Abstract

Red blood cells (RBC) in two-photon excited fluorescence (TPEF) microscopy usually appear as dark disks because of their low fluorescent signal. Here we use 15fs 800nm pulses for TPEF, 45fs 1060nm pulses for three-photon excited fluorescence, and third harmonic generation (THG) imaging. We find sufficient fluorescent signal that we attribute to hemoglobin fluorescence after comparing time and wavelength resolved spectra of other expected RBC endogenous fluorophores: NADH, FAD, biliverdin, and bilirubin. We find that both TPEF and THG microscopy can be used to examine erythrocyte morphology non-invasively without breaching a blood storage bag.

© 2016 Optical Society of America

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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2015 (2)

K. Jaferzadeh and I. Moon, “Quantitative investigation of red blood cell three-dimensional geometric and chemical changes in the storage lesion using digital holographic microscopy,” J. Biomed. Opt. 20(11), 111218 (2015).
[Crossref] [PubMed]

Q. Sun, W. Zheng, J. Wang, Y. Luo, and J. Y. Qu, “Mechanism of two-photon excited hemoglobin fluorescence emission,” J. Biomed. Opt. 20(10), 105014 (2015).
[Crossref] [PubMed]

2014 (2)

Y. Wang, A. Giebink, and D. M. Spence, “Microfluidic evaluation of red cells collected and stored in modified processing solutions used in blood banking,” Integr. Biol. 6(1), 65–75 (2014).
[Crossref] [PubMed]

O. N. Salaria, V. M. Barodka, C. W. Hogue, D. E. Berkowitz, P. M. Ness, J. O. Wasey, and S. M. Frank, “Impaired red blood cell deformability after transfusion of stored allogeneic blood but not autologous salvaged blood in cardiac surgery patients,” Anesth. Analg. 118(6), 1179–1187 (2014).
[Crossref] [PubMed]

2013 (4)

S. M. Frank, B. Abazyan, M. Ono, C. W. Hogue, D. B. Cohen, D. E. Berkowitz, P. M. Ness, and V. M. Barodka, “Decreased erythrocyte deformability after transfusion and the effects of erythrocyte storage duration,” Anesth. Analg. 116(5), 975–981 (2013).
[Crossref] [PubMed]

I. Moon, F. Yi, Y. H. Lee, B. Javidi, D. Boss, and P. Marquet, “Automated quantitative analysis of 3D morphology and mean corpuscular hemoglobin in human red blood cells stored in different periods,” Opt. Express 21(25), 30947–30957 (2013).
[Crossref] [PubMed]

I. Moon, F. Yi, Y. H. Lee, B. Javidi, D. Boss, and P. Marquet, “Automated quantitative analysis of 3D morphology and mean corpuscular hemoglobin in human red blood cells stored in different periods,” Opt. Express 21(25), 30947–30957 (2013).
[Crossref] [PubMed]

Y. Zeng, B. Yan, Q. Sun, S. K. Teh, W. Zhang, Z. Wen, and J. Y. Qu, “Label-free in vivo imaging of human leukocytes using two-photon excited endogenous fluorescence,” J. Biomed. Opt. 18(4), 040504 (2013).
[Crossref] [PubMed]

2012 (2)

2011 (4)

B. Nie, D. Pestov, F. W. Wise, and M. Dantus, “An ultrafast fiber laser with self-similar evolution in the gain segment,” Opt. Photonics News 22(12), 47 (2011).
[Crossref]

D. Li, W. Zheng, Y. Zeng, Y. Luo, and J. Y. Qu, “Two-photon excited hemoglobin fluorescence provides contrast mechanism for label-free imaging of microvasculature in vivo,” Opt. Lett. 36(6), 834–836 (2011).
[Crossref] [PubMed]

A. H. M. van Straten, M. A. Soliman Hamad, A. A. van Zundert, E. J. Martens, J. F. ter Woorst, A. M. de Wolf, and V. Scharnhorst, “Effect of duration of red blood cell storage on early and late mortality after coronary artery bypass grafting,” J. Thorac. Cardiovasc. Surg. 141(1), 231–237 (2011).
[Crossref] [PubMed]

W. Zheng, D. Li, Y. Zeng, Y. Luo, and J. Y. Qu, “Two-photon excited hemoglobin fluorescence,” Biomed. Opt. Express 2(1), 71–79 (2011).
[Crossref] [PubMed]

2010 (4)

G. Edgren, M. Kamper-Jørgensen, S. Eloranta, K. Rostgaard, B. Custer, H. Ullum, E. L. Murphy, M. P. Busch, M. Reilly, M. Melbye, H. Hjalgrim, and O. Nyrén, “Duration of red blood cell storage and survival of transfused patients (CME),” Transfusion 50(6), 1185–1195 (2010).
[Crossref] [PubMed]

S. D. Robinson, C. Janssen, E. B. Fretz, B. Berry, A. J. Chase, A. D. Siega, R. G. Carere, A. Fung, G. Simkus, W. P. Klinke, and J. D. Hilton, “Red blood cell storage duration and mortality in patients undergoing percutaneous coronary intervention,” Am. Heart J. 159(5), 876–881 (2010).
[Crossref] [PubMed]

S. Lu, W. Min, S. Chong, G. R. Holtom, and X. S. Xie, “Label-free imaging of heme proteins with two-photon excited photothermal lens microscopy,” Appl. Phys. Lett. 96(11), 113701 (2010).
[Crossref]

R. Dasgupta, S. Ahlawat, R. S. Verma, A. Uppal, and P. K. Gupta, “Hemoglobin degradation in human erythrocytes with long-duration near-infrared laser exposure in Raman optical tweezers,” J. Biomed. Opt. 15(5), 055009 (2010).
[Crossref] [PubMed]

2009 (3)

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, and X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature 461(7267), 1105–1109 (2009).
[Crossref] [PubMed]

P. Xi, Y. Andegeko, D. Pestov, V. V. Lovozoy, and M. Dantus, “Two-photon imaging using adaptive phase compensated ultrashort laser pulses,” J. Biomed. Opt. 14(1), 014002 (2009).
[Crossref] [PubMed]

A. B. Zimrin and J. R. Hess, “Current issues relating to the transfusion of stored red blood cells,” Vox Sang. 96(2), 93–103 (2009).
[Crossref] [PubMed]

2007 (4)

D. Fu, T. Ye, T. E. Matthews, B. J. Chen, G. Yurtserver, and W. S. Warren, “High-resolution in vivo imaging of blood vessels without labeling,” Opt. Lett. 32(18), 2641–2643 (2007).
[Crossref] [PubMed]

G. O. Clay, C. B. Schaffer, and D. Kleinfeld, “Large two-photon absorptivity of hemoglobin in the infrared range of 780-880 nm,” J. Chem. Phys. 126(2), 025102 (2007).
[Crossref] [PubMed]

J. A. Meyer, J. M. Froelich, G. E. Reid, W. K. Karunarathne, and D. M. Spence, “Metal-activated C-peptide Facilitates Glucose Clearance and the Release of a Nitric Oxide Stimulus via the GLUT1 Transporter,” Diabetologia 51(1), 175–182 (2007).
[Crossref] [PubMed]

D. Débarre, N. Olivier, and E. Beaurepaire, “Signal epidetection in third-harmonic generation microscopy of turbid media,” Opt. Express 15(14), 8913–8924 (2007).
[Crossref] [PubMed]

2006 (1)

2003 (1)

E. Chaigneau, M. Oheim, E. Audinat, and S. Charpak, “Two-photon imaging of capillary blood flow in olfactory bulb glomeruli,” Proc. Natl. Acad. Sci. U.S.A. 100(22), 13081–13086 (2003).
[Crossref] [PubMed]

2002 (1)

R. Jimenez and F. E. Romesberg, “Excited state dynamics and heterogeneity of folded and unfolded states of cytochrome C,” J. Phys. Chem. B 106(35), 9172–9180 (2002).
[Crossref]

2000 (1)

R. D. Schaller, J. C. Johnson, and R. J. Saykally, “Nonlinear chemical imaging microscopy: near-field third harmonic generation imaging of human red blood cells,” Anal. Chem. 72(21), 5361–5364 (2000).
[Crossref] [PubMed]

1997 (1)

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
[Crossref]

1996 (1)

C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, “Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 93(20), 10763–10768 (1996).
[Crossref] [PubMed]

1995 (1)

