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Biomedical Engineering Letters

, Volume 4, Issue 3, pp 213–222 | Cite as

Acoustic resolution photoacoustic microscopy

  • Sungjo Park
  • Changho Lee
  • Jeesu Kim
  • Chulhong Kim
Review Article

Abstract

Even if conventional optical imaging systems such as multiphoton microscopy (MPM), confocal microscopy (CM), fluorescence microscopy (FM), and optical coherence tomography (OCT) are regarded as revolutionary microscopic imaging modalities to reveal the inner information of biological tissues with very high spatial resolution, it is inherently restricted to image deep tissues due to strong optical scatting in biological tissues. Photoacoustic imaging (PAI) is a hybrid imaging modality to combine strong optical contrast and high ultrasonic resolution in deep tissues. In a microscopic imaging perspective, photoaocustic microscopy (PAM) can be implemented in two forms: optical-resolution (OR) and acoustic-resolution (AR) PAM. In OR-PAM, the lateral spatial resolution is determined by tight optical focusing, but the penetration depth is limited to one optical transport mean free path. In AR-PAM, the lateral spatial resolution is determined by loose acoustic focusing, but the penetration depth can be much enhanced and reach to several centimeters. Therefore, AR-PAM gains great attention for both preclinical and clinical applications. This review explains the principle, implementation, and applications of AR-PAM.

Keywords

Photoacoustic tomography Acoustic-resolution photoacoustic microscopy Preclinical imaging 

