DOI QR코드

DOI QR Code

Review of Photoacoustic Imaging for Imaging-Guided Spinal Surgery

  • Han, Seung Hee (Division of Biophotonics, Princess Margaret Hospital, University Health Network)
  • Received : 2018.09.07
  • Accepted : 2018.11.10
  • Published : 2018.12.31

Abstract

This review introduces the current technique of photoacoustic imaging as it is applied in imaging-guided surgery (IGS), which provides the surgeon with image visualization and analysis capabilities during surgery. Numerous imaging techniques have been developed to help surgeons perform complex operations more safely and quickly. Although surgeons typically use these kinds of images to visualize targets hidden by bone and other tissues, it is nonetheless more difficult to perform surgery with static reference images (e.g., computed tomography scans and magnetic resonance images) of internal structures. Photoacoustic imaging could enable real-time visualization of regions of interest during surgery. Several researchers have shown that photoacoustic imaging has potential for the noninvasive diagnosis of various types of tissues, including bone. Previous studies of the surgical application of photoacoustic imaging have focused on cancer surgery, but photoacoustic imaging has also recently attracted interest for spinal surgery, because it could be useful for avoiding pedicle breaches and for choosing an appropriate starting point before drilling or pedicle probe insertion. This review describes the current instruments and clinical applications of photoacoustic imaging. Its primary objective is to provide a comprehensive overview of photoacoustic IGS in spinal surgery.