B. Kierdaszuk, I. Gryczynski, A. Modrak-Wojcik, A. Bzowska, D. Shugar, and J. R. Lakowicz, “Fluorescence of tyrosine and tryptophan in proteins using one- and two-photon excitation,” Photochem. Photobiol. 61(4), 319–324 (1995).
[Crossref] [PubMed]

1993 (1)

A. A. Rehms and P. R. Callis, “Two-photon fluorescence excitation spectra of aromatic amino acids,” Chem. Phys. Lett. 208(3-4), 276–282 (1993).
[Crossref]

1985 (1)

L. M. Snyder, F. Garver, S. C. Liu, L. Leb, J. Trainor, and N. L. Fortier, “Demonstration of haemoglobin associated with isolated, purified spectrin from senescent human red cells,” Br. J. Haematol. 61(3), 415–419 (1985).
[Crossref] [PubMed]

1979 (1)

P. P. Ho and R. R. Alfano, “Optical Kerr Effect in Liquids,” Phys. Rev. A 20(5), 2170–2187 (1979).
[Crossref]

1978 (1)

S. D. Shukla, R. Coleman, J. B. Finean, and R. H. Michell, “The use of phospholipase c to detect structural changes in the membranes of human erythrocytes aged by storage,” Biochim. Biophys. Acta 512(2), 341–349 (1978).
[Crossref] [PubMed]

1975 (1)

S. Yoshida, T. Iizuka, T. Nozawa, and M. Hatano, “Studies on the charge transfer band in high spin state of ferric myoglobin and hemoglobin by low temperature optical and magnetic circular dichroism spectroscopy,” Biochim. Biophys. Acta 405(1), 122–135 (1975).
[Crossref] [PubMed]

1972 (1)

G. Brecher and M. Bessis, “Present status of spiculed red cells and their relationship to the discocyte-echinocyte transformation: a critical review,” Blood 40(3), 333–344 (1972).
[PubMed]

1963 (1)

J. T. Dodge, C. Mitchell, and D. J. Hanahan, “The preparation and chemical characteristics of hemoglobin-free ghosts of human erythrocytes,” Arch. Biochem. Biophys. 100(1), 119–130 (1963).
[Crossref] [PubMed]

Abazyan, B.

S. M. Frank, B. Abazyan, M. Ono, C. W. Hogue, D. B. Cohen, D. E. Berkowitz, P. M. Ness, and V. M. Barodka, “Decreased erythrocyte deformability after transfusion and the effects of erythrocyte storage duration,” Anesth. Analg. 116(5), 975–981 (2013).
[Crossref] [PubMed]

Ahlawat, S.

R. Dasgupta, S. Ahlawat, R. S. Verma, A. Uppal, and P. K. Gupta, “Hemoglobin degradation in human erythrocytes with long-duration near-infrared laser exposure in Raman optical tweezers,” J. Biomed. Opt. 15(5), 055009 (2010).
[Crossref] [PubMed]

Alfano, R. R.

P. P. Ho and R. R. Alfano, “Optical Kerr Effect in Liquids,” Phys. Rev. A 20(5), 2170–2187 (1979).
[Crossref]

Andegeko, Y.

P. Xi, Y. Andegeko, D. Pestov, V. V. Lovozoy, and M. Dantus, “Two-photon imaging using adaptive phase compensated ultrashort laser pulses,” J. Biomed. Opt. 14(1), 014002 (2009).
[Crossref] [PubMed]

Arkhipov, S. N.

Audinat, E.

E. Chaigneau, M. Oheim, E. Audinat, and S. Charpak, “Two-photon imaging of capillary blood flow in olfactory bulb glomeruli,” Proc. Natl. Acad. Sci. U.S.A. 100(22), 13081–13086 (2003).
[Crossref] [PubMed]

Aus-der-Au, J.

Barad, Y.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
[Crossref]

Barodka, V. M.

O. N. Salaria, V. M. Barodka, C. W. Hogue, D. E. Berkowitz, P. M. Ness, J. O. Wasey, and S. M. Frank, “Impaired red blood cell deformability after transfusion of stored allogeneic blood but not autologous salvaged blood in cardiac surgery patients,” Anesth. Analg. 118(6), 1179–1187 (2014).
[Crossref] [PubMed]

S. M. Frank, B. Abazyan, M. Ono, C. W. Hogue, D. B. Cohen, D. E. Berkowitz, P. M. Ness, and V. M. Barodka, “Decreased erythrocyte deformability after transfusion and the effects of erythrocyte storage duration,” Anesth. Analg. 116(5), 975–981 (2013).
[Crossref] [PubMed]

Beaurepaire, E.

Berkowitz, D. E.

O. N. Salaria, V. M. Barodka, C. W. Hogue, D. E. Berkowitz, P. M. Ness, J. O. Wasey, and S. M. Frank, “Impaired red blood cell deformability after transfusion of stored allogeneic blood but not autologous salvaged blood in cardiac surgery patients,” Anesth. Analg. 118(6), 1179–1187 (2014).
[Crossref] [PubMed]

S. M. Frank, B. Abazyan, M. Ono, C. W. Hogue, D. B. Cohen, D. E. Berkowitz, P. M. Ness, and V. M. Barodka, “Decreased erythrocyte deformability after transfusion and the effects of erythrocyte storage duration,” Anesth. Analg. 116(5), 975–981 (2013).
[Crossref] [PubMed]

Berry, B.

S. D. Robinson, C. Janssen, E. B. Fretz, B. Berry, A. J. Chase, A. D. Siega, R. G. Carere, A. Fung, G. Simkus, W. P. Klinke, and J. D. Hilton, “Red blood cell storage duration and mortality in patients undergoing percutaneous coronary intervention,” Am. Heart J. 159(5), 876–881 (2010).
[Crossref] [PubMed]

Bessis, M.

G. Brecher and M. Bessis, “Present status of spiculed red cells and their relationship to the discocyte-echinocyte transformation: a critical review,” Blood 40(3), 333–344 (1972).
[PubMed]

Blasi, B.

B. Blasi, A. D’Alessandro, N. Ramundo, and L. Zolla, “Red blood cell storage and cell morphology,” Transfus. Med. 22(2), 90–96 (2012).
[Crossref] [PubMed]

Boss, D.

Brecher, G.

G. Brecher and M. Bessis, “Present status of spiculed red cells and their relationship to the discocyte-echinocyte transformation: a critical review,” Blood 40(3), 333–344 (1972).
[PubMed]

Busch, M. P.

G. Edgren, M. Kamper-Jørgensen, S. Eloranta, K. Rostgaard, B. Custer, H. Ullum, E. L. Murphy, M. P. Busch, M. Reilly, M. Melbye, H. Hjalgrim, and O. Nyrén, “Duration of red blood cell storage and survival of transfused patients (CME),” Transfusion 50(6), 1185–1195 (2010).
[Crossref] [PubMed]

Bzowska, A.

B. Kierdaszuk, I. Gryczynski, A. Modrak-Wojcik, A. Bzowska, D. Shugar, and J. R. Lakowicz, “Fluorescence of tyrosine and tryptophan in proteins using one- and two-photon excitation,” Photochem. Photobiol. 61(4), 319–324 (1995).
[Crossref] [PubMed]

Callis, P. R.

A. A. Rehms and P. R. Callis, “Two-photon fluorescence excitation spectra of aromatic amino acids,” Chem. Phys. Lett. 208(3-4), 276–282 (1993).
[Crossref]

Carere, R. G.

S. D. Robinson, C. Janssen, E. B. Fretz, B. Berry, A. J. Chase, A. D. Siega, R. G. Carere, A. Fung, G. Simkus, W. P. Klinke, and J. D. Hilton, “Red blood cell storage duration and mortality in patients undergoing percutaneous coronary intervention,” Am. Heart J. 159(5), 876–881 (2010).
[Crossref] [PubMed]

Chaigneau, E.

E. Chaigneau, M. Oheim, E. Audinat, and S. Charpak, “Two-photon imaging of capillary blood flow in olfactory bulb glomeruli,” Proc. Natl. Acad. Sci. U.S.A. 100(22), 13081–13086 (2003).
[Crossref] [PubMed]

Charpak, S.

E. Chaigneau, M. Oheim, E. Audinat, and S. Charpak, “Two-photon imaging of capillary blood flow in olfactory bulb glomeruli,” Proc. Natl. Acad. Sci. U.S.A. 100(22), 13081–13086 (2003).
[Crossref] [PubMed]

Chase, A. J.

