Photoacoustic Imaging
- 887 Downloads
Abstract
Photoacoustic imaging (PAI) is an emerging imaging modality that shows great potential for preclinical research and clinical practice. As a hybrid technique, PAI uniquely combines the advantages of optical excitation and of acoustic detection. Optical excitation provides a rich contrast mechanism from either endogenous or exogenous chromophores, allowing PAI to perform biochemical, functional, and molecular imaging. Acoustic detection benefits from the low scattering of ultrasound in biological tissue, enabling PAI to generate high-resolution images in both the optical ballistic and diffusive regimes. Accordingly, this hybrid imaging modality features high sensitivity to optical absorption and wide scalability of spatial resolution with the desired imaging depth. Over the past two decades, the photoacoustic technique has led to a variety of exciting discoveries and applications from laboratory research to clinical patient care. In biological research, PAI has become an irreplaceable tool, providing functional optical contrast with high spatiotemporal resolution. Translational PAI also attracted growing interest in clinical applications including tumor margin examination, internal organ imaging, breast cancer screening, and sentinel lymph node mapping, among others.
References
- 1.Wang LV, Wu H-i (2012) Biomedical optics: principles and imaging. John Wiley & Sons, New York, NYGoogle Scholar
- 2.Culver J, Ntziachristos V, Holboke M, Yodh A (2001) Optimization of optode arrangements for diffuse optical tomography: a singular-value analysis. Opt Lett 26(10):701–703PubMedCrossRefPubMedCentralGoogle Scholar
- 3.Wang LV, Hu S (2012) Photoacoustic tomography: in vivo imaging from organelles to organs. Science 335(6075):1458–1462PubMedPubMedCentralCrossRefGoogle Scholar
- 4.Guo Z, Li L, Wang LV (2009) On the speckle-free nature of photoacoustic tomography. Med Phys 36(9 Part 1):4084–4088PubMedPubMedCentralCrossRefGoogle Scholar
- 5.Shah J, Park S, Aglyamov SR, Larson T, Ma L, Sokolov KV, Johnston KP, Milner TE, Emelianov SY (2008) Photoacoustic imaging and temperature measurement for photothermal cancer therapy. J Biomed Opt 13(3):034024PubMedCrossRefPubMedCentralGoogle Scholar
- 6.Xu M, Wang LV (2005) Universal back-projection algorithm for photoacoustic computed tomography. Phys Rev E 71(1):016706CrossRefGoogle Scholar
- 7.Wang LV (2008) Tutorial on photoacoustic microscopy and computed tomography. IEEE J Select Top Quant Electronics 14(1):171–179CrossRefGoogle Scholar
- 8.Wang LV (2009) Multiscale photoacoustic microscopy and computed tomography. Nat Photonics 3(9):503PubMedPubMedCentralCrossRefGoogle Scholar
- 9.Hristova Y, Kuchment P, Nguyen L (2008) Reconstruction and time reversal in thermoacoustic tomography in acoustically homogeneous and inhomogeneous media. Inverse Probl 24(5):055006CrossRefGoogle Scholar
- 10.Hu S, Wang LV (2013) Optical-resolution photoacoustic microscopy: auscultation of biological systems at the cellular level. Biophys J 105(4):841–847PubMedPubMedCentralCrossRefGoogle Scholar
- 11.American National Standards Institute (2000) American national standard for the safe use of lasers. ANSI Standard Z136.1. ANSI, New York, NYGoogle Scholar
- 12.Hu S, Maslov K, Wang LV (2011) Second-generation optical-resolution photoacoustic microscopy with improved sensitivity and speed. Opt Lett 36(7):1134–1136PubMedPubMedCentralCrossRefGoogle Scholar