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References

  1. [1]
    Wang LV, Wu HI. Biomedical optics: principles and imaging. 1st ed. Wiley-Interscience; 2007.Google Scholar
  2. [2]
    Calasso IG, Craig W, Diebold GJ. Photoacoustic point source. Phys Rev Lett. 2001; 86(16):3550–3.CrossRefGoogle Scholar
  3. [3]
    Grashin PS, Karabutov AA, Oraevsky AA, Pelivanov IM, Podymova NB, Savateeva EVe, Solomatin VS. Distribution of the laser radiation intensity in turbid media: Monte Carlo simulations, theoretical analysis, and results of optoacoustic measurements. Quantum Electron. 2002; doi: 10.1070/QE2002v032n10ABEH002308.Google Scholar
  4. [4]
    Andreev VG, Karabutov AA, Oraevsky AA. Detection of ultrawide-band ultrasound pulses in optoacoustic tomography. IEEE T Ultrason Ferr. 2003; 50(10):1383–90.CrossRefGoogle Scholar
  5. [5]
    Zhang EZ, Laufer JG, Pedley RB, Beard PC. In vivo highresolution 3D photoacoustic imaging of superficial vascular anatomy. Phys Med Biol. 2009; 54(4):1035–46.CrossRefGoogle Scholar
  6. [6]
    Zhang HF, Maslov K, Stoica G, Wang LV. Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging. Nat Biotechnol. 2006; 24(7):848–51.CrossRefGoogle Scholar
  7. [7]
    Maslov K, Zhang HF, Hu S, Wang LV. Optical-resolution photoacoustic microscopy for in vivo imaging of single capillaries. Opt Lett. 2008; 33(9):929–31.CrossRefGoogle Scholar
  8. [8]
    Chen SL, Burnett J, Sun D, Wei X, Xie Z, Wang X. Photoacoustic microscopy: a potential new tool for evaluation of angiogenesis inhibitor. Biomed Opt Express. 2013; 4(11):2657–66.CrossRefGoogle Scholar
  9. [9]
    Ruan Q, Xi L, Boye SL, Han S, Chen ZJ, Hauswirth WW, Lewin AS, Boulton ME, Law BK, Jiang WG, Jiang H, Cai J. Development of an anti-angiogenic therapeutic model combining scAAV2-delivered siRNAs and noninvasive photoacoustic imaging of tumor vasculature development. Cancer Lett. 2013; 332(1):120–9.CrossRefGoogle Scholar
  10. [10]
    Foo SS, Abbott DF, Lawrentschuk N, Scott AM. Functional imaging of intratumoral hypoxia. Mol Imaging Biol. 2004; 6(5):291–305.CrossRefGoogle Scholar
  11. [11]
    Jo JG, Yang XM. Functional photoacoustic imaging to observe regional brain activation induced by cocaine hydrochloride. J Biomed Opt. 2011; doi: 10.1117/1.3626576.Google Scholar
  12. [12]
    Yao J, Maslov KI, Zhang Y, Xia Y, Wang LV. Label-free oxygen-metabolic photoacoustic microscopy in vivo. J Biomed Opt. 2011; doi: 10.1117/1.3594786.Google Scholar
  13. [13]
    Brunker J, Beard P. Pulsed photoacoustic Doppler flowmetry using time-domain cross-correlation: accuracy, resolution and scalability. J Acoust Soc Am. 2012; 132(3):1780–91.CrossRefGoogle Scholar
  14. [14]
    Shah J, Park S, Aglyamov S, Larson T, Ma L, Sokolov K, Johnston K, Milner T, Emelianov SY. Photoacoustic imaging and temperature measurement for photothermal cancer therapy. J Biomed Opt. 2008; doi: 10.1117/1.2940362.Google Scholar
  15. [15]
    Pramanik M, Wang LV. Thermoacoustic and photoacoustic sensing of temperature. J Biomed Opt. 2009; doi: 10.1117/1.3247155.Google Scholar
  16. [16]
    Liu T, Wei Q, Wang J, Jiao S, Zhang HF. Combined photoacoustic microscopy and optical coherence tomography can measure metabolic rate of oxygen. Biomed Opt Express. 2011; 2(5):1359–65.CrossRefGoogle Scholar
  17. [17]
    Yao J, Xia J, Maslov KI, Nasiriavanaki M, Tsytsarev V, Demchenko AV, Wang LV. Noninvasive photoacoustic computed tomography of mouse brain metabolism in vivo. Neuroimage. 2013; 64:257–66.CrossRefGoogle Scholar