S. D. Robinson, C. Janssen, E. B. Fretz, B. Berry, A. J. Chase, A. D. Siega, R. G. Carere, A. Fung, G. Simkus, W. P. Klinke, and J. D. Hilton, “Red blood cell storage duration and mortality in patients undergoing percutaneous coronary intervention,” Am. Heart J. 159(5), 876–881 (2010).
[Crossref] [PubMed]

Chen, B. J.

Chong, A.

Chong, S.

S. Lu, W. Min, S. Chong, G. R. Holtom, and X. S. Xie, “Label-free imaging of heme proteins with two-photon excited photothermal lens microscopy,” Appl. Phys. Lett. 96(11), 113701 (2010).
[Crossref]

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, and X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature 461(7267), 1105–1109 (2009).
[Crossref] [PubMed]

Clay, G. O.

Cohen, D. B.

S. M. Frank, B. Abazyan, M. Ono, C. W. Hogue, D. B. Cohen, D. E. Berkowitz, P. M. Ness, and V. M. Barodka, “Decreased erythrocyte deformability after transfusion and the effects of erythrocyte storage duration,” Anesth. Analg. 116(5), 975–981 (2013).
[Crossref] [PubMed]

Coleman, R.

S. D. Shukla, R. Coleman, J. B. Finean, and R. H. Michell, “The use of phospholipase c to detect structural changes in the membranes of human erythrocytes aged by storage,” Biochim. Biophys. Acta 512(2), 341–349 (1978).
[Crossref] [PubMed]

Custer, B.

G. Edgren, M. Kamper-Jørgensen, S. Eloranta, K. Rostgaard, B. Custer, H. Ullum, E. L. Murphy, M. P. Busch, M. Reilly, M. Melbye, H. Hjalgrim, and O. Nyrén, “Duration of red blood cell storage and survival of transfused patients (CME),” Transfusion 50(6), 1185–1195 (2010).
[Crossref] [PubMed]

D’Alessandro, A.

B. Blasi, A. D’Alessandro, N. Ramundo, and L. Zolla, “Red blood cell storage and cell morphology,” Transfus. Med. 22(2), 90–96 (2012).
[Crossref] [PubMed]

Dantus, M.

B. Nie, I. Saytashev, A. Chong, H. Liu, S. N. Arkhipov, F. W. Wise, and M. Dantus, “Multimodal microscopy with sub-30 fs Yb fiber laser oscillator,” Biomed. Opt. Express 3(7), 1750–1756 (2012).
[Crossref] [PubMed]

B. Nie, D. Pestov, F. W. Wise, and M. Dantus, “An ultrafast fiber laser with self-similar evolution in the gain segment,” Opt. Photonics News 22(12), 47 (2011).
[Crossref]

P. Xi, Y. Andegeko, D. Pestov, V. V. Lovozoy, and M. Dantus, “Two-photon imaging using adaptive phase compensated ultrashort laser pulses,” J. Biomed. Opt. 14(1), 014002 (2009).
[Crossref] [PubMed]

Dasgupta, R.

R. Dasgupta, S. Ahlawat, R. S. Verma, A. Uppal, and P. K. Gupta, “Hemoglobin degradation in human erythrocytes with long-duration near-infrared laser exposure in Raman optical tweezers,” J. Biomed. Opt. 15(5), 055009 (2010).
[Crossref] [PubMed]

de Wolf, A. M.

A. H. M. van Straten, M. A. Soliman Hamad, A. A. van Zundert, E. J. Martens, J. F. ter Woorst, A. M. de Wolf, and V. Scharnhorst, “Effect of duration of red blood cell storage on early and late mortality after coronary artery bypass grafting,” J. Thorac. Cardiovasc. Surg. 141(1), 231–237 (2011).
[Crossref] [PubMed]

Débarre, D.

Dodge, J. T.

J. T. Dodge, C. Mitchell, and D. J. Hanahan, “The preparation and chemical characteristics of hemoglobin-free ghosts of human erythrocytes,” Arch. Biochem. Biophys. 100(1), 119–130 (1963).
[Crossref] [PubMed]

Edgren, G.

G. Edgren, M. Kamper-Jørgensen, S. Eloranta, K. Rostgaard, B. Custer, H. Ullum, E. L. Murphy, M. P. Busch, M. Reilly, M. Melbye, H. Hjalgrim, and O. Nyrén, “Duration of red blood cell storage and survival of transfused patients (CME),” Transfusion 50(6), 1185–1195 (2010).
[Crossref] [PubMed]

Eisenberg, H.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
[Crossref]

Eloranta, S.

G. Edgren, M. Kamper-Jørgensen, S. Eloranta, K. Rostgaard, B. Custer, H. Ullum, E. L. Murphy, M. P. Busch, M. Reilly, M. Melbye, H. Hjalgrim, and O. Nyrén, “Duration of red blood cell storage and survival of transfused patients (CME),” Transfusion 50(6), 1185–1195 (2010).
[Crossref] [PubMed]

Finean, J. B.

S. D. Shukla, R. Coleman, J. B. Finean, and R. H. Michell, “The use of phospholipase c to detect structural changes in the membranes of human erythrocytes aged by storage,” Biochim. Biophys. Acta 512(2), 341–349 (1978).
[Crossref] [PubMed]

Fortier, N. L.

L. M. Snyder, F. Garver, S. C. Liu, L. Leb, J. Trainor, and N. L. Fortier, “Demonstration of haemoglobin associated with isolated, purified spectrin from senescent human red cells,” Br. J. Haematol. 61(3), 415–419 (1985).
[Crossref] [PubMed]

Frank, S. M.

O. N. Salaria, V. M. Barodka, C. W. Hogue, D. E. Berkowitz, P. M. Ness, J. O. Wasey, and S. M. Frank, “Impaired red blood cell deformability after transfusion of stored allogeneic blood but not autologous salvaged blood in cardiac surgery patients,” Anesth. Analg. 118(6), 1179–1187 (2014).
[Crossref] [PubMed]

S. M. Frank, B. Abazyan, M. Ono, C. W. Hogue, D. B. Cohen, D. E. Berkowitz, P. M. Ness, and V. M. Barodka, “Decreased erythrocyte deformability after transfusion and the effects of erythrocyte storage duration,” Anesth. Analg. 116(5), 975–981 (2013).
[Crossref] [PubMed]

Fretz, E. B.

S. D. Robinson, C. Janssen, E. B. Fretz, B. Berry, A. J. Chase, A. D. Siega, R. G. Carere, A. Fung, G. Simkus, W. P. Klinke, and J. D. Hilton, “Red blood cell storage duration and mortality in patients undergoing percutaneous coronary intervention,” Am. Heart J. 159(5), 876–881 (2010).
[Crossref] [PubMed]

Froelich, J. M.

J. A. Meyer, J. M. Froelich, G. E. Reid, W. K. Karunarathne, and D. M. Spence, “Metal-activated C-peptide Facilitates Glucose Clearance and the Release of a Nitric Oxide Stimulus via the GLUT1 Transporter,” Diabetologia 51(1), 175–182 (2007).
[Crossref] [PubMed]

Fu, D.

Fung, A.

S. D. Robinson, C. Janssen, E. B. Fretz, B. Berry, A. J. Chase, A. D. Siega, R. G. Carere, A. Fung, G. Simkus, W. P. Klinke, and J. D. Hilton, “Red blood cell storage duration and mortality in patients undergoing percutaneous coronary intervention,” Am. Heart J. 159(5), 876–881 (2010).
[Crossref] [PubMed]

Garver, F.

L. M. Snyder, F. Garver, S. C. Liu, L. Leb, J. Trainor, and N. L. Fortier, “Demonstration of haemoglobin associated with isolated, purified spectrin from senescent human red cells,” Br. J. Haematol. 61(3), 415–419 (1985).
[Crossref] [PubMed]

Giebink, A.

Y. Wang, A. Giebink, and D. M. Spence, “Microfluidic evaluation of red cells collected and stored in modified processing solutions used in blood banking,” Integr. Biol. 6(1), 65–75 (2014).
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Gryczynski, I.

B. Kierdaszuk, I. Gryczynski, A. Modrak-Wojcik, A. Bzowska, D. Shugar, and J. R. Lakowicz, “Fluorescence of tyrosine and tryptophan in proteins using one- and two-photon excitation,” Photochem. Photobiol. 61(4), 319–324 (1995).
[Crossref] [PubMed]

Gupta, P. K.

