Biomedical Applications of Photoacoustic Imaging with Exogenous Contrast Agents

Photoacoustic imaging is a biomedical imaging modality that provides functional information, and, with the help of exogenous contrast agents, cellular and molecular signatures of tissue. In this article, we review the biomedical applications of photoacoustic imaging assisted with exogenous contrast agents. Dyes, noble metal nanoparticles, and other constructs are contrast agents which absorb strongly in the near-infrared band of the optical spectrum and generate strong photoacoustic response. These contrast agents, which can be specifically targeted to molecules or cells, have been coupled with photoacoustic imaging for preclinical and clinical applications ranging from detection of cancer cells, sentinel lymph nodes, and micrometastasis to angiogenesis to characterization of atherosclerotic plaques. Multi-functional agents have also been developed, which can carry drugs or simultaneously provide contrast in multiple imaging modalities. Furthermore, contrast agents were used to guide and monitor the therapeutic procedures. Overall, photoacoustic imaging shows significant promise in its ability to assist in diagnosis, therapy planning, and monitoring of treatment outcome for cancer, cardiovascular disease, and other pathologies.

[1]  Matthew O'Donnell,et al.  Multimodality Cardiovascular Molecular Imaging Technology , 2010, Journal of Nuclear Medicine.

[2]  Stanislav Emelianov,et al.  Multiwavelength photoacoustic imaging and plasmon resonance coupling of gold nanoparticles for selective detection of cancer. , 2009, Nano letters.

[3]  Stanislav Emelianov,et al.  Multiplex photoacoustic molecular imaging using targeted silica-coated gold nanorods , 2011, Biomedical optics express.

[4]  Zhuang Liu,et al.  Carbon nanotubes as photoacoustic molecular imaging agents in living mice. , 2008, Nature nanotechnology.

[5]  C. Alpers,et al.  αvβ3 Integrin Expression in Normal and Atherosclerotic Artery , 1995 .

[6]  Ennis,et al.  Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. , 2001, The New England journal of medicine.

[7]  Lihong V. Wang,et al.  Photoacoustic imaging and characterization of the microvasculature. , 2010, Journal of biomedical optics.

[8]  Lihong V. Wang,et al.  Noninvasive photoacoustic identification of sentinel lymph nodes containing methylene blue in vivo in a rat model. , 2008, Journal of biomedical optics.

[9]  S. Emelianov,et al.  Silica-coated gold nanorods as photoacoustic signal nanoamplifiers. , 2011, Nano letters.

[10]  Stanislav Emelianov,et al.  Photoacoustic imaging of clinical metal needles in tissue. , 2010, Journal of biomedical optics.

[11]  Pai-Chi Li,et al.  Multiple targeting in photoacoustic imaging using bioconjugated gold nanorods , 2006, SPIE BiOS.

[12]  Keith M. Stantz,et al.  Molecular imaging of neutropilin-1 receptor using photoacoustic spectroscopy in breast tumors , 2010, BiOS.

[13]  Mostafa A. El-Sayed,et al.  Preparation and Growth Mechanism of Gold Nanorods (NRs) Using Seed-Mediated Growth Method , 2003 .

[14]  A. Wear CIRCULATION , 1964, The Lancet.

[15]  M. Davies,et al.  The expression of the adhesion molecules ICAM‐1, VCAM‐1, PECAM, and E‐selectin in human atherosclerosis , 1993, The Journal of pathology.

[16]  Valery V Tuchin,et al.  In vivo multispectral, multiparameter, photoacoustic lymph flow cytometry with natural cell focusing, label‐free detection and multicolor nanoparticle probes , 2008, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[17]  D L Morton,et al.  Technical details of intraoperative lymphatic mapping for early stage melanoma. , 1992, Archives of surgery.

[18]  D. Weaver,et al.  Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. , 1993, Surgical oncology.

[19]  W Godolphin,et al.  Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. , 1989, Science.

[20]  James H. Adair,et al.  Near-infrared emitting fluorophore-doped calcium phosphate nanoparticles for in vivo imaging of human breast cancer. , 2008, ACS nano.

[21]  Lawrence Tamarkin,et al.  Colloidal Gold: A Novel Nanoparticle Vector for Tumor Directed Drug Delivery , 2004, Drug delivery.

[22]  Zahi A. Fayad,et al.  Imaging of atherosclerotic cardiovascular disease , 2008, Nature.

[23]  Stanislav Y. Emelianov,et al.  Ultrasound and photoacoustic image-guided photothermal therapy using silica-coated gold nanorods: In-vivo study , 2010, 2010 IEEE International Ultrasonics Symposium.