- 13.Yao J, Wang L, Yang J-M, Maslov KI, Wong TT, Li L, Huang C-H, Zou J, Wang LV (2015) High-speed label-free functional photoacoustic microscopy of mouse brain in action. Nat Methods 12(5):407PubMedPubMedCentralCrossRefGoogle Scholar
- 14.Yao D-K, Maslov KI, Wang LV, Chen R, Zhou Q (2012) Optimal ultraviolet wavelength for in vivo photoacoustic imaging of cell nuclei. J Biomed Opt 17(5):056004PubMedPubMedCentralCrossRefGoogle Scholar
- 15.Favazza CP, Wang LV, Jassim OW, Cornelius LA (2011) In vivo photoacoustic microscopy of human cutaneous microvasculature and a nevus. J Biomed Opt 16(1):016015PubMedPubMedCentralCrossRefGoogle Scholar
- 16.Kothapalli S-R, Wang LV (2009) Ex vivo blood vessel imaging using ultrasound-modulated optical microscopy. J Biomed Opt 14(1):014015PubMedCrossRefPubMedCentralGoogle Scholar
- 17.Yang J-M, Maslov K, Yang H-C, Zhou Q, Shung KK, Wang LV (2009) Photoacoustic endoscopy. Opt Lett 34(10):1591–1593PubMedPubMedCentralCrossRefGoogle Scholar
- 18.Lutzweiler C, Razansky D (2013) Optoacoustic imaging and tomography: reconstruction approaches and outstanding challenges in image performance and quantification. Sensors 13(6):7345–7384PubMedPubMedCentralCrossRefGoogle Scholar
- 19.Shu W, Ai M, Salcudean T, Rohling R, Abolmaesumi P, Tang S (2016) Broadening the detection view of 2D photoacoustic tomography using two linear array transducers. Opt Express 24(12):12755–12768PubMedCrossRefPubMedCentralGoogle Scholar
- 20.Kim C, Erpelding TN, Jankovic L, Pashley MD, Wang LV (2010) Deeply penetrating in vivo photoacoustic imaging using a clinical ultrasound array system. Biomed Opt Express 1(1):278–284PubMedPubMedCentralCrossRefGoogle Scholar
- 21.Wang Y, Guo Z, Wang LV, Erpelding TN, Jankovic L, Robert J-L, David G (2012) In vivo three-dimensional photoacoustic imaging based on a clinical matrix array ultrasound probe. J Biomed Opt 17(6):061208PubMedPubMedCentralCrossRefGoogle Scholar
- 22.Jathoul AP, Laufer J, Ogunlade O, Treeby B, Cox B, Zhang E, Johnson P, Pizzey AR, Philip B, Marafioti T (2015) Deep in vivo photoacoustic imaging of mammalian tissues using a tyrosinase-based genetic reporter. Nat Photonics 9(4):239CrossRefGoogle Scholar
- 23.Li L, Zhu L, Ma C, Lin L, Yao J, Wang L, Maslov K, Zhang R, Chen W, Shi J (2017) Single-impulse panoramic photoacoustic computed tomography of small-animal whole-body dynamics at high spatiotemporal resolution. Nat Biomed Eng 1(5):0071PubMedPubMedCentralCrossRefGoogle Scholar
- 24.Ermilov SA, Su R, Conjusteau A, Oruganti T, Wang K, Anis F, Anastasio MA, Oraevsky AA (2015) Three-dimensional laser optoacoustic and laser ultrasound imaging system for biomedical research. In: Photons plus ultrasound: imaging and sensing 2015. International Society for Optics and Photonics, Bellingham, WAGoogle Scholar
- 25.Deán-Ben XL, Fehm TF, Ford SJ, Gottschalk S, Razansky D (2017) Spiral volumetric optoacoustic tomography visualizes multi-scale dynamics in mice. Light-Sci Appl 6(4):e16247PubMedPubMedCentralCrossRefGoogle Scholar
- 26.Xu M, Wang LV (2017) Analysis of spatial resolution in photoacoustic tomography. In: Photoacoustic imaging and spectroscopy. CRC Press, Boca Raton, FL, pp 47–60CrossRefGoogle Scholar
- 27.Lin L, Hu P, Shi J, Appleton CM, Maslov K, Li L, Zhang R, Wang LV (2018) Single-breath-hold photoacoustic computed tomography of the breast. Nat Commun 9(1):2352PubMedPubMedCentralCrossRefGoogle Scholar
- 28.Xia J, Yao J, Wang LV (2014) Photoacoustic tomography: principles and advances. Electromagn Waves (Camb) 147:1–22CrossRefGoogle Scholar