R. Dasgupta, S. Ahlawat, R. S. Verma, A. Uppal, and P. K. Gupta, “Hemoglobin degradation in human erythrocytes with long-duration near-infrared laser exposure in Raman optical tweezers,” J. Biomed. Opt. 15(5), 055009 (2010).
[Crossref] [PubMed]

Hanahan, D. J.

J. T. Dodge, C. Mitchell, and D. J. Hanahan, “The preparation and chemical characteristics of hemoglobin-free ghosts of human erythrocytes,” Arch. Biochem. Biophys. 100(1), 119–130 (1963).
[Crossref] [PubMed]

Hatano, M.

S. Yoshida, T. Iizuka, T. Nozawa, and M. Hatano, “Studies on the charge transfer band in high spin state of ferric myoglobin and hemoglobin by low temperature optical and magnetic circular dichroism spectroscopy,” Biochim. Biophys. Acta 405(1), 122–135 (1975).
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Hess, J. R.

A. B. Zimrin and J. R. Hess, “Current issues relating to the transfusion of stored red blood cells,” Vox Sang. 96(2), 93–103 (2009).
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Hilton, J. D.

S. D. Robinson, C. Janssen, E. B. Fretz, B. Berry, A. J. Chase, A. D. Siega, R. G. Carere, A. Fung, G. Simkus, W. P. Klinke, and J. D. Hilton, “Red blood cell storage duration and mortality in patients undergoing percutaneous coronary intervention,” Am. Heart J. 159(5), 876–881 (2010).
[Crossref] [PubMed]

Hjalgrim, H.

G. Edgren, M. Kamper-Jørgensen, S. Eloranta, K. Rostgaard, B. Custer, H. Ullum, E. L. Murphy, M. P. Busch, M. Reilly, M. Melbye, H. Hjalgrim, and O. Nyrén, “Duration of red blood cell storage and survival of transfused patients (CME),” Transfusion 50(6), 1185–1195 (2010).
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P. P. Ho and R. R. Alfano, “Optical Kerr Effect in Liquids,” Phys. Rev. A 20(5), 2170–2187 (1979).
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Hogue, C. W.

O. N. Salaria, V. M. Barodka, C. W. Hogue, D. E. Berkowitz, P. M. Ness, J. O. Wasey, and S. M. Frank, “Impaired red blood cell deformability after transfusion of stored allogeneic blood but not autologous salvaged blood in cardiac surgery patients,” Anesth. Analg. 118(6), 1179–1187 (2014).
[Crossref] [PubMed]

S. M. Frank, B. Abazyan, M. Ono, C. W. Hogue, D. B. Cohen, D. E. Berkowitz, P. M. Ness, and V. M. Barodka, “Decreased erythrocyte deformability after transfusion and the effects of erythrocyte storage duration,” Anesth. Analg. 116(5), 975–981 (2013).
[Crossref] [PubMed]

Holtom, G. R.

S. Lu, W. Min, S. Chong, G. R. Holtom, and X. S. Xie, “Label-free imaging of heme proteins with two-photon excited photothermal lens microscopy,” Appl. Phys. Lett. 96(11), 113701 (2010).
[Crossref]

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, and X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature 461(7267), 1105–1109 (2009).
[Crossref] [PubMed]

Horowitz, M.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
[Crossref]

Iizuka, T.

S. Yoshida, T. Iizuka, T. Nozawa, and M. Hatano, “Studies on the charge transfer band in high spin state of ferric myoglobin and hemoglobin by low temperature optical and magnetic circular dichroism spectroscopy,” Biochim. Biophys. Acta 405(1), 122–135 (1975).
[Crossref] [PubMed]

Jaferzadeh, K.

K. Jaferzadeh and I. Moon, “Quantitative investigation of red blood cell three-dimensional geometric and chemical changes in the storage lesion using digital holographic microscopy,” J. Biomed. Opt. 20(11), 111218 (2015).
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Janssen, C.

S. D. Robinson, C. Janssen, E. B. Fretz, B. Berry, A. J. Chase, A. D. Siega, R. G. Carere, A. Fung, G. Simkus, W. P. Klinke, and J. D. Hilton, “Red blood cell storage duration and mortality in patients undergoing percutaneous coronary intervention,” Am. Heart J. 159(5), 876–881 (2010).
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Javidi, B.

Jimenez, R.

R. Jimenez and F. E. Romesberg, “Excited state dynamics and heterogeneity of folded and unfolded states of cytochrome C,” J. Phys. Chem. B 106(35), 9172–9180 (2002).
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Johnson, J. C.

R. D. Schaller, J. C. Johnson, and R. J. Saykally, “Nonlinear chemical imaging microscopy: near-field third harmonic generation imaging of human red blood cells,” Anal. Chem. 72(21), 5361–5364 (2000).
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Kamper-Jørgensen, M.

G. Edgren, M. Kamper-Jørgensen, S. Eloranta, K. Rostgaard, B. Custer, H. Ullum, E. L. Murphy, M. P. Busch, M. Reilly, M. Melbye, H. Hjalgrim, and O. Nyrén, “Duration of red blood cell storage and survival of transfused patients (CME),” Transfusion 50(6), 1185–1195 (2010).
[Crossref] [PubMed]

Karunarathne, W. K.

J. A. Meyer, J. M. Froelich, G. E. Reid, W. K. Karunarathne, and D. M. Spence, “Metal-activated C-peptide Facilitates Glucose Clearance and the Release of a Nitric Oxide Stimulus via the GLUT1 Transporter,” Diabetologia 51(1), 175–182 (2007).
[Crossref] [PubMed]

Kierdaszuk, B.

B. Kierdaszuk, I. Gryczynski, A. Modrak-Wojcik, A. Bzowska, D. Shugar, and J. R. Lakowicz, “Fluorescence of tyrosine and tryptophan in proteins using one- and two-photon excitation,” Photochem. Photobiol. 61(4), 319–324 (1995).
[Crossref] [PubMed]

Kleinfeld, D.

Klinke, W. P.

S. D. Robinson, C. Janssen, E. B. Fretz, B. Berry, A. J. Chase, A. D. Siega, R. G. Carere, A. Fung, G. Simkus, W. P. Klinke, and J. D. Hilton, “Red blood cell storage duration and mortality in patients undergoing percutaneous coronary intervention,” Am. Heart J. 159(5), 876–881 (2010).
[Crossref] [PubMed]

Lakowicz, J. R.

B. Kierdaszuk, I. Gryczynski, A. Modrak-Wojcik, A. Bzowska, D. Shugar, and J. R. Lakowicz, “Fluorescence of tyrosine and tryptophan in proteins using one- and two-photon excitation,” Photochem. Photobiol. 61(4), 319–324 (1995).
[Crossref] [PubMed]

Leb, L.

L. M. Snyder, F. Garver, S. C. Liu, L. Leb, J. Trainor, and N. L. Fortier, “Demonstration of haemoglobin associated with isolated, purified spectrin from senescent human red cells,” Br. J. Haematol. 61(3), 415–419 (1985).
[Crossref] [PubMed]

Lee, Y. H.

Li, D.

Liu, H.

Liu, S. C.

L. M. Snyder, F. Garver, S. C. Liu, L. Leb, J. Trainor, and N. L. Fortier, “Demonstration of haemoglobin associated with isolated, purified spectrin from senescent human red cells,” Br. J. Haematol. 61(3), 415–419 (1985).
[Crossref] [PubMed]

Lovozoy, V. V.

P. Xi, Y. Andegeko, D. Pestov, V. V. Lovozoy, and M. Dantus, “Two-photon imaging using adaptive phase compensated ultrashort laser pulses,” J. Biomed. Opt. 14(1), 014002 (2009).
[Crossref] [PubMed]

Lu, S.

S. Lu, W. Min, S. Chong, G. R. Holtom, and X. S. Xie, “Label-free imaging of heme proteins with two-photon excited photothermal lens microscopy,” Appl. Phys. Lett. 96(11), 113701 (2010).
[Crossref]

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, and X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature 461(7267), 1105–1109 (2009).
[Crossref] [PubMed]

Luo, Y.

Marquet, P.

Martens, E. J.

A. H. M. van Straten, M. A. Soliman Hamad, A. A. van Zundert, E. J. Martens, J. F. ter Woorst, A. M. de Wolf, and V. Scharnhorst, “Effect of duration of red blood cell storage on early and late mortality after coronary artery bypass grafting,” J. Thorac. Cardiovasc. Surg. 141(1), 231–237 (2011).
[Crossref] [PubMed]

Matthews, T. E.