[24]  Mark A. Anastasio,et al.  3D photoacoustic imaging , 2010, Photonics North.

[25]  Sabine Neuss,et al.  Size-dependent cytotoxicity of gold nanoparticles. , 2007, Small.

[26]  H. V. van Beusekom,et al.  Intravascular photoacoustic imaging of human coronary atherosclerosis. , 2011, Optics letters.

[27]  M. O’Donnell,et al.  Multifunctional nanoparticles as coupled contrast agents. , 2010, Nature communications.

[28]  Kaushal Rege,et al.  Inorganic nanoparticles for cancer imaging and therapy. , 2011, Journal of controlled release : official journal of the Controlled Release Society.

[29]  Vasilis Ntziachristos,et al.  Multispectral optoacoustic tomography resolves smart probe activation in vulnerable plaques , 2011, BiOS.

[30]  Nastassja A. Lewinski,et al.  Cytotoxicity of nanoparticles. , 2008, Small.

[31]  Da Xing,et al.  Real-time optoacoustic monitoring of vascular damage during photodynamic therapy treatment of tumor. , 2007, Journal of biomedical optics.

[32]  Chad A Mirkin,et al.  Colloidal gold and silver triangular nanoprisms. , 2009, Small.

[33]  R. Esenaliev,et al.  Sensitivity of laser opto-acoustic imaging in detection of small deeply embedded tumors , 1999 .

[34]  V. Ntziachristos,et al.  Video rate optoacoustic tomography of mouse kidney perfusion. , 2010, Optics letters.

[35]  M. Ross,et al.  Multi-institutional melanoma lymphatic mapping experience: the prognostic value of sentinel lymph node status in 612 stage I or II melanoma patients. , 1999, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[36]  Vasilis Ntziachristos,et al.  Multispectral Optoacoustic Tomography of Matrix Metalloproteinase Activity in Vulnerable Human Carotid Plaques , 2011, Molecular Imaging and Biology.

[37]  Geng Ku,et al.  Deeply penetrating photoacoustic tomography in biological tissues enhanced with an optical contrast agent. , 2005, Optics letters.

[38]  Chulhong Kim,et al.  Multifunctional microbubbles and nanobubbles for photoacoustic and ultrasound imaging. , 2010, Journal of biomedical optics.

[39]  Sheng-Wen Huang,et al.  Targeted gold nanorod contrast agent for prostate cancer detection by photoacoustic imaging , 2007 .

[40]  Sibaprasad Bhattacharyya,et al.  Synthesis and evaluation of near-infrared (NIR) dye-herceptin conjugates as photoacoustic computed tomography (PCT) probes for HER2 expression in breast cancer. , 2008, Bioconjugate chemistry.

[41]  Lihong V. Wang,et al.  Photoacoustic tomography of a nanoshell contrast agent in the in vivo rat brain , 2004 .

[42]  Michele Follen,et al.  Real-time vital optical imaging of precancer using anti-epidermal growth factor receptor antibodies conjugated to gold nanoparticles. , 2003, Cancer research.

[43]  Konstantin Sokolov,et al.  Plasmonic intravascular photoacoustic imaging for detection of macrophages in atherosclerotic plaques. , 2009, Nano letters.

[44]  Sheng-Wen Huang,et al.  Indocyanine-green-embedded PEBBLEs as a contrast agent for photoacoustic imaging. , 2007, Journal of biomedical optics.

[45]  H. Maeda The enhanced permeability and retention (EPR) effect in tumor vasculature: the key role of tumor-selective macromolecular drug targeting. , 2001, Advances in enzyme regulation.

[46]  Stanislav Y. Emelianov,et al.  Development of a catheter for combined intravascular ultrasound and photoacoustic imaging. , 2010, The Review of scientific instruments.

[47]  P. Avti,et al.  A novel nanoparticle-enhanced photoacoustic stimulus for bone tissue engineering. , 2011, Tissue engineering. Part A.

[48]  Qizhi Zhang,et al.  Gold nanoparticles as a contrast agent for in vivo tumor imaging with photoacoustic tomography , 2009, Nanotechnology.

[49]  Nastassja A. Lewinski,et al.  A new era for cancer treatment: gold-nanoparticle-mediated thermal therapies. , 2011, Small.

[50]  Geng Ku,et al.  Noninvasive photoacoustic angiography of animal brains in vivo with near-infrared light and an optical contrast agent. , 2004, Optics letters.

