Abstract

Indocyanine green (ICG) is the only near-infrared dye approved by the U.S. Food and Drug Administration for clinical use. When injected in blood, ICG binds primarily to plasma proteins and lipoproteins, resulting in enhanced fluorescence. Recently, the optofluidic laser has emerged as a novel tool in bio-analysis. Laser emission has advantages over fluorescence in signal amplification, narrow linewidth, and strong intensity, leading to orders of magnitude increase in detection sensitivity and imaging contrast. Here we successfully demonstrate, to the best of our knowledge, the first ICG lasing in human serum and whole blood with the clinical ICG concentrations and the pump intensity far below the clinically permissible level. Furthermore, we systematically study ICG laser emission within each major serological component (albumins, globulins, and lipoproteins) and reveal the critical elements and conditions responsible for lasing. Our work marks a critical step toward eventual clinical and biomedical applications of optofluidic lasers using FDA approved fluorophores, which may complement or even supersede conventional fluorescence-based sensing and imaging.

© 2016 Optical Society of America

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References

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2016 (4)

C. Fang, K. Wang, C. Zeng, C. Chi, W. Shang, J. Ye, Y. Mao, Y. Fan, J. Yang, and N. Xiang, “Illuminating necrosis: from mechanistic exploration to preclinical application using fluorescence molecular imaging with indocyanine green,” Sci. Rep. 6, 21013 (2016).

M. Aas, Q. Chen, A. Jonáš, A. Kiraz, and X. Fan, “Optofluidic FRET lasers and their applications in novel photonic devices and biochemical sensing,” IEEE J. Sel. Top. Quantum Electron. 22, 1–15 (2016).
[Crossref]

Y.-C. Chen, Q. Chen, and X. Fan, “Optofluidic chlorophyll lasers,” Lab Chip 16, 2228–2235 (2016).
[Crossref]

Q. Chen, A. Kiraz, and X. Fan, “Optofluidic FRET lasers using aqueous quantum dots as donors,” Lab Chip 16, 353–359 (2016).
[Crossref]

2015 (9)

D. Holt, A. B. Parthasarathy, O. Okusanya, J. Keating, O. Venegas, C. Deshpande, G. Karakousis, B. Madajewski, A. Durham, and S. Nie, “Intraoperative near-infrared fluorescence imaging and spectroscopy identifies residual tumor cells in wounds,” J. Biomed. Opt. 20, 076002 (2015).
[Crossref]

M. Humar and S. H. Yun, “Intracellular microlasers,” Nat. Photonics 9, 572–576 (2015).
[Crossref]

V. Sabapathy, J. Mentam, P. M. Jacob, and S. Kumar, “Noninvasive optical imaging and in vivo cell tracking of indocyanine green labeled human stem cells transplanted at superficial or in-depth tissue of SCID mice,” Stem Cells Int. 2015, 606415 (2015).

K. Wang, W. Sun, C. T. Richie, B. K. Harvey, E. Betzig, and N. Ji, “Direct wavefront sensing for high-resolution in vivo imaging in scattering tissue,” Nat. Commun. 6, 7276 (2015).

R. P. Judy, J. J. Keating, E. M. DeJesus, J. X. Jiang, O. T. Okusanya, S. Nie, D. E. Holt, S. P. Arlauckas, P. S. Low, and E. J. Delikatny, “Quantification of tumor fluorescence during intraoperative optical cancer imaging,” Sci. Rep. 5, 16208 (2015).

L. Boni, G. David, A. Mangano, G. Dionigi, S. Rausei, S. Spampatti, E. Cassinotti, and A. Fingerhut, “Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery,” Surg. Endosc. 29, 2046–2055 (2015).
[Crossref]

W. Wang, C. Zhou, T. Zhang, J. Chen, S. Liu, and X. Fan, “Optofluidic laser array based on stable high-Q Fabry–Pérot microcavities,” Lab Chip 15, 3862–3869 (2015).
[Crossref]

J. Ziegler, M. Djiango, C. Vidal, C. Hrelescu, and T. A. Klar, “Gold nanostars for random lasing enhancement,” Opt. Express 23, 15152–15159 (2015).
[Crossref]

J. Zheng, N. Muhanna, R. D. Souza, H. Wada, H. Chan, M. K. Akens, T. Anayama, K. Yasufuku, S. Serra, J. Irish, C. Allen, and D. Jaffray, “A multimodal nano agent for image-guided cancer surgery,” Biomaterials 67, 160–168 (2015).
[Crossref]

2014 (7)

S. Lee, M. W. Lee, H. S. Cho, J. W. Song, H. S. Nam, D. J. Oh, K. Park, W.-Y. Oh, H. Yoo, and J. W. Kim, “Fully integrated high-speed intravascular optical coherence tomography/near-infrared fluorescence structural/molecular imaging in vivo using a clinically available near-infrared fluorescence-emitting indocyanine green to detect inflamed lipid-rich atheromata in coronary-sized vessels,” Circulation 7, 560–569 (2014).

B. Jung, V. I. Vullev, and B. Anvari, “Revisiting indocyanine green: effects of serum and physiological temperature on absorption and fluorescence characteristics,” IEEE J. Sel. Top. Quantum Electron. 20, 149–157 (2014).
[Crossref]

J. C. Kraft and R. J. Ho, “Interactions of indocyanine green and lipid in enhancing near-infrared fluorescence properties: the basis for near-infrared imaging in vivo,” Biochemistry 53, 1275–1283 (2014).
[Crossref]

G. Lu and B. Fei, “Medical hyperspectral imaging: a review,” J. Biomed. Opt. 19, 010901 (2014).
[Crossref]

X. Wu, M. K. Khaing Oo, K. Reddy, Q. Chen, Y. Sun, and X. Fan, “Optofluidic laser for dual-mode sensitive biomolecular detection with a large dynamic range,” Nat. Commun. 5, 3779 (2014).

