Diagnostic prospects and preclinical development of optical technologies using gold nanostructure contrast agents to boost endogenous tissue contrast

Numerous developments in optical biomedical imaging research utilizing gold nanostructures as contrast agents have advanced beyond basic research towards demonstrating potential as diagnostic tools; some of which are translating into clinical applications. Recent advances in optics, lasers and detection instrumentation along with the extensive, yet developing, knowledge-base in tailoring the optical properties of gold nanostructures has significantly improved the prospect of near-infrared (NIR) optical detection technologies. Of particular interest are optical coherence tomography (OCT), photoacoustic imaging (PAI), multispectral optoacoustic tomography (MSOT), Raman spectroscopy (RS) and surface enhanced spatially offset Raman spectroscopy (SESORS), due to their respective advancements. Here we discuss recent technological developments, as well as provide a prediction of their potential to impact on clinical diagnostics. A brief summary of each techniques' capability to distinguish abnormal (disease sites) from normal tissues, using endogenous signals alone is presented. We then elaborate on the use of exogenous gold nanostructures as contrast agents providing enhanced performance in the above-mentioned techniques. Finally, we consider the potential of these approaches to further catalyse advances in pre-clinical and clinical optical diagnostic technologies.

[1]  P. Matousek,et al.  Optical characterization of porcine tissues from various organs in the 650–1100 nm range using time-domain diffuse spectroscopy , 2020, Biomedical optics express.

[2]  Ariane M. Vartanian,et al.  Surface Chemistry of Gold Nanorods. , 2016, Langmuir : the ACS journal of surfaces and colloids.

[3]  Y. S. Zhang,et al.  Plasmonic Nanoprobe of (Gold Triangular Nanoprism Core)/(Polyaniline Shell) for Real-Time Three-Dimensional pH Imaging of Anterior Chamber. , 2017, Analytical chemistry.

[4]  Gang Su,et al.  Corrigendum: Hinge-like structure induced unusual properties of black phosphorus and new strategies to improve the thermoelectric performance , 2016, Scientific Reports.

[5]  Lihong V. Wang,et al.  Single-breath-hold photoacoustic computed tomography of the breast , 2018, Nature Communications.

[6]  Qi-Zhen He,et al.  Structural‐Engineering Rationales of Gold Nanoparticles for Cancer Theranostics , 2016, Advanced materials.

[7]  Liming Wang,et al.  In vivo pharmacokinetic features and biodistribution of star and rod shaped gold nanoparticles by multispectral optoacoustic tomography , 2015 .

[8]  Jutaek Nam,et al.  pH-Induced aggregation of gold nanoparticles for photothermal cancer therapy. , 2009, Journal of the American Chemical Society.

[9]  M. Brust,et al.  Multimodal cell tracking from systemic administration to tumour growth by combining gold nanorods and reporter genes , 2017, bioRxiv.

[10]  P. Matousek,et al.  Direct monitoring of light mediated hyperthermia induced within mammalian tissues using surface enhanced spatially offset Raman spectroscopy (T-SESORS). , 2019, The Analyst.

[11]  H. Rigneault,et al.  Assessment of Compressive Raman versus Hyperspectral Raman for Microcalcification Chemical Imaging. , 2018, Analytical chemistry.

[12]  K. Thurecht,et al.  Tagged Core-Satellite Nanoassemblies: Role of Assembling Sequence on Surface-Enhanced Raman Scattering (SERS) Performance , 2019, Applied spectroscopy.

[13]  C. Joo,et al.  Detection of pH-induced aggregation of "smart" gold nanoparticles with photothermal optical coherence tomography. , 2013, Optics letters.

[14]  P. Matousek,et al.  Smart Gold Nanostructures for Light Mediated Cancer Theranostics: Combining Optical Diagnostics with Photothermal Therapy , 2020, Advanced science.

[15]  Martin Wolf,et al.  A review on continuous wave functional near-infrared spectroscopy and imaging instrumentation and methodology , 2014, NeuroImage.

[16]  P. Matousek,et al.  Determination of inclusion depth in ex vivo animal tissues using surface enhanced deep Raman spectroscopy , 2019, Journal of biophotonics.

[17]  K. Thurecht,et al.  Hyperbranched polymer-gold nanoparticle assemblies: role of polymer architecture in hybrid assembly formation and SERS activity. , 2014, Langmuir : the ACS journal of surfaces and colloids.

