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Multimodal photoacoustic imaging as a tool for sentinel lymph node identification and biopsy guidance

Biomedical Engineering Letters volume 8, pages 183–191 (2018)Cite this article

Abstract

As a minimally invasive method, sentinel lymph node biopsy (SLNB) in conjunction with guidance methods is the standard method to determine cancer metastasis in breast. The desired guidance methods for SLNB should be capable of precise SLN localization for accurate diagnosis of micro-metastases at an early stage of cancer progression and thus facilitate reducing the number of SLN biopsies for minimal surgical complications. For this, high sensitivity to the administered dyes, high spatial and contrast resolutions, deep imaging depth, and real-time imaging capability are pivotal requirements. Currently, various methods have been used for SLNB guidance, each with their own advantages and disadvantages, but no methods meet the requirements. In this review, we discuss the conventional SLNB guidance methods in this perspective. In addition, we focus on the role of the PA imaging modality on real-time SLN identification and biopsy guidance. In particular, PA-based hybrid imaging methods for precise SLN identification and efficient biopsy guidance are introduced, and their unique features, advantages, and disadvantages are discussed.

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References

  1. Wang X, Fowlkes JB, Cannata JM, Hu C, Carson PL. Photoacoustic imaging with a commercial ultrasound system and a custom probe. Ultrasound Med Biol. 2011;37(3):484–92.

    Article  Google Scholar 

  2. Yoon C, Yoo Y, Song TK, Chang JH. Pixel based focusing for photoacoustic and ultrasound dual-modality imaging. Ultrasonics. 2014;54(8):2126–33.

    Article  Google Scholar 

  3. Kang J, Chang JH, Wilson BC, Veilleux I, Bai Y, DaCosta R, Kim K, Ha S, Lee JG, Kim JS, Lee SG, Kim SM, Lee HJ, Ahn YB, Han S, Yoo Y, Song TK. A prototype hand-held tri-model instrument for in vivo ultrasound, photoacoustic, and fluorescence imaging. Rev Sci Instrum. 2015;86:034901.

    Article  Google Scholar 

  4. Kim J, Park S, Jung Y, Chang S, Park J, Zhang Y, Lovell JF, Kim C. Programmable real-time clinical photoacoustic and ultrasound imaging system. Sci Rep. 2016;6:35137.

    Article  Google Scholar 

  5. Beard P. Biomedical photoacoustic imaging. Interface Focus. 2011;2(4):602–31.

    Article  Google Scholar 

  6. Zhang HF, Maslov K, Sivaramakrishnan M, Stoica G, Wang LV. Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy. Appl Phys Lett. 2007;90:053901.

    Article  Google Scholar 

  7. Wang LV, Hu S. Photoacoustic tomography: in vivo imaging from organelles to organs. Science. 2012;335(6075):1458–62.

    Article  Google Scholar 

  8. Taruttis A, Timmermans AC, Wouters PC, Kacprowicz M, van Dam GM, Ntziachristos V. Optoacoustic imaging of human vasculature: feasibility by using a handheld probe. Radiology. 2016;281(1):256–63.

    Article  Google Scholar 

  9. Wang B, Karpiouk A, Yeager D, Amirian J, Litovsky S, Smalling R, Emelianov S. Intravascular photoacoustic imaging of lipid in atherosclerotic plaques in the presence of luminal blood. Opt Lett. 2012;37(7):1244–6.

    Article  Google Scholar 

  10. VanderLaan D, Karpiouk AB, Yeager D, Emelianov S. Real-time intravascular ultrasound and photoacoustic imaging. IEEE Trans Ultrason Ferroelectr Freq Control. 2017;64(1):141–9.

    Article  Google Scholar 

  11. Kang J, Kim EK, Kwak JY, Yoo Y, Song TK, Chang JH. Optimal laser wavelength for photoacoustic imaging of breast microcalcifications. Appl Phys Lett. 2011;99:153702.

    Article  Google Scholar 

  12. Kang J, Kim EK, Kim GR, Yoon C, Song TK, Chang JH. Photoacoustic imaging of breast microcalcifications: a validation study with 3-dimensional ex vivo data and spectrophotometric measurement. J Biophoton. 2015;8:71–80.

