Abstract

The aim of this study was to examine neurotoxicity indocyanine green (ICG). We assessed viability of primary cerebellar granule cell culture (CGC) exposed to ICG to test two mechanisms that could be the first triggers causing neuronal toxicity: imbalance in calcium homeostasis and the degree of oligomerization of ICG molecules. We have observed this imbalance in CGC after exposure to 75-125μΜ ICG and dose and application sequence dependent protective effect of Gadovist on surviving neurons in vitro when used with ICG. Spectroscopic studies suggest the major cause of toxicity of the ICG is connected with oligomers formation. ICG at concentration of 25 μM (which is about 4 times higher than the highest concentration of ICG in the brain applied in in-vivo human studies) is not neurotoxic in the cell culture.

© 2014 Optical Society of America

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2014 (2)

D. Milej, A. Gerega, M. Kacprzak, P. Sawosz, W. Weigl, R. Maniewski, and A. Liebert, “Time-resolved multi-channel optical system for assessment of brain oxygenation and perfusion by monitoring of diffuse reflectance and fluorescence,” Opto-Electron. Rev. 22(1), 55–67 (2014).
[CrossRef]

W. Weigl, D. Milej, A. Gerega, B. Toczylowska, M. Kacprzak, P. Sawosz, M. Botwicz, R. Maniewski, E. Mayzner-Zawadzka, and A. Liebert, “Assessment of cerebral perfusion in post-traumatic brain injury patients with the use of ICG-bolus tracking method,” Neuroimage 85(Pt 1), 555–565 (2014).
[CrossRef] [PubMed]

2013 (1)

H. Obrig, “NIRS in clinical neurology - a 'promising' tool?” Neuroimage 85, 535–546 (2013).
[PubMed]

2012 (4)

C. Wack, T. Steger-Hartmann, L. Mylecraine, and R. Hofmeister, “Toxicological safety evaluation of gadobutrol,” Invest. Radiol. 47(11), 611–623 (2012).
[CrossRef] [PubMed]

A. Gerega, D. Milej, W. Weigl, M. Botwicz, N. Zolek, M. Kacprzak, W. Wierzejski, B. Toczylowska, E. Mayzner-Zawadzka, R. Maniewski, and A. Liebert, “Multiwavelength time-resolved detection of fluorescence during the inflow of indocyanine green into the adult’s brain,” J. Biomed. Opt. 17(8), 087001 (2012).
[CrossRef] [PubMed]

D. Milej, A. Gerega, N. Zołek, W. Weigl, M. Kacprzak, P. Sawosz, J. Mączewska, K. Fronczewska, E. Mayzner-Zawadzka, L. Królicki, R. Maniewski, and A. Liebert, “Time-resolved detection of fluorescent light during inflow of ICG to the brain-a methodological study,” Phys. Med. Biol. 57(20), 6725–6742 (2012).
[CrossRef] [PubMed]

E. Ziemińska, A. Stafiej, B. Toczyłowska, and J. W. Lazarewicz, “Synergistic neurotoxicity of oxygen-glucose deprivation and tetrabromobisphenol A in vitro: role of oxidative stress,” Pharmacol. Rep. 64(5), 1166–1178 (2012).
[PubMed]

2011 (2)

A. Liebert, P. Sawosz, D. Milej, M. Kacprzak, W. Weigl, M. Botwicz, J. Maczewska, K. Fronczewska, E. Mayzner-Zawadzka, L. Królicki, and R. Maniewski, “Assessment of inflow and washout of indocyanine green in the adult human brain by monitoring of diffuse reflectance at large source-detector separation,” J. Biomed. Opt. 16(4), 046011 (2011).
[CrossRef] [PubMed]

H. Obrig and J. Steinbrink, “Non-invasive optical imaging of stroke,” Philos. Trans. A Math, Phys. Eng Sci. 369(1955), 4470–4494 (2011).
[CrossRef]

2010 (5)

S. Noura, M. Ohue, Y. Seki, K. Tanaka, M. Motoori, K. Kishi, I. Miyashiro, H. Ohigashi, M. Yano, O. Ishikawa, and Y. Miyamoto, “Feasibility of a lateral region sentinel node biopsy of lower rectal cancer guided by indocyanine green using a near-infrared camera system,” Ann. Surg. Oncol. 17(1), 144–151 (2010).
[CrossRef] [PubMed]

Y. Tajima, M. Murakami, K. Yamazaki, Y. Masuda, M. Kato, A. Sato, S. Goto, K. Otsuka, T. Kato, and M. Kusano, “Sentinel node mapping guided by indocyanine green fluorescence imaging during laparoscopic surgery in gastric cancer,” Ann. Surg. Oncol. 17(7), 1787–1793 (2010).
[CrossRef] [PubMed]

M. Diop, K. M. Tichauer, J. T. Elliott, M. Migueis, T. Y. Lee, and K. St Lawrence, “Comparison of time-resolved and continuous-wave near-infrared techniques for measuring cerebral blood flow in piglets,” J. Biomed. Opt. 15(5), 057004 (2010).
[CrossRef] [PubMed]

E. Zieminska, B. Toczylowska, A. Stafiej, and J. W. Lazarewicz, “Low molecular weight thiols reduce thimerosal neurotoxicity in vitro: modulation by proteins,” Toxicology 276(3), 154–163 (2010).
[CrossRef] [PubMed]

X. Feng, Q. Xia, L. Yuan, X. Yang, and K. Wang, “Impaired mitochondrial function and oxidative stress in rat cortical neurons: implications for gadolinium-induced neurotoxicity,” Neurotoxicology 31(4), 391–398 (2010).
[CrossRef] [PubMed]

2009 (12)

T. Ishizawa, N. Fukushima, J. Shibahara, K. Masuda, S. Tamura, T. Aoki, K. Hasegawa, Y. Beck, M. Fukayama, and N. Kokudo, “Real-time identification of liver cancers by using indocyanine green fluorescent imaging,” Cancer 115(11), 2491–2504 (2009).
[CrossRef] [PubMed]

