A dual modal silver bumpy nanoprobe for photoacoustic imaging and SERS multiplexed identification of in vivo lymph nodes.

Multimodal imaging can provide complementary biomedical information which has huge potential in pre-clinical and clinical imaging and sensing. In this study, we introduce dual modal NIR silver bumpy nanoprobes for in vivo imaging and multiplexed detection of biomolecules by both photoacoustic imaging (PAI) and surface-enhanced Raman scattering (SERS) techniques. For this study, we used silica-coated silver bumpy nanoshell probes (AgNS@SiO2). AgNS@SiO2 have strong NIR-absorption and scattering properties compared with other nanostructures, and therefore, can be a good candidate for photoacoustic (PA) and SERS multimodal imaging. We obtained PA images of the skin and SLNs of rats by injecting various kinds of Raman-labeled AgNS@SiO2. Multiplexed identification of the injected AgNS@SiO2 was achieved by measuring SERS signals. AgNS@SiO2 have the potential to be applied in detecting cancer biomarkers by locating biomarkers quickly using PA imaging, and identification by multiplexed target measurement using SERS signals in vivo.

[1]  Yong-Kweon Kim,et al.  Direct Identification of On-Bead Peptides Using Surface-Enhanced Raman Spectroscopic Barcoding System for High-Throughput Bioanalysis , 2015, Scientific Reports.

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

[3]  Wang Li,et al.  SERS-fluorescence joint spectral encoding using organic-metal-QD hybrid nanoparticles with a huge encoding capacity for high-throughput biodetection: putting theory into practice. , 2012, Journal of the American Chemical Society.

[4]  C. Brennan,et al.  A Brain Tumor Molecular Imaging Strategy Using A New Triple-Modality MRI-Photoacoustic-Raman Nanoparticle , 2011, Nature Medicine.

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

[6]  Liang Song,et al.  Dual-color photoacoustic lymph node imaging using nanoformulated naphthalocyanines. , 2015, Biomaterials.

[7]  Chulhong Kim,et al.  Nonionizing photoacoustic cystography in vivo. , 2011, Optics letters.

[8]  Yung Doug Suh,et al.  Nanogap-engineerable Raman-active nanodumbbells for single-molecule detection. , 2010, Nature materials.

[9]  Liming Nie,et al.  Structural and functional photoacoustic molecular tomography aided by emerging contrast agents. , 2014, Chemical Society reviews.

[10]  Sanjiv S. Gambhir,et al.  Multiplexed imaging of surface enhanced Raman scattering nanotags in living mice using noninvasive Raman spectroscopy , 2009, Proceedings of the National Academy of Sciences.

[11]  D. McCready,et al.  Lymph node assessment in melanoma , 2009, Journal of surgical oncology.

[12]  N. Shah,et al.  Surface-enhanced Raman spectroscopy. , 2008, Annual review of analytical chemistry.

[13]  A. Bogdanov,et al.  Synthesis and Testing of Modular Dual-Modality Nanoparticles for Magnetic Resonance and Multispectral Photoacoustic Imaging. , 2016, Bioconjugate chemistry.

[14]  W. Stöber,et al.  Controlled growth of monodisperse silica spheres in the micron size range , 1968 .

[15]  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.

[16]  H. P. Curutchet,et al.  Sentinel Lymph Node , 2004, Molecular Diagnosis.

[17]  A. Rosato,et al.  Magneto-plasmonic Au-Fe alloy nanoparticles designed for multimodal SERS-MRI-CT imaging. , 2014, Small.

[18]  I. Kwon,et al.  Squaraine‐Doped Functional Nanoprobes: Lipophilically Protected Near‐Infrared Fluorescence for Bioimaging , 2010 .

[19]  Ning Zhang,et al.  Ultrasensitive, Multiplex Raman Frequency Shift Immunoassay of Liver Cancer Biomarkers in Physiological Media. , 2016, ACS nano.

[20]  F. R. Castiello,et al.  A study of the depth and size of concave cube Au nanoparticles as highly sensitive SERS probes. , 2016, Nanoscale.

[21]  H. Cody,et al.  Intradermal Radiocolloid and Intraparenchymal Blue Dye Injection Optimize Sentinel Node Identification in Breast Cancer Patients , 1999, Annals of Surgical Oncology.

[22]  M. Lens,et al.  Sentinel lymph node biopsy in melanoma patients , 2010, Journal of the European Academy of Dermatology and Venereology : JEADV.