  18. [18]
    Pu K, Shuhendler AJ, Jokerst JV, Mei J, Gambhir SS, Bao Z, Rao J. Semiconducting polymer nanoparticles as photoacoustic molecular imaging probes in living mice. Nat Nanotechnol. 2014; 9(3):233–9.CrossRefGoogle Scholar
  19. [19]
    Huynh E, Lovell JF, Helfield BL, Jeon M, Kim C, Goertz DE, Wilson BC, Zheng G. Porphyrin shell microbubbles with intrinsic ultrasound and photoacoustic properties. J Am Chem Soc. 2012; 134(40):16464–7.CrossRefGoogle Scholar
  20. [20]
    Kim G, Huang SW, Day KC, O’Donnell M, Agayan RR, Day MA, Kopelman R, Ashkenazi S. Indocyanine-green-embedded PEBBLEs as a contrast agent for photoacoustic imaging. J Biomed Opt. 2007; doi: 10.1117/1.2771530.Google Scholar
  21. [21]
    Li K, Liu B. Polymer-encapsulated organic nanoparticles for fluorescence and photoacoustic imaging. Chem Soc Rev. 2014; 43(18):6570–97.CrossRefGoogle Scholar
  22. [22]
    Cho EC, Kim C, Zhou F, Cobley CM, Song KH, Chen J, Li ZY, Wang LV, Xia Y. Measuring the optical absorption cross sections of Au Ag nanocages and Au nanorods by photoacoustic imaging. J Phys Chem C Nanomater Interfaces. 2009; 113(21): 9023–8.CrossRefGoogle Scholar
  23. [23]
    Zhang Y, Jeon M, Rich LJ, Hong H, Geng J, Zhang Y, Shi S, Barnhart TE, Alexandridis P, Huizinga JD, Seshadri M, Cai W, Kim C, Lovell JF. Non-invasive multimodal functional imaging of the intestine with frozen micellar naphthalocyanines. Nat Nanotechnol. 2014; 9(8):631–8.CrossRefGoogle Scholar
  24. [24]
    Li PC, Wei CW, Liao CK, Chen CD, Pao KC, Wang CR, Wu YN, Shieh DB. Photoacoustic imaging of multiple targets using gold nanorods. IEEE T Ultrason Ferr. 2007; 54(8):1642–7.CrossRefGoogle Scholar
  25. [25]
    Pramanik M, Swierczewska M, Wang LV, Green D, Sitharaman B. Single-walled carbon nanotubes as a multimodal-thermoacoustic and photoacoustic-contrast agent. J Biomed Opt. 2009; doi: 10.1117/1.3147407.Google Scholar
  26. [26]
    Pan D, Pramanik M, Senpan A, Yang X, Song KH, Scott MJ, Zhang H, Gaffney PJ, Wickline SA, Wang LV, Lanza GM. Molecular photoacoustic tomography with colloidal nanobeacons. Angewandte Chemie International Edition. 2009; 48(23):4170–3.CrossRefGoogle Scholar
  27. [27]
    Jeon M, Song W, Huynh E, Kim J, Kim J, Helfield BL, Leung BY, Goertz DE, Zheng G, Oh J. Methylene blue microbubbles as a model dual-modality contrast agent for ultrasound and activatable photoacoustic imaging. J Biomed Opt. 2014; 19(1):16005. doi: 10.1117/1.JBO.19.1.016005.CrossRefGoogle Scholar
  28. [28]
    Ohulchanskyy TY, Kopwitthaya A, Jeon M, Guo M, Law W-C, Furlani EP, Kim C, Prasad PN. Phospholipid micelle-based magneto-plasmonic nanoformulation for magnetic field-directed, imaging-guided photo-induced cancer therapy. Nanomedicine: Nanotechnol Biol Med. 2013; 9(8):1192–202.CrossRefGoogle Scholar
  29. [29]
    Kim C, Favazza C, Wang LV. In vivo photoacoustic tomography of chemicals: high-resolution functional and molecular optical imaging at new depths. Chem Rev. 2010; 110(5):2756–82.CrossRefGoogle Scholar
  30. [30]
    Wang LV. Tutorial on photoacoustic microscopy and computed tomography. IEEE J Sel Top Quant. 2008; 14(1):171–9.CrossRefGoogle Scholar
  31. [31]
    Yao J, Wang L. Multi-scale multi-contrast photoacoustic microscopy. Frontiers Opt. 2013; doi: 10.1364/FIO.2013.FM4A.1.Google Scholar
  32. [32]