Melbye, M.

G. Edgren, M. Kamper-Jørgensen, S. Eloranta, K. Rostgaard, B. Custer, H. Ullum, E. L. Murphy, M. P. Busch, M. Reilly, M. Melbye, H. Hjalgrim, and O. Nyrén, “Duration of red blood cell storage and survival of transfused patients (CME),” Transfusion 50(6), 1185–1195 (2010).
[Crossref] [PubMed]

Meyer, J. A.

J. A. Meyer, J. M. Froelich, G. E. Reid, W. K. Karunarathne, and D. M. Spence, “Metal-activated C-peptide Facilitates Glucose Clearance and the Release of a Nitric Oxide Stimulus via the GLUT1 Transporter,” Diabetologia 51(1), 175–182 (2007).
[Crossref] [PubMed]

Michell, R. H.

S. D. Shukla, R. Coleman, J. B. Finean, and R. H. Michell, “The use of phospholipase c to detect structural changes in the membranes of human erythrocytes aged by storage,” Biochim. Biophys. Acta 512(2), 341–349 (1978).
[Crossref] [PubMed]

Millard, A. C.

Min, W.

S. Lu, W. Min, S. Chong, G. R. Holtom, and X. S. Xie, “Label-free imaging of heme proteins with two-photon excited photothermal lens microscopy,” Appl. Phys. Lett. 96(11), 113701 (2010).
[Crossref]

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, and X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature 461(7267), 1105–1109 (2009).
[Crossref] [PubMed]

Mitchell, C.

J. T. Dodge, C. Mitchell, and D. J. Hanahan, “The preparation and chemical characteristics of hemoglobin-free ghosts of human erythrocytes,” Arch. Biochem. Biophys. 100(1), 119–130 (1963).
[Crossref] [PubMed]

Modrak-Wojcik, A.

B. Kierdaszuk, I. Gryczynski, A. Modrak-Wojcik, A. Bzowska, D. Shugar, and J. R. Lakowicz, “Fluorescence of tyrosine and tryptophan in proteins using one- and two-photon excitation,” Photochem. Photobiol. 61(4), 319–324 (1995).
[Crossref] [PubMed]

Moon, I.

Murphy, E. L.

G. Edgren, M. Kamper-Jørgensen, S. Eloranta, K. Rostgaard, B. Custer, H. Ullum, E. L. Murphy, M. P. Busch, M. Reilly, M. Melbye, H. Hjalgrim, and O. Nyrén, “Duration of red blood cell storage and survival of transfused patients (CME),” Transfusion 50(6), 1185–1195 (2010).
[Crossref] [PubMed]

Ness, P. M.

O. N. Salaria, V. M. Barodka, C. W. Hogue, D. E. Berkowitz, P. M. Ness, J. O. Wasey, and S. M. Frank, “Impaired red blood cell deformability after transfusion of stored allogeneic blood but not autologous salvaged blood in cardiac surgery patients,” Anesth. Analg. 118(6), 1179–1187 (2014).
[Crossref] [PubMed]

S. M. Frank, B. Abazyan, M. Ono, C. W. Hogue, D. B. Cohen, D. E. Berkowitz, P. M. Ness, and V. M. Barodka, “Decreased erythrocyte deformability after transfusion and the effects of erythrocyte storage duration,” Anesth. Analg. 116(5), 975–981 (2013).
[Crossref] [PubMed]

Nie, B.

B. Nie, I. Saytashev, A. Chong, H. Liu, S. N. Arkhipov, F. W. Wise, and M. Dantus, “Multimodal microscopy with sub-30 fs Yb fiber laser oscillator,” Biomed. Opt. Express 3(7), 1750–1756 (2012).
[Crossref] [PubMed]

B. Nie, D. Pestov, F. W. Wise, and M. Dantus, “An ultrafast fiber laser with self-similar evolution in the gain segment,” Opt. Photonics News 22(12), 47 (2011).
[Crossref]

Nozawa, T.

S. Yoshida, T. Iizuka, T. Nozawa, and M. Hatano, “Studies on the charge transfer band in high spin state of ferric myoglobin and hemoglobin by low temperature optical and magnetic circular dichroism spectroscopy,” Biochim. Biophys. Acta 405(1), 122–135 (1975).
[Crossref] [PubMed]

Nyrén, O.

G. Edgren, M. Kamper-Jørgensen, S. Eloranta, K. Rostgaard, B. Custer, H. Ullum, E. L. Murphy, M. P. Busch, M. Reilly, M. Melbye, H. Hjalgrim, and O. Nyrén, “Duration of red blood cell storage and survival of transfused patients (CME),” Transfusion 50(6), 1185–1195 (2010).
[Crossref] [PubMed]

Oheim, M.

E. Chaigneau, M. Oheim, E. Audinat, and S. Charpak, “Two-photon imaging of capillary blood flow in olfactory bulb glomeruli,” Proc. Natl. Acad. Sci. U.S.A. 100(22), 13081–13086 (2003).
[Crossref] [PubMed]

Olivier, N.

Ono, M.

S. M. Frank, B. Abazyan, M. Ono, C. W. Hogue, D. B. Cohen, D. E. Berkowitz, P. M. Ness, and V. M. Barodka, “Decreased erythrocyte deformability after transfusion and the effects of erythrocyte storage duration,” Anesth. Analg. 116(5), 975–981 (2013).
[Crossref] [PubMed]

Pestov, D.

B. Nie, D. Pestov, F. W. Wise, and M. Dantus, “An ultrafast fiber laser with self-similar evolution in the gain segment,” Opt. Photonics News 22(12), 47 (2011).
[Crossref]

P. Xi, Y. Andegeko, D. Pestov, V. V. Lovozoy, and M. Dantus, “Two-photon imaging using adaptive phase compensated ultrashort laser pulses,” J. Biomed. Opt. 14(1), 014002 (2009).
[Crossref] [PubMed]

Qu, J. Y.

Q. Sun, W. Zheng, J. Wang, Y. Luo, and J. Y. Qu, “Mechanism of two-photon excited hemoglobin fluorescence emission,” J. Biomed. Opt. 20(10), 105014 (2015).
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Y. Zeng, B. Yan, Q. Sun, S. K. Teh, W. Zhang, Z. Wen, and J. Y. Qu, “Label-free in vivo imaging of human leukocytes using two-photon excited endogenous fluorescence,” J. Biomed. Opt. 18(4), 040504 (2013).
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D. Li, W. Zheng, Y. Zeng, Y. Luo, and J. Y. Qu, “Two-photon excited hemoglobin fluorescence provides contrast mechanism for label-free imaging of microvasculature in vivo,” Opt. Lett. 36(6), 834–836 (2011).
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W. Zheng, D. Li, Y. Zeng, Y. Luo, and J. Y. Qu, “Two-photon excited hemoglobin fluorescence,” Biomed. Opt. Express 2(1), 71–79 (2011).
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Ramundo, N.

B. Blasi, A. D’Alessandro, N. Ramundo, and L. Zolla, “Red blood cell storage and cell morphology,” Transfus. Med. 22(2), 90–96 (2012).
[Crossref] [PubMed]

Rehms, A. A.

A. A. Rehms and P. R. Callis, “Two-photon fluorescence excitation spectra of aromatic amino acids,” Chem. Phys. Lett. 208(3-4), 276–282 (1993).
[Crossref]

Reid, G. E.

J. A. Meyer, J. M. Froelich, G. E. Reid, W. K. Karunarathne, and D. M. Spence, “Metal-activated C-peptide Facilitates Glucose Clearance and the Release of a Nitric Oxide Stimulus via the GLUT1 Transporter,” Diabetologia 51(1), 175–182 (2007).
[Crossref] [PubMed]

Reilly, M.

G. Edgren, M. Kamper-Jørgensen, S. Eloranta, K. Rostgaard, B. Custer, H. Ullum, E. L. Murphy, M. P. Busch, M. Reilly, M. Melbye, H. Hjalgrim, and O. Nyrén, “Duration of red blood cell storage and survival of transfused patients (CME),” Transfusion 50(6), 1185–1195 (2010).
[Crossref] [PubMed]

Robinson, S. D.

S. D. Robinson, C. Janssen, E. B. Fretz, B. Berry, A. J. Chase, A. D. Siega, R. G. Carere, A. Fung, G. Simkus, W. P. Klinke, and J. D. Hilton, “Red blood cell storage duration and mortality in patients undergoing percutaneous coronary intervention,” Am. Heart J. 159(5), 876–881 (2010).
[Crossref] [PubMed]

Romesberg, F. E.