    Article  Google Scholar 

  13. Kim GR, Kang J, Kwak JY, Chang JH, Kim SI, Youk JH, Moon HJ, Kim MJ, Kim EK. Photoacoustic imaging of breast microcalcifications: a preliminary study with 8-gauge core-biopsied breast specimens. PLoS ONE. 2014;9(8):e105878.

    Article  Google Scholar 

  14. Chae HD, Lee JY, Jang JY, Chang JH, Kang J, Kang MJ, Han JK. Photoacoustic imaging for differential diagnosis of benign polyps versus malignant polyps of the gallbladder: a preliminary study. Korean J Radiol. 2017;18(5):821–7.

    Article  Google Scholar 

  15. 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 XY, Dai HJ, Khuri-Yakub BT, Gambhir SS. Carbon nanotubes as photoacoustic molecular imaging agents in living mice. Nat Nanotechnol. 2008;3:557–62.

    Article  Google Scholar 

  16. Mallidi S, Larson T, Tam J, Joshi PP, Karpiouk A, Sokolov K, Emelianov S. Multiwavelength photoacoustic imaging and plasmon resonance coupling of gold nanoparticles for selective detection of cancer. Nano Lett. 2009;9:2825–31.

    Article  Google Scholar 

  17. Song KH, Kim CH, Cobley CM, Xia YN, Wang LV. Near-infrared gold nanocages as a new class of tracers for photoacoustic sentinel lymph node mapping on a rat model. Nano Lett. 2009;9:183–8.

    Article  Google Scholar 

  18. Chen YS, Frey W, Kim S, Kruizinga P, Homan K, Emelianov S. Silica-coated gold nanorods as photoacoustic signal nanoamplifiers. Nano Lett. 2011;11:348–54.

    Article  Google Scholar 

  19. Wilson K, Homan K, Emelianov S. Biomedical photoacoustics beyond thermal expansion using triggered nanodroplet vaporization for contrast-enhanced imaging. Nat Commun. 2012;3:618–27.

    Article  Google Scholar 

  20. Moon H, Kumar D, Kim H, Sim C, Chang JH, Kim JM, Kim H, Lim DK. Amplified photoacoustic performance and enhanced photothermal stability of reduced graphene oxide-coated gold nanorods for sensitive photoacoustic imaging. ACS Nano. 2015;9(3):2711–9.

    Article  Google Scholar 

  21. Sim C, Kim H, Moon H, Lee H, Chang JH, Kim H. Photoacoustic-based nanomedicine for cancer diagnosis and therapy. J Control Release. 2015;203:118–25.

    Article  Google Scholar 

  22. Moon H, Kang J, Sim C, Kim J, Lee H, Chang JH, Kim H. Multifunctional theranostic contrast agent for photoacoustics- and ultrasound-based tumor diagnosis and ultrasound-stimulated local tumor therapy. J Control Release. 2015;218:63–71.

    Article  Google Scholar 

  23. Ju KY, Kang J, Pyo J, Lim J, Chang JH, Lee JK. pH-induced aggregated melanin nanoparticles for photoacoustic signal amplification. Nanoscale. 2016;8:14448–56.

    Article  Google Scholar 

  24. Alitalo K, Carmeliet P. Molecular mechanisms of lymphangiogenesis in health and disease. Cancer Cell. 2002;1:219–27.

    Article  Google Scholar 

  25. Gould EA, Winship T, Philbin PH, Hyland Kerr H. Observations on a “sentinel node” in cancer of the parotid. Cancer. 1960;13:77–8.

    Article  Google Scholar 

  26. Sleeman JP, Thiele W. Tumor metastasis and the lymphatic vasculature. Int J Cancer. 2009;125:2747–56.

    Article  Google Scholar 

  27. Pesce C, Morrow M. The need for lymph node dissection in nonmetastatic breast cancer. Annu Rev Med. 2013;64:119–29.

    Article  Google Scholar 

  28. Lucci A, McCall LM, Beitsch PD, Whitworth PW, Reintgen DS, Blumencranz PW, Leitch AM, Saha S, Hunt KK, Giuliano AE. Surgical complications associated with sentinel lymph node dissection (SLND) plus axillary lymph node dissection compared with SLND alone in the American College of Surgeons Oncology Group Trial Z0011. J Clin Oncol. 2007;25:3657–63.

