In vivo, noninvasive, label-free detection and eradication of circulating metastatic melanoma cells using two-color photoacoustic flow cytometry with a diode laser.

The circulating tumor cell (CTC) count has been shown as a prognostic marker for metastasis development. However, its clinical utility for metastasis prevention remains unclear, because metastases may already be present at the time of initial diagnosis with existing assays. Their sensitivity ex vivo is limited by a small blood sample volume, whereas in vivo examination of larger blood volumes may be clinically restricted by the toxicity of labels used for targeting of CTCs. We introduce a method for in vivo photoacoustic blood cancer testing with a high-pulse-repetition-rate diode laser that, when applied to melanoma, is free of this limitation. It uses the overexpression of melanin clusters as intrinsic, spectrally-specific cancer markers and signal amplifiers, thus providing higher photoacoustic contrast of melanoma cells compared with a blood background. In tumor-bearing mouse models and melanoma-spiked human blood samples, we showed a sensitivity level of 1 CTC/mL with the potential to improve this sensitivity 10(3)-fold in humans in vivo, which is impossible with existing assays. Additional advances of this platform include decreased background signals from blood through changes in its oxygenation, osmolarity, and hematocrit within physiologic norms, assessment of CTCs in deep vessels, in vivo CTC enrichment, and photoacoustic-guided photothermal ablation of CTCs in the bloodstream. These advances make feasible the early diagnosis of melanoma during the initial parallel progression of primary tumor and CTCs, and laser blood purging using noninvasive or hemodialysis-like schematics for the prevention of metastasis.

[1]  Valery V Tuchin,et al.  In vivo photothermal flow cytometry: Imaging and detection of individual cells in blood and lymph flow , 2006, Journal of cellular biochemistry.

[2]  Valery V Tuchin,et al.  In vivo photoacoustic flow cytometry for monitoring of circulating single cancer cells and contrast agents. , 2006, Optics letters.

[3]  R. Kerbel,et al.  Highly pigmented human melanoma variant which metastasizes widely in nude mice, including to skin and brain. , 1988, Cancer research.

[4]  A. Oseroff,et al.  Irradiation of pigmented melanoma cells with high intensity pulsed radiation generates acoustic waves and kills cells , 1990, Lasers in surgery and medicine.

[5]  J. Weinstein,et al.  Biomarkers in Cancer Staging, Prognosis and Treatment Selection , 2005, Nature Reviews Cancer.

[6]  V. Zharov,et al.  Photothermal imaging of nanoparticles and cells , 2005, IEEE Journal of Selected Topics in Quantum Electronics.

[7]  Alessandro Ambrosi,et al.  The Prognostic Value of Circulating Tumor Cells in Patients with Melanoma: A Systematic Review and Meta-analysis , 2006, Clinical Cancer Research.

[8]  D. Prough,et al.  Multiwavelength optoacoustic system for noninvasive monitoring of cerebral venous oxygenation: a pilot clinical test in the internal jugular vein. , 2006, Optics letters.

[9]  P. Płonka,et al.  Melanin synthesis in microorganisms--biotechnological and medical aspects. , 2006, Acta biochimica Polonica.

[10]  Vladimir P Zharov,et al.  Quantum dots as multimodal photoacoustic and photothermal contrast agents. , 2008, Nano letters.

[11]  John A Viator,et al.  Photoacoustic detection of metastatic melanoma cells in the human circulatory system. , 2006, Optics letters.

[12]  V. Zharov,et al.  Infrared imaging of subcutaneous veins , 2004, Lasers in surgery and medicine.

[13]  E. A. Wachter,et al.  Treatment of Murine Cutaneous Melanoma with Near Infrared Light¶ , 2002 .

[14]  Stanley E. Charm,et al.  Blood flow and microcirculation , 1974 .

[15]  R. Marais,et al.  Melanoma biology and new targeted therapy , 2007, Nature.

[16]  V. Tuchin,et al.  Photothermal flow cytometry in vitro for detection and imaging of individual moving cells , 2007, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[17]  Myles G Cockburn,et al.  Increasing burden of melanoma in the United States. , 2009, The Journal of investigative dermatology.

[18]  Fred P. Seeber,et al.  OP-TEC national center for optics and photonics education and ANSI Z136.5 American National Standard for the safe use of lasers in educational institutions – How they will work together to improve laser safety in educational institutions , 2009 .