[18]  P. Prasad,et al.  Au-Cu2-xSe heterogeneous nanocrystals for efficient photothermal heating for cancer therapy. , 2017, Journal of materials chemistry. B.

[19]  C. Kendall,et al.  Raman spectroscopy for medical diagnostics--From in-vitro biofluid assays to in-vivo cancer detection. , 2015, Advanced drug delivery reviews.

[20]  Zhihong Huang,et al.  High‐intensity‐focused ultrasound and phase‐sensitive optical coherence tomography for high resolution surface acoustic wave elastography , 2018, Journal of biophotonics.

[21]  Eden P. Paul,et al.  Diagnosis of immunomarkers in vivo via multiplexed surface enhanced Raman spectroscopy with gold nanostars. , 2018, Nanoscale.

[22]  Liguang Xu,et al.  Regiospecific plasmonic assemblies for in situ Raman spectroscopy in live cells. , 2012, Journal of the American Chemical Society.

[23]  Hugh Barr,et al.  Near‐infrared Raman spectroscopy for the classification of epithelial pre‐cancers and cancers , 2002 .

[24]  S. Ourselin,et al.  Photoacoustic imaging of the human placental vasculature , 2019, Journal of biophotonics.

[25]  Bo Yan,et al.  Surface Charge Controls the Suborgan Biodistributions of Gold Nanoparticles. , 2016, ACS nano.

[26]  P. Matousek,et al.  Spatially Offset and Transmission Raman Spectroscopy for Determination of Depth of Inclusion in Turbid Matrix , 2019, Analytical chemistry.

[27]  Jinping Wang,et al.  MSOT/CT/MR imaging-guided and hypoxia-maneuvered oxygen self-supply radiotherapy based on one-pot MnO2-mSiO2@Au nanoparticles. , 2019, Nanoscale.

[28]  Na Li,et al.  Anisotropic gold nanoparticles: synthesis, properties, applications, and toxicity. , 2014, Angewandte Chemie.

[29]  Betty Y. S. Kim,et al.  How to design preclinical studies in nanomedicine and cell therapy to maximize the prospects of clinical translation , 2018, Nature Biomedical Engineering.

[30]  Valery V Tuchin,et al.  Polarized light interaction with tissues , 2016, Journal of biomedical optics.

[31]  J. Nolan,et al.  Optimization of SERS Tag Intensity, Binding Footprint, and Emittance , 2014, Bioconjugate chemistry.

[32]  K. Thurecht,et al.  Self assembly of plasmonic core-satellite nano-assemblies mediated by hyperbranched polymer linkers. , 2014, Journal of materials chemistry. B.

[33]  K. Faulds,et al.  Through tissue imaging of a live breast cancer tumour model using handheld surface enhanced spatially offset resonance Raman spectroscopy (SESORRS)† †Electronic supplementary information (ESI) available. See DOI: 10.1039/c8sc00994e , 2018, Chemical science.

[34]  G. Lloyd,et al.  Surface enhanced spatially offset Raman spectroscopic (SESORS) imaging – the next dimension , 2011 .

[35]  K. Hamad-Schifferli,et al.  Extinction Coefficient of Gold Nanostars. , 2015, The journal of physical chemistry. C, Nanomaterials and interfaces.

[36]  Richard P Van Duyne,et al.  In vivo, transcutaneous glucose sensing using surface-enhanced spatially offset Raman spectroscopy: multiple rats, improved hypoglycemic accuracy, low incident power, and continuous monitoring for greater than 17 days. , 2011, Analytical chemistry.

[37]  V. Tuchin,et al.  Depth-Resolved Enhanced Spectral-Domain OCT Imaging of Live Mammalian Embryos Using Gold Nanoparticles as Contrast Agent. , 2019, Small.

[38]  S. Jeffrey,et al.  Gold Nanobipyramids as Second Near Infrared Optical Coherence Tomography Contrast Agents for In Vivo Multiplexing Studies. , 2020, Nano letters.

[39]  Direk Limmathurotsakul,et al.  Development and Validation of Burkholderia pseudomallei-Specific Real-Time PCR Assays for Clinical, Environmental or Forensic Detection Applications , 2012, PloS one.

[40]  Holly J. Butler,et al.  Using Raman spectroscopy to characterize biological materials , 2016, Nature Protocols.

