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Current Status of Optical Imaging for Evaluating Lymph Nodes and Lymphatic System

  • Lee, Eun Seong (Department of Nuclear Medicine, Research Institute and Hospital, National Cancer Center) ;
  • Kim, Tae Sung (Department of Nuclear Medicine, Research Institute and Hospital, National Cancer Center) ;
  • Kim, Seok-Ki (Department of Nuclear Medicine, Research Institute and Hospital, National Cancer Center)
  • Received : 2014.06.06
  • Accepted : 2014.07.30
  • Published : 2015.02.01

Abstract

Optical imaging techniques use visual and near infrared rays. Despite their considerably poor penetration depth, they are widely used due to their safe and intuitive properties and potential for intraoperative usage. Optical imaging techniques have been actively investigated for clinical imaging of lymph nodes and lymphatic system. This article summarizes a variety of optical tracers and techniques used for lymph node and lymphatic imaging, and reviews their clinical applications. Emerging new optical imaging techniques and their potential are also described.

Keywords

Acknowledgement

Grant : 유방암 유방보존치료술용 근적외선형광기반 미세유방병변 국소화 및 감시림프절 표지 임상기술 개발.

References

  1. van der Vorst JR, Schaafsma BE, Hutteman M, Verbeek FP, Liefers GJ, Hartgrink HH, et al. Near-infrared fluorescence-guided resection of colorectal liver metastases. Cancer 2013;119:3411-3418 https://doi.org/10.1002/cncr.28203
  2. Vellekoop IM, Aegerter CM. Focusing light through living tissue. Proc SPIE 2010;7554:755430 https://doi.org/10.1117/12.841159
  3. ASGE Technology Committee, Song LM, Banerjee S, Desilets D, Diehl DL, Farraye FA, et al. Autofluorescence imaging. Gastrointest Endosc 2011;73:647-650 https://doi.org/10.1016/j.gie.2010.11.006
  4. Yoshida Y, Goda K, Tajiri H, Urashima M, Yoshimura N, Kato T. Assessment of novel endoscopic techniques for visualizing superficial esophageal squamous cell carcinoma: autofluorescence and narrow-band imaging. Dis Esophagus 2009;22:439-446 https://doi.org/10.1111/j.1442-2050.2008.00925.x
  5. Suzuki H, Saito Y, Ikehara H, Oda I. Evaluation of visualization of squamous cell carcinoma of esophagus and pharynx using an autofluorescence imaging videoendoscope system. J Gastroenterol Hepatol 2009;24:1834-1839 https://doi.org/10.1111/j.1440-1746.2009.05941.x
  6. Uedo N, Iishi H, Tatsuta M, Yamada T, Ogiyama H, Imanaka K, et al. A novel videoendoscopy system by using autofluorescence and reflectance imaging for diagnosis of esophagogastric cancers. Gastrointest Endosc 2005;62:521-528 https://doi.org/10.1016/j.gie.2005.06.031
  7. Falk GW. Autofluorescence endoscopy. Gastrointest Endosc Clin N Am 2009;19:209-220 https://doi.org/10.1016/j.giec.2009.02.004
  8. Berlier JE, Rothe A, Buller G, Bradford J, Gray DR, Filanoski BJ, et al. Quantitative comparison of long-wavelength Alexa Fluor dyes to Cy dyes: fluorescence of the dyes and their bioconjugates. J Histochem Cytochem 2003;51:1699-1712 https://doi.org/10.1177/002215540305101214
  9. Zhang F, Niu G, Lu G, Chen X. Preclinical lymphatic imaging. Mol Imaging Biol 2011;13:599-612 https://doi.org/10.1007/s11307-010-0421-y
  10. Hama Y, Koyama Y, Urano Y, Choyke PL, Kobayashi H. Two-color lymphatic mapping using Ig-conjugated near infrared optical probes. J Invest Dermatol 2007;127:2351-2356 https://doi.org/10.1038/sj.jid.5700892
