.
        Ultrason Imaging. 2006; 28: 65-82
        • Errico C
        • Pierre J
        • Pezet S
        • Desailly Y
        • Lenkei Z
        • Couture O
        • Tanter M
        Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging.
        Nature. 2015; 527: 499-502
        • Foiret J
        • Zhang H
        • Mahakian L
        • Tam S
        • Ferrara KW
        Super-localization of contrast agents in moving organs, first experiments in a rat kidney.
        Proc IEEE Int Ultrason Symp. 2016; : 1-4
        • Goertz DE
        • De Jong N
        • Van der Steen AFW
        Attenuation and size distribution measurements of DefinityTM and manipulated DefinityTM populations.
        Ultrasound Med Biol. 2007; 33: 1376-1388
        • Gorce JM
        • Arditi M
        • Schneider M
        Influence of bubble size distribution on the echogenicity of ultrasound contrast agents: a study of SonoVue.
        Invest Radiol. 2000; 35: 661-671
        • Haritonova A
        • Liu D
        • Ebbini ES
        In vivo application and localization of transcranial focused ultrasound using dual-mode ultrasound arrays.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2015; 62: 2031-2042
        • Hasegawa H
        • Kanai H
        High frame rate echocardiography using diverging beams.
        Proc IEEE Int Ultrason Symp. 2011; : 132-135
        • Kasoji SK
        • Chang EH
        • Mullin LB
        • Chong WK
        • Rathmell WK
        • Dayton PA
        A pilot clinical study in characterization of malignant renal-cell carcinoma subtype with contrast-enhanced ultrasound.
        Ultrason Imaging. 2016; 39: 126-136
        • Kaya M
        • Feingold S
        • Hettiarachchi K
        • Lee AP
        • Dayton PA
        Acoustic responses of monodisperse lipid encapsulated microbubble contrast agents produced by flow focusing.
        Bubble Sci Eng Technol. 2010; 2: 33-40
        • Kennedy JE
        High-intensity focused ultrasound in the treatment of solid tumors.
        Nat Rev Cancer. 2005; 5: 321-327
        • Kotopoulis S
        • Dimcevski G
        • Gilja OH
        • Hoem D
        • Postema M
        Treatment of human pancreatic cancer using combined ultrasound, microbubbles, and gemcitabine: A clinical case study.
        Med Phys. 2013; 40072902
        • Kruse DE
        • Lai C
        • Stephens DN
        • Sutcliffe P
        • Paoli EE
        • Barnes SH
        • Ferrara KW
        Spatial and temporal-controlled tissue heating on a modified clinical ultrasound scanner for generating mild hyperthermia in tumors.
        IEEE Trans Biomed Eng. 2010; 57: 155-166
        • Leow CH
        • Bazigou E
        • Eckersley RJ
        • Yu ACH
        • Weinberg PD
        • Tang MX
        High-frame-rate plane wave utrasound and image tracking: Methods and initial in vitro and in vivo evaluation.
        Ultrasound Med Biol. 2015; 41: 2913-2925
        • Lin F
        • Shelton SE
        • Espíndola D
        • Rojas JD
        • Pinton G
        • Dayton PA
        3-D Ultrasound localization microscopy for identifying microvascular morphology features of tumor angiogenesis at a resolution beyond the diffraction limit of conventional ultrasound.
        Theranostics. 2017; 7: 196-204
        • Liu J
        • Foiret J
        • Stephens DN
        • Le Baron O
        • Ferrara KW
        Development of a spherically focused phased array transducer for ultrasonic image-guided hyperthermia.
        Phys Med Biol. 2016; 61: 5275-5296
        • McDannold N
        • Vykhodtseva N
        • Hynynen K
        Targeted disruption of the blood–brain barrier with focused ultrasound: Association with inertial cavitation.
        Proc IEEE Ultrason Symp. 2005; 2: 1249-1252
        • Medwin H.
        Counting bubbles acoustically: A review.
        Ultrasonics. 1977; 15: 7-13
        • Montaldo G
        • Tanter M
        • Bercoff J
        • Benech N
        • Fink M
        Coherent plane-wave compounding for very high frame rate ultrasonography and transient elastography.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2009; 56: 489-506
        • Morgan KE
        • Allen JS
        • Chomas JE
        • Klibanov AL
        • Ferrara KW
        Experimental and theoretical evaluation of ultrasonic contrast agent behavior: Effect of transmitted phase and bubble size.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2001; 47: 1494-1509
        • Papadacci C
        • Pernot M
        • Couade M
        • Fink M
        High contrast ultrafast imaging of the human heart.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2014; 61: 1-29
        • Qin S
        • Caskey CF
        • Ferrara KW
        Ultrasound contrast microbubbles in imaging and therapy: Physical principles and engineering.
        Phys Med Biol. 2009; 54: R27
        • Simpson DH
        • Chin CT
        • Burns PN
        Pulse inversion Doppler: A new method for detecting nonlinear echoes from microbubble contrast agents.
        IEEE Trans Ultrason Ferroelectr Freq Control. 1999; 46: 372-382
        • Toulemonde M
        • Duncan WC
        • Leow CH
        • Sboros V
        • Li Y
        • Eckersley RJ
        • Lin S
        • Tang MX
        • Butler M
        Cardiac flow mapping using high frame rate diverging wave contrast enhanced ultrasound and image tracking.
        Proc IEEE Int Ultrason Symp. 2017; : 1-4
        • Tremblay-Darveau C
        • Williams R
        • Milot L
        • Bruce M
        • Burns PN
        Visualizing the tumor microvasculature with a nonlinear plane-wave Doppler imaging scheme based on amplitude modulation.
        IEEE Trans Med Imaging. 2016; 35: 699-709
        • Tung YS
        • Choi JJ
        • Baseri B
        • Konofagou EE
        Identifying the intertial cavitation threshold and skull effects in a vessel phantom using focused ultrasound and microbubbles.
        Ultrasound Med Biol. 2010; 36: 840-852
        • Viti J
        • Vos HJ
        • De Jong N
        • Guidi F
        • Tortoli P
        • Jong NDe
        • Guidi F
        Detection of contrast agents: Plane wave vs focused transmission.
        IEEE Trans Ultrason Ferroelectr Freq Control. 2016; 63: 203-211
        • Wang T
        • Woo J
        • Pu K
        • Devulapally R
        • Bachawal S
        • Machtaler S
        • Mullick S
        • Luong R
        • Tian L
        • Khuri-yakub B
        • Rao J
        • Paulmurugan R
        • Willmann JK
        Ultrasound-guided delivery of microRNA loaded nanoparticles into cancer.
        J Control Release. 2015; 203: 99-108
        • Willmann JK
        • Bonomo L
        • Testa AC
        • Rinaldi P
        • Rindi G
        • Valluru KS
        • Petrone G
        • Martini M
        • Lutz AM
        • Gambhir SS
        Ultrasound molecular imaging with BR55 in patients with breast and ovarian lesions: First-in-human results.
        J Clin Oncol. 2017; 35: 2133-2140