Label-Free Optical Imaging of Lymphatic Vessels Within Tissue Beds IN VIVO

Lymphatic vessels are a part of the circulatory system in vertebrates that maintain tissue fluid homeostasis and drain excess fluid and large cells that cannot easily find their way back into venous system. Due to the lack of noninvasive monitoring tools, lymphatic vessels are known as forgotten circulation. However, the lymphatic system plays an important role in diseases such as cancer and inflammatory conditions. In this paper, we start to briefly review the current existing methods for imaging lymphatic vessels, mostly involving dye/targeting cell injection. We then show the capability of optical coherence tomography (OCT) for label-free noninvasive in vivo imaging of lymph vessels and nodes. One of the advantages of using OCT over other imaging modalities is its ability to assess label-free blood flow perfusion that can be simultaneously observed along with lymphatic vessels for imaging the microcirculatory system within tissue beds. Imaging the microcirculatory system including blood and lymphatic vessels can be utilized for imaging and better understanding pathologic mechanisms and the treatment technique development in some critical diseases such as inflammation, malignant cancer angiogenesis, and metastasis.

[1]  E C Nice,et al.  Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF‐C/D receptor VEGFR‐3 , 2001, The EMBO journal.

[2]  Ruikang K. Wang,et al.  Theory, developments and applications of optical coherence tomography , 2005 .

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

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

[5]  PDZ interaction site in ephrinB2 is required for the remodeling of lymphatic vasculature. , 2005, Genes & development.

[6]  Kecheng Liu,et al.  A review on MR vascular image processing algorithms: acquisition and prefiltering: part I , 2002, IEEE Transactions on Information Technology in Biomedicine.

[7]  Kinmonth Jb,et al.  Lymphangiography in man; a method of outlining lymphatic trunks at operation. , 1952 .

[8]  Sanjiv S Gambhir,et al.  US imaging of tumor angiogenesis with microbubbles targeted to vascular endothelial growth factor receptor type 2 in mice. , 2008, Radiology.

[9]  Fan Zhang,et al.  Preclinical Lymphatic Imaging , 2011, Molecular Imaging and Biology.

[10]  Tatiana V. Petrova,et al.  Lymphangiogenesis in development and human disease , 2005, Nature.

[11]  Hisataka Kobayashi,et al.  Two-color lymphatic mapping using Ig-conjugated near infrared optical probes. , 2007, The Journal of investigative dermatology.

[12]  G. Kwant,et al.  Light-absorbing properties, stability, and spectral stabilization of indocyanine green. , 1976, Journal of applied physiology.

[13]  Rolf A. Brekken,et al.  Monitoring Response to Anticancer Therapy by Targeting Microbubbles to Tumor Vasculature , 2007, Clinical Cancer Research.

[14]  C. Baum,et al.  Normal Cutaneous Wound Healing: Clinical Correlation with Cellular and Molecular Events , 2005, Dermatologic surgery : official publication for American Society for Dermatologic Surgery [et al.].

[15]  西峯 康雄 Lymphangiography (癌の新しい診断(特集)) , 1966 .

[16]  P. Choyke,et al.  Imaging of the lymphatic system: new horizons. , 2006, Contrast media & molecular imaging.

[17]  Ruikang K. Wang,et al.  Depth-resolved imaging of capillary networks in retina and choroid using ultrahigh sensitive optical microangiography. , 2010, Optics letters.

[18]  William R Wagner,et al.  Ultrasound Imaging of Acute Cardiac Transplant Rejection With Microbubbles Targeted to Intercellular Adhesion Molecule-1 , 2003, Circulation.

[19]  Isabelle Bloch,et al.  A review of 3D vessel lumen segmentation techniques: Models, features and extraction schemes , 2009, Medical Image Anal..

[20]  J A Ramos-Vara,et al.  Technical Aspects of Immunohistochemistry , 2005, Veterinary pathology.

[21]  Ruikang K. Wang,et al.  Using ultrahigh sensitive optical microangiography to achieve comprehensive depth resolved microvasculature mapping for human retina. , 2011, Journal of biomedical optics.