[19]  Tayyaba Hasan,et al.  Flow Cytometry : A New Method for Enumerating Circulating Cancer Cells , 2004 .

[20]  W. Tolleson Human Melanocyte Biology, Toxicology, and Pathology , 2005, Journal of environmental science and health. Part C, Environmental carcinogenesis & ecotoxicology reviews.

[21]  R. Halaban Pigmentation in melanomas: changes manifesting underlying oncogenic and metabolic activities. , 2002, Oncology research.

[22]  M. Nolte,et al.  Effects of fluorescent and nonfluorescent tracing methods on lymphocyte migration in vivo , 2004, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[23]  Vladimir P. Zharov,et al.  Photothermal and accompanied phenomena of selective nanophotothermolysis with gold nanoparticles and laser pulses , 2008 .

[24]  Martin A Weinstock,et al.  Cutaneous melanoma: public health approach to early detection , 2006, Dermatologic therapy.

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

[26]  Valery V Tuchin,et al.  Photoacoustic flow cytometry: principle and application for real-time detection of circulating single nanoparticles, pathogens, and contrast dyes in vivo. , 2007, Journal of biomedical optics.

[27]  Thomas Kelly,et al.  Synergistic enhancement of selective nanophotothermolysis with gold nanoclusters: Potential for cancer therapy , 2005, Lasers in surgery and medicine.

[28]  B. Thiers,et al.  Identification of cells initiating human melanomas , 2009 .

[29]  A. Roggan,et al.  Optical Properties of Circulating Human Blood in the Wavelength Range 400-2500 nm. , 1999, Journal of biomedical optics.

[30]  Charles P. Lin,et al.  Selective cell killing by microparticle absorption of pulsed laser radiation , 1999 .

[31]  S. Digumarthy,et al.  Isolation of rare circulating tumour cells in cancer patients by microchip technology , 2007, Nature.

[32]  Vladimir P Zharov,et al.  Self-assembling nanoclusters in living systems: application for integrated photothermal nanodiagnostics and nanotherapy. , 2005, Nanomedicine : nanotechnology, biology, and medicine.

[33]  Brigitte Rack,et al.  Detection of Circulating Tumor Cells in Peripheral Blood of Patients with Metastatic Breast Cancer: A Validation Study of the CellSearch System , 2007, Clinical Cancer Research.

[34]  Peter Kuhn,et al.  A rare-cell detector for cancer. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[35]  I. Fidler,et al.  Metastasis: Quantitative Analysis of Distribution and Fate of Tumor Emboli Labeled With 125I-5-Iodo-2′ -deoxyuridine , 1970 .

[36]  Xu Xiao Photoacoustic imaging in biomedicine , 2008 .

[37]  Charles P. Lin,et al.  In vivo flow cytometer for real-time detection and quantification of circulating cells. , 2004, Optics letters.

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

[39]  G. Nash,et al.  Effects of fluorescent dyes on selectin and integrin-mediated stages of adhesion and migration of flowing leukocytes. , 2000, Journal of immunological methods.

[40]  Philip S Low,et al.  In vivo quantitation of rare circulating tumor cells by multiphoton intravital flow cytometry , 2007, Proceedings of the National Academy of Sciences.

[41]  A. V. Alekseeva,et al.  Preparation and optical scattering characterization of gold nanorods and their application to a dot-immunogold assay. , 2005, Applied optics.

[42]  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.

[43]  Y. Huang,et al.  Oral delivery of tumor‐targeting Salmonella for cancer therapy in murine tumor models , 2007, Cancer science.

[44]  E. Antecka,et al.  Identification of circulating malignant cells and its correlation with prognostic factors and treatment in uveal melanoma. A prospective longitudinal study , 2007, Eye.

[45]  Alison Abbott,et al.  Cancer: The root of the problem , 2006, Nature.

[46]  P. Schludermann,et al.  The Root of the Problem , 2007, Science.

[47]  Xunbin Wei,et al.  Selective uptake of indocyanine green by reticulocytes in circulation. , 2003, Investigative ophthalmology & visual science.

[48]  G. Woude,et al.  Apoptosis and melanogenesis in human melanoma cells induced by anthrax lethal factor inactivation of mitogen-activated protein kinase kinase , 2002, Proceedings of the National Academy of Sciences of the United States of America.