  11. McElroy M, Hayashi K, Garmy-Susini B, Kaushal S, Varner JA, Moossa AR, et al. Fluorescent LYVE-1 antibody to image dynamically lymphatic trafficking of cancer cells in vivo. J Surg Res 2009;151:68-73 https://doi.org/10.1016/j.jss.2007.12.769
  12. Alford R, Simpson HM, Duberman J, Hill GC, Ogawa M, Regino C, et al. Toxicity of organic fluorophores used in molecular imaging: literature review. Mol Imaging 2009;8:341-354
  13. Fox IJ, Brooker LG, Heseltine DW, Essex HE, Wood EH. A tricarbocyanine dye for continuous recording of dilution curves in whole blood independent of variations in blood oxygen saturation. Proc Staff Meet Mayo Clin 1957;32:478-484
  14. Bjerregaard J, Pandia MP, Jaffe RA. Occurrence of severe hypotension after indocyanine green injection during the intraoperative period. A&A Case Reports 2013;1:26-30 https://doi.org/10.1097/ACC.0b013e3182933c12
  15. Benya R, Quintana J, Brundage B. Adverse reactions to indocyanine green: a case report and a review of the literature. Cathet Cardiovasc Diagn 1989;17:231-233 https://doi.org/10.1002/ccd.1810170410
  16. Jung SY, Kim SK, Kim SW, Kwon Y, Lee ES, Kang HS, et al. Comparison of sentinel lymph node biopsy guided by the multimodal method of indocyanine green fluorescence, radioisotope, and blue dye versus the radioisotope method in breast cancer: a randomized controlled trial. Ann Surg Oncol 2014;21:1254-1259 https://doi.org/10.1245/s10434-013-3437-0
  17. Motomura K, Inaji H, Komoike Y, Kasugai T, Noguchi S, Koyama H. Sentinel node biopsy guided by indocyanine green dye in breast cancer patients. Jpn J Clin Oncol 1999;29:604-607 https://doi.org/10.1093/jjco/29.12.604
  18. Kitai T, Inomoto T, Miwa M, Shikayama T. Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer. Breast Cancer 2005;12:211-215 https://doi.org/10.2325/jbcs.12.211
  19. Chan WC, Maxwell DJ, Gao X, Bailey RE, Han M, Nie S. Luminescent quantum dots for multiplexed biological detection and imaging. Curr Opin Biotechnol 2002;13:40-46 https://doi.org/10.1016/S0958-1669(02)00282-3
  20. Michalet X, Pinaud FF, Bentolila LA, Tsay JM, Doose S, Li JJ, et al. Quantum dots for live cells, in vivo imaging, and diagnostics. Science 2005;307:538-544 https://doi.org/10.1126/science.1104274
  21. Hama Y, Koyama Y, Urano Y, Choyke PL, Kobayashi H. Simultaneous two-color spectral fluorescence lymphangiography with near infrared quantum dots to map two lymphatic flows from the breast and the upper extremity. Breast Cancer Res Treat 2007;103:23-28 https://doi.org/10.1007/s10549-006-9347-0
  22. Kosaka N, Ogawa M, Sato N, Choyke PL, Kobayashi H. In vivo real-time, multicolor, quantum dot lymphatic imaging. J Invest Dermatol 2009;129:2818-2822 https://doi.org/10.1038/jid.2009.161
  23. Alivisatos AP, Gu W, Larabell C. Quantum dots as cellular probes. Annu Rev Biomed Eng 2005;7:55-76 https://doi.org/10.1146/annurev.bioeng.7.060804.100432
  24. Gao X, Yang L, Petros JA, Marshall FF, Simons JW, Nie S. In vivo molecular and cellular imaging with quantum dots. Curr Opin Biotechnol 2005;16:63-72 https://doi.org/10.1016/j.copbio.2004.11.003
  25. Hardman R. A toxicologic review of quantum dots: toxicity depends on physicochemical and environmental factors. Environ Health Perspect 2006;114:165-172 https://doi.org/10.1289/ehp.8284