    Jeon M, Kim J, Kim C. Multiplane spectroscopic whole-body photoacoustic imaging of small animals in vivo. Med Biol Eng Comput. 2014; doi: 10.1007/s11517-014-1182-6.Google Scholar
  33. [33]
    Maslov K, Stoica G, Wang LV. In vivo dark-field reflectionmode photoacoustic microscopy. Opt Lett. 2005; 30(6):625–7.CrossRefGoogle Scholar
  34. [34]
    Hu S, Maslov K, Wang LV. Second-generation opticalresolution photoacoustic microscopy with improved sensitivity and speed. Opt Lett. 2011; 36(7):1134–6.CrossRefGoogle Scholar
  35. [35]
    Han S, Lee C, Kim S, Jeon M, Kim J, Kim C. In vivo virtual intraoperative surgical photoacoustic microscopy. Appl Phys Lett. 2013; 103(20):2037–2.CrossRefGoogle Scholar
  36. [36]
    Cai X, Paratala BS, Hu S, Sitharaman B, Wang LV. Multiscale photoacoustic microscopy of single-walled carbon nanotubeincorporated tissue engineering scaffolds. Tissue Eng Part CMethods. 2012; 18(4):310–7.CrossRefGoogle Scholar
  37. [37]
    Xing WX, Wang LD, Maslov K, Wang LV. Integrated opticaland acoustic-resolution photoacoustic microscopy based on an optical fiber bundle. Opt Lett. 2013; 38(1):52–4.CrossRefGoogle Scholar
  38. [38]
    Purushotham AD, Upponi S, Klevesath MB, Bobrow L, Millar K, Myles JP, Duffy SW. Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial. J Clin Oncol. 2005; 23(19):4312–21.CrossRefGoogle Scholar
  39. [39]
    Krishnamurthy S, Sneige N, Bedi DG, Edieken BS, Fornage BD, Kuerer HM, Singletary SE, Hunt KK. Role of ultrasoundguided fine-needle aspiration of indeterminate and suspicious axillary lymph nodes in the initial staging of breast carcinoma. Cancer. 2002; 95(5):982–8.CrossRefGoogle Scholar
  40. [40]
    Baluk P, Fuxe J, Hashizume H, Romano T, Lashnits E, Butz S, Vestweber D, Corada M, Molendini C, Dejana E, McDonald DM. Functionally specialized junctions between endothelial cells of lymphatic vessels. J Exper Med. 2007; 204(10):2349–62.CrossRefGoogle Scholar
  41. [41]
    Li L, Liu C, Ren H, Wang QH. Adaptive liquid iris based on electrowetting. Opt Lett. 2013; 38(13):2336–8.CrossRefGoogle Scholar
  42. [42]
    Song L, Kim C, Maslov K, Shung KK, Wang LV. High-speed dynamic 3D photoacoustic imaging of sentinel lymph node in a murine model using an ultrasound array. Med Phys. 2009; 36(8):3724–9.CrossRefGoogle Scholar
  43. [43]
    Kim C, Song KH, Gao F, Wang LV. Sentinel lymph nodes and lymphatic vessels: noninvasive dual-modality in vivo mapping by using indocyanine green in rats-volumetric spectroscopic photoacoustic imaging and planar fluorescence imaging. Radiology. 2010; 255(2):442–50.CrossRefGoogle Scholar
  44. [44]
    Liu X, Lee C, Law WC, Zhu DW, Liu MX, Jeon M, Kim J, Prasad PN, Kim C, Swihart MT. Au-Cu2-xSe heterodimer nanoparticles with broad localized surface plasmon resonance as contrast agents for deep tissue imaging. Nano Lett. 2013; 13(9):4333–9.CrossRefGoogle Scholar
  45. [45]
    Luther JM, Jain PK, Ewers T, Alivisatos AP. Localized surface plasmon resonances arising from free carriers in doped quantum dots. Nat Mater. 2011; 10(5):361–6.CrossRefGoogle Scholar
  46. [46]
    Dorfs D, Hartling T, Miszta K, Bigall NC, Kim MR, Genovese A, Falqui A, Povia M, Manna L. Reversible tunability of the near-infrared valence band plasmon resonance in Cu(2-x)Se nanocrystals. J Am Chem Soc. 2011; 133(29):11175–80.CrossRefGoogle Scholar
  47. [47]
    Zhao Y, Pan H, Lou Y, Qiu X, Zhu J, Burda C. Plasmonic Cu2 x S nanocrystals: optical and structural properties of copper-deficient copper (I) Sulfides. J Am Chem Soc. 2009; 131(12):4253–61.CrossRefGoogle Scholar