X. Fan and S.-H. Yun, “The potential of optofluidic biolasers,” Nat. Methods 11, 141–147 (2014).
[Crossref]

Q. Chen, M. Ritt, S. Sivaramakrishnan, Y. Sun, and X. Fan, “Optofluidic lasers with a single molecular layer of gain,” Lab Chip 14, 4590–4595 (2014).
[Crossref]

2013 (2)

Q. Chen, X. Zhang, Y. Sun, M. Ritt, S. Sivaramakrishnan, and X. Fan, “Highly sensitive fluorescent protein FRET detection using optofluidic lasers,” Lab Chip 13, 2679–2681 (2013).
[Crossref]

P. Liu, C. Yue, B. Shi, G. Gao, M. Li, B. Wang, Y. Ma, and L. Cai, “Dextran based sensitive theranostic nanoparticles for near-infrared imaging and photothermal therapy in vitro,” Chem. Commun. 49, 6143–6145 (2013).
[Crossref]

2012 (7)

N. Lue, J. W. Kang, C.-C. Yu, I. Barman, N. C. Dingari, M. S. Feld, R. R. Dasari, and M. Fitzmaurice, “Portable optical fiber probe-based spectroscopic scanner for rapid cancer diagnosis: a new tool for intraoperative margin assessment,” PLoS One 7, e30887 (2012).
[Crossref]

Y. Sun and X. Fan, “Distinguishing DNA by analog-to-digital-like conversion by using optofluidic lasers,” Angew. Chem. Int. Ed. 51, 1236–1239 (2012).

X. Zhang, W. Lee, and X. Fan, “Bio-switchable optofluidic lasers based on DNA Holliday junctions,” Lab Chip 12, 3673–3675 (2012).
[Crossref]

C. Zheng, M. Zheng, P. Gong, D. Jia, P. Zhang, B. Shi, Z. Sheng, Y. Ma, and L. Cai, “Indocyanine green-loaded biodegradable tumor targeting nanoprobes for in vitro and in vivo imaging,” Biomaterials 33, 5603–5609 (2012).
[Crossref]

J. T. Alander, I. Kaartinen, A. Laakso, T. Pätilä, T. Spillmann, V. V. Tuchin, M. Venermo, and P. Välisuo, “A review of indocyanine green fluorescent imaging in surgery,” Int. J. Biomed. Imaging 2012, 940585 (2012).

N. Kokudo and T. Ishizawa, “Clinical application of fluorescence imaging of liver cancer using indocyanine green,” Liver Cancer 1, 15–21 (2012).
[Crossref]

W. Lee and X. Fan, “Intracavity DNA melting analysis with optofluidic lasers,” Anal. Chem. 84, 9558–9563 (2012).

2011 (6)

M. Y. Berezin, K. Guo, W. Akers, J. Livingston, M. Solomon, H. Lee, K. Liang, A. Agee, and S. Achilefu, “Rational approach to select small peptide molecular probes labeled with fluorescent cyanine dyes for in vivo optical imaging,” Biochemistry 50, 2691–2700 (2011).
[Crossref]

M. C. Gather and S. H. Yun, “Single-cell biological lasers,” Nat. Photonics 5, 406–410 (2011).
[Crossref]

C. Vinegoni, I. Botnaru, E. Aikawa, M. A. Calfon, Y. Iwamoto, E. J. Folco, V. Ntziachristos, R. Weissleder, P. Libby, and F. A. Jaffer, “Indocyanine green enables near-infrared fluorescence imaging of lipid-rich, inflamed atherosclerotic plaques,” Sci. Transl. Med. 3, 84ra45 (2011).
[Crossref]

B. E. Schaafsma, J. S. D. Mieog, M. Hutteman, J. R. Van der Vorst, P. J. Kuppen, C. W. Löwik, J. V. Frangioni, C. J. Van de Velde, and A. L. Vahrmeijer, “The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery,” J. Surg. Oncol. 104, 323–332 (2011).
[Crossref]

D. Mordant, I. Al-Abboud, G. Muyo, A. Gorman, A. Sallam, P. Ritchie, A. Harvey, and A. McNaught, “Spectral imaging of the retina,” Eye 25, 309–320 (2011).
[Crossref]

M. Mihara, I. Kisu, H. Hara, T. Iida, T. Yamamoto, J. Araki, Y. Hayashi, H. Moriguchi, M. Narushima, and K. Banno, “Uterus autotransplantation in cynomolgus macaques: intraoperative evaluation of uterine blood flow using indocyanine green,” Hum. Reprod. 26, 3019–3027 (2011).
[Crossref]

2009 (4)

M. A. Noginov, G. Zhu, A. M. Belgrave, R. Bakker, V. M. Shalaev, E. E. Narimanov, S. Stout, E. Herz, T. Suteewong, and U. Wiesner, “Demonstration of a spaser-based nanolaser,” Nature 460, 1110–1112 (2009).
[Crossref]

M. Ogawa, N. Kosaka, P. L. Choyke, and H. Kobayashi, “In vivo molecular imaging of cancer with a quenching near-infrared fluorescent probe using conjugates of monoclonal antibodies and indocyanine green,” Cancer Res. 69, 1268–1272 (2009).
[Crossref]