    Article  Google Scholar 

  29. Wetzig N, Gill PG, Espinoza D. Sentinel-lymph-node-based management or routine axillary clearance? Five-year outcomes of the RACS Sentinel Node Biopsy Versus Axillary Clearance (SNAC) 1 Trial: assessment and incidence of true lymphedema. Ann Surg Oncol. 2017;24:1064–70.

    Article  Google Scholar 

  30. Jimenez RE, Panageas K, Busan KJ, Brady MS. Prognostic implications of multiple lymphatic basin drainage in patients with truncal melanoma. J Clin Oncol. 2005;23:518–24.

    Article  Google Scholar 

  31. Pereira CT, Marques FL, Williams J, Martin BW, Bombonato PP. 99M TC-labeled dextran for mammary lymphoscintigraphy in dogs. Vet Radiol Ultrasound. 2008;49(5):487–91.

    Article  Google Scholar 

  32. Harivardhan Reddy L, Sharma RK, Chuttani K, Mishra AK, Murthy RS. Influence of administration route on tumor uptake and biodistribution of etoposide loaded solid lipid nanoparticles in Dalton’s lymphoma tumor bearing mice. J Control Release. 2005;105:185–98.

    Article  Google Scholar 

  33. Bergqvist L, Strand SE, Persson B, Hafström L, Jönsson PE. Dosimetryin lymphoscintigraphy of Tc-99m antimony sulfide colloid. J Nucl Med. 1982;23:698–705.

    Google Scholar 

  34. Ho AM, Avery R, Krupinski EA, Warneke J, Kuo PH. Predictive pole of imaging in sentinel lymph node dissection for melanoma. Lymphology. 2014;47:134–41.

    Google Scholar 

  35. Harvey NL, Srinivasan RS, Dillard ME, Johnson NC, Witte MH, Boyd K, Sleeman MW, Oliver G. Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity. Nat Genet. 2015;37:1072–81.

    Article  Google Scholar 

  36. Kajiya K, Hirakawa S, Detmar M. Vascular endothelial growth factor-A mediates ultraviolet B-induced impairment of lymphatic vessel function. Am J Pathol. 2006;169(4):1496–503.

    Article  Google Scholar 

  37. Zhang F, Niu G, Lu G, Chen X. Preclinical lymphatic imaging. Mol Imaging Biol. 2011;13(4):599–612.

    Article  Google Scholar 

  38. Nune SK, Gunda P, Majeti BK, Thallapally PK, Forrest ML. Advances in lymphatic imaging and drug delivery. Adv Drug Deliv Rev. 2011;64:876–86.

    Article  Google Scholar 

  39. Khaifi A, Schneebaum S, Fliss DM, Lerman H, Metser U, Ben-Yosef R, Gil Z, Reider-Trejo L, Genadi L, Sapir EE. Lymphoscintigraphy for sentinel node mapping using a hybrid single photon emission CT (SPECT)/CT system in oral cavity squamous cell carcinoma. Head Neck. 2006;28:874–9.

    Article  Google Scholar 

  40. Lohrmann C, Foeldi E, Bartholoma J-P, Langer M. Interstitial MR lymphangiography—a diagnostic imaging method for the evaluation of patients with clinically advanced stages of lymphedema. Acta Trop. 2007;104:8–15.

    Article  Google Scholar 

  41. Wua H, Xu X, Ying H, Hoffman MR, Shen N, Sha Y, Zhou L. Preliminary study of indirect CT lymphography-guided sentinel lymph node biopsy in a tongue VX2 carcinoma model. Int J Oral Maxillofac Surg. 2009;38:1268–72.

    Article  Google Scholar 

  42. Suga K, Ogasawara N, Okada M, Matsunaga N. Interstitial CT lymphography-guided localization of breast sentinel lymph node: preliminary results. Surgery. 2003;133:170–9.

    Article  Google Scholar 

  43. Aviv H, Bartling S, Kieslling F, Margel S. Radiopaque iodinated copolymeric nanoparticles for X-ray imaging applications. Biomaterials. 2009;30(29):5610–6.

    Article  Google Scholar 

  44. Rabin O, Perez JM, Grimm J, Wojtkiewicz G, Weissleder R. An X-ray computed tomography imaging agent based on long-circulating bismuth sulphide nanoparticles. Nat Mater. 2006;5:118–22.