M. Reekers, M. J. Simon, F. Boer, R. A. Mooren, J. W. van Kleef, A. Dahan, and J. Vuyk, “Cardiovascular monitoring by pulse dye densitometry or arterial indocyanine green dilution,” Anesth. Analg. 109(2), 441–446 (2009).
[CrossRef] [PubMed]

S. Balaiya, V. S. Brar, R. K. Murthy, and K. Chalam, “Effects of Indocyanine green on cultured retinal ganglion cells in-vitro,” BMC Res. Notes 2(1), 236 (2009).
[CrossRef] [PubMed]

T. Handa, R. G. Katare, S. Sasaguri, and T. Sato, “Preliminary experience for the evaluation of the intraoperative graft patency with real color charge-coupled device camera system: an advanced device for simultaneous capturing of color and near-infrared images during coronary artery bypass graft,” Interact. Cardiovasc. Thorac. Surg. 9(2), 150–154 (2009).
[CrossRef] [PubMed]

B. D. Killory, P. Nakaji, L. F. Gonzales, F. A. Ponce, S. D. Wait, and R. F. Spetzler, “Prospective evaluation of surgical microscope-integrated intraoperative near-infrared indocyanine green angiography during cerebral arteriovenous malformation surgery,” Neurosurgery 65(3), 456–462 (2009).
[CrossRef] [PubMed]

T. Ishizawa, Y. Bandai, and N. Kokudo, “Fluorescent cholangiography using indocyanine green for laparoscopic cholecystectomy: an initial experience,” Arch. Surg. 144(4), 381–382 (2009).
[CrossRef] [PubMed]

M. Suzuki, N. Unno, N. Yamamoto, M. Nishiyama, D. Sagara, H. Tanaka, Y. Mano, and H. Konno, “Impaired lymphatic function recovered after great saphenous vein stripping in patients with varicose vein: venodynamic and lymphodynamic results,” J. Vasc. Surg. 50(5), 1085–1091 (2009).
[CrossRef] [PubMed]

J. C. Rasmussen, I. C. Tan, M. V. Marshall, C. E. Fife, and E. M. Sevick-Muraca, “Lymphatic imaging in humans with near-infrared fluorescence,” Curr. Opin. Biotechnol. 20(1), 74–82 (2009).
[CrossRef] [PubMed]

M. Fujiwara, T. Mizukami, A. Suzuki, and H. Fukamizu, “Sentinel lymph node detection in skin cancer patients using real-time fluorescence navigation with indocyanine green: preliminary experience,” J. Plast. Reconstr. Aesthet. Surg. 62(10), e373–e378 (2009).
[CrossRef] [PubMed]

S. L. Troyan, V. Kianzad, S. L. Gibbs-Strauss, S. Gioux, A. Matsui, R. Oketokoun, L. Ngo, A. Khamene, F. Azar, and J. V. Frangioni, “The FLARE intraoperative near-infrared fluorescence imaging system: a first-in-human clinical trial in breast cancer sentinel lymph node mapping,” Ann. Surg. Oncol. 16(10), 2943–2952 (2009).
[CrossRef] [PubMed]

Y. Tsujino, K. Mizumoto, Y. Matsuzaka, H. Niihara, and E. Morita, “Fluorescence navigation with indocyanine green for detecting sentinel nodes in extramammary Paget’s disease and squamous cell carcinoma,” J. Dermatol. 36(2), 90–94 (2009).
[CrossRef] [PubMed]

D. Murawa, C. Hirche, S. Dresel, and M. Hünerbein, “Sentinel lymph node biopsy in breast cancer guided by indocyanine green fluorescence,” Br. J. Surg. 96(11), 1289–1294 (2009).
[CrossRef] [PubMed]

2008 (5)

I. Miyashiro, N. Miyoshi, M. Hiratsuka, K. Kishi, T. Yamada, M. Ohue, H. Ohigashi, M. Yano, O. Ishikawa, and S. Imaoka, “Detection of sentinel node in gastric cancer surgery by indocyanine green fluorescence imaging: comparison with infrared imaging,” Ann. Surg. Oncol. 15(6), 1640–1643 (2008).
[CrossRef] [PubMed]

N. Tagaya, R. Yamazaki, A. Nakagawa, A. Abe, K. Hamada, K. Kubota, and T. Oyama, “Intraoperative identification of sentinel lymph nodes by near-infrared fluorescence imaging in patients with breast cancer,” Am. J. Surg. 195(6), 850–853 (2008).
[CrossRef] [PubMed]

N. Unno, M. Suzuki, N. Yamamoto, K. Inuzuka, D. Sagara, M. Nishiyama, H. Tanaka, and H. Konno, “Indocyanine green fluorescence angiography for intraoperative assessment of blood flow: a feasibility study,” Eur. J. Vasc. Endovasc. Surg. 35(2), 205–207 (2008).
[CrossRef] [PubMed]

Y. Ogasawara, H. Ikeda, M. Takahashi, K. Kawasaki, and H. Doihara, “Evaluation of breast lymphatic pathways with indocyanine green fluorescence imaging in patients with breast cancer,” World J. Surg. 32(9), 1924–1929 (2008).
[CrossRef] [PubMed]

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology 246(3), 734–741 (2008).
[CrossRef] [PubMed]

2007 (3)

H. Kunikata, H. Tomita, T. Abe, H. Murata, Y. Sagara, H. Sato, Y. Wada, N. Fuse, Y. Nakagawa, M. Tamai, and K. Nishida, “Hypothermia protects cultured human retinal pigment epithelial cells against indocyanine green toxicity,” J. Ocul. Pharmacol. Ther. 23(1), 35–39 (2007).
[CrossRef] [PubMed]

F. Ogata, M. Narushima, M. Mihara, R. Azuma, Y. Morimoto, and I. Koshima, “Intraoperative lymphography using indocyanine green dye for near-infrared fluorescence labeling in lymphedema,” Ann. Plast. Surg. 59(2), 180–184 (2007).
[CrossRef] [PubMed]

N. Unno, K. Inuzuka, M. Suzuki, N. Yamamoto, D. Sagara, M. Nishiyama, and H. Konno, “Preliminary experience with a novel fluorescence lymphography using indocyanine green in patients with secondary lymphedema,” J. Vasc. Surg. 45(5), 1016–1021 (2007).
[CrossRef] [PubMed]