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, 2943–2952 (2009).
[Crossref]

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, 236 (2009).
[Crossref]

2008 (1)

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, 205–207 (2008).
[Crossref]

2007 (2)

2005 (1)

J. Woitzik, P. Horn, P. Vajkoczy, and P. Schmiedek, “Intraoperative control of extracranial-intracranial bypass patency by near-infrared indocyanine green videoangiography,” J. Neurosurg. 102, 692–698 (2005).
[Crossref]

2004 (1)

R. C. Polson and Z. V. Vardeny, “Random lasing in human tissues,” Appl. Phys. Lett. 85, 1289–1291 (2004).
[Crossref]

2002 (1)

T. Yamada, M. Yoshikawa, S. Kanda, Y. Kato, Y. Nakajima, S. Ishizaka, and Y. Tsunoda, “In vitro differentiation of embryonic stem cells into hepatocyte-like cells identified by cellular uptake of indocyanine green,” Stem Cells 20, 146–154 (2002).
[Crossref]

2000 (2)

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

R. Matthes, C. P. Cain, D. Courant, D. A. Freund, B. A. Grossman, P. A. Kennedy, D. J. Lund, M. A. Mainster, A. A. Manenkov, W. J. Marshall, R. McCally, B. A. Rockwell, D. H. Sliney, P. A. Smith, B. E. Stuc, S. A. Tell, M. L. Wolbarsht, and G. I. Zheltov, “Revision of guidelines on limits of exposure to laser radiation of wavelengths between 400  nm and 1.4  μm,” Health Phys. 79, 431–440 (2000).
[Crossref]

1998 (3)

C. Abels, S. Karrer, W. Bäumler, A. E. Goetz, M. Landthaler, and R. M. Szeimies, “Indocyanine green and laser light for the treatment of AIDS-associated cutaneous Kaposi’s sarcoma,” Br. J. Cancer 77, 1021–1024 (1998).
[Crossref]

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S. Mordon, J. M. Devoisselle, S. Soulie-Begu, and T. Desmettre, “Indocyanine green: physicochemical factors affecting its fluorescence in vivo,” Microvasc. Res. 55, 146–152 (1998).
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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, 592–600 (1960).
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M. Aas, Q. Chen, A. Jonáš, A. Kiraz, and X. Fan, “Optofluidic FRET lasers and their applications in novel photonic devices and biochemical sensing,” IEEE J. Sel. Top. Quantum Electron. 22, 1–15 (2016).
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C. Abels, S. Karrer, W. Bäumler, A. E. Goetz, M. Landthaler, and R. M. Szeimies, “Indocyanine green and laser light for the treatment of AIDS-associated cutaneous Kaposi’s sarcoma,” Br. J. Cancer 77, 1021–1024 (1998).
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J. Zheng, N. Muhanna, R. D. Souza, H. Wada, H. Chan, M. K. Akens, T. Anayama, K. Yasufuku, S. Serra, J. Irish, C. Allen, and D. Jaffray, “A multimodal nano agent for image-guided cancer surgery,” Biomaterials 67, 160–168 (2015).
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J. Zheng, N. Muhanna, R. D. Souza, H. Wada, H. Chan, M. K. Akens, T. Anayama, K. Yasufuku, S. Serra, J. Irish, C. Allen, and D. Jaffray, “A multimodal nano agent for image-guided cancer surgery,” Biomaterials 67, 160–168 (2015).
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J. Zheng, N. Muhanna, R. D. Souza, H. Wada, H. Chan, M. K. Akens, T. Anayama, K. Yasufuku, S. Serra, J. Irish, C. Allen, and D. Jaffray, “A multimodal nano agent for image-guided cancer surgery,” Biomaterials 67, 160–168 (2015).
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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, 2943–2952 (2009).
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M. A. Noginov, G. Zhu, A. M. Belgrave, R. Bakker, V. M. Shalaev, E. E. Narimanov, S. Stout, E. Herz, T. Suteewong, and U. Wiesner, “Demonstration of a spaser-based nanolaser,” Nature 460, 1110–1112 (2009).
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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, 236 (2009).
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M. Mihara, I. Kisu, H. Hara, T. Iida, T. Yamamoto, J. Araki, Y. Hayashi, H. Moriguchi, M. Narushima, and K. Banno, “Uterus autotransplantation in cynomolgus macaques: intraoperative evaluation of uterine blood flow using indocyanine green,” Hum. Reprod. 26, 3019–3027 (2011).
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Barman, I.

N. Lue, J. W. Kang, C.-C. Yu, I. Barman, N. C. Dingari, M. S. Feld, R. R. Dasari, and M. Fitzmaurice, “Portable optical fiber probe-based spectroscopic scanner for rapid cancer diagnosis: a new tool for intraoperative margin assessment,” PLoS One 7, e30887 (2012).
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Bäumler, W.