    Article  Google Scholar 

  45. Tins B. Technical aspects of CT imaging of the spine. Insights Imaging. 2010;1:349–59.

    Article  Google Scholar 

  46. Mahmoudi M, Simchi A, Imani M, Milani AS, Stroeve P. Optimal design and characterization of superparamagnetic iron oxide nanoparticles coated with polyvinyl alcohol for targeted delivery and imaging. J Phys Chem B. 2008;112:14470–81.

    Article  Google Scholar 

  47. Lewinski N, Colvin V, Drezek R. A critical review of the in vitro cytotoxicity data currently available for three classes of nanoparticles including QDs. Cytotoxicity of nanoparticles. Small. 2008;4:26–49.

    Article  Google Scholar 

  48. Na HB, Song IC, Hyeon T. Inorganic nanoparticles for MRI contrast agents. Adv Mater. 2009;21:2133–48.

    Article  Google Scholar 

  49. Waters EA, Wickline SA. Contrast agents for MRI. Basic Res Cardiol. 2008;103:114–21.

    Article  Google Scholar 

  50. Kvistad KA, Rydland J, Smethurst H-B, Lundgren S, Fjosne HE, Gribbestad IS, Nilsen G, Haraldseth O. Axillary lymph node metastases in breast cancer: preoperative detection with dynamic contrast enhanced MRI. Eur Radiol. 2000;10:1464–71.

    Article  Google Scholar 

  51. Willmann JK, van Bruggen N, Dinkelborg LM, Gambhir SS. Molecular imaging in drug development. Nat Rev Drug Discov. 2008;7:591–607.

    Article  Google Scholar 

  52. Tang J, Salloum D, Carney B, Brand C, Kossatz S, Sadique A, Lewis JS, Weber WA, Wendel H-G, Reiner T. Targeted PET imaging strategy to differentiate malignant from inflamed lymph nodes in diffuse large B-cell lymphoma. Proc Natl Acad Sci. 2017;114(36):7441–9.

    Article  Google Scholar 

  53. Rubaltelli L, Khadivi Y, Tregnaghi A, Stramare R, Ferro F, Borsate S, Fiocco U, Adami F, Rossi CR. Evaluation of lymph node perfusion using continuous mode harmonic ultrasonography with a second-generation contrast agent. J Ultrasound Med. 2004;23(6):829–36.

    Article  Google Scholar 

  54. Sorace AG, Saini R, Mahoney M, Hoyt K. Molecular ultrasound imaging using a targeted contrast agent for assessing early tumor response to antiangiogenic therapy. Am Inst Ultrasound Med. 2012;31(10):1543–50.

    Article  Google Scholar 

  55. Simon JR, Kalbhen CL, Cooper RA, Flisak ME. Accuracy and complication rates of US-guided vacuum-assisted core breast biopsy: initial results. Radiology. 2000;215:694–7.

    Article  Google Scholar 

  56. Scoggins CR, Chagpar AB, Martin RC, McMasters KM. Should sentinel lymph-node biopsy be used routinely for staging melanoma and breast cancers? Nat Clin Pract Oncol. 2005;2:448–55.

    Article  Google Scholar 

  57. Ahrendt GM, Laud P, Tjoe J, Eastwood D, Walker AP, Otterson MF, Redlich PN. Does breast tumor location influence success of sentinel lymph node biopsy? J Am Coll Surg. 2002;194:278–84.

    Article  Google Scholar 

  58. Benson J. Indocyanine green fluorescence for sentinel lymph node detection in early breast cancer. Ann Surg Oncol. 2016;23:6–8.

    Article  Google Scholar 

  59. Osmonob DK, Heimann D, Janßen I, Aksenov A, Kalz A, Juenemann KP. Sensitivity and specificity of PET/CT regarding the detection of lymph node metastases in prostate cancer recurrence. Springerplus. 2014;3:340–7.

    Article  Google Scholar 

  60. Harnan SE, Cooper KL, Meng Y, Ward SE, Fitzgerld P, Papaioannou D, Ingram C, Lorenz E, Wilkinson ID, Wyld L. Magnetic resonance for assessment of axillary lymph node status in early breast cancer: a systematic review and metaanalysis. Eur J Surg Oncol. 2011;37:928–36.

    Article  Google Scholar 

  61. Bakhtiar N, Jaleel F, Moosa FA, Qureshi NA, Jawaid M. Sentinel lymph node identification by blue dye in patients with breast carcinoma. Pak J Med. 2016;32:448–51.