2006 (4)

Y. Sato, H. Tomita, E. Sugano, H. Isago, M. Yoshida, and M. Tamai, “Evaluation of indocyanine green toxicity to rat retinas,” Ophthalmologica 220(3), 153–158 (2006).
[CrossRef] [PubMed]

C. Holm, M. Mayr, E. Höfter, and M. Ninkovic, “Perfusion zones of the DIEP flap revisited: a clinical study,” Plast. Reconstr. Surg. 117(1), 37–43 (2006).
[CrossRef] [PubMed]

P. Saikia, T. Maisch, K. Kobuch, T. L. Jackson, W. Bäumler, R. M. Szeimies, V. P. Gabel, and J. Hillenkamp, “Safety testing of indocyanine green in an ex vivo porcine retina model,” Invest. Ophthalmol. Vis. Sci. 47(11), 4998–5003 (2006).
[CrossRef] [PubMed]

A. Liebert, H. Wabnitz, H. Obrig, R. Erdmann, M. Möller, R. Macdonald, H. Rinneberg, A. Villringer, and J. Steinbrink, “Non-invasive detection of fluorescence from exogenous chromophores in the adult human brain,” Neuroimage 31(2), 600–608 (2006).
[CrossRef] [PubMed]

2005 (3)

T. L. Jackson, “Indocyanine green accused,” Br. J. Ophthalmol. 89(4), 395–396 (2005).
[CrossRef] [PubMed]

W. Baulig, E. O. Bernhard, D. Bettex, D. Schmidlin, and E. R. Schmid, “Cardiac output measurement by pulse dye densitometry in cardiac surgery,” Anaesthesia 60(10), 968–973 (2005).
[CrossRef] [PubMed]

T. Kitai, T. Inomoto, M. Miwa, and T. Shikayama, “Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer,” Breast Cancer 12(3), 211–215 (2005).
[CrossRef] [PubMed]

2004 (4)

B. Hameed, D. M. Smith, J. J. Verrechio, J. D. Schmidt, L. E. Gillooley, M. C. Valenzano, S. A. Lewis, and J. M. Mullin, “Indocyanine green alters transepithelial electrical parameters of the distal colon,” Dig. Dis. Sci. 49(9), 1381–1386 (2004).
[CrossRef] [PubMed]

C. Terborg, S. Bramer, S. Harscher, M. Simon, and O. W. Witte, “Bedside assessment of cerebral perfusion reductions in patients with acute ischaemic stroke by near-infrared spectroscopy and indocyanine green,” J. Neurol. Neurosurg. Psychiatry 75(1), 38–42 (2004).
[PubMed]

J. M. Maarek, D. P. Holschneider, J. Harimoto, J. Yang, O. U. Scremin, and E. H. Rubinstein, “Measurement of cardiac output with indocyanine green transcutaneous fluorescence dilution technique,” Anesthesiology 100(6), 1476–1483 (2004).
[CrossRef] [PubMed]

T. S. Leung, N. Aladangady, C. E. Elwell, D. T. Delpy, and K. Costeloe, “A new method for the measurement of cerebral blood volume and total circulating blood volume using near infrared spatially resolved spectroscopy and indocyanine green: Application and validation in neonates,” Pediatr. Res. 55(1), 134–141 (2004).
[CrossRef] [PubMed]

2003 (3)

F. B. Dietz and R. A. Jaffe, “Indocyanine green: evidence of neurotoxicity in spinal root axons,” Anesthesiology 98(2), 516–520 (2003).
[CrossRef] [PubMed]

E. Keller, A. Nadler, H. Alkadhi, S. S. Kollias, Y. Yonekawa, and P. Niederer, “Noninvasive measurement of regional cerebral blood flow and regional cerebral blood volume by near-infrared spectroscopy and indocyanine green dye dilution,” Neuroimage 20(2), 828–839 (2003).
[CrossRef] [PubMed]

E. Ziemińska, A. Stafiej, and J. W. Łazarewicz, “Role of group I metabotropic glutamate receptors and NMDA receptors in homocysteine-evoked acute neurodegeneration of cultured cerebellar granule neurones,” Neurochem. Int. 43(4-5), 481–492 (2003).
[CrossRef] [PubMed]

2002 (4)

E. Keller, H. Ishihara, A. Nadler, P. Niederer, B. Seifert, Y. Yonekawa, and K. Frei, “Evaluation of brain toxicity following near infrared light exposure after indocyanine green dye injection,” J. Neurosci. Methods 117(1), 23–31 (2002).
[CrossRef] [PubMed]

A. Contestabile, “Cerebellar granule cells as a model to study mechanisms of neuronal apoptosis or survival in vivo and in vitro,” Cerebellum 1(1), 41–55 (2002).
[CrossRef] [PubMed]

F. Bremer, A. Schiele, and K. Tschaikowsky, “Cardiac output measurement by pulse dye densitometry: a comparison with the Fick’s principle and thermodilution method,” Intensive Care Med. 28(4), 399–405 (2002).
[CrossRef] [PubMed]

S. G. Sakka, K. Reinhart, K. Wegscheider, and A. Meier-Hellmann, “Comparison of cardiac output and circulatory blood volumes by transpulmonary thermo-dye dilution and transcutaneous indocyanine green measurement in critically ill patients,” Chest 121(2), 559–565 (2002).
[CrossRef] [PubMed]

2000 (2)

T. Imai, C. Mitaka, T. Nosaka, A. Koike, S. Ohki, Y. Isa, and F. Kunimoto, “Accuracy and repeatability of blood volume measurement by pulse dye densitometry compared to the conventional method using 51Cr-labeled red blood cells,” Intensive Care Med. 26(9), 1343–1349 (2000).
[CrossRef] [PubMed]

T. Desmettre, J. M. Devoisselle, and S. Mordon, “Fluorescence properties and metabolic features of indocyanine green (ICG) as related to angiography,” Surv. Ophthalmol. 45(1), 15–27 (2000).
[CrossRef] [PubMed]

1999 (3)