C. Abels, S. Karrer, W. Bäumler, A. E. Goetz, M. Landthaler, and R. M. Szeimies, “Indocyanine green and laser light for the treatment of AIDS-associated cutaneous Kaposi’s sarcoma,” Br. J. Cancer 77, 1021–1024 (1998).
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M. A. Noginov, G. Zhu, A. M. Belgrave, R. Bakker, V. M. Shalaev, E. E. Narimanov, S. Stout, E. Herz, T. Suteewong, and U. Wiesner, “Demonstration of a spaser-based nanolaser,” Nature 460, 1110–1112 (2009).
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M. Y. Berezin, K. Guo, W. Akers, J. Livingston, M. Solomon, H. Lee, K. Liang, A. Agee, and S. Achilefu, “Rational approach to select small peptide molecular probes labeled with fluorescent cyanine dyes for in vivo optical imaging,” Biochemistry 50, 2691–2700 (2011).
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L. Boni, G. David, A. Mangano, G. Dionigi, S. Rausei, S. Spampatti, E. Cassinotti, and A. Fingerhut, “Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery,” Surg. Endosc. 29, 2046–2055 (2015).
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C. Vinegoni, I. Botnaru, E. Aikawa, M. A. Calfon, Y. Iwamoto, E. J. Folco, V. Ntziachristos, R. Weissleder, P. Libby, and F. A. Jaffer, “Indocyanine green enables near-infrared fluorescence imaging of lipid-rich, inflamed atherosclerotic plaques,” Sci. Transl. Med. 3, 84ra45 (2011).
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Brar, V. 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, 236 (2009).
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P. Liu, C. Yue, B. Shi, G. Gao, M. Li, B. Wang, Y. Ma, and L. Cai, “Dextran based sensitive theranostic nanoparticles for near-infrared imaging and photothermal therapy in vitro,” Chem. Commun. 49, 6143–6145 (2013).
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C. Zheng, M. Zheng, P. Gong, D. Jia, P. Zhang, B. Shi, Z. Sheng, Y. Ma, and L. Cai, “Indocyanine green-loaded biodegradable tumor targeting nanoprobes for in vitro and in vivo imaging,” Biomaterials 33, 5603–5609 (2012).
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Calfon, M. A.

C. Vinegoni, I. Botnaru, E. Aikawa, M. A. Calfon, Y. Iwamoto, E. J. Folco, V. Ntziachristos, R. Weissleder, P. Libby, and F. A. Jaffer, “Indocyanine green enables near-infrared fluorescence imaging of lipid-rich, inflamed atherosclerotic plaques,” Sci. Transl. Med. 3, 84ra45 (2011).
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Cassinotti, E.

L. Boni, G. David, A. Mangano, G. Dionigi, S. Rausei, S. Spampatti, E. Cassinotti, and A. Fingerhut, “Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery,” Surg. Endosc. 29, 2046–2055 (2015).
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Chalam, K.

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, 236 (2009).
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Chan, H.

J. Zheng, N. Muhanna, R. D. Souza, H. Wada, H. Chan, M. K. Akens, T. Anayama, K. Yasufuku, S. Serra, J. Irish, C. Allen, and D. Jaffray, “A multimodal nano agent for image-guided cancer surgery,” Biomaterials 67, 160–168 (2015).
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Chen, J.

W. Wang, C. Zhou, T. Zhang, J. Chen, S. Liu, and X. Fan, “Optofluidic laser array based on stable high-Q Fabry–Pérot microcavities,” Lab Chip 15, 3862–3869 (2015).
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Chen, Q.

M. Aas, Q. Chen, A. Jonáš, A. Kiraz, and X. Fan, “Optofluidic FRET lasers and their applications in novel photonic devices and biochemical sensing,” IEEE J. Sel. Top. Quantum Electron. 22, 1–15 (2016).
[Crossref]

Y.-C. Chen, Q. Chen, and X. Fan, “Optofluidic chlorophyll lasers,” Lab Chip 16, 2228–2235 (2016).
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Q. Chen, A. Kiraz, and X. Fan, “Optofluidic FRET lasers using aqueous quantum dots as donors,” Lab Chip 16, 353–359 (2016).
[Crossref]

Q. Chen, M. Ritt, S. Sivaramakrishnan, Y. Sun, and X. Fan, “Optofluidic lasers with a single molecular layer of gain,” Lab Chip 14, 4590–4595 (2014).
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X. Wu, M. K. Khaing Oo, K. Reddy, Q. Chen, Y. Sun, and X. Fan, “Optofluidic laser for dual-mode sensitive biomolecular detection with a large dynamic range,” Nat. Commun. 5, 3779 (2014).

Q. Chen, X. Zhang, Y. Sun, M. Ritt, S. Sivaramakrishnan, and X. Fan, “Highly sensitive fluorescent protein FRET detection using optofluidic lasers,” Lab Chip 13, 2679–2681 (2013).
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Chen, Y.-C.

Y.-C. Chen, Q. Chen, and X. Fan, “Optofluidic chlorophyll lasers,” Lab Chip 16, 2228–2235 (2016).
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Cherrick, G. R.

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, 592–600 (1960).
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Chi, C.

C. Fang, K. Wang, C. Zeng, C. Chi, W. Shang, J. Ye, Y. Mao, Y. Fan, J. Yang, and N. Xiang, “Illuminating necrosis: from mechanistic exploration to preclinical application using fluorescence molecular imaging with indocyanine green,” Sci. Rep. 6, 21013 (2016).

Cho, H. S.

S. Lee, M. W. Lee, H. S. Cho, J. W. Song, H. S. Nam, D. J. Oh, K. Park, W.-Y. Oh, H. Yoo, and J. W. Kim, “Fully integrated high-speed intravascular optical coherence tomography/near-infrared fluorescence structural/molecular imaging in vivo using a clinically available near-infrared fluorescence-emitting indocyanine green to detect inflamed lipid-rich atheromata in coronary-sized vessels,” Circulation 7, 560–569 (2014).

Choyke, P. L.