- 29.Roggenbuck M, Walker R, Catenacci J, Patch S (2013) Volumetric thermoacoustic imaging over large fields of view. Ultrason Imaging 35(1):57–67PubMedCrossRefPubMedCentralGoogle Scholar
- 30.Yan A, Lin L, Liu C, Shi J, Na S, Wang LV (2019) Microwave-induced thermoacoustic tomography through an adult human skull. Med Phys 46(4):1793–1797PubMedCrossRefPubMedCentralGoogle Scholar
- 31.Wong TT, Zhang R, Hai P, Zhang C, Pleitez MA, Aft RL, Novack DV, Wang LV (2017) Fast label-free multilayered histology-like imaging of human breast cancer by photoacoustic microscopy. Sci Adv 3(5):e1602168PubMedPubMedCentralCrossRefGoogle Scholar
- 32.Shi J, Wong TT, He Y, Li L, Zhang R, Yung CS, Hwang J, Maslov K, Wang LV (2019) High-resolution, high-contrast mid-infrared imaging of fresh biological samples with ultraviolet-localized photoacoustic microscopy. Nat Photonics 13:609PubMedPubMedCentralCrossRefGoogle Scholar
- 33.Zhang HF, Maslov K, Stoica G, Wang LV (2006) Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging. Nat Biotechnol 24(7):848PubMedCrossRefPubMedCentralGoogle Scholar
- 34.Fang H, Maslov K, Wang LV (2007) Photoacoustic Doppler effect from flowing small light-absorbing particles. Phys Rev Lett 99(18):184501PubMedCrossRefPubMedCentralGoogle Scholar
- 35.Yao J, Maslov KI, Shi Y, Taber LA, Wang LV (2010) In vivo photoacoustic imaging of transverse blood flow by using Doppler broadening of bandwidth. Opt Lett 35(9):1419–1421PubMedPubMedCentralCrossRefGoogle Scholar
- 36.Yao J, Maslov KI, Zhang Y, Xia Y, Wang LV (2011) Label-free oxygen-metabolic photoacoustic microscopy in vivo. J Biomed Opt 16(7):076003PubMedPubMedCentralCrossRefGoogle Scholar
- 37.Ranasinghesagara JC, Zemp RJ (2010) Combined photoacoustic and oblique-incidence diffuse reflectance system for quantitative photoacoustic imaging in turbid media. J Biomed Opt 15(4):046016PubMedCrossRefPubMedCentralGoogle Scholar
- 38.Bauer AQ, Nothdurft RE, Culver JP, Erpelding TN, Wang LV (2011) Quantitative photoacoustic imaging: correcting for heterogeneous light fluence distributions using diffuse optical tomography. J Biomed Opt 16(9):096016PubMedPubMedCentralCrossRefGoogle Scholar
- 39.Kim C, Cho EC, Chen J, Song KH, Au L, Favazza C, Zhang Q, Cobley CM, Gao F, Xia Y (2010) In vivo molecular photoacoustic tomography of melanomas targeted by bioconjugated gold nanocages. ACS Nano 4(8):4559–4564PubMedPubMedCentralCrossRefGoogle Scholar
- 40.Jin Y, Jia C, Huang S-W, O’donnell M, Gao X (2010) Multifunctional nanoparticles as coupled contrast agents. Nat Commun 1:41PubMedCrossRefPubMedCentralGoogle Scholar
- 41.Garcia-Uribe A, Erpelding TN, Krumholz A, Ke H, Maslov K, Appleton C, Margenthaler JA, Wang LV (2015) Dual-modality photoacoustic and ultrasound imaging system for noninvasive sentinel lymph node detection in patients with breast cancer. Sci Rep 5:15748PubMedPubMedCentralCrossRefGoogle Scholar
- 42.Beziere N, Lozano N, Nunes A, Salichs J, Queiros D, Kostarelos K, Ntziachristos V (2015) Dynamic imaging of PEGylated indocyanine green (ICG) liposomes within the tumor microenvironment using multi-spectral optoacoustic tomography (MSOT). Biomaterials 37:415–424PubMedCrossRefPubMedCentralGoogle Scholar
- 43.Brunker J, Yao J, Laufer J, Bohndiek SE (2017) Photoacoustic imaging using genetically encoded reporters: a review. J Biomed Opt 22(7):070901CrossRefGoogle Scholar
- 44.Yao J, Kaberniuk AA, Li L, Shcherbakova DM, Zhang R, Wang L, Li G, Verkhusha VV, Wang LV (2016) Multiscale photoacoustic tomography using reversibly switchable bacterial phytochrome as a near-infrared photochromic probe. Nat Methods 13(1):67PubMedCrossRefPubMedCentralGoogle Scholar