R. Jimenez and F. E. Romesberg, “Excited state dynamics and heterogeneity of folded and unfolded states of cytochrome C,” J. Phys. Chem. B 106(35), 9172–9180 (2002).
[Crossref]

Rostgaard, K.

G. Edgren, M. Kamper-Jørgensen, S. Eloranta, K. Rostgaard, B. Custer, H. Ullum, E. L. Murphy, M. P. Busch, M. Reilly, M. Melbye, H. Hjalgrim, and O. Nyrén, “Duration of red blood cell storage and survival of transfused patients (CME),” Transfusion 50(6), 1185–1195 (2010).
[Crossref] [PubMed]

Roy, R.

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, and X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature 461(7267), 1105–1109 (2009).
[Crossref] [PubMed]

Salaria, O. N.

O. N. Salaria, V. M. Barodka, C. W. Hogue, D. E. Berkowitz, P. M. Ness, J. O. Wasey, and S. M. Frank, “Impaired red blood cell deformability after transfusion of stored allogeneic blood but not autologous salvaged blood in cardiac surgery patients,” Anesth. Analg. 118(6), 1179–1187 (2014).
[Crossref] [PubMed]

Saykally, R. J.

R. D. Schaller, J. C. Johnson, and R. J. Saykally, “Nonlinear chemical imaging microscopy: near-field third harmonic generation imaging of human red blood cells,” Anal. Chem. 72(21), 5361–5364 (2000).
[Crossref] [PubMed]

Saytashev, I.

Schaffer, C. B.

Schaller, R. D.

R. D. Schaller, J. C. Johnson, and R. J. Saykally, “Nonlinear chemical imaging microscopy: near-field third harmonic generation imaging of human red blood cells,” Anal. Chem. 72(21), 5361–5364 (2000).
[Crossref] [PubMed]

Scharnhorst, V.

A. H. M. van Straten, M. A. Soliman Hamad, A. A. van Zundert, E. J. Martens, J. F. ter Woorst, A. M. de Wolf, and V. Scharnhorst, “Effect of duration of red blood cell storage on early and late mortality after coronary artery bypass grafting,” J. Thorac. Cardiovasc. Surg. 141(1), 231–237 (2011).
[Crossref] [PubMed]

Shear, J. B.

C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, “Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 93(20), 10763–10768 (1996).
[Crossref] [PubMed]

Shugar, D.

B. Kierdaszuk, I. Gryczynski, A. Modrak-Wojcik, A. Bzowska, D. Shugar, and J. R. Lakowicz, “Fluorescence of tyrosine and tryptophan in proteins using one- and two-photon excitation,” Photochem. Photobiol. 61(4), 319–324 (1995).
[Crossref] [PubMed]

Shukla, S. D.

S. D. Shukla, R. Coleman, J. B. Finean, and R. H. Michell, “The use of phospholipase c to detect structural changes in the membranes of human erythrocytes aged by storage,” Biochim. Biophys. Acta 512(2), 341–349 (1978).
[Crossref] [PubMed]

Siega, A. D.

S. D. Robinson, C. Janssen, E. B. Fretz, B. Berry, A. J. Chase, A. D. Siega, R. G. Carere, A. Fung, G. Simkus, W. P. Klinke, and J. D. Hilton, “Red blood cell storage duration and mortality in patients undergoing percutaneous coronary intervention,” Am. Heart J. 159(5), 876–881 (2010).
[Crossref] [PubMed]

Silberberg, Y.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
[Crossref]

Simkus, G.

S. D. Robinson, C. Janssen, E. B. Fretz, B. Berry, A. J. Chase, A. D. Siega, R. G. Carere, A. Fung, G. Simkus, W. P. Klinke, and J. D. Hilton, “Red blood cell storage duration and mortality in patients undergoing percutaneous coronary intervention,” Am. Heart J. 159(5), 876–881 (2010).
[Crossref] [PubMed]

Snyder, L. M.

L. M. Snyder, F. Garver, S. C. Liu, L. Leb, J. Trainor, and N. L. Fortier, “Demonstration of haemoglobin associated with isolated, purified spectrin from senescent human red cells,” Br. J. Haematol. 61(3), 415–419 (1985).
[Crossref] [PubMed]

Soliman Hamad, M. A.

A. H. M. van Straten, M. A. Soliman Hamad, A. A. van Zundert, E. J. Martens, J. F. ter Woorst, A. M. de Wolf, and V. Scharnhorst, “Effect of duration of red blood cell storage on early and late mortality after coronary artery bypass grafting,” J. Thorac. Cardiovasc. Surg. 141(1), 231–237 (2011).
[Crossref] [PubMed]

Spence, D. M.

Y. Wang, A. Giebink, and D. M. Spence, “Microfluidic evaluation of red cells collected and stored in modified processing solutions used in blood banking,” Integr. Biol. 6(1), 65–75 (2014).
[Crossref] [PubMed]

J. A. Meyer, J. M. Froelich, G. E. Reid, W. K. Karunarathne, and D. M. Spence, “Metal-activated C-peptide Facilitates Glucose Clearance and the Release of a Nitric Oxide Stimulus via the GLUT1 Transporter,” Diabetologia 51(1), 175–182 (2007).
[Crossref] [PubMed]

Squier, J. A.

Sun, Q.

Q. Sun, W. Zheng, J. Wang, Y. Luo, and J. Y. Qu, “Mechanism of two-photon excited hemoglobin fluorescence emission,” J. Biomed. Opt. 20(10), 105014 (2015).
[Crossref] [PubMed]

Y. Zeng, B. Yan, Q. Sun, S. K. Teh, W. Zhang, Z. Wen, and J. Y. Qu, “Label-free in vivo imaging of human leukocytes using two-photon excited endogenous fluorescence,” J. Biomed. Opt. 18(4), 040504 (2013).
[Crossref] [PubMed]

Teh, S. K.

Y. Zeng, B. Yan, Q. Sun, S. K. Teh, W. Zhang, Z. Wen, and J. Y. Qu, “Label-free in vivo imaging of human leukocytes using two-photon excited endogenous fluorescence,” J. Biomed. Opt. 18(4), 040504 (2013).
[Crossref] [PubMed]

ter Woorst, J. F.

A. H. M. van Straten, M. A. Soliman Hamad, A. A. van Zundert, E. J. Martens, J. F. ter Woorst, A. M. de Wolf, and V. Scharnhorst, “Effect of duration of red blood cell storage on early and late mortality after coronary artery bypass grafting,” J. Thorac. Cardiovasc. Surg. 141(1), 231–237 (2011).
[Crossref] [PubMed]

Trainor, J.

L. M. Snyder, F. Garver, S. C. Liu, L. Leb, J. Trainor, and N. L. Fortier, “Demonstration of haemoglobin associated with isolated, purified spectrin from senescent human red cells,” Br. J. Haematol. 61(3), 415–419 (1985).
[Crossref] [PubMed]

Tsai, P. S.

Ullum, H.

G. Edgren, M. Kamper-Jørgensen, S. Eloranta, K. Rostgaard, B. Custer, H. Ullum, E. L. Murphy, M. P. Busch, M. Reilly, M. Melbye, H. Hjalgrim, and O. Nyrén, “Duration of red blood cell storage and survival of transfused patients (CME),” Transfusion 50(6), 1185–1195 (2010).
[Crossref] [PubMed]

Uppal, A.

R. Dasgupta, S. Ahlawat, R. S. Verma, A. Uppal, and P. K. Gupta, “Hemoglobin degradation in human erythrocytes with long-duration near-infrared laser exposure in Raman optical tweezers,” J. Biomed. Opt. 15(5), 055009 (2010).
[Crossref] [PubMed]

van Straten, A. H. M.

A. H. M. van Straten, M. A. Soliman Hamad, A. A. van Zundert, E. J. Martens, J. F. ter Woorst, A. M. de Wolf, and V. Scharnhorst, “Effect of duration of red blood cell storage on early and late mortality after coronary artery bypass grafting,” J. Thorac. Cardiovasc. Surg. 141(1), 231–237 (2011).
[Crossref] [PubMed]

van Zundert, A. A.

A. H. M. van Straten, M. A. Soliman Hamad, A. A. van Zundert, E. J. Martens, J. F. ter Woorst, A. M. de Wolf, and V. Scharnhorst, “Effect of duration of red blood cell storage on early and late mortality after coronary artery bypass grafting,” J. Thorac. Cardiovasc. Surg. 141(1), 231–237 (2011).
[Crossref] [PubMed]

Verma, R. S.