M. Ogawa, N. Kosaka, P. L. Choyke, and H. Kobayashi, “In vivo molecular imaging of cancer with a quenching near-infrared fluorescent probe using conjugates of monoclonal antibodies and indocyanine green,” Cancer Res. 69, 1268–1272 (2009).
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Courant, D.

R. Matthes, C. P. Cain, D. Courant, D. A. Freund, B. A. Grossman, P. A. Kennedy, D. J. Lund, M. A. Mainster, A. A. Manenkov, W. J. Marshall, R. McCally, B. A. Rockwell, D. H. Sliney, P. A. Smith, B. E. Stuc, S. A. Tell, M. L. Wolbarsht, and G. I. Zheltov, “Revision of guidelines on limits of exposure to laser radiation of wavelengths between 400  nm and 1.4  μm,” Health Phys. 79, 431–440 (2000).
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Cupps, J. M.

Dasari, R. R.

N. Lue, J. W. Kang, C.-C. Yu, I. Barman, N. C. Dingari, M. S. Feld, R. R. Dasari, and M. Fitzmaurice, “Portable optical fiber probe-based spectroscopic scanner for rapid cancer diagnosis: a new tool for intraoperative margin assessment,” PLoS One 7, e30887 (2012).
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David, G.

L. Boni, G. David, A. Mangano, G. Dionigi, S. Rausei, S. Spampatti, E. Cassinotti, and A. Fingerhut, “Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery,” Surg. Endosc. 29, 2046–2055 (2015).
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Davidson, C. S.

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, 592–600 (1960).
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DeJesus, E. M.

R. P. Judy, J. J. Keating, E. M. DeJesus, J. X. Jiang, O. T. Okusanya, S. Nie, D. E. Holt, S. P. Arlauckas, P. S. Low, and E. J. Delikatny, “Quantification of tumor fluorescence during intraoperative optical cancer imaging,” Sci. Rep. 5, 16208 (2015).

Delikatny, E. J.

R. P. Judy, J. J. Keating, E. M. DeJesus, J. X. Jiang, O. T. Okusanya, S. Nie, D. E. Holt, S. P. Arlauckas, P. S. Low, and E. J. Delikatny, “Quantification of tumor fluorescence during intraoperative optical cancer imaging,” Sci. Rep. 5, 16208 (2015).

Deshpande, C.

D. Holt, A. B. Parthasarathy, O. Okusanya, J. Keating, O. Venegas, C. Deshpande, G. Karakousis, B. Madajewski, A. Durham, and S. Nie, “Intraoperative near-infrared fluorescence imaging and spectroscopy identifies residual tumor cells in wounds,” J. Biomed. Opt. 20, 076002 (2015).
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Desmettre, T.

T. Desmettre, J. Devoisselle, and S. Mordon, “Fluorescence properties and metabolic features of indocyanine green (ICG) as related to angiography,” Surv. Ophthalmol. 45, 15–27 (2000).
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S. Mordon, J. M. Devoisselle, S. Soulie-Begu, and T. Desmettre, “Indocyanine green: physicochemical factors affecting its fluorescence in vivo,” Microvasc. Res. 55, 146–152 (1998).
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Devoisselle, J.

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

S. Mordon, J. M. Devoisselle, S. Soulie-Begu, and T. Desmettre, “Indocyanine green: physicochemical factors affecting its fluorescence in vivo,” Microvasc. Res. 55, 146–152 (1998).
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Dingari, N. C.

N. Lue, J. W. Kang, C.-C. Yu, I. Barman, N. C. Dingari, M. S. Feld, R. R. Dasari, and M. Fitzmaurice, “Portable optical fiber probe-based spectroscopic scanner for rapid cancer diagnosis: a new tool for intraoperative margin assessment,” PLoS One 7, e30887 (2012).
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Dionigi, G.

L. Boni, G. David, A. Mangano, G. Dionigi, S. Rausei, S. Spampatti, E. Cassinotti, and A. Fingerhut, “Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery,” Surg. Endosc. 29, 2046–2055 (2015).
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Durham, A.

D. Holt, A. B. Parthasarathy, O. Okusanya, J. Keating, O. Venegas, C. Deshpande, G. Karakousis, B. Madajewski, A. Durham, and S. Nie, “Intraoperative near-infrared fluorescence imaging and spectroscopy identifies residual tumor cells in wounds,” J. Biomed. Opt. 20, 076002 (2015).
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Duvoll-Young, J.

S. Yoneya, T. Saito, Y. Komatsu, I. Koyama, K. Takahashi, and J. Duvoll-Young, “Binding properties of indocyanine green in human blood,” Invest. Ophthalmol. Vis. Sci. 39, 1286–1290 (1998).

Fan, X.

M. Aas, Q. Chen, A. Jonáš, A. Kiraz, and X. Fan, “Optofluidic FRET lasers and their applications in novel photonic devices and biochemical sensing,” IEEE J. Sel. Top. Quantum Electron. 22, 1–15 (2016).
[Crossref]

Y.-C. Chen, Q. Chen, and X. Fan, “Optofluidic chlorophyll lasers,” Lab Chip 16, 2228–2235 (2016).
[Crossref]

Q. Chen, A. Kiraz, and X. Fan, “Optofluidic FRET lasers using aqueous quantum dots as donors,” Lab Chip 16, 353–359 (2016).
[Crossref]

W. Wang, C. Zhou, T. Zhang, J. Chen, S. Liu, and X. Fan, “Optofluidic laser array based on stable high-Q Fabry–Pérot microcavities,” Lab Chip 15, 3862–3869 (2015).
[Crossref]

Q. Chen, M. Ritt, S. Sivaramakrishnan, Y. Sun, and X. Fan, “Optofluidic lasers with a single molecular layer of gain,” Lab Chip 14, 4590–4595 (2014).
[Crossref]

X. Wu, M. K. Khaing Oo, K. Reddy, Q. Chen, Y. Sun, and X. Fan, “Optofluidic laser for dual-mode sensitive biomolecular detection with a large dynamic range,” Nat. Commun. 5, 3779 (2014).