P. Hopton, T. S. Walsh, and A. Lee, “Measurement of cerebral blood volume using near-infrared spectroscopy and indocyanine green elimination,” J. Appl. Physiol. 87(5), 1981–1987 (1999).
[PubMed]

A. El-Desoky, A. M. Seifalian, M. Cope, D. T. Delpy, and B. R. Davidson, “Experimental study of liver dysfunction evaluated by direct indocyanine green clearance using near infrared spectroscopy,” Br. J. Surg. 86(8), 1005–1011 (1999).
[CrossRef] [PubMed]

J. S. Reynolds, T. L. Troy, R. H. Mayer, A. B. Thompson, D. J. Waters, K. K. Cornell, P. W. Snyder, and E. M. Sevick-Muraca, “Imaging of spontaneous canine mammary tumors using fluorescent contrast agents,” Photochem. Photobiol. 70(1), 87–94 (1999).
[CrossRef] [PubMed]

1998 (3)

M. Haruna, K. Kumon, N. Yahagi, Y. Watanabe, Y. Ishida, N. Kobayashi, and T. Aoyagi, “Blood volume measurement at the bedside using ICG pulse spectrophotometry,” Anesthesiology 89(6), 1322–1328 (1998).
[CrossRef] [PubMed]

W. M. Kuebler, A. Sckell, O. Habler, M. Kleen, G. E. H. Kuhnle, M. Welte, K. Messmer, and A. E. Goetz, “Noninvasive measurement of regional cerebral blood flow by near-infrared spectroscopy and indocyanine green,” J. Cereb. Blood Flow Metab. 18(4), 445–456 (1998).
[CrossRef] [PubMed]

J. Patel, K. Marks, I. Roberts, D. Azzopardi, and A. D. Edwards, “Measurement of cerebral blood flow in newborn infants using near infrared spectroscopy with indocyanine green,” Pediatr. Res. 43(1), 34–39 (1998).
[CrossRef] [PubMed]

1997 (2)

F. Rotermund, R. Weigand, and A. Penzkofer, “J-aggregation and disaggregation of indocyanine green in water,” Chem. Phys. 220(3), 385–392 (1997).
[CrossRef]

R. Weigand, F. Rotermund, and A. Penzkofer, “Aggregation dependent absorption reduction of indocyanine green,” J. Phys. Chem. A 101(42), 7729–7734 (1997).
[CrossRef]

1996 (4)

H. Shinohara, A. Tanaka, T. Kitai, N. Yanabu, T. Inomoto, S. Satoh, E. Hatano, Y. Yamaoka, and K. Hirao, “Direct measurement of hepatic indocyanine green clearance with near-infrared spectroscopy: separate evaluation of uptake and removal,” Hepatology 23(1), 137–144 (1996).
[CrossRef] [PubMed]

M. Takahashi, H. Tsutsui, C. Murayama, T. Miyazawa, and B. Fritz-Zieroth, “Neurotoxicity of gadolinium contrast agents for magnetic resonance imaging in rats with osmotically disrupted blood-brain barrier,” Magn. Reson. Imaging 14(6), 619–623 (1996).
[CrossRef] [PubMed]

D. E. Ray, J. B. Cavanagh, C. C. Nolan, and S. C. Williams, “Neurotoxic effects of gadopentetate dimeglumine: behavioral disturbance and morphology after intracerebroventricular injection in rats,” AJNR Am. J. Neuroradiol. 17(2), 365–373 (1996).
[PubMed]

T. W. Olsen, J. I. Lim, A. Capone, R. A. Myles, and J. P. Gilman, “Anaphylactic shock following indocyanine green angiography,” Arch. Ophthalmol. 114(1), 97 (1996).
[CrossRef] [PubMed]

1995 (2)

H. Vogler, J. Platzek, G. Schuhmann-Giampieri, T. Frenzel, H. J. Weinmann, B. Radüchel, and W. R. Press, “Pre-clinical evaluation of gadobutrol: a new, neutral, extracellular contrast agent for magnetic resonance imaging,” Eur. J. Radiol. 21(1), 1–10 (1995).
[CrossRef] [PubMed]

M. P. Mattson and Y. Goodman, “Different amyloidogenic peptides share a similar mechanism of neurotoxicity involving reactive oxygen species and calcium,” Brain Res. 676(1), 219–224 (1995).
[CrossRef] [PubMed]

1994 (3)

M. Hope-Ross, L. A. Yannuzzi, E. S. Gragoudas, D. R. Guyer, J. S. Slakter, J. A. Sorenson, S. Krupsky, D. A. Orlock, and C. A. Puliafito, “Adverse reactions due to indocyanine green,” Ophthalmology 101(3), 529–533 (1994).
[CrossRef] [PubMed]

J. Fishbaugh, “Retina: indocyanine green (ICG) angiography,” Insight 19(3), 30–32 (1994).
[PubMed]

J. F. Zhou, M. P. Chin, and S. A. Schafer, “Aggregation and degradation of mdocyanine green,” Proc. SPIE 2128, 495–505 (1994).
[CrossRef]

1988 (1)

R. Speich, B. Saesseli, U. Hoffmann, K. A. Neftel, and J. Reichen, “Anaphylactoid reactions after indocyanine-green administration,” Ann. Intern. Med. 109(4), 345–346 (1988).
[CrossRef] [PubMed]

1985 (1)

A. Schousboe, J. Drejer, G. H. Hansen, and E. Meier, “Cultured neurons as model systems for biochemical and pharmacological studies on receptors for neurotransmitter amino acids,” Dev. Neurosci. 7(5-6), 252–262 (1985).
[CrossRef] [PubMed]

1978 (1)

T. R. Garski, B. J. Staller, G. Hepner, V. S. Banka, and R. A. Finney., “Adverse Reactions After Administration of Indocyanine Green,” JAMA 240(7), 635b (1978).
[CrossRef] [PubMed]

1971 (1)

B. F. Hochheimer, “Angiography of the retina with indocyanine green,” Arch. Ophthalmol. 86(5), 564–565 (1971).
[CrossRef] [PubMed]

1966 (1)