  26. Nahrendorf M, Keliher E, Marinelli B, Waterman P, Feruglio PF, Fexon L, et al. Hybrid PET-optical imaging using targeted probes. Proc Natl Acad Sci U S A 2010;107:7910-7915 https://doi.org/10.1073/pnas.0915163107
  27. Cai W, Chen K, Li ZB, Gambhir SS, Chen X. Dual-function probe for PET and near-infrared fluorescence imaging of tumor vasculature. J Nucl Med 2007;48:1862-1870 https://doi.org/10.2967/jnumed.107.043216
  28. Culver J, Akers W, Achilefu S. Multimodality molecular imaging with combined optical and SPECT/PET modalities. J Nucl Med 2008;49:169-172 https://doi.org/10.2967/jnumed.107.043331
  29. Koyama Y, Talanov VS, Bernardo M, Hama Y, Regino CA, Brechbiel MW, et al. A dendrimer-based nanosized contrast agent dual-labeled for magnetic resonance and optical fluorescence imaging to localize the sentinel lymph node in mice. J Magn Reson Imaging 2007;25:866-871 https://doi.org/10.1002/jmri.20852
  30. Abe H, Mori T, Umeda T, Tanaka M, Kawai Y, Shimizu T, et al. Indocyanine green fluorescence imaging system for sentinel lymph node biopsies in early breast cancer patients. Surg Today 2011;41:197-202 https://doi.org/10.1007/s00595-009-4254-8
  31. Sharma R, Wang W, Rasmussen JC, Joshi A, Houston JP, Adams KE, et al. Quantitative imaging of lymph function. Am J Physiol Heart Circ Physiol 2007;292:H3109-H3118 https://doi.org/10.1152/ajpheart.01223.2006
  32. Sampath L, Wang W, Sevick-Muraca EM. Near infrared fluorescent optical imaging for nodal staging. J Biomed Opt 2008;13:041312 https://doi.org/10.1117/1.2953498
  33. Sampath L, Kwon S, Hall MA, Price RE, Sevick-Muraca EM. Detection of Cancer Metastases with a Dual-labeled Near-Infrared/Positron Emission Tomography Imaging Agent. Transl Oncol 2010;3:307-317 https://doi.org/10.1593/tlo.10139
  34. Hall MA, Kwon S, Robinson H, Lachance PA, Azhdarinia A, Ranganathan R, et al. Imaging prostate cancer lymph node metastases with a multimodality contrast agent. Prostate 2012;72:129-146 https://doi.org/10.1002/pros.21413
  35. Song KH, Stoica G, Wang LV. In vivo three-dimensional photoacoustic tomography of a whole mouse head. Opt Lett 2006;31:2453-2455 https://doi.org/10.1364/OL.31.002453
  36. Wang X, Pang Y, Ku G, Xie X, Stoica G, Wang LV. Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain. Nat Biotechnol 2003;21:803-806 https://doi.org/10.1038/nbt839
  37. Song KH, Stein EW, Margenthaler JA, Wang LV. Noninvasive photoacoustic identification of sentinel lymph nodes containing methylene blue in vivo in a rat model. J Biomed Opt 2008;13:054033 https://doi.org/10.1117/1.2976427
  38. Erpelding TN, Garcia-Uribe A, Krumholz A, Ke H, Maslov K, Appleton C, et al. A dual-modality photoacoustic and ultrasound imaging system for noninvasive sentinel lymph node detection: preliminary clinical results. Proc SPIE 2014;8943:894359 https://doi.org/10.1117/12.2040475
  39. Corlu A, Choe R, Durduran T, Rosen MA, Schweiger M, Arridge SR, et al. Three-dimensional in vivo fluorescence diffuse optical tomography of breast cancer in humans. Opt Express 2007;15:6696-6716 https://doi.org/10.1364/OE.15.006696
  40. Jain R, Dandekar P, Patravale V. Diagnostic nanocarriers for sentinel lymph node imaging. J Control Release 2009;138:90-102 https://doi.org/10.1016/j.jconrel.2009.05.010