X. Fan and S.-H. Yun, “The potential of optofluidic biolasers,” Nat. Methods 11, 141–147 (2014).
[Crossref]

Q. Chen, X. Zhang, Y. Sun, M. Ritt, S. Sivaramakrishnan, and X. Fan, “Highly sensitive fluorescent protein FRET detection using optofluidic lasers,” Lab Chip 13, 2679–2681 (2013).
[Crossref]

X. Zhang, W. Lee, and X. Fan, “Bio-switchable optofluidic lasers based on DNA Holliday junctions,” Lab Chip 12, 3673–3675 (2012).
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Y. Sun and X. Fan, “Distinguishing DNA by analog-to-digital-like conversion by using optofluidic lasers,” Angew. Chem. Int. Ed. 51, 1236–1239 (2012).

W. Lee and X. Fan, “Intracavity DNA melting analysis with optofluidic lasers,” Anal. Chem. 84, 9558–9563 (2012).

S. Lacey, I. M. White, Y. Sun, S. I. Shopova, J. M. Cupps, P. Zhang, and X. Fan, “Versatile microfluidic lasers based on opto-fluidic ring resonators,” Opt. Express 15, 15523–15530 (2007).
[Crossref]

S. I. Shopova, H. Zhu, X. Fan, and P. Zhang, “Optofluidic ring resonator based dye laser,” Appl. Phys. Lett. 90, 221101 (2007).
[Crossref]

Fan, Y.

C. Fang, K. Wang, C. Zeng, C. Chi, W. Shang, J. Ye, Y. Mao, Y. Fan, J. Yang, and N. Xiang, “Illuminating necrosis: from mechanistic exploration to preclinical application using fluorescence molecular imaging with indocyanine green,” Sci. Rep. 6, 21013 (2016).

Fang, C.

C. Fang, K. Wang, C. Zeng, C. Chi, W. Shang, J. Ye, Y. Mao, Y. Fan, J. Yang, and N. Xiang, “Illuminating necrosis: from mechanistic exploration to preclinical application using fluorescence molecular imaging with indocyanine green,” Sci. Rep. 6, 21013 (2016).

Fei, B.

G. Lu and B. Fei, “Medical hyperspectral imaging: a review,” J. Biomed. Opt. 19, 010901 (2014).
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Feld, M. S.

N. Lue, J. W. Kang, C.-C. Yu, I. Barman, N. C. Dingari, M. S. Feld, R. R. Dasari, and M. Fitzmaurice, “Portable optical fiber probe-based spectroscopic scanner for rapid cancer diagnosis: a new tool for intraoperative margin assessment,” PLoS One 7, e30887 (2012).
[Crossref]

Fingerhut, A.

L. Boni, G. David, A. Mangano, G. Dionigi, S. Rausei, S. Spampatti, E. Cassinotti, and A. Fingerhut, “Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery,” Surg. Endosc. 29, 2046–2055 (2015).
[Crossref]

Fitzmaurice, M.

N. Lue, J. W. Kang, C.-C. Yu, I. Barman, N. C. Dingari, M. S. Feld, R. R. Dasari, and M. Fitzmaurice, “Portable optical fiber probe-based spectroscopic scanner for rapid cancer diagnosis: a new tool for intraoperative margin assessment,” PLoS One 7, e30887 (2012).
[Crossref]

Folco, E. J.

C. Vinegoni, I. Botnaru, E. Aikawa, M. A. Calfon, Y. Iwamoto, E. J. Folco, V. Ntziachristos, R. Weissleder, P. Libby, and F. A. Jaffer, “Indocyanine green enables near-infrared fluorescence imaging of lipid-rich, inflamed atherosclerotic plaques,” Sci. Transl. Med. 3, 84ra45 (2011).
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Frangioni, J. V.

B. E. Schaafsma, J. S. D. Mieog, M. Hutteman, J. R. Van der Vorst, P. J. Kuppen, C. W. Löwik, J. V. Frangioni, C. J. Van de Velde, and A. L. Vahrmeijer, “The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery,” J. Surg. Oncol. 104, 323–332 (2011).
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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, 2943–2952 (2009).
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Freund, D. A.

R. Matthes, C. P. Cain, D. Courant, D. A. Freund, B. A. Grossman, P. A. Kennedy, D. J. Lund, M. A. Mainster, A. A. Manenkov, W. J. Marshall, R. McCally, B. A. Rockwell, D. H. Sliney, P. A. Smith, B. E. Stuc, S. A. Tell, M. L. Wolbarsht, and G. I. Zheltov, “Revision of guidelines on limits of exposure to laser radiation of wavelengths between 400  nm and 1.4  μm,” Health Phys. 79, 431–440 (2000).
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Gao, G.

P. Liu, C. Yue, B. Shi, G. Gao, M. Li, B. Wang, Y. Ma, and L. Cai, “Dextran based sensitive theranostic nanoparticles for near-infrared imaging and photothermal therapy in vitro,” Chem. Commun. 49, 6143–6145 (2013).
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Gather, M. C.