    Google Scholar 

  62. Matsuzawa F, Omoto K, Einama T, Abe H, Suzuki T, Hamaguchi J, Kaga T, Sato M, Oomira M, Takata Y, Fujibe A, Takeda C, Tamura E, Taketomi A, Kyuno K. Accurate evaluation of axillary sentinel lymph node metastasis using contrast-enhanced ultrasonography with Sonazoid in breast cancer: a preliminary clinical trial. Springerplus. 2015;4:509.

    Article  Google Scholar 

  63. Emile SH, Elfeki H, Shalaby M, Sakr A, Sileri P, Lauberg S, Wexner SD. Sensitivity and specificity of indocyanine green near-infrared fluorescence imaging in detection of metastatic lymph nodes in colorectal cancer: systematic review and meta-analysis. J Surg Oncol. 2017;116(6):730–40.

    Article  Google Scholar 

  64. Stoffels I, Dissemond J, Poeppel T, Klotgen K, Hillen U, Korber A, Schadendorf D, Klode J. Advantages of preoperative ultrasound in conjunction with lymphoscintigraphy in detecting malignant melanoma metastases in sentinel lymph nodes: a retrospective analysis in 221 patients with malignant melanoma AJCC stages I and II. J Eur Acad Dermatol Venereol. 2012;26(1):79–85.

    Article  Google Scholar 

  65. Schijven MP, Vingerhoets AJ, Rutten HJ, Nieuwenhuijzen GA, Rounmen RM, Bussel ME. Comparison of morbidity between axillary lymph node dissection and sentinel node biopsy. Eur J Surg Oncol. 2003;29:341–50.

    Article  Google Scholar 

  66. Chen SL, Iddings DM, Scheri RP, Bilckik AJ. Lymphatic mapping and sentinel node analysis: current concepts and applications. CA Cancer J Clin. 2006;56:292–309.

    Article  Google Scholar 

  67. Wong SL, Abell TD, Chao C, Edwards MH, McMasters KM. Optimal use of sentinel lymph node biopsy versus axillary lymph node dissection in patients with breast carcinoma. Am Cancer Soc. 2002;95:478–87.

    Google Scholar 

  68. Okada RC, Wascher RA, Elashoff D, Giuliano AE. Long-term morbidity of sentinel node biopsy versus complete axillary dissection for unilateral breast cancer. Ann Surg Oncol. 2008;15(7):1996–2005.

    Article  Google Scholar 

  69. Swenson KK, Nissen MJ, Ceronsky C, Swenson L, Lee MW, Tuttle TM. Comparison of side effects between sentinel lymph node and axillary lymph node dissection for breast cancer. Ann Surg Oncol. 2002;9(8):745–53.

    Article  Google Scholar 

  70. 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;23:4312–21.

    Article  Google Scholar 

  71. Rautiainen S, Masarwah A, Sudah M, Sutela A, Pelkonen O, Joukainen S, Sironen R, Kärjä V, Vanninen R. Axillary lymph node biopsy in newly diagnosed invasive breast cancer: comparative accuracy of fine-needle aspiration biopsy versus core-needle biopsy. Radiology. 2013;269:54–60.

    Article  Google Scholar 

  72. Song KH, Stein EW, Margenthaler JA, Wang LV. Noninvasive photoacoustic identification of sentinel lymph nodes containing methylene blue in vivo in a rat model. J Biomed Opt. 2008;13(5):054033.

    Article  Google Scholar 

  73. 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.

    Article  Google Scholar 

  74. Landsman ML, Kwant G, Mook GA, Zijlstra WG. Light-absorbing properties, stability, and spectral stabilization of indo- cyanine green. J Appl Physiol. 1976;40(4):575–83.

    Article  Google Scholar 

  75. Pan D, Pramanik M, Senpan A, Ghosh S, Wickline SA, Wang LV, Lanza GM. Near infrared photoacoustic detection of sentinel lymph nodes with gold nanobeacons. Biomaterials. 2010;31:4088–93.

    Article  Google Scholar 

  76. Song KH, Kim C, Maslov K, Wang LV. Noninvasive in vivo spectroscopic nanorod-contrast photoacoustic mapping of sentinel lymph nodes. Eur J Radiol. 2009;70:227–31.

    Article  Google Scholar 

  77. 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.