[51]  Stanislav Emelianov,et al.  Ultrasound and photoacoustic imaging to monitor mesenchymal stem cells labeled with gold nanoparticles , 2011, BiOS.

[52]  Younan Xia,et al.  Gold Nanocages: Synthesis, Properties, and Applications , 2009 .

[53]  Glenn P. Goodrich,et al.  Photothermal Efficiencies of Nanoshells and Nanorods for Clinical Therapeutic Applications , 2009 .

[54]  E. Boerwinkle,et al.  From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: Part I. , 2003, Circulation.

[55]  Zhuang Liu,et al.  Drug delivery with carbon nanotubes for in vivo cancer treatment. , 2008, Cancer research.

[56]  Pai-Chi Li,et al.  Integrated intravascular ultrasound and photoacoustic imaging scan head. , 2010, Optics letters.

[57]  Joseph Irudayaraj,et al.  Gold nanorod/Fe3O4 nanoparticle "nano-pearl-necklaces" for simultaneous targeting, dual-mode imaging, and photothermal ablation of cancer cells. , 2009, Angewandte Chemie.

[58]  A. Agarwal,et al.  Dual-mode imaging with radiolabeled gold nanorods. , 2011, Journal of biomedical optics.

[59]  O. Lindvall,et al.  Stem cell therapy for human neurodegenerative disorders–how to make it work , 2004, Nature Medicine.

[60]  Lihong V. Wang,et al.  Optical-resolution photoacoustic microscopy for in vivo imaging of single capillaries. , 2008, Optics letters.

[61]  S. Emelianov,et al.  Multifunctional, multimodality cancer imaging with water-soluble synthetic polymer nanoparticles , 2011 .

[62]  Stanislav Emelianov,et al.  Magneto-photo-acoustic imaging , 2011, Biomedical optics express.

[63]  Da Xing,et al.  Noninvasive photoacoustic imaging of the developing vasculature during early tumor growth , 2008, Physics in medicine and biology.

[64]  Vladimir P Zharov,et al.  In vivo, noninvasive, label-free detection and eradication of circulating metastatic melanoma cells using two-color photoacoustic flow cytometry with a diode laser. , 2009, Cancer research.

[65]  B. Nikoobakht,et al.  種結晶を媒介とした成長法を用いた金ナノロッド(NR)の調製と成長メカニズム , 2003 .

[66]  Xinmai Yang,et al.  Photoacoustic tomography of a rat cerebral cortex in vivo with au nanocages as an optical contrast agent. , 2007, Nano letters.

[67]  Marilena Loizidou,et al.  Liposomes and nanoparticles: nanosized vehicles for drug delivery in cancer. , 2009, Trends in pharmacological sciences.

[68]  C. Alpers,et al.  Alpha-v beta-3 integrin expression in normal and atherosclerotic artery. , 1995, Circulation research.

[69]  A. P. Leonov,et al.  Gyromagnetic imaging: dynamic optical contrast using gold nanostars with magnetic cores. , 2009, Journal of the American Chemical Society.

[70]  Stanislav Emelianov,et al.  Methodical study on plaque characterization using integrated vascular ultrasound, strain and spectroscopic photoacoustic imaging , 2011, BiOS.

[71]  V. Zharov,et al.  Golden carbon nanotubes as multimodal photoacoustic and photothermal high-contrast molecular agents. , 2009, Nature nanotechnology.

[72]  Manojit Pramanik,et al.  Near infrared photoacoustic detection of sentinel lymph nodes with gold nanobeacons. , 2010, Biomaterials.

[73]  Seung Yun Nam,et al.  Function of mesenchymal stem cells following loading of gold nanotracers , 2011, International journal of nanomedicine.

[74]  Minghua Xu,et al.  Analytic explanation of spatial resolution related to bandwidth and detector aperture size in thermoacoustic or photoacoustic reconstruction. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[75]  Xinmai Yang,et al.  Growth of melanoma brain tumors monitored by photoacoustic microscopy. , 2010, Journal of biomedical optics.

[76]  Congxian Jia,et al.  Dynamic manipulation of magnetic contrast agents in photoacoustic imaging , 2011, BiOS.

[77]  S. Stoeckli,et al.  Sentinel Lymph Node Evaluation in Squamous Cell Carcinoma of the Head and Neck , 2001, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[78]  Luis M Liz-Marzán,et al.  Shape control in gold nanoparticle synthesis. , 2008, Chemical Society reviews.

[79]  Manojit Pramanik,et al.  Molecular photoacoustic imaging of angiogenesis with integrin‐targeted gold nanobeacons , 2011, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[80]  T. Fleming,et al.  Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. , 2001, The New England journal of medicine.