  41. Morton DL, Wen DR, Wong JH, Economou JS, Cagle LA, Storm FK, et al. Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg 1992;127:392-399 https://doi.org/10.1001/archsurg.1992.01420040034005
  42. Giuliano AE, Kirgan DM, Guenther JM, Morton DL. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 1994;220:391-398; discussion 398-401 https://doi.org/10.1097/00000658-199409000-00015
  43. Krag DN, Weaver DL, Alex JC, Fairbank JT. Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol 1993;2:335-339; discussion 340 https://doi.org/10.1016/0960-7404(93)90064-6
  44. Sondak VK, Wong SL, Gershenwald JE, Thompson JF. Evidence-based clinical practice guidelines on the use of sentinel lymph node biopsy in melanoma. Am Soc Clin Oncol Educ Book 2013. http://dx.doi.org/10.1200/EdBook_AM.2013.33.e320
  45. Lyman GH, Giuliano AE, Somerfield MR, Benson AB 3rd, Bodurka DC, Burstein HJ, et al. American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. J Clin Oncol 2005;23:7703-7720 https://doi.org/10.1200/JCO.2005.08.001
  46. Straver ME, Meijnen P, van Tienhoven G, van de Velde CJ, Mansel RE, Bogaerts J, et al. Sentinel node identification rate and nodal involvement in the EORTC 10981-22023 AMAROS trial. Ann Surg Oncol 2010;17:1854-1861 https://doi.org/10.1245/s10434-010-0945-z
  47. Xiong L, Gazyakan E, Yang W, Engel H, Hunerbein M, Kneser U, et al. Indocyanine green fluorescence-guided sentinel node biopsy: a meta-analysis on detection rate and diagnostic performance. Eur J Surg Oncol 2014;40:843-849 https://doi.org/10.1016/j.ejso.2014.02.228
  48. Verbeek FP, Troyan SL, Mieog JS, Liefers GJ, Moffitt LA, Rosenberg M, et al. Near-infrared fluorescence sentinel lymph node mapping in breast cancer: a multicenter experience. Breast Cancer Res Treat 2014;143:333-342 https://doi.org/10.1007/s10549-013-2802-9
  49. Jain V, Phillips BT, Conkling N, Pameijer C. Sentinel lymph node detection using laser-assisted indocyanine green dye lymphangiography in patients with melanoma. Int J Surg Oncol 2013;2013:904214
  50. Crane LM, Themelis G, Arts HJ, Buddingh KT, Brouwers AH, Ntziachristos V, et al. Intraoperative near-infrared fluorescence imaging for sentinel lymph node detection in vulvar cancer: first clinical results. Gynecol Oncol 2011;120:291-295 https://doi.org/10.1016/j.ygyno.2010.10.009
  51. Miyashiro I, Hiratsuka M, Kishi K, Takachi K, Yano M, Takenaka A, et al. Intraoperative diagnosis using sentinel node biopsy with indocyanine green dye in gastric cancer surgery: an institutional trial by experienced surgeons. Ann Surg Oncol 2013;20:542-546 https://doi.org/10.1245/s10434-012-2608-8
  52. Hirche C, Murawa D, Mohr Z, Kneif S, Hunerbein M. ICG fluorescence-guided sentinel node biopsy for axillary nodal staging in breast cancer. Breast Cancer Res Treat 2010;121:373-378 https://doi.org/10.1007/s10549-010-0760-z
  53. Hojo T, Nagao T, Kikuyama M, Akashi S, Kinoshita T. Evaluation of sentinel node biopsy by combined fluorescent and dye method and lymph flow for breast cancer. Breast 2010;19:210-213 https://doi.org/10.1016/j.breast.2010.01.014
  54. Tagaya N, Nakagawa A, Abe A, Iwasaki Y, Kubota K. Non-invasive identification of sentinel lymph nodes using indocyanine green fluorescence imaging in patients with breast cancer. Open Surg Oncol J 2010;2:71-74 https://doi.org/10.2174/1876504101002020071