M. C. Gather and S. H. Yun, “Single-cell biological lasers,” Nat. Photonics 5, 406–410 (2011).
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Gibbs-Strauss, S. L.

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, 2943–2952 (2009).
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Gioux, S.

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Anal. Chem. (1)

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Ann. Biomed. Eng. (1)

P. R. van den Biesen, F. H. Jongsma, G. J. Tangelder, and D. W. Slaaf, “Yield of fluorescence from indocyanine green in plasma and flowing blood,” Ann. Biomed. Eng. 23, 475–481 (1995).
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Ann. Surg. Oncol. (1)

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Appl. Phys. Lett. (2)

R. C. Polson and Z. V. Vardeny, “Random lasing in human tissues,” Appl. Phys. Lett. 85, 1289–1291 (2004).
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Biochemistry (2)

M. Y. Berezin, K. Guo, W. Akers, J. Livingston, M. Solomon, H. Lee, K. Liang, A. Agee, and S. Achilefu, “Rational approach to select small peptide molecular probes labeled with fluorescent cyanine dyes for in vivo optical imaging,” Biochemistry 50, 2691–2700 (2011).
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C. Zheng, M. Zheng, P. Gong, D. Jia, P. Zhang, B. Shi, Z. Sheng, Y. Ma, and L. Cai, “Indocyanine green-loaded biodegradable tumor targeting nanoprobes for in vitro and in vivo imaging,” Biomaterials 33, 5603–5609 (2012).
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Chem. Commun. (1)

P. Liu, C. Yue, B. Shi, G. Gao, M. Li, B. Wang, Y. Ma, and L. Cai, “Dextran based sensitive theranostic nanoparticles for near-infrared imaging and photothermal therapy in vitro,” Chem. Commun. 49, 6143–6145 (2013).
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Circulation (1)

S. Lee, M. W. Lee, H. S. Cho, J. W. Song, H. S. Nam, D. J. Oh, K. Park, W.-Y. Oh, H. Yoo, and J. W. Kim, “Fully integrated high-speed intravascular optical coherence tomography/near-infrared fluorescence structural/molecular imaging in vivo using a clinically available near-infrared fluorescence-emitting indocyanine green to detect inflamed lipid-rich atheromata in coronary-sized vessels,” Circulation 7, 560–569 (2014).

Eur. J. Vasc. Endovasc. Surg. (1)

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Health Phys. (1)

R. Matthes, C. P. Cain, D. Courant, D. A. Freund, B. A. Grossman, P. A. Kennedy, D. J. Lund, M. A. Mainster, A. A. Manenkov, W. J. Marshall, R. McCally, B. A. Rockwell, D. H. Sliney, P. A. Smith, B. E. Stuc, S. A. Tell, M. L. Wolbarsht, and G. I. Zheltov, “Revision of guidelines on limits of exposure to laser radiation of wavelengths between 400  nm and 1.4  μm,” Health Phys. 79, 431–440 (2000).
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Hum. Reprod. (1)

M. Mihara, I. Kisu, H. Hara, T. Iida, T. Yamamoto, J. Araki, Y. Hayashi, H. Moriguchi, M. Narushima, and K. Banno, “Uterus autotransplantation in cynomolgus macaques: intraoperative evaluation of uterine blood flow using indocyanine green,” Hum. Reprod. 26, 3019–3027 (2011).
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IEEE J. Sel. Top. Quantum Electron. (2)

B. Jung, V. I. Vullev, and B. Anvari, “Revisiting indocyanine green: effects of serum and physiological temperature on absorption and fluorescence characteristics,” IEEE J. Sel. Top. Quantum Electron. 20, 149–157 (2014).
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Int. J. Biomed. Imaging (1)

J. T. Alander, I. Kaartinen, A. Laakso, T. Pätilä, T. Spillmann, V. V. Tuchin, M. Venermo, and P. Välisuo, “A review of indocyanine green fluorescent imaging in surgery,” Int. J. Biomed. Imaging 2012, 940585 (2012).

Invest. Ophthalmol. Vis. Sci. (1)

S. Yoneya, T. Saito, Y. Komatsu, I. Koyama, K. Takahashi, and J. Duvoll-Young, “Binding properties of indocyanine green in human blood,” Invest. Ophthalmol. Vis. Sci. 39, 1286–1290 (1998).

J. Biomed. Opt. (2)

G. Lu and B. Fei, “Medical hyperspectral imaging: a review,” J. Biomed. Opt. 19, 010901 (2014).
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J. Woitzik, P. Horn, P. Vajkoczy, and P. Schmiedek, “Intraoperative control of extracranial-intracranial bypass patency by near-infrared indocyanine green videoangiography,” J. Neurosurg. 102, 692–698 (2005).
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J. Surg. Oncol. (1)

B. E. Schaafsma, J. S. D. Mieog, M. Hutteman, J. R. Van der Vorst, P. J. Kuppen, C. W. Löwik, J. V. Frangioni, C. J. Van de Velde, and A. L. Vahrmeijer, “The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery,” J. Surg. Oncol. 104, 323–332 (2011).
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Lab Chip (6)