[41]  Seok Hyun Yun,et al.  Light in diagnosis, therapy and surgery , 2016, Nature Biomedical Engineering.

[42]  L. Motte,et al.  Raspberry-like small multicore gold nanostructures for efficient photothermal conversion in the first and second near-infrared windows. , 2019, Chemical communications.

[43]  Gold Nanoparticles Radio-Sensitize and Reduce Cell Survival in Lewis Lung Carcinoma , 2020, Nanomaterials.

[44]  A. Brolo,et al.  Improved synthesis of gold and silver nanoshells. , 2013, Langmuir.

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

[46]  Ren Hu,et al.  Surface-Enhanced Raman Spectroscopy for Bioanalysis: Reliability and Challenges. , 2018, Chemical reviews.

[47]  Edmund J. Crampin,et al.  Minimum information reporting in bio–nano experimental literature , 2018, Nature Nanotechnology.

[48]  J. Jagdeo,et al.  Transcranial Red and Near Infrared Light Transmission in a Cadaveric Model , 2012, PloS one.

[49]  Richard W. Taylor,et al.  Optimizing SERS from Gold Nanoparticle Clusters: Addressing the Near Field by an Embedded Chain Plasmon Model , 2016 .

[50]  M. Döblinger,et al.  Switching Plasmons: Gold Nanorod-Copper Chalcogenide Core-Shell Nanoparticle Clusters with Selectable Metal/Semiconductor NIR Plasmon Resonances. , 2015, Journal of the American Chemical Society.

[51]  R. V. Van Duyne,et al.  Seeing through bone with surface-enhanced spatially offset Raman spectroscopy. , 2013, Journal of the American Chemical Society.

[52]  Vasilis Ntziachristos,et al.  Real-time imaging of cardiovascular dynamics and circulating gold nanorods with multispectral optoacoustic tomography. , 2010, Optics express.

[53]  A. Mikhailovsky,et al.  Scalable routes to gold nanoshells with tunable sizes and response to near-infrared pulsed-laser irradiation. , 2008, Small.

[54]  P. Kuo,et al.  Self-assembly of gold nanoparticles induced by poly(oxypropylene)diamines. , 2005, The journal of physical chemistry. B.

[55]  P. Matousek,et al.  High sensitivity non‐invasive detection of calcifications deep inside biological tissue using Transmission Raman Spectroscopy , 2018, Journal of biophotonics.

[56]  Jun Zhang,et al.  Fast and simple high-capacity quantum cryptography with error detection , 2017, Scientific Reports.

[57]  J. Rodríguez-Fernández,et al.  Gold Nanorod Assemblies: The Roles of Hot-Spot Positioning and Anisotropy in Plasmon Coupling and SERS , 2020, Nanomaterials.

[58]  Scott L. Rudder,et al.  Non-invasive In Vivo Imaging of Cancer Using Surface-Enhanced Spatially Offset Raman Spectroscopy (SESORS) , 2019, Theranostics.

[59]  Derek W. Yecies,et al.  Gold Nanoprisms as Optical Coherence Tomography Contrast Agents in the Second Near-Infrared Window for Enhanced Angiography in Live Animals. , 2018, ACS nano.

[60]  M. Kinnunen,et al.  Plasmon-Resonant Gold Nanostars With Variable Size as Contrast Agents for Imaging Applications , 2016, IEEE Journal of Selected Topics in Quantum Electronics.

[61]  Martin Moskovits,et al.  Electromagnetic theories of surface-enhanced Raman spectroscopy. , 2017, Chemical Society reviews.

[62]  Lim Wei Yap,et al.  Multilayered core-satellite nanoassemblies with fine-tunable broadband plasmon resonances. , 2015, Nanoscale.

[63]  Patrick Couvreur,et al.  Nanotheranostics for personalized medicine. , 2016, Advanced drug delivery reviews.

[64]  Charles H. Camp,et al.  High-Speed Coherent Raman Fingerprint Imaging of Biological Tissues , 2014, Nature Photonics.

[65]  Pietro Strobbia,et al.  Recent advances in plasmonic nanostructures for sensing: a review , 2015 .

[66]  S. Guo,et al.  Raman tags: Novel optical probes for intracellular sensing and imaging. , 2017, Biotechnology advances.