- 45.Li L, Zhang HF, Zemp RJ, Maslov K, Wang LV (2008) Simultaneous imaging of a lacZ-marked tumor and microvasculature morphology in vivo by dual-wavelength photoacoustic microscopy. J Innov Opt Health Sci 1(02):207–215PubMedPubMedCentralCrossRefGoogle Scholar
- 46.Razansky D, Distel M, Vinegoni C, Ma R, Perrimon N, Köster RW, Ntziachristos V (2009) Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo. Nat Photonics 3(7):412CrossRefGoogle Scholar
- 47.Wang L, Zhang C, Wang LV (2014) Grueneisen relaxation photoacoustic microscopy. Phys Rev Lett 113(17):174301PubMedPubMedCentralCrossRefGoogle Scholar
- 48.Beaven G, Holiday E (1952) Ultraviolet absorption spectra of proteins and amino acids. In: Advances in protein chemistry. Elsevier, Amsterdam, pp 319–386Google Scholar
- 49.Quickenden T, Irvin J (1980) The ultraviolet absorption spectrum of liquid water. J Chem Phys 72(8):4416–4428CrossRefGoogle Scholar
- 50.Zhang P, Li L, Lin L, Hu P, Shi J, He Y, Zhu L, Zhou Y, Wang LV (2018) High-resolution deep functional imaging of the whole mouse brain by photoacoustic computed tomography in vivo. J Biophotonics 11(1):e201700024CrossRefGoogle Scholar
- 51.Cao R, Li J, Ning B, Sun N, Wang T, Zuo Z, Hu S (2017) Functional and oxygen-metabolic photoacoustic microscopy of the awake mouse brain. NeuroImage 150:77–87PubMedCrossRefPubMedCentralGoogle Scholar
- 52.Yao J, Xia J, Maslov KI, Nasiriavanaki M, Tsytsarev V, Demchenko AV, Wang LV (2013) Noninvasive photoacoustic computed tomography of mouse brain metabolism in vivo. NeuroImage 64:257–266PubMedCrossRefPubMedCentralGoogle Scholar
- 53.Ron A, Davoudi N, Deán-Ben XL, Razansky D (2019) Self-gated respiratory motion rejection for optoacoustic tomography. Appl Sci 9(13):2737CrossRefGoogle Scholar
- 54.Wu Z, Li L, Yang Y, Hu P, Li Y, Yang S-Y, Wang LV, Gao W (2019) A microrobotic system guided by photoacoustic computed tomography for targeted navigation in intestines in vivo. Sci Robot 4(32):eaax0613PubMedPubMedCentralCrossRefGoogle Scholar
- 55.Lin L, Zhang P, Xu S, Shi J, Li L, Yao J, Wang L, Zou J, Wang LV (2016) Handheld optical-resolution photoacoustic microscopy. J Biomed Opt 22(4):041002PubMedCentralCrossRefGoogle Scholar
- 56.Liu M, Chen Z, Zabihian B, Sinz C, Zhang E, Beard PC, Ginner L, Hoover E, Minneman MP, Leitgeb RA, Kittler H, Drexler W (2016) Combined multi-modal photoacoustic tomography, optical coherence tomography (OCT) and OCT angiography system with an articulated probe for in vivo human skin structure and vasculature imaging. Biomed Opt Express 7(9):3390–3402PubMedPubMedCentralCrossRefGoogle Scholar
- 57.Chen Z, Rank E, Meiburger KM, Sinz C, Hodul A, Zhang E, Hoover E, Minneman M, Ensher J, Beard PC, Kittler H, Leitgeb RA, Drexler W, Liu M (2017) Non-invasive multimodal optical coherence and photoacoustic tomography for human skin imaging. Sci Rep 7(1):17975PubMedPubMedCentralCrossRefGoogle Scholar
- 58.Meiburger KM, Nam SY, Chung E, Suggs LJ, Emelianov SY, Molinari F (2016) Skeletonization algorithm-based blood vessel quantification using in vivo 3D photoacoustic imaging. Phys Med Biol 61(22):7994–8009PubMedCrossRefPubMedCentralGoogle Scholar
- 59.Yang JM, Li C, Chen R, Rao B, Yao J, Yeh CH, Danielli A, Maslov K, Zhou Q, Shung KK, Wang LV (2015) Optical-resolution photoacoustic endomicroscopy in vivo. Biomed Opt Express 6(3):918–932PubMedPubMedCentralCrossRefGoogle Scholar