[23]  H. Cody,et al.  A Prospective Analysis of the Effect of Blue-Dye Volume on Sentinel Lymph Node Mapping Success and Incidence of Allergic Reaction in Patients With Breast Cancer , 2004, Annals of Surgical Oncology.

[24]  Homan Kang,et al.  Ag shell-Au satellite hetero-nanostructure for ultra-sensitive, reproducible, and homogeneous NIR SERS activity. , 2014, ACS applied materials & interfaces.

[25]  Hongyu Chen,et al.  Revisiting the Stöber method: inhomogeneity in silica shells. , 2011, Journal of the American Chemical Society.

[26]  Qian Huang,et al.  Copper sulfide nanoparticles as a new class of photoacoustic contrast agent for deep tissue imaging at 1064 nm. , 2012, ACS nano.

[27]  Chulhong Kim,et al.  Porphysome nanovesicles generated by porphyrin bilayers for use as multimodal biophotonic contrast agents. , 2011, Nature materials.

[28]  S. Schlücker Surface-enhanced Raman spectroscopy: concepts and chemical applications. , 2014, Angewandte Chemie.

[29]  Todd N. Erpelding,et al.  Performance benchmarks of an array-based hand-held photoacoustic probe adapted from a clinical ultrasound system for non-invasive sentinel lymph node imaging , 2011, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

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

[31]  Chulhong Kim,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. , 2010, Radiology.

[32]  Yuejun Kang,et al.  Near-Infrared Squaraine Dye Encapsulated Micelles for in Vivo Fluorescence and Photoacoustic Bimodal Imaging. , 2015, ACS nano.

[33]  Zhe Wang,et al.  Biodegradable gold nanovesicles with an ultrastrong plasmonic coupling effect for photoacoustic imaging and photothermal therapy. , 2013, Angewandte Chemie.

[34]  Yibin Ying,et al.  Multidimensional SERS Barcodes on Flexible Patterned Plasmonic Metafilm for Anticounterfeiting Applications , 2016 .

[35]  Changhui Li,et al.  Biocompatible polypyrrole nanoparticles as a novel organic photoacoustic contrast agent for deep tissue imaging. , 2013, Nanoscale.

[36]  John F. Thompson,et al.  Patterns of lymphatic drainage from the skin in patients with melanoma. , 2003, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[37]  Lihong V. Wang,et al.  Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo , 2012, Nature Medicine.

[38]  T. Mihaljevic,et al.  Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping , 2004, Nature Biotechnology.

[39]  H. Carmalt,et al.  SPECT/CT scans allow precise anatomical location of sentinel lymph nodes in breast cancer and redefine lymphatic drainage from the breast to the axilla. , 2012, Breast.

[40]  Lihong V. Wang,et al.  Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain , 2003, Nature Biotechnology.

[41]  Jesse V Jokerst,et al.  Gold nanorods for ovarian cancer detection with photoacoustic imaging and resection guidance via Raman imaging in living mice. , 2012, ACS nano.

[42]  P. Schlag,et al.  Sentinel lymph node biopsy for gastrointestinal cancers , 2007, Journal of surgical oncology.

[43]  Jesse V. Jokerst,et al.  Semiconducting Polymer Nanoparticles as Photoacoustic Molecular Imaging Probes in Living Mice , 2014, Nature nanotechnology.

[44]  Homan Kang,et al.  Single-step and rapid growth of silver nanoshells as SERS-active nanostructures for label-free detection of pesticides. , 2014, ACS applied materials & interfaces.

[45]  U. S. Dinish,et al.  Multiplex targeted in vivo cancer detection using sensitive near-infrared SERS nanotags , 2012 .

[46]  Chulhong Kim,et al.  Multiplane spectroscopic whole-body photoacoustic imaging of small animals in vivo , 2014, Medical & Biological Engineering & Computing.

[47]  Michael Detmar,et al.  Use of a PEG-conjugated bright near-infrared dye for functional imaging of rerouting of tumor lymphatic drainage after sentinel lymph node metastasis. , 2013, Biomaterials.

[48]  D. Lee,et al.  Fluorescence-Raman Dual Modal Endoscopic System for Multiplexed Molecular Diagnostics , 2015, Scientific Reports.

[49]  Peter T C So,et al.  High resolution live cell Raman imaging using subcellular organelle-targeting SERS-sensitive gold nanoparticles with highly narrow intra-nanogap. , 2015, Nano letters.