X. Zhang, W. Lee, and X. Fan, “Bio-switchable optofluidic lasers based on DNA Holliday junctions,” Lab Chip 12, 3673–3675 (2012).
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Q. Chen, X. Zhang, Y. Sun, M. Ritt, S. Sivaramakrishnan, and X. Fan, “Highly sensitive fluorescent protein FRET detection using optofluidic lasers,” Lab Chip 13, 2679–2681 (2013).
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Q. Chen, A. Kiraz, and X. Fan, “Optofluidic FRET lasers using aqueous quantum dots as donors,” Lab Chip 16, 353–359 (2016).
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Q. Chen, M. Ritt, S. Sivaramakrishnan, Y. Sun, and X. Fan, “Optofluidic lasers with a single molecular layer of gain,” Lab Chip 14, 4590–4595 (2014).
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Y.-C. Chen, Q. Chen, and X. Fan, “Optofluidic chlorophyll lasers,” Lab Chip 16, 2228–2235 (2016).
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W. Wang, C. Zhou, T. Zhang, J. Chen, S. Liu, and X. Fan, “Optofluidic laser array based on stable high-Q Fabry–Pérot microcavities,” Lab Chip 15, 3862–3869 (2015).
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Supplementary Material (1)

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Figures (6)

Fig. 1.
Fig. 1. (a) Schematic diagram showing the composition of blood. The diagram in the rightmost column lists the serological components along with their respective typical concentrations in serum, which we have investigated in the current work. Green checks denote that lasing was achieved with those components when indocyanine green (ICG) within the clinically acceptable concentration range was added, whereas the red cross denotes the component that no lasing was observed from ICG. In addition to testing with serological components, lasing from ICG (within the clinically acceptable concentration range) was observed when it was added to serum and whole blood. (b) Schematic of the ICG laser using a high Q -factor optofluidic ring resonator (OFRR). It also illustrates that ICG lasing can only be achieved when ICG binds to serological components such as albumin and lipoprotein. The green circles denote ICG molecules, whereas the red circles denote serological components. During the experiment, ICG was excited by a pulsed optical parametric oscillator (OPO) (pulsewidth, 5 ns; wavelength, 660 nm). (c) Comparison among various emission spectra of ICG. Curve 1, ICG alone in PBS; Curve 2, ICG alone in DI water; Curve 3, ICG with albumin (BSA) in PBS. All curves were obtained under the same pump energy density of 4.8    μJ / mm 2 with the same ICG concentration of 0.4 mM. Curves are vertically shifted for clarity.
Fig. 2.
Fig. 2. (a) Lasing spectra of ICG bound to albumin (BSA) with different molar ratios (BSA:ICG varying from 2 1 to 3.3 1 ). All curves were obtained at the same concentration of ICG (0.4 mM) and the same pump energy density of 1.4    μJ / mm 2 . Curves are vertically shifted for clarity. (b) Spectrally integrated (900–930 nm) laser output as a function of pump energy density extracted from the spectra in (a). The solid lines represent the linear fit above the lasing threshold. (c) Lasing threshold as a function of the BSA:ICG molar ratio extracted from the linear fit in (b). The minimum threshold of 0.38    μJ / mm 2 was observed around 3 1 . The dashed curve is a quadratic fit to guide an eye. (d)–(f) Lasing spectra of (d) 0.4 mM ICG, (e) 0.2 mM ICG, and (f) 0.04 mM ICG bound to BSA under various pump energy densities. Multimode lasing with irregular spacing was observed as pump intensity increases. All curves in (d)–(f) were obtained with the same BSA:ICG molar ratio of 3 1 . Curves are vertically shifted for clarity. (g) Spectrally integrated (900–930 nm) laser output as a function of pump energy density extracted from the spectra in (d)–(f). The threshold based on the linear fit (solid lines) is approximately 0.4, 2.3, and 5.3    μJ / mm 2 , respectively, for 0.4, 0.2, and 0.04 mM of ICG.
Fig. 3.
Fig. 3. Emission spectra of the mixture of ICG (0.2 mM) and γ -globulins of different concentrations. All curves were pumped under a pump energy density of 25    μJ / mm 2 . In humans, the average concentration of γ-globulins was approximately 0.25 mM, within the concentration range that we investigated in the current work. No lasing was observed. Curves are vertically shifted for clarity.
Fig. 4.
Fig. 4. (a) Lasing spectra of ICG bound to low-density lipoprotein (LDL) under various pump energy densities. The respective concentration of ICG and LDL was 0.2 and 0.01 mM, respectively. Curves are vertically shifted for clarity. (b) Spectrally integrated (920–940 nm) laser output as a function of pump energy density extracted from the lasing spectra. The threshold obtained from the linear fit is approximately 0.17    μJ / mm 2 .
Fig. 5.
Fig. 5. (a) Lasing spectra of ICG bound to human serum under various pump energy densities. The concentration of ICG was 0.2 mM. Curves are vertically shifted for clarity. (b) Spectrally integrated (920–940 nm) laser output as a function of pump energy density extracted from (a). The threshold obtained from the linear fit is approximately 0.45    μJ / mm 2 .
Fig. 6.
Fig. 6. (a) Schematic showing the excitation process of human whole blood flowing through an OFRR. RBC, red blood cell; WBC, white blood cell (leukocytes). (b) “Blood” lasing spectra under various pump energy densities when ICG (0.04 mM) was injected into the OFRR along with real human whole blood ( 2 × diluted with PBS buffer to avoid clogging). Curves are vertically shifted for clarity. (c) Spectrally integrated (900–930 nm) laser output as a function of pump energy density extracted from the lasing spectra. (d) Concentration dependent study of the “blood” lasing with various ICG concentrations (0.01–0.06 mM) in human whole blood ( 2 × dilution with PBS buffer to avoid clogging). A red shift is observed as the pump increases. No lasing emission was observed when the ICG concentration was above 0.06 mM. The pump energy density was fixed at 20    μJ / mm 2 . Curves are vertically shifted for clarity.

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