K. J. Baker, “Binding of sulfobromophthalein (BSP) sodium and indocyanine green (ICG) by plasma alpha-1 lipoproteins,” Proc. Soc. Exp. Biol. Med. 122(4), 957–963 (1966).
[CrossRef] [PubMed]

1961 (1)

J. Caesar, S. Shaldon, L. Chiandussi, L. Guevara, and S. Sherlock, “The use of indocyanine green in the measurement of hepatic blood flow and as a test of hepatic function,” Clin. Sci. 21, 43–57 (1961).
[PubMed]

1960 (2)

G. R. Cherrick, S. W. Stein, C. M. Leevy, and C. S. Davidson, “Indocyanine green: observations on its physical properties, plasma decay, and hepatic extraction,” J. Clin. Invest. 39(4), 592–600 (1960).
[CrossRef] [PubMed]

I. J. Fox and E. H. Wood, “Indocyanine green: physical and physiologic properties,” Proc. Staff Meet. Mayo Clin. 35, 732–744 (1960).
[PubMed]

Abe, A.

N. Tagaya, R. Yamazaki, A. Nakagawa, A. Abe, K. Hamada, K. Kubota, and T. Oyama, “Intraoperative identification of sentinel lymph nodes by near-infrared fluorescence imaging in patients with breast cancer,” Am. J. Surg. 195(6), 850–853 (2008).
[CrossRef] [PubMed]

Abe, T.

H. Kunikata, H. Tomita, T. Abe, H. Murata, Y. Sagara, H. Sato, Y. Wada, N. Fuse, Y. Nakagawa, M. Tamai, and K. Nishida, “Hypothermia protects cultured human retinal pigment epithelial cells against indocyanine green toxicity,” J. Ocul. Pharmacol. Ther. 23(1), 35–39 (2007).
[CrossRef] [PubMed]

Adams, K. E.

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology 246(3), 734–741 (2008).
[CrossRef] [PubMed]

Aladangady, N.

T. S. Leung, N. Aladangady, C. E. Elwell, D. T. Delpy, and K. Costeloe, “A new method for the measurement of cerebral blood volume and total circulating blood volume using near infrared spatially resolved spectroscopy and indocyanine green: Application and validation in neonates,” Pediatr. Res. 55(1), 134–141 (2004).
[CrossRef] [PubMed]

Alkadhi, H.

E. Keller, A. Nadler, H. Alkadhi, S. S. Kollias, Y. Yonekawa, and P. Niederer, “Noninvasive measurement of regional cerebral blood flow and regional cerebral blood volume by near-infrared spectroscopy and indocyanine green dye dilution,” Neuroimage 20(2), 828–839 (2003).
[CrossRef] [PubMed]

Aoki, T.

T. Ishizawa, N. Fukushima, J. Shibahara, K. Masuda, S. Tamura, T. Aoki, K. Hasegawa, Y. Beck, M. Fukayama, and N. Kokudo, “Real-time identification of liver cancers by using indocyanine green fluorescent imaging,” Cancer 115(11), 2491–2504 (2009).
[CrossRef] [PubMed]

Aoyagi, T.

M. Haruna, K. Kumon, N. Yahagi, Y. Watanabe, Y. Ishida, N. Kobayashi, and T. Aoyagi, “Blood volume measurement at the bedside using ICG pulse spectrophotometry,” Anesthesiology 89(6), 1322–1328 (1998).
[CrossRef] [PubMed]

Azar, F.

S. L. Troyan, V. Kianzad, S. L. Gibbs-Strauss, S. Gioux, A. Matsui, R. Oketokoun, L. Ngo, A. Khamene, F. Azar, and J. V. Frangioni, “The FLARE intraoperative near-infrared fluorescence imaging system: a first-in-human clinical trial in breast cancer sentinel lymph node mapping,” Ann. Surg. Oncol. 16(10), 2943–2952 (2009).
[CrossRef] [PubMed]

Azuma, R.

F. Ogata, M. Narushima, M. Mihara, R. Azuma, Y. Morimoto, and I. Koshima, “Intraoperative lymphography using indocyanine green dye for near-infrared fluorescence labeling in lymphedema,” Ann. Plast. Surg. 59(2), 180–184 (2007).
[CrossRef] [PubMed]

Azzopardi, D.

J. Patel, K. Marks, I. Roberts, D. Azzopardi, and A. D. Edwards, “Measurement of cerebral blood flow in newborn infants using near infrared spectroscopy with indocyanine green,” Pediatr. Res. 43(1), 34–39 (1998).
[CrossRef] [PubMed]

Baker, K. J.

K. J. Baker, “Binding of sulfobromophthalein (BSP) sodium and indocyanine green (ICG) by plasma alpha-1 lipoproteins,” Proc. Soc. Exp. Biol. Med. 122(4), 957–963 (1966).
[CrossRef] [PubMed]

Balaiya, S.

S. Balaiya, V. S. Brar, R. K. Murthy, and K. Chalam, “Effects of Indocyanine green on cultured retinal ganglion cells in-vitro,” BMC Res. Notes 2(1), 236 (2009).
[CrossRef] [PubMed]

Bandai, Y.

T. Ishizawa, Y. Bandai, and N. Kokudo, “Fluorescent cholangiography using indocyanine green for laparoscopic cholecystectomy: an initial experience,” Arch. Surg. 144(4), 381–382 (2009).
[CrossRef] [PubMed]

Banka, V. S.

T. R. Garski, B. J. Staller, G. Hepner, V. S. Banka, and R. A. Finney., “Adverse Reactions After Administration of Indocyanine Green,” JAMA 240(7), 635b (1978).
[CrossRef] [PubMed]

Baulig, W.

W. Baulig, E. O. Bernhard, D. Bettex, D. Schmidlin, and E. R. Schmid, “Cardiac output measurement by pulse dye densitometry in cardiac surgery,” Anaesthesia 60(10), 968–973 (2005).
[CrossRef] [PubMed]

Bäumler, W.

P. Saikia, T. Maisch, K. Kobuch, T. L. Jackson, W. Bäumler, R. M. Szeimies, V. P. Gabel, and J. Hillenkamp, “Safety testing of indocyanine green in an ex vivo porcine retina model,” Invest. Ophthalmol. Vis. Sci. 47(11), 4998–5003 (2006).
[CrossRef] [PubMed]

Beck, Y.