[50]  Xianmao Lu,et al.  Highly Symmetric Gold Nanostars: Crystallographic Control and Surface-Enhanced Raman Scattering Property. , 2015, Journal of the American Chemical Society.

[51]  R. Simmons,et al.  Methylene blue dye as an alternative to isosulfan blue dye for sentinel lymph node localization. , 2003, The breast journal.

[52]  Samuel Achilefu,et al.  Multimodal sentinel lymph node mapping with single-photon emission computed tomography (SPECT)/computed tomography (CT) and photoacoustic tomography. , 2012, Translational research : the journal of laboratory and clinical medicine.

[53]  Lihong V. Wang,et al.  In vivo photoacoustic tomography of chemicals: high-resolution functional and molecular optical imaging at new depths. , 2010, Chemical reviews.

[54]  Jeehyun Kim,et al.  In vivo non-ionizing photoacoustic mapping of sentinel lymph nodes and bladders with ICG-enhanced carbon nanotubes , 2012, Physics in medicine and biology.

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

[56]  Lihong V. Wang,et al.  Photoacoustic Tomography: In Vivo Imaging from Organelles to Organs , 2012, Science.

[57]  Junjie Yao,et al.  Optical-resolution photoacoustic microscopy for volumetric and spectral analysis of histological and immunochemical samples. , 2014, Angewandte Chemie.

[58]  S. Nathanson,et al.  Sentinel lymph node metastases in cancer: causes, detection and their role in disease progression. , 2015, Seminars in cell & developmental biology.

[59]  Chulhong Kim,et al.  Biodegradable Nitrogen-Doped Carbon Nanodots for Non-Invasive Photoacoustic Imaging and Photothermal Therapy , 2016, Theranostics.

[60]  Homan Kang,et al.  PSA Detection with Femtomolar Sensitivity and a Broad Dynamic Range Using SERS Nanoprobes and an Area-Scanning Method , 2016 .

[61]  H. Cody,et al.  Clinical aspects of sentinel node biopsy , 2001, Breast Cancer Research.

[62]  A. Moore,et al.  Noninvasive MRI-SERS imaging in living mice using an innately bimodal nanomaterial. , 2011, ACS nano.

[63]  Chulhong Kim,et al.  Biodegradable Photonic Melanoidin for Theranostic Applications. , 2016, ACS nano.

[64]  Homan Kang,et al.  One-step synthesis of silver nanoshells with bumps for highly sensitive near-IR SERS nanoprobes. , 2014, Journal of materials chemistry. B.

[65]  M. Olivo,et al.  Single Molecule with Dual Function on Nanogold: Biofunctionalized Construct for In Vivo Photoacoustic Imaging and SERS Biosensing , 2015 .

[66]  Masakazu Toi,et al.  Comparison of the Indocyanine Green Fluorescence and Blue Dye Methods in Detection of Sentinel Lymph Nodes in Early-stage Breast Cancer , 2013, Annals of Surgical Oncology.

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

[68]  L. Newman,et al.  Sentinel lymph node biopsy for breast cancer: How many nodes are enough? , 2007, Journal of surgical oncology.

[69]  N. Khashab,et al.  Folding Up of Gold Nanoparticle Strings into Plasmonic Vesicles for Enhanced Photoacoustic Imaging. , 2015, Angewandte Chemie.

[70]  Eun Kyu Lee,et al.  SERS-based competitive immunoassay of troponin I and CK-MB markers for early diagnosis of acute myocardial infarction. , 2014, Chemical communications.

[71]  A. Luini,et al.  Sentinel Lymph Node Biopsy in Breast Cancer: Ten-Year Results of a Randomized Controlled Study , 2010, Annals of surgery.

[72]  De-gang Fu,et al.  Multiplex bioassays encoded by photonic crystal beads and SERS nanotags. , 2016, Nanoscale.

[73]  I. V. D. van der Ploeg,et al.  The Additional Value of SPECT/CT in Lymphatic Mapping in Breast Cancer and Melanoma , 2007, Journal of Nuclear Medicine.

[74]  Lihong V. Wang,et al.  Optical drug monitoring: photoacoustic imaging of nanosensors to monitor therapeutic lithium in vivo. , 2015, ACS nano.

[75]  Xin Cai,et al.  Multi-Scale Molecular Photoacoustic Tomography of Gene Expression , 2012, PloS one.