- 60.Qu Y, Li C, Shi J, Chen R, Xu S, Rafsanjani H, Maslov K, Krigman H, Garvey L, Hu P, Zhao P, Meyers K, Diveley E, Pizzella S, Muench L, Punyamurthy N, Goldstein N, Onwumere O, Alisio M, Meyenburg K, Maynard J, Helm K, Slaughter J, Barber S, Burger T, Kramer C, Chubiz J, Anderson M, McCarthy R, England SK, Macones GA, Zhou Q, Shung KK, Zou J, Stout MJ, Tuuli M, Wang LV (2018) Transvaginal fast-scanning optical-resolution photoacoustic endoscopy. J Biomed Opt 23(12):1–4PubMedCrossRefPubMedCentralGoogle Scholar
- 61.Durduran T, Choe R, Culver JP, Zubkov L, Holboke MJ, Giammarco J, Chance B, Yodh AG (2002) Bulk optical properties of healthy female breast tissue. Phys Med Biol 47(16):2847–2861PubMedCrossRefPubMedCentralGoogle Scholar
- 62.Schneider BP, Miller KD (2005) Angiogenesis of breast cancer. J Clin Oncol 23(8):1782–1790PubMedCrossRefPubMedCentralGoogle Scholar
- 63.Matsumoto Y, Asao Y, Sekiguchi H, Yoshikawa A, Ishii T, Nagae K, Kobayashi S, Tsuge I, Saito S, Takada M, Ishida Y, Kataoka M, Sakurai T, Yagi T, Kabashima K, Suzuki S, Togashi K, Shiina T, Toi M (2018) Visualising peripheral arterioles and venules through high-resolution and large-area photoacoustic imaging. Sci Rep 8:14930PubMedPubMedCentralCrossRefGoogle Scholar
- 64.Diepstraten SC, Sever AR, Buckens CF, Veldhuis WB, van Dalen T, van den Bosch MA, Mali WP, Verkooijen HM (2014) Value of preoperative ultrasound-guided axillary lymph node biopsy for preventing completion axillary lymph node dissection in breast cancer: a systematic review and meta-analysis. Ann Surg Oncol 21(1):51–59PubMedCrossRefPubMedCentralGoogle Scholar
- 65.Ho CY, Shanahan CM (2016) Medial arterial calcification: an overlooked player in peripheral arterial disease. Arterioscler Thromb Vasc Biol 36(8):1475–1482PubMedCrossRefPubMedCentralGoogle Scholar
- 66.Nagae K, Asao Y, Sudo Y, Murayama N, Tanaka Y, Ohira K, Ishida Y, Otsuka A, Matsumoto Y, Saito S, Furu M, Murata K, Sekiguchi H, Kataoka M, Yoshikawa A, Ishii T, Togashi K, Shiina T, Kabashima K, Toi M, Yagi T (2018) Real-time 3D photoacoustic visualization system with a wide field of view for imaging human limbs. F1000Res 7:1813PubMedCrossRefPubMedCentralGoogle Scholar
- 67.Knieling F, Neufert C, Hartmann A, Claussen J, Urich A, Egger C, Vetter M, Fischer S, Pfeifer L, Hagel A, Kielisch C, Gortz RS, Wildner D, Engel M, Rother J, Uter W, Siebler J, Atreya R, Rascher W, Strobel D, Neurath MF, Waldner MJ (2017) Multispectral optoacoustic tomography for assessment of Crohn’s disease activity. N Engl J Med 376(13):1292–1294PubMedCrossRefPubMedCentralGoogle Scholar
- 68.Buj C, Munter M, Schmarbeck B, Horstmann J, Huttmann G, Brinkmann R (2017) Noncontact holographic detection for photoacoustic tomography. J Biomed Opt 22(10):1–14PubMedCrossRefPubMedCentralGoogle Scholar
- 69.Tzoumas S, Nunes A, Olefir I, Stangl S, Symvoulidis P, Glasl S, Bayer C, Multhoff G, Ntziachristos V (2016) Eigenspectra optoacoustic tomography achieves quantitative blood oxygenation imaging deep in tissues. Nat Commun 7:12121PubMedPubMedCentralCrossRefGoogle Scholar
- 70.Steenbergen W, Molenaar R, Daoudi K (2011) Combined application of photoacoustic and acousto-optic imaging for model-free quantitative optical absorption mapping. J Acoust Soc Am 129:2641CrossRefGoogle Scholar
- 71.Cox BT, Laufer JG, Beard PC (2010) Quantitative photoacoustic image reconstruction using fluence dependent chromophores. Biomed Opt Express 1(1):201–208PubMedPubMedCentralCrossRefGoogle Scholar
- 72.Liu Y, Jiang H, Yuan Z (2016) Two schemes for quantitative photoacoustic tomography based on Monte Carlo simulation. Med Phys 43(7):3987PubMedCrossRefPubMedCentralGoogle Scholar