[22]  Label-free 3D imaging of microstructure, blood, and lymphatic vessels within tissue beds in vivo. , 2012, Optics letters.

[23]  J. Fujimoto,et al.  Imaging needle for optical coherence tomography. , 2000, Optics letters.

[24]  Ruikang K. Wang,et al.  Optical microangiography provides an ability to monitor responses of cerebral microcirculation to hypoxia and hyperoxia in mice. , 2011, Journal of biomedical optics.

[25]  Ruikang K. Wang,et al.  Eigendecomposition-Based Clutter Filtering Technique for Optical Microangiography , 2011, IEEE Transactions on Biomedical Engineering.

[26]  Ruikang K. Wang,et al.  Three dimensional optical angiography. , 2007, Optics express.

[27]  Alejandro F. Frangi,et al.  Muliscale Vessel Enhancement Filtering , 1998, MICCAI.

[28]  M. Abbas,et al.  Who Is At Risk for Developing Chronic Anal Fistula or Recurrent Anal Sepsis After Initial Perianal Abscess? , 2009, Diseases of the colon and rectum.

[29]  D. Hammer,et al.  In vivo fluorescence imaging: a personal perspective. , 2009, Wiley interdisciplinary reviews. Nanomedicine and nanobiotechnology.

[30]  T. Petrova,et al.  Developmental and pathological lymphangiogenesis: from models to human disease , 2008, Histochemistry and Cell Biology.

[31]  Michael Detmar,et al.  An Important Role of Blood and Lymphatic Vessels in Inflammation and Allergy , 2013, Journal of allergy.

[32]  A. Luciani,et al.  Imaging the lymphatic system: possibilities and clinical applications , 2004, European Radiology.

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

[34]  J. Chang,et al.  Benign and malignant breast masses and axillary nodes: evaluation with echo-enhanced color power Doppler US. , 2001, Radiology.

[35]  Jan Grimm,et al.  An X-ray computed tomography imaging agent based on long-circulating bismuth sulphide nanoparticles , 2006, Nature materials.

[36]  Ruikang K. Wang,et al.  Tracking Dynamic Microvascular Changes during Healing after Complete Biopsy Punch on the Mouse Pinna Using Optical Microangiography , 2013, PloS one.

[37]  Ruikang K. Wang,et al.  Label-free optical lymphangiography: development of an automatic segmentation method applied to optical coherence tomography to visualize lymphatic vessels using Hessian filters , 2013, Journal of biomedical optics.

[38]  S. Hirakawa,et al.  Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[39]  R. Foster,et al.  The sentinel node in breast cancer--a multicenter validation study. , 1998, The New England journal of medicine.

[40]  M. Brezinski Optical Coherence Tomography: Principles and Applications , 2006 .

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

[42]  D. Jackson The lymphatics revisited: new perspectives from the hyaluronan receptor LYVE-1. , 2003, Trends in cardiovascular medicine.

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

[44]  Benjamin J Vakoc,et al.  Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging , 2009, Nature Medicine.

[45]  J. B. Kinmonth,et al.  Lymphangiography in man; a method of outlining lymphatic trunks at operation. , 1952, Clinical science.

[46]  Ruikang K. Wang,et al.  Three-dimensional high-resolution imaging of gold nanorods uptake in sentinel lymph nodes. , 2011, Nano letters.

[47]  T. Shaw,et al.  Wound repair at a glance , 2009, Journal of Cell Science.

[48]  G. Ripandelli,et al.  Optical coherence tomography. , 1998, Seminars in ophthalmology.

[49]  Y. Kono,et al.  Model to quantify lymph node enhancement on indirect sonographic lymphography. , 2004, AJR. American journal of roentgenology.

[50]  B. Misselwitz MR contrast agents in lymph node imaging. , 2006, European journal of radiology.

[51]  K. Wernecke,et al.  Differentiation of benign from malignant superficial lymphadenopathy: the role of high-resolution US. , 1992, Radiology.

[52]  J. B. Kinmonth,et al.  Lymphangiography; a technique for its clinical use in the lower limb. , 1955, British medical journal.

[53]  Ruikang K. Wang,et al.  In vivo volumetric imaging of microcirculation within human skin under psoriatic conditions using optical microangiography , 2011, Lasers in surgery and medicine.