[81]  Stanislav Emelianov,et al.  Prospects of molecular photoacoustic imaging at 1064 nm wavelength. , 2010, Optics letters.

[82]  Wei Lu,et al.  Photoacoustic imaging of living mouse brain vasculature using hollow gold nanospheres. , 2010, Biomaterials.

[83]  Wei Wang,et al.  Simultaneous Molecular and Hypoxia Imaging of Brain Tumors In Vivo Using Spectroscopic Photoacoustic Tomography , 2008, Proceedings of the IEEE.

[84]  Stanislav Emelianov,et al.  Intravascular photoacoustic imaging of macrophages using molecularly targeted gold nanoparticles , 2010, BiOS.

[85]  Lihong V. Wang Photoacoustic imaging and spectroscopy , 2009 .

[86]  Stanislav Emelianov,et al.  Photoacoustic and ultrasound imaging contrast enhancement using a dual contrast agent , 2010, BiOS.

[87]  E. Wickstrom,et al.  Single-wall carbon nanotube nanobomb agents for killing breast cancer cells , 2005 .

[88]  Stanislav Emelianov,et al.  Enhanced thermal stability of silica-coated gold nanorods for photoacoustic imaging and image-guided therapy , 2010, Optics express.

[89]  A. Carson,et al.  Detection and monitoring of the multiple inflammatory responses by photoacoustic molecular imaging using selectively targeted gold nanorods , 2011, Biomedical optics express.

[90]  Feng Gao,et al.  In vivo molecular photoacoustic tomography of melanomas targeted by bioconjugated gold nanocages. , 2010, ACS nano.

[91]  S. Emelianov,et al.  Photoacoustic imaging and temperature measurement for photothermal cancer therapy. , 2008, Journal of biomedical optics.

[92]  Tyler Harrison,et al.  Coregistered photoacoustic-ultrasound imaging applied to brachytherapy. , 2011, Journal of biomedical optics.

[93]  Lihong V. Wang,et al.  Photoacoustic imaging in biomedicine , 2006 .

[94]  Stanislav Emelianov,et al.  Synthesis of a dual contrast agent for ultrasound and photoacoustic imaging , 2010, BiOS.

[95]  Younan Xia,et al.  Near-infrared gold nanocages as a new class of tracers for photoacoustic sentinel lymph node mapping on a rat model. , 2009, Nano letters.

[96]  P. Jain,et al.  Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: applications in biological imaging and biomedicine. , 2006, The journal of physical chemistry. B.

[97]  Manojit Pramanik,et al.  Single-walled carbon nanotubes as a multimodal-thermoacoustic and photoacoustic-contrast agent. , 2009, Journal of biomedical optics.

[98]  Cheng-Dah Chen,et al.  The Shape Transition of Gold Nanorods , 1999 .

[99]  Lihong V. Wang,et al.  Dark-Field Confocal Photoacoustic Microscopy , 2009 .

[100]  S. Emelianov,et al.  Intravascular photoacoustic imaging using an IVUS imaging catheter , 2007, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[101]  S. Emelianov,et al.  Detection of lipid in atherosclerotic vessels using ultrasound-guided spectroscopic intravascular photoacoustic imaging , 2010, Optics express.

[102]  Bo Wang,et al.  Photoacoustic imaging of coronary artery stents. , 2009, Optics express.

[103]  Stanislav Y. Emelianov,et al.  Photoacoustic imaging of prostate brachytherapy seeds , 2011, Biomedical optics express.

[104]  Stanislav Emelianov,et al.  Ultrasound and photoacoustic imaging to monitor vascular growth in tissue engineered constructs , 2009, BiOS.

[105]  Da Xing,et al.  Gold nanoshell-based photoacoustic imaging application in biomedicine , 2006, 2006 International Symposium on Biophotonics, Nanophotonics and Metamaterials.

[106]  Danielle E. Green,et al.  The effect of nanoparticle-enhanced photoacoustic stimulation on multipotent marrow stromal cells. , 2009, ACS nano.

[107]  Frank P Barry,et al.  Stem cell therapy in a caprine model of osteoarthritis. , 2003, Arthritis and rheumatism.

[108]  P. Vaupel,et al.  Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. , 2001, Journal of the National Cancer Institute.

[109]  Takuro Niidome,et al.  PEG-modified gold nanorods with a stealth character for in vivo applications. , 2006, Journal of controlled release : official journal of the Controlled Release Society.