Keywords

References

  1. Jolesz FA. Definition of image guided therapy. In: Jolesz FA, editor. Intraopeative imaging and image-guided therapy. New York: Springer; 2014. p. 1-23.
  2. Eddins B, Bell MA. Design of a multifiber light delivery system for photoacoustic-guided surgery. J Biomed Opt 2017;22:41011. https://doi.org/10.1117/1.JBO.22.4.041011
  3. Bell AG. On the production and reproduction of sound by light. Am J Sci 1880;20:305-24.
  4. Wang LV. Tutorial on photoacoustic microscopy and computed tomography. IEEE J Sel Top Quantum Electron 2008;14:171-9. https://doi.org/10.1109/JSTQE.2007.913398
  5. Beard P. Biomedical photoacoustic imaging. Interface Focus 2011;1:602-31. https://doi.org/10.1098/rsfs.2011.0028
  6. Rao NA. Ultrasound imaging. Hoboken (NJ): John Wiley & Sons; 2002.
  7. Valluru KS, Willmann JK. Clinical photoacoustic imaging of cancer. Ultrasonography 2016;35:267-80. https://doi.org/10.14366/usg.16035
  8. Singh MK, Steenbergen W, Manohar S. Handheld probebased dual mode ultrasound/photoacoustics for biomedical imaging. In: Olivo M, Dinish US, editors. Frontiers in biophotonics for translational medicine in the celebration of year of light (2015). Singapore: Springer; 2015. p. 209-47.
  9. Zou C, Wu B, Dong Y, et al. Biomedical photoacoustics: fundamentals, instrumentation and perspectives on nanomedicine. Int J Nanomedicine 2016;12:179-95. https://doi.org/10.2147/IJN.S124218
  10. Piras D, Xia W, Steenbergen W, et al. Photoacoustic imaging of the breast using the twente photoacoustic mammoscope: present status and future perspectives. IEEE J Sel Top Quantum Electron 2010;16:730-9. https://doi.org/10.1109/JSTQE.2009.2034870
  11. Heijblom M, Piras D, van den Engh FM, et al. The state of the art in breast imaging using the Twente Photoacoustic Mammoscope: results from 31 measurements on malignancies. Eur Radiol 2016;26:3874-87. https://doi.org/10.1007/s00330-016-4240-7
  12. Wittekind C, Neid M. Cancer invasion and metastasis. Oncology 2005;69 Suppl 1:14-6. https://doi.org/10.1159/000086626
  13. Veronesi U, Paganelli G, Galimberti V, et al. Sentinel-node biopsy to avoid axillary dissection in breast cancer with clinically negative lymph-nodes. Lancet 1997;349:1864-7. https://doi.org/10.1016/S0140-6736(97)01004-0
  14. Song KH, Stein EW, Margenthaler JA, et al. Noninvasive photoacoustic identification of sentinel lymph nodes containing methylene blue in vivo in a rat model. J Biomed Opt 2008;13:054033. https://doi.org/10.1117/1.2976427
  15. Kim C, Song KH, Gao F, et al. 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;255:442-50. https://doi.org/10.1148/radiol.10090281
  16. Wang X, Roberts WW, Carson PL, et al. Photoacoustic tomography: a potential new tool for prostate cancer. Biomed Opt Express 2010;1:1117-26. https://doi.org/10.1364/BOE.1.001117
  17. Olafsson R, Bauer DR, Montilla LG, et al. contrast enhanced photoacoustic imaging of cancer in a mouse window chamber. Opt Express 2010;18:18625-32. https://doi.org/10.1364/OE.18.018625
  18. Bauer DR, Olafsson R, Montilla LG, et al. 3-D photoacoustic and pulse echo imaging of prostate tumor progression in the mouse window chamber. J Biomed Opt 2011;16:026012. https://doi.org/10.1117/1.3540668
  19. Yaseen MA, Brecht HP, Ermilov SA, et al. Hybrid optoacoustic and ultrasonic imaging system for detection of prostate malignancies. In: Proceedings of SPIE - The International Society for Optical Engineering 6856. 2008;6856:68560T-2.
  20. Yaseen MA, Ermilov SA, Brecht HP, et al. Optoacoustic imaging of the prostate: development toward image-guided biopsy. J Biomed Opt 2010;15:021310. https://doi.org/10.1117/1.3333548
  21. Agarwal A, Huang SW, O'Donnell M, et al. Targeted gold nanorod contrast agent for prostate cancer detection by photoacoustic imaging. J Appl Phys 2007;102:064701. https://doi.org/10.1063/1.2777127
  22. Levi J, Sathirachinda A, Gambhir SS. A high-affinity, highstability photoacoustic agent for imaging gastrin-releasing peptide receptor in prostate cancer. Clin Cancer Res 2014;20:3721-9. https://doi.org/10.1158/1078-0432.CCR-13-3405
  23. Aguirre A, Ardeshirpour Y, Sanders MM, et al. Potential role of coregistered photoacoustic and ultrasound imaging in ovarian cancer detection and characterization. Transl Oncol 2011;4:29-37. https://doi.org/10.1593/tlo.10187
  24. Kumavor PD, Alqasemi U, Tavakoli B, et al. Co-registered pulse-echo/photoacoustic transvaginal probe for real time imaging of ovarian tissue. J Biophotonics 2013;6:475-84. https://doi.org/10.1002/jbio.201200163
  25. Alqasemi U, Li H, Yuan G, et al. Ultrafast ultrasound and photoacoustic co-registered imaging system based on FPGA parallel processing. In: Oraevsky AA, Wang LV, editors. Proceedings of SPIE: medical imaging 2012-photons plus ultrasound: imaging and sensing 2012. Bellingham (WA): International Society for Optics and Photonics; 2012:82232U.
  26. Xi L, Grobmyer SR, Wu L, et al. Evaluation of breast tumor margins in vivo with intraoperative photoacoustic imaging. Opt Express 2012;20:8726-31. https://doi.org/10.1364/OE.20.008726
  27. Lediju Bell MA, Ostrowski AK, Li K, et al. Localization of transcranial targets for photoacoustic-guided endonasal surgeries. Photoacoustics 2015;3:78-87. https://doi.org/10.1016/j.pacs.2015.05.002
  28. Gandhi N, Allard M, Kim S, et al, Photoacoustic-based approach to surgical guidance performed with and without a da Vinci robot. J Biomed Opt 2017;22:121606.