    Article  Google Scholar 

  78. Lee C, Kim J, Zhang Y, Jeon M, Liu C, Song L, Lovell JF, Kim C. Dual-color photoacoustic lymph node imaging using nanoformulated naphthalocyanines. Biomaterials. 2015;73:142–8.

    Article  Google Scholar 

  79. Luke GP, Bashyam A, Homan KA, Makhija S, Chen YS, Emelianov SY. Silica-coated gold nanoplates as stable photoacoustic contrast agents for sentinel lymph node imaging. Nanotechnology. 2013;24:455101.

    Article  Google Scholar 

  80. 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;57:7853–62.

    Article  Google Scholar 

  81. McCormack D, AI-Shaer M, Goldschmidt BS, Dale PS, Henry C, Papageorgio C, Bhattacharyya K, Viator JA. Photoacoustic detection of melanoma micrometastasis in sentinel lymph nodes. J Biomech Eng. 2009;131:07519.

    Article  Google Scholar 

  82. Luke GP, Emelianov SY. Label-free detection of lymph node metastases with US-guided functional photoacoustic imaging. Radiology. 2015;277(2):435–42.

    Article  Google Scholar 

  83. Erpelding TN, Kim C, Pramanik M, Jankovic L, Maslov K, Guo Z, Margenthaler JA, Pashley MD, Wang LV. Sentinal lymph nodes in the rat: noninvasive photoacoustic and US imaging with a clinical US system. Radiology. 2010;256:102–10.

    Article  Google Scholar 

  84. Luke GP, Myers JN, Emelianov SY, Sokolov KV. Sentinel lymph node biopsy revisited: ultrasound-guided photoacoustic detection of micrometastases using molecularly target plasmonic nanosensors. Cancer Res. 2014;74(19):5397–408.

    Article  Google Scholar 

  85. Jeon M, Kim C. Multimodal photoacoustic tomography. IEEE Trans Multimed. 2013;15(5):975–82.

    Article  Google Scholar 

  86. Garcia-Uribe A, Erpelding TN, Krumholz A, Ke H, Maslov K, Appleton C, Margenthaler JA, Wang LV. Dual-modality photoacoustic and ultrasound imaging system for noninvasive sentinel lymph node detection in patients with breast cancer. Sci Rep. 2015;5:15748.

    Article  Google Scholar 

  87. Sivasubramanian K, Periyasamy V, Pramanik M. Non-invasive sentinel lymph node mapping and needle guidance using clinical handheld photoacoustic imaging system in small animal. J Biophotonics. 2018;11:201700061.

    Article  Google Scholar 

  88. Yang L, Cheng J, Chen Y, Yu S, Liu F, Sun Y, Chen Y, Ran H. Phase-transition nanodroplets for real-time photoacoustic/ultrasound dual-modality imaging and photothermal therapy of sentinel lymph node in breast cancer. Sci Rep. 2017;7:45213.

    Article  Google Scholar 

  89. Kim H, Kang J, Chang JH. Thermal therapeutic method for selective treatment of deep-lying tissue by combining laser and high-intensity focused ultrasound energy. Opt Lett. 2014;39(9):2806–9.

    Article  Google Scholar 

  90. Akers WJ, Edwards WB, Kim C, Xu B, Erpelding TN, Wang LV, Achilefu S. Multimodal sentinel lymph node mapping with SPECT/CT and photoacoustic tomography. Transl Res. 2012;159:175–81.

    Article  Google Scholar 

  91. Liu Q, Zhou M, Li P, Ku G, Huang G, Li C, Song S. 64CuS-labeled nanoparticles: a new sentinel-lymph-node-mapping agent for PET-CT and photoacoustic tomography. Contrast Media Mol Imaging. 2016;11:475–81.

    Article  Google Scholar 

  92. Wang B, Zhao Q, Barkey NM, Morse DL, Jiang H. Photoacoustic tomography and fluorescence molecular tomography: a comparative study based on indocyanine green. Med Phys. 2012;39(5):2512–7.

    Article  Google Scholar 

  93. Chen J, Liu C, Zeng G, You Y, Wang H, Gong X, Zheng R, Kim J, Kim C, Song L. Indocyanine green loaded reduced graphene oxide for in vivo photoacoustic/fluorescence dual-modality tumor imaging. Nanoscale Res Lett. 2016;11:85.