[54]  Ruikang K. Wang,et al.  Highly sensitive imaging of renal microcirculation in vivo using ultrahigh sensitive optical microangiography , 2011, Biomedical optics express.

[55]  Ruikang K. Wang,et al.  Ultrahigh sensitive optical microangiography for in vivo imaging of microcirculations within human skin tissue beds. , 2010, Optics express.

[56]  A. Szuba,et al.  The third circulation: radionuclide lymphoscintigraphy in the evaluation of lymphedema. , 2003, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[57]  P. Muzzio,et al.  Ultrasonographic evaluation of superficial lymph node metastases in melanoma. , 1997, European journal of radiology.

[58]  Jacqueline D. Niles,et al.  Sentinel lymph node mapping of invasive urinary bladder cancer in animal models using invisible light. , 2007, European urology.

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

[60]  E. Tschachler,et al.  Angiosarcomas express mixed endothelial phenotypes of blood and lymphatic capillaries: podoplanin as a specific marker for lymphatic endothelium. , 1999, The American journal of pathology.

[61]  S. Nie,et al.  In vivo cancer targeting and imaging with semiconductor quantum dots , 2004, Nature Biotechnology.

[62]  Ruikang K. Wang,et al.  Three-dimensional optical micro-angiography maps directional blood perfusion deep within microcirculation tissue beds in vivo , 2007, Physics in medicine and biology.

[63]  K. Alitalo,et al.  Lymphangiogenesis: Molecular Mechanisms and Future Promise , 2010, Cell.

[64]  H. Partsch,et al.  The dermal lymphatics in lymphoedema visualized by indirect lymphography , 1984, The British journal of dermatology.

[65]  D. Patton,et al.  Whole-body lymphangioscintigraphy: preferred method for initial assessment of the peripheral lymphatic system. , 1989, Radiology.

[66]  P. Mortimer,et al.  Clinical assessment of human lymph flow using removal rate constants of interstitial macromolecules: a critical review of lymphoscintigraphy. , 2007, Lymphatic research and biology.

[67]  K. Alitalo,et al.  In vivo imaging of lymphatic vessels in development, wound healing, inflammation, and tumor metastasis , 2012, Proceedings of the National Academy of Sciences.

[68]  Vyacheslav Kalchenko,et al.  Label free in vivo laser speckle imaging of blood and lymph vessels. , 2012, Journal of biomedical optics.

[69]  Hisataka Kobayashi,et al.  In vivo real-time, multicolor, quantum dot lymphatic imaging. , 2009, The Journal of investigative dermatology.

[70]  G. V. von Schulthess,et al.  Staging of non-small-cell lung cancer with integrated positron-emission tomography and computed tomography. , 2003, The New England journal of medicine.

[71]  A. Chatziioannou,et al.  Adenovirus-mediated gene expression imaging to directly detect sentinel lymph node metastasis of prostate cancer , 2008, Nature Medicine.

[72]  M. Detmar,et al.  Molecular mechanisms and imaging of lymphatic metastasis. , 2013, Experimental cell research.

[73]  Ruikang K Wang,et al.  Three-dimensional optical imaging of microvascular networks within intact lymph node in vivo. , 2010, Journal of biomedical optics.

[74]  Guillermo Oliver,et al.  Lymphatic vasculature development , 2004, Nature Reviews Immunology.

[75]  Quan-Yong Luo,et al.  The role of radionuclide lymphoscintigraphy in extremity lymphedema , 2006, Annals of nuclear medicine.

[76]  A. Tangoku,et al.  Visualization of Breast Lymphatic Pathways With an Indirect Computed Tomography Lymphography Using a Nonionic Monometric Contrast Medium Iopamidol: Preliminary Results , 2003, Investigative radiology.

[77]  Baris Turkbey,et al.  New approaches to lymphatic imaging. , 2009, Lymphatic research and biology.

[78]  S. Duffy,et al.  Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[79]  K. Alitalo,et al.  Molecular regulation of angiogenesis and lymphangiogenesis , 2007, Nature Reviews Molecular Cell Biology.