  29. Allard M, Shubert J, Bell MAL. Feasibility of photoacousticguided teleoperated hysterectomies. J Med Imaging (Bellingham) 2018;5:021213.
  30. Allard M, Shubert J, Lediju Bell MA. Technical note: feasibility of photoacoustic guided hysterectomies with the da Vinci robot. Proceedings Volume 10576, Medical Imaging 2018: image-guided procedures, robotic interventions, and modeling; 105760A; 2018 Mar 12; Houston (TX), USA. https://doi.org/10.1117/12.2293176.
  31. Kazanzidesy P, Chen Z, Deguet A, et al. An open-source research kit for the da $Vinci^{(R)}$ Surgical System. In: 2014 IEEE International Conference on Robotics & Automation (ICRA); 2014 May 31-Jun 7; Hong Kong. IEEE 2014:6434-9.
  32. Laufer J, Zhang E, Raivich G, et al. Three-dimensional noninvasive imaging of the vasculature in the mouse brain using a high resolution photoacoustic scanner. Appl Opt 2009;48:D299-306. https://doi.org/10.1364/AO.48.00D299
  33. Burton NC, Patel M, Morscher S, et al. Multispectral optoacoustic tomography (MSOT) of the brain and glioblastoma characterization. Neuroimage 2013;65:522-8. https://doi.org/10.1016/j.neuroimage.2012.09.053
  34. Yao J, Xia J, Maslov KI, et al. Noninvasive photoacoustic computed tomography of mouse brain metabolism in vivo. Neuroimage 2013;64:257-66. https://doi.org/10.1016/j.neuroimage.2012.08.054
  35. Nasiriavanaki M, Xia J, Wan H, et al. High-resolution photoacoustic tomography of resting-state functional connectivity in the mouse brain. Proc Natl Acad Sci U S A 2014;111:21-6. https://doi.org/10.1073/pnas.1311868111
  36. Jo J, Yang X. Functional photoacoustic imaging to observe regional brain activation induced by cocaine hydrochloride. J Biomed Opt 2011;16:090506. https://doi.org/10.1117/1.3626576
  37. Liao LD, Li ML, Lai HY, et al. Imaging brain hemodynamic changes during rat forepaw electrical stimulation using functional photoacoustic microscopy. Neuroimage 2010;52:562-70. https://doi.org/10.1016/j.neuroimage.2010.03.065
  38. Pilatou MC, Marani E, de Mul FF, et al. Photoacoustic imaging of brain perfusion on albino rats by using evans blue as contrast agent. Arch Physiol Biochem 2003;111:389-97. https://doi.org/10.3109/13813450312331337649
  39. Yao J, Wang LV. Photoacoustic brain imaging: from microscopic to macroscopic scales. Neurophotonics 2014;1.
  40. Deng Z, Wang Z, Yang X, et al. In vivo imaging of hemodynamics and oxygen metabolism in acute focal cerebral ischemic rats with laser speckle imaging and functional photoacoustic microscopy. J Biomed Opt 2012;17:081415-1. https://doi.org/10.1117/1.JBO.17.8.081415
  41. Tsytsarev V, Rao B, Maslov KI, et al. Photoacoustic and optical coherence tomography of epilepsy with high temporal and spatial resolution and dual optical contrasts. J Neurosci Methods 2013;216:142-5. https://doi.org/10.1016/j.jneumeth.2013.04.001
  42. Xu Z, Zhu Q, Wang LV. In vivo photoacoustic tomography of mouse cerebral edema induced by cold injury. J Biomed Opt 2011;16:066020. https://doi.org/10.1117/1.3584847
  43. Tang J, Xi L, Zhou J, et al. Noninvasive high-speed photoacoustic tomography of cerebral hemodynamics in awakemoving rats. J Cereb Blood Flow Metab 2015;35:1224-32. https://doi.org/10.1038/jcbfm.2015.138
  44. van den Berg PJ, Daoudi K, Bernelot Moens HJ, et al. Feasibility of photoacoustic/ultrasound imaging of synovitis in finger joints using a point-of-care system. Photoacoustics 2017;8:8-14. https://doi.org/10.1016/j.pacs.2017.08.002
  45. Daoudi K, van den Berg PJ, Rabot O, et al. Handheld probe integrating laser diode and ultrasound transducer array for ultrasound/photoacoustic dual modality imaging. Opt Express 2014;22:26365-74. https://doi.org/10.1364/OE.22.026365
  46. Thella AK, Rizkalla J, Helmy A, et al. Non-invasive photo acoustic approach for human bone diagnosis. J Orthop 2016; 13:394-400. https://doi.org/10.1016/j.jor.2016.07.004
  47. Lashkari B, Mandelis A. Coregistered photoacoustic and ultrasonic signatures of early bone density variations. J Biomed Opt 2014;19:36015. https://doi.org/10.1117/1.JBO.19.3.036015
  48. Feng T, Perosky JE, Kozloff KM, et al. Characterization of bone microstructure using photoacoustic spectrum analysis. Opt Express 2015;23:25217-24. https://doi.org/10.1364/OE.23.025217
  49. He W, Zhu Y, Feng T, et al. Comparison study on the feasibility of photoacoustic power spectrum analysis in osteoporosis detection. Proceedings of SPIE 10064, Photons Plus Ultrasound: Imaging and Sensing 2017, 100645H; 2017 March 3; San Francisco (CA), USA. https://doi.org/10.1117/12.2250677.
  50. Shubert J, Lediju Bell MA. Photoacoustic imaging of a human vertebra: implications for guiding spinal fusion surgeries. Phys Med Biol 2018;63:144001. https://doi.org/10.1088/1361-6560/aacdd3
  51. Zackrisson S, van de Ven SM, Gambhir SS. Light in and sound out: emerging translational strategies for photoacoustic imaging. Cancer Res 2014;74:979-1004. https://doi.org/10.1158/0008-5472.CAN-13-2387
  52. Yao J, Wang L, Yang JM, et al. High-speed label-free functional photoacoustic microscopy of mouse brain in action. Nat Methods 2015;12:407-10. https://doi.org/10.1038/nmeth.3336
  53. Wang L, Maslov K, Wang LV. Single-cell label-free photoacoustic flowoxigraphy in vivo. Proc Natl Acad Sci U S A 2013;110:5759-64. https://doi.org/10.1073/pnas.1215578110
  54. Jathoul AP, Laufer J, Ogunlade O, et al. Deep in vivo photoacoustic imaging of mammalian tissues using a tyrosinasebased genetic reporter. Nat Photonics 2015;9:239-46. https://doi.org/10.1038/nphoton.2015.22