R. Dasgupta, S. Ahlawat, R. S. Verma, A. Uppal, and P. K. Gupta, “Hemoglobin degradation in human erythrocytes with long-duration near-infrared laser exposure in Raman optical tweezers,” J. Biomed. Opt. 15(5), 055009 (2010).
[Crossref] [PubMed]

Wang, J.

Q. Sun, W. Zheng, J. Wang, Y. Luo, and J. Y. Qu, “Mechanism of two-photon excited hemoglobin fluorescence emission,” J. Biomed. Opt. 20(10), 105014 (2015).
[Crossref] [PubMed]

Wang, Y.

Y. Wang, A. Giebink, and D. M. Spence, “Microfluidic evaluation of red cells collected and stored in modified processing solutions used in blood banking,” Integr. Biol. 6(1), 65–75 (2014).
[Crossref] [PubMed]

Warren, W. S.

Wasey, J. O.

O. N. Salaria, V. M. Barodka, C. W. Hogue, D. E. Berkowitz, P. M. Ness, J. O. Wasey, and S. M. Frank, “Impaired red blood cell deformability after transfusion of stored allogeneic blood but not autologous salvaged blood in cardiac surgery patients,” Anesth. Analg. 118(6), 1179–1187 (2014).
[Crossref] [PubMed]

Webb, W. W.

C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, “Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 93(20), 10763–10768 (1996).
[Crossref] [PubMed]

Wen, Z.

Y. Zeng, B. Yan, Q. Sun, S. K. Teh, W. Zhang, Z. Wen, and J. Y. Qu, “Label-free in vivo imaging of human leukocytes using two-photon excited endogenous fluorescence,” J. Biomed. Opt. 18(4), 040504 (2013).
[Crossref] [PubMed]

Williams, R. M.

C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, “Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 93(20), 10763–10768 (1996).
[Crossref] [PubMed]

Wise, F. W.

B. Nie, I. Saytashev, A. Chong, H. Liu, S. N. Arkhipov, F. W. Wise, and M. Dantus, “Multimodal microscopy with sub-30 fs Yb fiber laser oscillator,” Biomed. Opt. Express 3(7), 1750–1756 (2012).
[Crossref] [PubMed]

B. Nie, D. Pestov, F. W. Wise, and M. Dantus, “An ultrafast fiber laser with self-similar evolution in the gain segment,” Opt. Photonics News 22(12), 47 (2011).
[Crossref]

Xi, P.

P. Xi, Y. Andegeko, D. Pestov, V. V. Lovozoy, and M. Dantus, “Two-photon imaging using adaptive phase compensated ultrashort laser pulses,” J. Biomed. Opt. 14(1), 014002 (2009).
[Crossref] [PubMed]

Xie, X. S.

S. Lu, W. Min, S. Chong, G. R. Holtom, and X. S. Xie, “Label-free imaging of heme proteins with two-photon excited photothermal lens microscopy,” Appl. Phys. Lett. 96(11), 113701 (2010).
[Crossref]

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, and X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature 461(7267), 1105–1109 (2009).
[Crossref] [PubMed]

Xu, C.

C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, “Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 93(20), 10763–10768 (1996).
[Crossref] [PubMed]

Yan, B.

Y. Zeng, B. Yan, Q. Sun, S. K. Teh, W. Zhang, Z. Wen, and J. Y. Qu, “Label-free in vivo imaging of human leukocytes using two-photon excited endogenous fluorescence,” J. Biomed. Opt. 18(4), 040504 (2013).
[Crossref] [PubMed]

Ye, T.

Yi, F.

Yoshida, S.

S. Yoshida, T. Iizuka, T. Nozawa, and M. Hatano, “Studies on the charge transfer band in high spin state of ferric myoglobin and hemoglobin by low temperature optical and magnetic circular dichroism spectroscopy,” Biochim. Biophys. Acta 405(1), 122–135 (1975).
[Crossref] [PubMed]

Yurtserver, G.

Zeng, Y.

Zhang, W.

Y. Zeng, B. Yan, Q. Sun, S. K. Teh, W. Zhang, Z. Wen, and J. Y. Qu, “Label-free in vivo imaging of human leukocytes using two-photon excited endogenous fluorescence,” J. Biomed. Opt. 18(4), 040504 (2013).
[Crossref] [PubMed]

Zheng, W.

Zimrin, A. B.

A. B. Zimrin and J. R. Hess, “Current issues relating to the transfusion of stored red blood cells,” Vox Sang. 96(2), 93–103 (2009).
[Crossref] [PubMed]

Zipfel, W.

C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, “Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 93(20), 10763–10768 (1996).
[Crossref] [PubMed]

Zolla, L.

B. Blasi, A. D’Alessandro, N. Ramundo, and L. Zolla, “Red blood cell storage and cell morphology,” Transfus. Med. 22(2), 90–96 (2012).
[Crossref] [PubMed]

Am. Heart J. (1)

S. D. Robinson, C. Janssen, E. B. Fretz, B. Berry, A. J. Chase, A. D. Siega, R. G. Carere, A. Fung, G. Simkus, W. P. Klinke, and J. D. Hilton, “Red blood cell storage duration and mortality in patients undergoing percutaneous coronary intervention,” Am. Heart J. 159(5), 876–881 (2010).
[Crossref] [PubMed]

Anal. Chem. (1)

R. D. Schaller, J. C. Johnson, and R. J. Saykally, “Nonlinear chemical imaging microscopy: near-field third harmonic generation imaging of human red blood cells,” Anal. Chem. 72(21), 5361–5364 (2000).
[Crossref] [PubMed]

Anesth. Analg. (2)

S. M. Frank, B. Abazyan, M. Ono, C. W. Hogue, D. B. Cohen, D. E. Berkowitz, P. M. Ness, and V. M. Barodka, “Decreased erythrocyte deformability after transfusion and the effects of erythrocyte storage duration,” Anesth. Analg. 116(5), 975–981 (2013).
[Crossref] [PubMed]

O. N. Salaria, V. M. Barodka, C. W. Hogue, D. E. Berkowitz, P. M. Ness, J. O. Wasey, and S. M. Frank, “Impaired red blood cell deformability after transfusion of stored allogeneic blood but not autologous salvaged blood in cardiac surgery patients,” Anesth. Analg. 118(6), 1179–1187 (2014).
[Crossref] [PubMed]

Appl. Phys. Lett. (2)

S. Lu, W. Min, S. Chong, G. R. Holtom, and X. S. Xie, “Label-free imaging of heme proteins with two-photon excited photothermal lens microscopy,” Appl. Phys. Lett. 96(11), 113701 (2010).
[Crossref]

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
[Crossref]

Arch. Biochem. Biophys. (1)

J. T. Dodge, C. Mitchell, and D. J. Hanahan, “The preparation and chemical characteristics of hemoglobin-free ghosts of human erythrocytes,” Arch. Biochem. Biophys. 100(1), 119–130 (1963).
[Crossref] [PubMed]

Biochim. Biophys. Acta (2)

S. D. Shukla, R. Coleman, J. B. Finean, and R. H. Michell, “The use of phospholipase c to detect structural changes in the membranes of human erythrocytes aged by storage,” Biochim. Biophys. Acta 512(2), 341–349 (1978).
[Crossref] [PubMed]

S. Yoshida, T. Iizuka, T. Nozawa, and M. Hatano, “Studies on the charge transfer band in high spin state of ferric myoglobin and hemoglobin by low temperature optical and magnetic circular dichroism spectroscopy,” Biochim. Biophys. Acta 405(1), 122–135 (1975).
[Crossref] [PubMed]

Biomed. Opt. Express (2)

Blood (1)

G. Brecher and M. Bessis, “Present status of spiculed red cells and their relationship to the discocyte-echinocyte transformation: a critical review,” Blood 40(3), 333–344 (1972).
[PubMed]

Br. J. Haematol. (1)

L. M. Snyder, F. Garver, S. C. Liu, L. Leb, J. Trainor, and N. L. Fortier, “Demonstration of haemoglobin associated with isolated, purified spectrin from senescent human red cells,” Br. J. Haematol. 61(3), 415–419 (1985).
[Crossref] [PubMed]

Chem. Phys. Lett. (1)