  48. [48]
    Liu X, Law WC, Jeon M, Wang X, Liu M, Kim C, Prasad PN, Swihart MT. Cu2-xSe nanocrystals with localized surface plasmon resonance as sensitive contrast agents for in vivo photoacoustic imaging: demonstration of sentinel lymph node mapping. Adv Healthc Mater. 2013; 2(7):952–7.CrossRefGoogle Scholar
  49. [49]
    Koo J, Jeon M, Oh Y, Kang HW, Kim J, Kim C, Oh J. In vivo non-ionizing photoacoustic mapping of sentinel lymph nodes and bladders with ICG-enhanced carbon nanotubes. Phys Med Biol. 2012; 57(23):7853–62.CrossRefGoogle Scholar
  50. [50]
    De La Zerda A, Zavaleta C, Keren S, Vaithilingam S, Bodapati S, Liu Z, Levi J, Smith BR, Ma TJ, Oralkan O, Cheng Z, Chen X, Dai H, Khuri-Yakub BT, Gambhir SS. Carbon nanotubes as photoacoustic molecular imaging agents in living mice. Nat Nanotechnol. 2008; 3(9):557–62.CrossRefGoogle Scholar
  51. [51]
    Liu Z, Tabakman S, Welsher K, Dai H. Carbon nanotubes in biology and medicine: in vitro and in vivo detection, imaging and drug delivery. Nano Res. 2009; 2(2):85–120.CrossRefGoogle Scholar
  52. [52]
    Pramanik M, Song KH, Swierczewska M, Green D, Sitharaman B, Wang LV. In vivo carbon nanotube-enhanced non-invasive photoacoustic mapping of the sentinel lymph node. Phys Med Biol. 2009; 54(11):3291–301.CrossRefGoogle Scholar
  53. [53]
    O’connell MJ, Bachilo SM, Huffman CB, Moore VC, Strano MS, Haroz EH, Rialon KL, Boul PJ, Noon WH, Kittrell C, Ma J, Hauge RH, Weisman RB, Smalley RE. Band gap fluorescence from individual single-walled carbon nanotubes. Science. 2002; 297(5581):593–6.CrossRefGoogle Scholar
  54. [54]
    Scardapane A, Pagliarulo V, Ianora AA, Pagliarulo A, Angelelli G. Contrast-enhanced multislice pneumo-CT-cystography in the evaluation of urinary bladder neoplasms. Eur J Radiol. 2008; 66(2):246–52.CrossRefGoogle Scholar
  55. [55]
    Rothwell RI, Ash DV, Jones WG. Radiation treatment planning for bladder cancer: a comparison of cystogram localisation with computed tomography. Clin Radiol. 1983; 34(1):103–11.CrossRefGoogle Scholar
  56. [56]
    Browne RF, Murphy SM, Grainger R, Hamilton S. CT cystography and virtual cystoscopy in the assessment of new and recurrent bladder neoplasms. Eur J Radiol. 2005; 53(1):147–53.CrossRefGoogle Scholar
  57. [57]
    Lim R. Vesicoureteral reflux and urinary tract infection: evolving practices and current controversies in pediatric imaging. Am J Roentgenol. 2009; 192(5):1197–208.CrossRefGoogle Scholar
  58. [58]
    Brown MC, Sutherst JR, Murray A, Richmond DH. Potential use of ultrasound in place of X-ray fluoroscopy in urodynamics. Br J Urol. 1985; 57(1):88–90.CrossRefGoogle Scholar
  59. [59]
    Vining DJ, Zagoria RJ, Liu K, Stelts D. CT cystoscopy: an innovation in bladder imaging. Am J Roentgenol. 1996; 166(2):409–10.CrossRefGoogle Scholar
  60. [60]
    Kim C, Jeon M, Wang LV. Nonionizing photoacoustic cystography in vivo. Opt Lett. 2011; 36(18):3599–601.CrossRefGoogle Scholar
  61. [61]
    Kim C, Cho EC, Chen J, Song KH, Au L, Favazza C, Zhang Q, Cobley CM, Gao F, Xia Y, Wang LV. In vivo molecular photoacoustic tomography of melanomas targeted by bioconjugated gold nanocages. ACS Nano. 2010; 4(8):4559–64.CrossRefGoogle Scholar
  62. [62]
    Jeon M, Jenkins S, Oh J, Kim J, Peterson T, Chen J, Kim C. Nonionizing photoacoustic cystography with near-infrared absorbing gold nanostructures as optical-opaque tracers. Nanomedicine. 2013; 9(9):1377–88.CrossRefGoogle Scholar