[110]  Adam de la Zerda,et al.  Ultrahigh sensitivity carbon nanotube agents for photoacoustic molecular imaging in living mice. , 2010, Nano letters.

[111]  Konstantin V Sokolov,et al.  Kinetic assembly of near-IR-active gold nanoclusters using weakly adsorbing polymers to control the size. , 2010, Langmuir : the ACS journal of surfaces and colloids.

[112]  Da Xing,et al.  Noninvasive monitoring of traumatic brain injury and post-traumatic rehabilitation with laser-induced photoacoustic imaging , 2007 .

[113]  Srivalleesha Mallidi,et al.  Utility of biodegradable plasmonic nanoclusters in photoacoustic imaging. , 2010, Optics letters.

[114]  Stanislav Y. Emelianov,et al.  In vivo three-dimensional spectroscopic photoacoustic imaging for monitoring nanoparticle delivery , 2011, Biomedical optics express.

[115]  Xueding Wang,et al.  Picomolar sensitivity MRI and photoacoustic imaging of cobalt nanoparticles , 2009, Proceedings of the National Academy of Sciences.

[116]  Lihong V. Wang,et al.  Functional transcranial brain imaging by optical-resolution photoacoustic microscopy. , 2009, Journal of biomedical optics.

[117]  Baowei Fei,et al.  Highly efficient drug delivery with gold nanoparticle vectors for in vivo photodynamic therapy of cancer. , 2008, Journal of the American Chemical Society.

[118]  Matthew O'Donnell,et al.  Photoacoustic imaging of early inflammatory response using gold nanorods , 2007 .

[119]  Jan Laufer,et al.  Evaluation of Absorbing Chromophores Used in Tissue Phantoms for Quantitative Photoacoustic Spectroscopy and Imaging , 2010, IEEE Journal of Selected Topics in Quantum Electronics.

[120]  S. Emelianov,et al.  Photoacoustic imaging in cancer detection, diagnosis, and treatment guidance. , 2011, Trends in biotechnology.

[121]  Te-Jen Ma,et al.  Design, synthesis, and imaging of an activatable photoacoustic probe. , 2010, Journal of the American Chemical Society.

[122]  Lihong V. Wang,et al.  Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging , 2006, Nature Biotechnology.

[123]  Kort Travis,et al.  Controlled assembly of biodegradable plasmonic nanoclusters for near-infrared imaging and therapeutic applications. , 2010, ACS nano.

[124]  Umberto Veronesi,et al.  Sentinel-node biopsy to avoid axillary dissection in breast cancer with clinically negative lymph-nodes , 1997, The Lancet.

[125]  Marc D Feldman,et al.  Small multifunctional nanoclusters (nanoroses) for targeted cellular imaging and therapy. , 2009, ACS nano.

[126]  Hongjie Dai,et al.  Supramolecular Chemistry on Water- Soluble Carbon Nanotubes for Drug Loading and Delivery , 2007 .

[127]  T. O’Brien,et al.  Stem cell therapy for cardiac disease , 2011, Expert opinion on biological therapy.

[128]  Shriram Sethuraman,et al.  Spectroscopic intravascular photoacoustic imaging to differentiate atherosclerotic plaques. , 2008, Optics express.

[129]  Lihong V. Wang Multiscale photoacoustic microscopy and computed tomography. , 2009, Nature photonics.

[130]  R. Nicholson,et al.  EGFR and cancer prognosis. , 2001, European journal of cancer.

[131]  Feifan Zhou,et al.  Photoacoustic molecular imaging with antibody-functionalized single-walled carbon nanotubes for early diagnosis of tumor. , 2009, Journal of biomedical optics.

[132]  Chulhong Kim,et al.  Noninvasive in vivo spectroscopic nanorod-contrast photoacoustic mapping of sentinel lymph nodes. , 2009, European journal of radiology.

[133]  Lihong V. Wang,et al.  In-vivo photoacoustic microscopy of nanoshell extravasation from solid tumor vasculature. , 2009, Journal of biomedical optics.

[134]  Antonio Colombo,et al.  From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: Part II. , 2003, Circulation.

[135]  Stanislav Emelianov,et al.  Silver nanosystems for photoacoustic imaging and image-guided therapy. , 2010, Journal of biomedical optics.

[136]  P. Choyke,et al.  Clearance properties of nano-sized particles and molecules as imaging agents: considerations and caveats. , 2008, Nanomedicine.

[137]  Younan Xia,et al.  Shape-controlled synthesis of metal nanocrystals: simple chemistry meets complex physics? , 2009, Angewandte Chemie.