    Article  Google Scholar 

  94. Peng D, Du Y, Shi Y, Mao D, Jia X, Li H, Zhu Y, Wang K, Tian J. Precise diagnosis in different scenarios using photoacoustic and fluorescence imaging with dual-modality nanoparticles. Nanoscale. 2016;8:14480.

    Article  Google Scholar 

  95. Liu Z, Rong P, Yu L, Zhang X, Yang C, Guo F, Zhao Y, Zhou K, Wang W, Zeng W. Dual-modality noninvasive mapping of sentinel lymph node by photoacoustic and near-infrared fluoscent imaging using dye-loaded mesoporous silica nanoparticles. Mol Pharm. 2015;12:3119–28.

    Article  Google Scholar 

  96. Akers WJ, Kim C, Berezin M, Guo K, Fuhrhop R, Lanza GM, Fischer GM, Daltrozzo E, Zumbusch A, Cai X, Wang LV, Achilefu S. Noninvasive photoacoustic and fluorescence sentinel lymph node identification using dye-loaded perfluorocarbon nanoparticles. ACS Nano. 2011;5:173–82.

    Article  Google Scholar 

  97. Kang J, Chang JH, Kim SM, Lee HJ, Kim H, Brian C, Wilson BC, Song T-K. Real-time sentinel lymph node biopsy guidance using combined ultrasound, photoacoustic, fluorescence imaging: in vivo proof-of-principle and validation with nodal obstruction. Sci Rep. 2017;7:45008.

    Article  Google Scholar 

  98. Lovell JF, Jin CS, Huynh E, Jin H, Kim C, Rubinstein JL, Chan WCW, Cao W, Wang LV, Zheng G. Porphysome nanovesicles generated by porphyrin bilayers for use as multimodal biophotonic contrast agents. Nat Mater. 2011;10:324–32.

    Article  Google Scholar 

  99. Kandukuri J, Yu S, Cheng B, Bandi V, D’Souza F, Nguyen KT, Hong Y, Yuan B. A dual-modality system for both multi-color ultrasound-switchable fluorescence and ultrasound imaging. Int J Mol Sci. 2017;18(2):323.

    Article  Google Scholar 

  100. Moon H, Kang J, Lee H, Lee M, Chang JH, Lee HJ, Kim H. Theragnostic nanodroplets for photoacoustic and ultrasound signal amplification and optically triggered vaporization-induced drug release. J Nanosci Nanotechnol. 2017;17(11):7978–85.

    Article  Google Scholar 

  101. Poland CA, Duffin R, Kinloch I, Maynard A, Wallace WAH, Seaton A, Stone V, Brown S, MacNee W, Donaldson K. Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nat Nanotechnol. 2008;3:423–8.

    Article  Google Scholar 

  102. Browning LM, Lee KJ, Huang T, Nallathamby PD, Lowman JE, Xu XHN. Random walk of single gold nanoparticles in zebrafish embryos leading to stochastic toxic effects on embryonic developments. Nanoscale. 2009;1:138–52.

    Article  Google Scholar 

  103. Yu J, Schuman JS, Lee JK, Lee SG, Chang JH, Kim K. A light illumination enhancement device for photoacoustic imaging: in vivo animal study. IEEE Trans Ultrason Ferroelectr Freq Control. 2017;64(8):1205–11.

    Article  Google Scholar 

  104. Kim H, Chang JH. Increased light penetration due to ultrasound-induced air bubbles in optical scattering media. Sci Rep. 2017;7:16105.

    Article  Google Scholar 

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Acknowledgements

This work was supported by the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT (NRF-2017R1A2B2002838).

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  1. Department of Biomedical Engineering, Sogang University, 35 Baekbeom-ro, Mapo-gu, Seoul, 04107, South Korea

    Haemin Kim & Jin Ho Chang

  2. Department of Electronic Engineering, Sogang University, 35 Baekbeom-ro, Mapo-gu, Seoul, 04107, South Korea

    Jin Ho Chang

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Kim, H., Chang, J.H. Multimodal photoacoustic imaging as a tool for sentinel lymph node identification and biopsy guidance. Biomed. Eng. Lett. 8, 183–191 (2018). https://doi.org/10.1007/s13534-018-0068-1

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  • DOI: https://doi.org/10.1007/s13534-018-0068-1

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