  55. Aoyama K, Kamio T, Ohchi T, Nishizawa M, Kameoka S. Sentinel lymph node biopsy for breast cancer patients using fluorescence navigation with indocyanine green. World J Surg Oncol 2011;9:157 https://doi.org/10.1186/1477-7819-9-157
  56. Hirche C, Mohr Z, Kneif S, Murawa D, Hunerbein M. High rate of solitary sentinel node metastases identification by fluorescence-guided lymphatic imaging in breast cancer. J Surg Oncol 2012;105:162-166 https://doi.org/10.1002/jso.22075
  57. Takeuchi M, Sugie T, Abdelazeem K, Kato H, Shinkura N, Takada M, et al. Lymphatic mapping with fluorescence navigation using indocyanine green and axillary surgery in patients with primary breast cancer. Breast J 2012;18:535-541 https://doi.org/10.1111/tbj.12004
  58. Hirano A, Kamimura M, Ogura K, Kim N, Hattori A, Setoguchi Y, et al. A comparison of indocyanine green fluorescence imaging plus blue dye and blue dye alone for sentinel node navigation surgery in breast cancer patients. Ann Surg Oncol 2012;19:4112-4116 https://doi.org/10.1245/s10434-012-2478-0
  59. Kitai T, Kawashima M. Transcutaneous detection and direct approach to the sentinel node using axillary compression technique in ICG fluorescence-navigated sentinel node biopsy for breast cancer. Breast Cancer 2012;19:343-348 https://doi.org/10.1007/s12282-011-0286-1
  60. Wishart GC, Loh SW, Jones L, Benson JR. A feasibility study (ICG-10) of indocyanine green (ICG) fluorescence mapping for sentinel lymph node detection in early breast cancer. Eur J Surg Oncol 2012;38:651-656 https://doi.org/10.1016/j.ejso.2012.05.007
  61. Sugie T, Sawada T, Tagaya N, Kinoshita T, Yamagami K, Suwa H, et al. Comparison of the indocyanine green fluorescence and blue dye methods in detection of sentinel lymph nodes in early-stage breast cancer. Ann Surg Oncol 2013;20:2213-2218 https://doi.org/10.1245/s10434-013-2890-0
  62. Ballardini B, Santoro L, Sangalli C, Gentilini O, Renne G, Lissidini G, et al. The indocyanine green method is equivalent to the 99mTc-labeled radiotracer method for identifying the sentinel node in breast cancer: a concordance and validation study. Eur J Surg Oncol 2013;39:1332-1336 https://doi.org/10.1016/j.ejso.2013.10.004
  63. Campisi C, Bellini C, Campisi C, Accogli S, Bonioli E, Boccardo F. Microsurgery for lymphedema: clinical research and long-term results. Microsurgery 2010;30:256-260
  64. Mihara M, Hara H, Araki J, Kikuchi K, Narushima M, Yamamoto T, et al. Indocyanine green (ICG) lymphography is superior to lymphoscintigraphy for diagnostic imaging of early lymphedema of the upper limbs. PLoS One 2012;7:e38182 https://doi.org/10.1371/journal.pone.0038182
  65. Mihara M, Hara H, Narushima M, Todokoro T, Iida T, Ohtsu H, et al. Indocyanine green lymphography is superior to lymphoscintigraphy in imaging diagnosis of secondary lymphedema of the lower limbs. J Vasc Surg Venous Lymphat Disord 2013;1:194-201 https://doi.org/10.1016/j.jvsv.2012.07.011
  66. Li C, Wang LV. Photoacoustic tomography and sensing in biomedicine. Phys Med Biol 2009;54:R59-R97 https://doi.org/10.1088/0031-9155/54/19/R01
  67. Tagaya N, Aoyagi H, Nakagawa A, Abe A, Iwasaki Y, Tachibana M, et al. A novel approach for sentinel lymph node identification using fluorescence imaging and image overlay navigation surgery in patients with breast cancer. World J Surg 2011;35:154-158 https://doi.org/10.1007/s00268-010-0811-y

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