A. A. Rehms and P. R. Callis, “Two-photon fluorescence excitation spectra of aromatic amino acids,” Chem. Phys. Lett. 208(3-4), 276–282 (1993).
[Crossref]

Diabetologia (1)

J. A. Meyer, J. M. Froelich, G. E. Reid, W. K. Karunarathne, and D. M. Spence, “Metal-activated C-peptide Facilitates Glucose Clearance and the Release of a Nitric Oxide Stimulus via the GLUT1 Transporter,” Diabetologia 51(1), 175–182 (2007).
[Crossref] [PubMed]

Integr. Biol. (1)

Y. Wang, A. Giebink, and D. M. Spence, “Microfluidic evaluation of red cells collected and stored in modified processing solutions used in blood banking,” Integr. Biol. 6(1), 65–75 (2014).
[Crossref] [PubMed]

J. Biomed. Opt. (5)

R. Dasgupta, S. Ahlawat, R. S. Verma, A. Uppal, and P. K. Gupta, “Hemoglobin degradation in human erythrocytes with long-duration near-infrared laser exposure in Raman optical tweezers,” J. Biomed. Opt. 15(5), 055009 (2010).
[Crossref] [PubMed]

K. Jaferzadeh and I. Moon, “Quantitative investigation of red blood cell three-dimensional geometric and chemical changes in the storage lesion using digital holographic microscopy,” J. Biomed. Opt. 20(11), 111218 (2015).
[Crossref] [PubMed]

Y. Zeng, B. Yan, Q. Sun, S. K. Teh, W. Zhang, Z. Wen, and J. Y. Qu, “Label-free in vivo imaging of human leukocytes using two-photon excited endogenous fluorescence,” J. Biomed. Opt. 18(4), 040504 (2013).
[Crossref] [PubMed]

P. Xi, Y. Andegeko, D. Pestov, V. V. Lovozoy, and M. Dantus, “Two-photon imaging using adaptive phase compensated ultrashort laser pulses,” J. Biomed. Opt. 14(1), 014002 (2009).
[Crossref] [PubMed]

Q. Sun, W. Zheng, J. Wang, Y. Luo, and J. Y. Qu, “Mechanism of two-photon excited hemoglobin fluorescence emission,” J. Biomed. Opt. 20(10), 105014 (2015).
[Crossref] [PubMed]

J. Chem. Phys. (1)

G. O. Clay, C. B. Schaffer, and D. Kleinfeld, “Large two-photon absorptivity of hemoglobin in the infrared range of 780-880 nm,” J. Chem. Phys. 126(2), 025102 (2007).
[Crossref] [PubMed]

J. Opt. Soc. Am. B (1)

J. Phys. Chem. B (1)

R. Jimenez and F. E. Romesberg, “Excited state dynamics and heterogeneity of folded and unfolded states of cytochrome C,” J. Phys. Chem. B 106(35), 9172–9180 (2002).
[Crossref]

J. Thorac. Cardiovasc. Surg. (1)

A. H. M. van Straten, M. A. Soliman Hamad, A. A. van Zundert, E. J. Martens, J. F. ter Woorst, A. M. de Wolf, and V. Scharnhorst, “Effect of duration of red blood cell storage on early and late mortality after coronary artery bypass grafting,” J. Thorac. Cardiovasc. Surg. 141(1), 231–237 (2011).
[Crossref] [PubMed]

Nature (1)

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, and X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature 461(7267), 1105–1109 (2009).
[Crossref] [PubMed]

Opt. Express (3)

Opt. Lett. (2)

Opt. Photonics News (1)

B. Nie, D. Pestov, F. W. Wise, and M. Dantus, “An ultrafast fiber laser with self-similar evolution in the gain segment,” Opt. Photonics News 22(12), 47 (2011).
[Crossref]

Photochem. Photobiol. (1)

B. Kierdaszuk, I. Gryczynski, A. Modrak-Wojcik, A. Bzowska, D. Shugar, and J. R. Lakowicz, “Fluorescence of tyrosine and tryptophan in proteins using one- and two-photon excitation,” Photochem. Photobiol. 61(4), 319–324 (1995).
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[Crossref] [PubMed]

C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, “Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 93(20), 10763–10768 (1996).
[Crossref] [PubMed]

Transfus. Med. (1)

B. Blasi, A. D’Alessandro, N. Ramundo, and L. Zolla, “Red blood cell storage and cell morphology,” Transfus. Med. 22(2), 90–96 (2012).
[Crossref] [PubMed]

Transfusion (1)

G. Edgren, M. Kamper-Jørgensen, S. Eloranta, K. Rostgaard, B. Custer, H. Ullum, E. L. Murphy, M. P. Busch, M. Reilly, M. Melbye, H. Hjalgrim, and O. Nyrén, “Duration of red blood cell storage and survival of transfused patients (CME),” Transfusion 50(6), 1185–1195 (2010).
[Crossref] [PubMed]

Vox Sang. (1)

A. B. Zimrin and J. R. Hess, “Current issues relating to the transfusion of stored red blood cells,” Vox Sang. 96(2), 93–103 (2009).
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Other (3)

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B. J. Bain, Blood Cells: A Practical Guide, 5 edition ed. (Wiley-Blackwell, Hoboken, NJ, 2015).

J. P. Greer, D. A. Arber, B. Glader, A. F. List, R. T. Means, F. Paraskevas, and G. M. Rodgers, Wintrobe’s Clinical Hematology, (Lippincott Williams & Wilkins, 2013), p. 3094.

Supplementary Material (2)

NameDescription
» Visualization 1: MP4 (3311 KB)      TPEF of flowing RBCs through storage bag
» Visualization 2: AVI (12556 KB)      THG of flowing RBCs

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Figures (9)

Fig. 1
Fig. 1 Schematic diagram of the microscopy setup for multi-photon imaging using different lasers. Ti:Sapphire or Yb-fiber laser oscillators can be used one at a time.
Fig. 2
Fig. 2 TPEF image of unstained human RBCs on a coverslip imaged by 15fs pulses with 10mW average power from the Ti:Sapphire laser tuned to 800 nm. Scale bar is 20µm.
Fig. 3
Fig. 3 TPEF image of RBCs detected through the PVC storage bag in the epi direction obtained with 10mW average power 15fs pulses from the Ti:Sapphire laser tuned to 800 nm. Scale bar is 20µm. Video of flowing RBCs (Visualization 1).
Fig. 4
Fig. 4 THG microscopy imaging of human RBCs on the glass cover slip obtained using a 1060 nm Yb-fiber laser emitting 45fs pulses with 8mW average power. a) Static image; b) Video of flowing RBCs (Visualization 2). Scale bar is 20µm.
Fig. 5
Fig. 5 THG images of RBCs detected through the PVC storage bag in trans direction (a) and in epi direction (b) excited by 7mW average power from an Yb-fiber laser. Scale bar is 10µm.
Fig. 6
Fig. 6 (a) One-photon excitation (355nm, 12 ps) fluorescence decay curves of hemoglobin, NADH, biliverdin, and riboflavin compared to (b) TPEF (800nm, 15fs) decay curves for RBCs, their membranes and reagent-grade hemoglobin, biliverdin, bilirubin, riboflavin, and NADH.
Fig. 7
Fig. 7 Hemoglobin fluorescence signal versus average excitation power from Ti:Sapphire laser (14 fs pulse duration FWHM) plotted in a logarithmic scale. The experimental points are fit by a linear function with slope equal to 1.89 ± 0.03, which is consistent with two-photon excited fluorescence.
Fig. 8
Fig. 8 (a) TPEF (800nm, 15 fs) emission spectra for RBCs, erythrocyte ghosts and reagent-grade fluorophores. (b) TPEF peak wavelength vs decay lifetimes for RBCs, their membranes and reagent-grade hemoglobin, biliverdin, bilirubin, and NADH.
Fig. 9
Fig. 9 a) Transient absorption measurements of PBS, hemoglobin solution and purified RBCs following 1040nm pump and 735nm probe. b) Absorption spectra of PBS solution with ghosts washed 1 to 4 times. Inset shows absorbance of ghosts after varying number of washes, probed at 414nm. Spectra were corrected for background and Rayleigh scattering.

Tables (3)

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Table 1 Fluorescence lifetime decays obtained from fitting one-photon excitation (355 nm) curves using single and double exponential models.

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Table 2 Fluorescence lifetime decays obtained from fitting two-photon excitation (800 nm) curves using single and double exponential models.

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Table 3 Pearson correlation coefficients of TPEF spectra

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