[67]  K. Thurecht,et al.  SERS-based detection of barcoded gold nanoparticle assemblies from within animal tissue , 2013 .

[68]  Tao Zhang,et al.  DNA origami based assembly of gold nanoparticle dimers for surface-enhanced Raman scattering , 2014, Nature Communications.

[69]  J. Ho,et al.  Nanotheranostics – a review of recent publications , 2012, International journal of nanomedicine.

[70]  R. A. Torres,et al.  Dynamic single gold nanoparticle visualization by clinical intracoronary optical coherence tomography , 2017, Journal of biophotonics.

[71]  Joseph J. Richardson,et al.  Nanomedicine toward 2040. , 2020, Nano letters.

[72]  M. Cecchini,et al.  Ultrastructural Characterization of the Lower Motor System in a Mouse Model of Krabbe Disease , 2016, Scientific Reports.

[73]  George C. Schatz,et al.  A Look at the Origin and Magnitude of the Chemical Contribution to the Enhancement Mechanism of Surface-Enhanced Raman Spectroscopy (SERS): Theory and Experiment , 2013 .

[74]  Menachem Motiei,et al.  A challenge for theranostics: is the optimal particle for therapy also optimal for diagnostics? , 2015, Nanoscale.

[75]  Dawei Gao,et al.  Combined Near Infrared Photothermal Therapy and Chemotherapy Using Gold Nanoshells Coated Liposomes to Enhance Antitumor Effect. , 2016, Small.

[76]  X. Xie,et al.  Video-Rate Molecular Imaging in Vivo with Stimulated Raman Scattering , 2010, Science.

[77]  Jeremy J. Baumberg,et al.  Nanooptics of Molecular-Shunted Plasmonic Nanojunctions , 2014, Nano letters.

[78]  J. Kumaradas,et al.  The role of morphology and coupling of gold nanoparticles in optical breakdown during picosecond pulse exposures , 2016, Beilstein journal of nanotechnology.

[79]  Ya Ding,et al.  Monodisperse Au-Fe2C Janus Nanoparticles: An Attractive Multifunctional Material for Triple-Modal Imaging-Guided Tumor Photothermal Therapy. , 2017, ACS nano.

[80]  Gordon C Jayson,et al.  Antiangiogenic therapy in oncology: current status and future directions , 2016, The Lancet.

[81]  Yue Zhao,et al.  In vivo mice brain microcirculation monitoring based on contrast-enhanced SD-OCT , 2019, Journal of Innovative Optical Health Sciences.

[82]  M. Brust,et al.  Preventing Plasmon Coupling between Gold Nanorods Improves the Sensitivity of Photoacoustic Detection of Labeled Stem Cells in Vivo. , 2016, ACS nano.

[83]  Yongsheng Li,et al.  Synthesis of gold Nanoshells through Improved Seed-Mediated Growth Approach: Brust-like, in Situ Seed Formation. , 2016, Langmuir : the ACS journal of surfaces and colloids.

[84]  G. Jékely,et al.  Neural circuitry of a polycystin-mediated hydrodynamic startle response for predator avoidance , 2018, bioRxiv.

[85]  Robert R. Alfano,et al.  Deep optical imaging of tissue using the second and third near-infrared spectral windows , 2014, Journal of biomedical optics.

[86]  Beibei Shan,et al.  Novel SERS labels: Rational design, functional integration and biomedical applications , 2018, Coordination Chemistry Reviews.

[87]  Nathan O. Loewke,et al.  A Real-Time Clinical Endoscopic System for Intraluminal, Multiplexed Imaging of Surface-Enhanced Raman Scattering Nanoparticles , 2015, PloS one.

[88]  G. Pazour,et al.  Ror2 signaling regulates Golgi structure and transport through IFT20 for tumor invasiveness , 2017, Scientific Reports.

[89]  Richard P Van Duyne,et al.  Creating, characterizing, and controlling chemistry with SERS hot spots. , 2013, Physical chemistry chemical physics : PCCP.

[90]  V. A. Apkarian,et al.  Orientation-Dependent Handedness of Chiral Plasmons on Nanosphere Dimers: How to Turn a Right Hand into a Left Hand , 2016 .

[91]  Pedro Pedrosa,et al.  Gold Nanotheranostics: Proof-of-Concept or Clinical Tool? , 2015, Nanomaterials.