  63. [63]
    Srivatsan A, Jenkins SV, Jeon M, Wu Z, Kim C, Chen J, Pandey RK. Gold nanocage-photosensitizer conjugates for dual-modal image-guided enhanced photodynamic therapy. Theranostics. 2014; 4(2):163–74.CrossRefGoogle Scholar
  64. [64]
    Soffer E. Small bowel motility: Ready for prime time?. Curr Gastroenterol Rep. 2000; 2(5):364–9.CrossRefGoogle Scholar
  65. [65]
    Ohama T, Hori M, Ozaki H. Mechanism of abnormal intestinal motility in inflammatory bowel disease: how smooth muscle contraction is reduced?. J Smooth Muscle Res. 2007; 43(2):43–54.CrossRefGoogle Scholar
  66. [66]
    Lembo A, Camilleri M. Chronic constipation. New England J Med. 2003; 349(14):1360–8.CrossRefGoogle Scholar
  67. [67]
    Abrahamsson H. Gastrointestinal motility disorders in patients with diabetes mellitus. J Intern Med. 1995; 237(4):403–9.CrossRefGoogle Scholar
  68. [68]
    Shafer RB, Prentiss RA, Bond JH. Gastrointestinal transit in thyroid disease. Gastroenterology. 1984; 86(5 Pt 1):852–5.Google Scholar
  69. [69]
    Jost WH. Gastrointestinal motility problems in patients with Parkinson’s disease. Drugs Aging. 1997; 10(4):249–58.CrossRefGoogle Scholar
  70. [70]
    Dye CE, Gaffney RR, Dykes TM, Moyer MT. Endoscopic and radiographic evaluation of the small bowel in 2012. Am J Med. 2012; doi:  10.1016/j.amjmed.2012.06.017.Google Scholar
  71. [71]
    Zhang Y, Jeon M, Rich LJ, Hong H, Geng J, Zhang Y, Shi S, Barnhart TE, Alexandridis P, Huizinga JD, Seshadri M, Cai W, Kim C, Lovell JF. Non-invasive multimodal functional imaging of the intestine with frozen micellar naphthalocyanines. Nat Nanotechnol. 2014; 9(8):631–8.CrossRefGoogle Scholar
  72. [72]
    Kagadis GC, Loudos G, Katsanos K, Langer SG, Nikiforidis GC. In vivo small animal imaging: current status and future prospects. Med Phys. 2010; 37(12):6421–42.CrossRefGoogle Scholar
  73. [73]
    Foster FS, Hossack J, Adamson SL. Micro-ultrasound for preclinical imaging. Interface Focus. 2011; 1(4):576–601.CrossRefGoogle Scholar
  74. [74]
    Ritman EL. Current status of developments and applications of micro-CT. Annu Rev Biomed Eng. 2011; 13:531–52.CrossRefGoogle Scholar
  75. [75]
    Goetz C, Breton E, Choquet P, Israel-Jost V, Constantinesco A. SPECT low-field MRI system for small-animal imaging. J Nucl Med. 2008; 49(1):88–93.CrossRefGoogle Scholar
  76. [76]
    Judenhofer MS, Cherry SR. Applications for preclinical PET/ MRI. Seminars Nucl Med. 2013; 43(1):19–29.CrossRefGoogle Scholar
  77. [77]
    Ntziachristos V. Going deeper than microscopy: the optical imaging frontier in biology. Nat Methods. 2010; 7(8):603–14.CrossRefGoogle Scholar
  78. [78]
    Biosphera Home Page. http://www.biosphera.com.br. Accessed 2-Oct-2014.Google Scholar

Copyright information

© Korean Society of Medical and Biological Engineering and Springer 2014

Authors and Affiliations

  • Sungjo Park
    • 1
  • Changho Lee
    • 2
  • Jeesu Kim
    • 3
  • Chulhong Kim
    • 2
    • 3
  1. 1.Department of Electrical Engineering, College of IT EngineeringKyungpook National UniversityDaeguRepublic of Korea
  2. 2.Department of Creative IT EngineeringPohang University of Science and TechnologyPohang, GyeongbukRepublic of Korea
  3. 3.Department of Electrical EngineeringPohang University of Science and TechnologyPohang, GyeongbukRepublic of Korea

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