T. Ishizawa, N. Fukushima, J. Shibahara, K. Masuda, S. Tamura, T. Aoki, K. Hasegawa, Y. Beck, M. Fukayama, and N. Kokudo, “Real-time identification of liver cancers by using indocyanine green fluorescent imaging,” Cancer 115(11), 2491–2504 (2009).
[CrossRef] [PubMed]

Bernhard, E. O.

W. Baulig, E. O. Bernhard, D. Bettex, D. Schmidlin, and E. R. Schmid, “Cardiac output measurement by pulse dye densitometry in cardiac surgery,” Anaesthesia 60(10), 968–973 (2005).
[CrossRef] [PubMed]

Bettex, D.

W. Baulig, E. O. Bernhard, D. Bettex, D. Schmidlin, and E. R. Schmid, “Cardiac output measurement by pulse dye densitometry in cardiac surgery,” Anaesthesia 60(10), 968–973 (2005).
[CrossRef] [PubMed]

Blanchard, D. K.

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology 246(3), 734–741 (2008).
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Boer, F.

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Y. Ogasawara, H. Ikeda, M. Takahashi, K. Kawasaki, and H. Doihara, “Evaluation of breast lymphatic pathways with indocyanine green fluorescence imaging in patients with breast cancer,” World J. Surg. 32(9), 1924–1929 (2008).
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T. Kitai, T. Inomoto, M. Miwa, and T. Shikayama, “Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer,” Breast Cancer 12(3), 211–215 (2005).
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T. Ishizawa, N. Fukushima, J. Shibahara, K. Masuda, S. Tamura, T. Aoki, K. Hasegawa, Y. Beck, M. Fukayama, and N. Kokudo, “Real-time identification of liver cancers by using indocyanine green fluorescent imaging,” Cancer 115(11), 2491–2504 (2009).
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E. Keller, A. Nadler, H. Alkadhi, S. S. Kollias, Y. Yonekawa, and P. Niederer, “Noninvasive measurement of regional cerebral blood flow and regional cerebral blood volume by near-infrared spectroscopy and indocyanine green dye dilution,” Neuroimage 20(2), 828–839 (2003).
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N. Unno, K. Inuzuka, M. Suzuki, N. Yamamoto, D. Sagara, M. Nishiyama, and H. Konno, “Preliminary experience with a novel fluorescence lymphography using indocyanine green in patients with secondary lymphedema,” J. Vasc. Surg. 45(5), 1016–1021 (2007).
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M. Hope-Ross, L. A. Yannuzzi, E. S. Gragoudas, D. R. Guyer, J. S. Slakter, J. A. Sorenson, S. Krupsky, D. A. Orlock, and C. A. Puliafito, “Adverse reactions due to indocyanine green,” Ophthalmology 101(3), 529–533 (1994).
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W. M. Kuebler, A. Sckell, O. Habler, M. Kleen, G. E. H. Kuhnle, M. Welte, K. Messmer, and A. E. Goetz, “Noninvasive measurement of regional cerebral blood flow by near-infrared spectroscopy and indocyanine green,” J. Cereb. Blood Flow Metab. 18(4), 445–456 (1998).
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M. Haruna, K. Kumon, N. Yahagi, Y. Watanabe, Y. Ishida, N. Kobayashi, and T. Aoyagi, “Blood volume measurement at the bedside using ICG pulse spectrophotometry,” Anesthesiology 89(6), 1322–1328 (1998).
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T. Imai, C. Mitaka, T. Nosaka, A. Koike, S. Ohki, Y. Isa, and F. Kunimoto, “Accuracy and repeatability of blood volume measurement by pulse dye densitometry compared to the conventional method using 51Cr-labeled red blood cells,” Intensive Care Med. 26(9), 1343–1349 (2000).
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Y. Tajima, M. Murakami, K. Yamazaki, Y. Masuda, M. Kato, A. Sato, S. Goto, K. Otsuka, T. Kato, and M. Kusano, “Sentinel node mapping guided by indocyanine green fluorescence imaging during laparoscopic surgery in gastric cancer,” Ann. Surg. Oncol. 17(7), 1787–1793 (2010).
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E. Ziemińska, A. Stafiej, B. Toczyłowska, and J. W. Lazarewicz, “Synergistic neurotoxicity of oxygen-glucose deprivation and tetrabromobisphenol A in vitro: role of oxidative stress,” Pharmacol. Rep. 64(5), 1166–1178 (2012).
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J. Caesar, S. Shaldon, L. Chiandussi, L. Guevara, and S. Sherlock, “The use of indocyanine green in the measurement of hepatic blood flow and as a test of hepatic function,” Clin. Sci. 21, 43–57 (1961).
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M. Suzuki, N. Unno, N. Yamamoto, M. Nishiyama, D. Sagara, H. Tanaka, Y. Mano, and H. Konno, “Impaired lymphatic function recovered after great saphenous vein stripping in patients with varicose vein: venodynamic and lymphodynamic results,” J. Vasc. Surg. 50(5), 1085–1091 (2009).
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D. Milej, A. Gerega, M. Kacprzak, P. Sawosz, W. Weigl, R. Maniewski, and A. Liebert, “Time-resolved multi-channel optical system for assessment of brain oxygenation and perfusion by monitoring of diffuse reflectance and fluorescence,” Opto-Electron. Rev. 22(1), 55–67 (2014).
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E. Keller, H. Ishihara, A. Nadler, P. Niederer, B. Seifert, Y. Yonekawa, and K. Frei, “Evaluation of brain toxicity following near infrared light exposure after indocyanine green dye injection,” J. Neurosci. Methods 117(1), 23–31 (2002).
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J. Ocul. Pharmacol. Ther. (1)