[92]  P. Matousek,et al.  Plasmonic Nanoassemblies: Tentacles Beat Satellites for Boosting Broadband NIR Plasmon Coupling Providing a Novel Candidate for SERS and Photothermal Therapy. , 2020, Small.

[93]  Subsurface Chemically Specific Measurement of pH Levels in Biological Tissues Using Combined Surface-Enhanced and Deep Raman , 2019, Analytical chemistry.

[94]  A. Goodship,et al.  Numerical Simulations of Subsurface Probing in Diffusely Scattering Media Using Spatially Offset Raman Spectroscopy , 2005, Applied spectroscopy.

[95]  Oliver A. C. Stevens,et al.  Endoscopic Raman spectroscopy enables objective diagnosis of dysplasia in Barrett's esophagus. , 2014, Gastrointestinal endoscopy.

[96]  Sanjiv S. Gambhir,et al.  Photoacoustic clinical imaging , 2019, Photoacoustics.

[97]  Vasilis Ntziachristos,et al.  Dual-Modality Surface-Enhanced Resonance Raman Scattering and Multispectral Optoacoustic Tomography Nanoparticle Approach for Brain Tumor Delineation. , 2018, Small.

[98]  Nicholas Stone,et al.  Raman spectroscopy--a new method for the intra-operative assessment of axillary lymph nodes. , 2010, The Analyst.

[99]  Daniel Razansky,et al.  Structural and Functional Analysis of Intact Hair Follicles and Pilosebaceous Units by Volumetric Multispectral Optoacoustic Tomography. , 2016, The Journal of investigative dermatology.

[100]  Frederik Haase,et al.  Highly stable and biocompatible gold nanorod–DNA conjugates as NIR probes for ultrafast sequence-selective DNA melting , 2016 .

[101]  H. Chiang,et al.  Near infrared surface-enhanced Raman scattering based on star-shaped gold/silver nanoparticles and hyperbolic metamaterial , 2017, Scientific Reports.

[102]  John C. Bischof,et al.  Quantitative Comparison of Photothermal Heat Generation between Gold Nanospheres and Nanorods , 2016, Scientific Reports.

[103]  Luis M Liz-Marzán,et al.  Universal analytical modeling of plasmonic nanoparticles. , 2017, Chemical Society reviews.

[104]  Xiaoyuan Chen,et al.  Rethinking cancer nanotheranostics. , 2017, Nature reviews. Materials.

[105]  M. Johnson,et al.  Circulating microRNAs in Sera Correlate with Soluble Biomarkers of Immune Activation but Do Not Predict Mortality in ART Treated Individuals with HIV-1 Infection: A Case Control Study , 2015, PloS one.

[106]  N. Stone,et al.  A Subcutaneous Raman Needle Probe , 2013, Applied spectroscopy.

[107]  G. Lloyd,et al.  Discrimination between benign, primary and secondary malignancies in lymph nodes from the head and neck utilising Raman spectroscopy and multivariate analysis. , 2013, The Analyst.

[108]  Liwei Liu,et al.  Optical windows for head tissues in near‐infrared and short‐wave infrared regions: Approaching transcranial light applications , 2018, Journal of biophotonics.

[109]  L. Bernstein,et al.  Intraoperative brain cancer detection with Raman spectroscopy in humans , 2015, Science Translational Medicine.

[110]  M. El-Sayed,et al.  Dependence of the enhanced optical scattering efficiency relative to that of absorption for gold metal nanorods on aspect ratio, size, end-cap shape, and medium refractive index. , 2005, The journal of physical chemistry. B.

[111]  Jin Ho Chang,et al.  Amplified photoacoustic performance and enhanced photothermal stability of reduced graphene oxide coated gold nanorods for sensitive photoacoustic imaging. , 2015, ACS nano.

[112]  L. Liz‐Marzán,et al.  Modelling the optical response of gold nanoparticles. , 2008, Chemical Society reviews.

[113]  Guoqing Wang,et al.  Gold nanostructures with near-infrared plasmonic resonance: Synthesis and surface functionalization , 2017 .

[114]  K. Thurecht,et al.  Self-assembled hyperbranched polymer-gold nanoparticle hybrids: understanding the effect of polymer coverage on assembly size and SERS performance. , 2013, Langmuir : the ACS journal of surfaces and colloids.