Cited by

  1. Photoacoustic imaging of tumor-targeted HSA-modified S-WS2 nanosheet probes vol.21, pp.5, 2018, https://doi.org/10.1007/s11051-019-4531-4
  2. CARS-imaging guidance for fs-laser ablation precision surgery vol.144, pp.24, 2019, https://doi.org/10.1039/c9an01545k
  3. Photoacoustic image-guided interventions vol.245, pp.4, 2018, https://doi.org/10.1177/1535370219889323
  4. Prospects of Photo- and Thermoacoustic Imaging in Neurosurgery vol.87, pp.1, 2020, https://doi.org/10.1093/neuros/nyz420
  5. In vivo photoacoustic guidance of stem cell injection and delivery for regenerative spinal cord therapies vol.7, pp.3, 2018, https://doi.org/10.1117/1.nph.7.3.030501
  6. Engineering Intelligent Nanosystems for Enhanced Medical Imaging vol.2, pp.10, 2020, https://doi.org/10.1002/aisy.202000087
  7. In Vivo Rodent Cervicothoracic Vasculature Imaging Using Photoacoustic Computed Tomography vol.8, pp.8, 2018, https://doi.org/10.3390/photonics8080312
  8. CuInS 2 Quantum Dot and Polydimethylsiloxane Nanocomposites for All‐Optical Ultrasound and Photoacoustic Imaging vol.8, pp.20, 2018, https://doi.org/10.1002/admi.202100518