H. Kunikata, H. Tomita, T. Abe, H. Murata, Y. Sagara, H. Sato, Y. Wada, N. Fuse, Y. Nakagawa, M. Tamai, and K. Nishida, “Hypothermia protects cultured human retinal pigment epithelial cells against indocyanine green toxicity,” J. Ocul. Pharmacol. Ther. 23(1), 35–39 (2007).
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R. Weigand, F. Rotermund, and A. Penzkofer, “Aggregation dependent absorption reduction of indocyanine green,” J. Phys. Chem. A 101(42), 7729–7734 (1997).
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M. Fujiwara, T. Mizukami, A. Suzuki, and H. Fukamizu, “Sentinel lymph node detection in skin cancer patients using real-time fluorescence navigation with indocyanine green: preliminary experience,” J. Plast. Reconstr. Aesthet. Surg. 62(10), e373–e378 (2009).
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N. Unno, K. Inuzuka, M. Suzuki, N. Yamamoto, D. Sagara, M. Nishiyama, and H. Konno, “Preliminary experience with a novel fluorescence lymphography using indocyanine green in patients with secondary lymphedema,” J. Vasc. Surg. 45(5), 1016–1021 (2007).
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M. Suzuki, N. Unno, N. Yamamoto, M. Nishiyama, D. Sagara, H. Tanaka, Y. Mano, and H. Konno, “Impaired lymphatic function recovered after great saphenous vein stripping in patients with varicose vein: venodynamic and lymphodynamic results,” J. Vasc. Surg. 50(5), 1085–1091 (2009).
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JAMA (1)

T. R. Garski, B. J. Staller, G. Hepner, V. S. Banka, and R. A. Finney., “Adverse Reactions After Administration of Indocyanine Green,” JAMA 240(7), 635b (1978).
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Magn. Reson. Imaging (1)

M. Takahashi, H. Tsutsui, C. Murayama, T. Miyazawa, and B. Fritz-Zieroth, “Neurotoxicity of gadolinium contrast agents for magnetic resonance imaging in rats with osmotically disrupted blood-brain barrier,” Magn. Reson. Imaging 14(6), 619–623 (1996).
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Neurochem. Int. (1)

E. Ziemińska, A. Stafiej, and J. W. Łazarewicz, “Role of group I metabotropic glutamate receptors and NMDA receptors in homocysteine-evoked acute neurodegeneration of cultured cerebellar granule neurones,” Neurochem. Int. 43(4-5), 481–492 (2003).
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Neuroimage (4)

A. Liebert, H. Wabnitz, H. Obrig, R. Erdmann, M. Möller, R. Macdonald, H. Rinneberg, A. Villringer, and J. Steinbrink, “Non-invasive detection of fluorescence from exogenous chromophores in the adult human brain,” Neuroimage 31(2), 600–608 (2006).
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H. Obrig, “NIRS in clinical neurology - a 'promising' tool?” Neuroimage 85, 535–546 (2013).
[PubMed]

E. Keller, A. Nadler, H. Alkadhi, S. S. Kollias, Y. Yonekawa, and P. Niederer, “Noninvasive measurement of regional cerebral blood flow and regional cerebral blood volume by near-infrared spectroscopy and indocyanine green dye dilution,” Neuroimage 20(2), 828–839 (2003).
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W. Weigl, D. Milej, A. Gerega, B. Toczylowska, M. Kacprzak, P. Sawosz, M. Botwicz, R. Maniewski, E. Mayzner-Zawadzka, and A. Liebert, “Assessment of cerebral perfusion in post-traumatic brain injury patients with the use of ICG-bolus tracking method,” Neuroimage 85(Pt 1), 555–565 (2014).
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Neurosurgery (1)

B. D. Killory, P. Nakaji, L. F. Gonzales, F. A. Ponce, S. D. Wait, and R. F. Spetzler, “Prospective evaluation of surgical microscope-integrated intraoperative near-infrared indocyanine green angiography during cerebral arteriovenous malformation surgery,” Neurosurgery 65(3), 456–462 (2009).
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Neurotoxicology (1)

X. Feng, Q. Xia, L. Yuan, X. Yang, and K. Wang, “Impaired mitochondrial function and oxidative stress in rat cortical neurons: implications for gadolinium-induced neurotoxicity,” Neurotoxicology 31(4), 391–398 (2010).
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Ophthalmologica (1)

Y. Sato, H. Tomita, E. Sugano, H. Isago, M. Yoshida, and M. Tamai, “Evaluation of indocyanine green toxicity to rat retinas,” Ophthalmologica 220(3), 153–158 (2006).
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Ophthalmology (1)

M. Hope-Ross, L. A. Yannuzzi, E. S. Gragoudas, D. R. Guyer, J. S. Slakter, J. A. Sorenson, S. Krupsky, D. A. Orlock, and C. A. Puliafito, “Adverse reactions due to indocyanine green,” Ophthalmology 101(3), 529–533 (1994).
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Opto-Electron. Rev. (1)

D. Milej, A. Gerega, M. Kacprzak, P. Sawosz, W. Weigl, R. Maniewski, and A. Liebert, “Time-resolved multi-channel optical system for assessment of brain oxygenation and perfusion by monitoring of diffuse reflectance and fluorescence,” Opto-Electron. Rev. 22(1), 55–67 (2014).
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Pediatr. Res. (2)

J. Patel, K. Marks, I. Roberts, D. Azzopardi, and A. D. Edwards, “Measurement of cerebral blood flow in newborn infants using near infrared spectroscopy with indocyanine green,” Pediatr. Res. 43(1), 34–39 (1998).
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Pharmacol. Rep. (1)

E. Ziemińska, A. Stafiej, B. Toczyłowska, and J. W. Lazarewicz, “Synergistic neurotoxicity of oxygen-glucose deprivation and tetrabromobisphenol A in vitro: role of oxidative stress,” Pharmacol. Rep. 64(5), 1166–1178 (2012).
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H. Obrig and J. Steinbrink, “Non-invasive optical imaging of stroke,” Philos. Trans. A Math, Phys. Eng Sci. 369(1955), 4470–4494 (2011).
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Photochem. Photobiol. (1)

J. S. Reynolds, T. L. Troy, R. H. Mayer, A. B. Thompson, D. J. Waters, K. K. Cornell, P. W. Snyder, and E. M. Sevick-Muraca, “Imaging of spontaneous canine mammary tumors using fluorescent contrast agents,” Photochem. Photobiol. 70(1), 87–94 (1999).
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Phys. Med. Biol. (1)

D. Milej, A. Gerega, N. Zołek, W. Weigl, M. Kacprzak, P. Sawosz, J. Mączewska, K. Fronczewska, E. Mayzner-Zawadzka, L. Królicki, R. Maniewski, and A. Liebert, “Time-resolved detection of fluorescent light during inflow of ICG to the brain-a methodological study,” Phys. Med. Biol. 57(20), 6725–6742 (2012).
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C. Holm, M. Mayr, E. Höfter, and M. Ninkovic, “Perfusion zones of the DIEP flap revisited: a clinical study,” Plast. Reconstr. Surg. 117(1), 37–43 (2006).
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K. J. Baker, “Binding of sulfobromophthalein (BSP) sodium and indocyanine green (ICG) by plasma alpha-1 lipoproteins,” Proc. Soc. Exp. Biol. Med. 122(4), 957–963 (1966).
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Proc. SPIE (1)

J. F. Zhou, M. P. Chin, and S. A. Schafer, “Aggregation and degradation of mdocyanine green,” Proc. SPIE 2128, 495–505 (1994).
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Proc. Staff Meet. Mayo Clin. (1)

I. J. Fox and E. H. Wood, “Indocyanine green: physical and physiologic properties,” Proc. Staff Meet. Mayo Clin. 35, 732–744 (1960).
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Radiology (1)

E. M. Sevick-Muraca, R. Sharma, J. C. Rasmussen, M. V. Marshall, J. A. Wendt, H. Q. Pham, E. Bonefas, J. P. Houston, L. Sampath, K. E. Adams, D. K. Blanchard, R. E. Fisher, S. B. Chiang, R. Elledge, and M. E. Mawad, “Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study,” Radiology 246(3), 734–741 (2008).
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Surv. Ophthalmol. (1)

T. Desmettre, J. M. Devoisselle, and S. Mordon, “Fluorescence properties and metabolic features of indocyanine green (ICG) as related to angiography,” Surv. Ophthalmol. 45(1), 15–27 (2000).
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Toxicology (1)

E. Zieminska, B. Toczylowska, A. Stafiej, and J. W. Lazarewicz, “Low molecular weight thiols reduce thimerosal neurotoxicity in vitro: modulation by proteins,” Toxicology 276(3), 154–163 (2010).
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World J. Surg. (1)

Y. Ogasawara, H. Ikeda, M. Takahashi, K. Kawasaki, and H. Doihara, “Evaluation of breast lymphatic pathways with indocyanine green fluorescence imaging in patients with breast cancer,” World J. Surg. 32(9), 1924–1929 (2008).
[CrossRef] [PubMed]

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Figures (9)

Fig. 1
Fig. 1

(a) – Viability of the neuronal cells after 30 min incubations with 25-250 µM ICG; (b) – viability of the neuronal cells after incubation with 0.1-50 mM concentrations of Gad. Means ± SD, n = 6, p<0.05. * - statistically significant differences vs. control.

Fig. 2
Fig. 2

(a) - NMR spectra of 25, 75 and 125 μM ICG in D2O/H2O. Signals at 6 to 9 ppm correspond to the protons from rings of the molecule (aromatic). Signals at 0 to 5 ppm correspond to aliphatic protons in ICG molecule; (b) - Vis-nIR absorption spectra of ICG in H2O (left) and Locke25 (right) for 25, 75 and 125μM ICG. The monomer maximum peak was observed at 770-785nm and the oligomers maximum peak at 700-713nm, depending on ICG concentration and solution.

Fig. 3
Fig. 3

Changes in the percentage of monomer in ICG for H2O/D2O (grey bars) and Locke25 (black bars) solutions

Fig. 4
Fig. 4

Protective effect of Gad on CGC viability after: (a) - 30 min of simultaneous exposure to mixture of ICG and Gad; (b) - 30 min of exposure to ICG and further 30 min incubation after application of Gad; (c) - 30 min preincubation with Gad and further 30 min of exposure after application of ICG. Two ICG concentrations, 75 and 125 μM, and three Gad concentrations, 0.1, 1.0 and 10 mM, were tested. Means ± SD, n = 6, p<0.05. * - differences statistically significant vs. control, # - vs. ICG alone.

Fig. 5
Fig. 5

The content of ICG monomer in the ICG-GAD mixture at the beginning and after 30 min of cell exposure. ICG/Gad - application of ICG and Gad at the same time for 30 min, ICG + Gad - addition ICG to the solvent for 30 min and then application of Gad for the next 30 min, Gad + ICG - application of Gad for 30 min and then ICG for the next 30 min

Fig. 6
Fig. 6

(a) - NMR spectra of 25 μM ICG in D2O/H2O; 25 μM ICG in 2.3 mM Ca2+ in D2O/H2O and for comparison regarding for matter of oligomers 125 μM ICG in D2O/H2O. (b) - The Vis-nIR absorption spectrum of 25 μM ICG in: Locke25, H2O, and H2O with added 2.3 mM Ca2+;

Fig. 7
Fig. 7

Fluo-3 as an indicator of relative fluorescence signal of calcium ions in 75 µM ICG and a mixture of 75 µM ICG and 0.1-10 mM Gad in Locke25. The Fluo-3 signal in Locke25 served as the reference. Fluo-3 was excited at 488 nm, and emission was measured with cutoff filter at 538 nm. Means ± SD, n = 6, p<0.05. * - statistically significant differences (p<0.05)

Fig. 8
Fig. 8

Changes in extracellular (a) and intracellular (b) Ca+2 concentration in CGC after addition of 25, 75 or 125 µM ICG. Lack of any effect of 30 min preincubation with 0.1-10 mM Gad on intracellular Ca+2 level in CGC after addition 75 µM ICG (c). Means ± SD, n = 4.

Fig. 9
Fig. 9

Application of 0.5 µM MK801 had no effect on fluorescence Fluo-3AM (a) or weak effect on the uptake of 45Ca2+ (b) in CGC after addition of 25-125 µM ICG. * - results statistically significant vs. ICG alone. Means ± SD, n = 6, p<0.05.

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