Abstract

Autofluorescence spectroscopy is a promising label-free approach to characterize biological samples with demonstrated potential to report structural and biochemical alterations in tissues in a number of clinical applications. We report a characterization of the ex vivo autofluorescence fingerprint of cardiac tissue, exploiting a Langendorff-perfused isolated rat heart model to induce physiological insults to the heart, with a view to understanding how metabolic alterations affect the autofluorescence signals. Changes in the autofluorescence intensity and lifetime signatures associated with reduced nicotinamide adenine dinucleotide (phosphate) (NAD(P)H) and flavin adenine dinucleotide (FAD) were characterized during oxygen- or glucose-depletion protocols. Results suggest that both NAD(P)H and FAD autofluorescence intensity and lifetime parameters are sensitive to changes in the metabolic state of the heart owing to oxygen deprivation. We also observed changes in NAD(P)H fluorescence intensity and FAD lifetime parameter on reperfusion of oxygen, which might provide information on reperfusion injury, and permanent tissue damage or changes to the tissue during recovery from oxygen deprivation. We found that changes in the autofluorescence signature following glucose-depletion are, in general, less pronounced, and most clearly visible in NAD(P)H related parameters. Overall, the results reported in this investigation can serve as baseline for future investigations of cardiac tissue involving autofluorescence measurements.

Published by The Optical Society under the terms of the Creative Commons Attribution 4.0 License. Further distribution of this work must maintain attribution to the author(s) and the published article's title, journal citation, and DOI.

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2018 (1)

M. F. la Cour, S. Mehrvar, J. S. Heisner, M. M. Motlagh, M. Medhora, M. Ranji, and A. K. S. Camara, “Optical metabolic imaging of irradiated rat heart exposed to ischemia-reperfusion injury,” J. Biomed. Opt. 23(1), 1–9 (2018).
[Crossref] [PubMed]

2016 (1)

T. S. Blacker and M. R. Duchen, “Investigating mitochondrial redox state using NADH and NADPH autofluorescence,” Free Radic. Biol. Med. 100, 53–65 (2016).
[Crossref] [PubMed]

2015 (3)

J. Lagarto, B. T. Dyer, C. Talbot, M. B. Sikkel, N. S. Peters, P. M. W. French, A. R. Lyon, and C. Dunsby, “Application of time-resolved autofluorescence to label-free in vivo optical mapping of changes in tissue matrix and metabolism associated with myocardial infarction and heart failure,” Biomed. Opt. Express 6(2), 324–346 (2015).
[Crossref] [PubMed]

S. Jentsch, D. Schweitzer, K. U. Schmidtke, S. Peters, J. Dawczynski, K. J. Bär, and M. Hammer, “Retinal fluorescence lifetime imaging ophthalmoscopy measures depend on the severity of Alzheimer’s disease,” Acta Ophthalmol. 93(4), e241–e247 (2015).
[Crossref] [PubMed]

R. C. I. Wüst, M. Helmes, and G. J. M. Stienen, “Rapid changes in NADH and flavin autofluorescence in rat cardiac trabeculae reveal large mitochondrial complex II reserve capacity,” J. Physiol. 593(8), 1829–1840 (2015).
[Crossref] [PubMed]

2014 (2)

G. Papayan, N. Petrishchev, and M. Galagudza, “Autofluorescence spectroscopy for NADH and flavoproteins redox state monitoring in the isolated rat heart subjected to ischemia-reperfusion,” Photodiagn. Photodyn. Ther. 11(3), 400–408 (2014).
[Crossref] [PubMed]

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5(1), 3936 (2014).
[Crossref] [PubMed]

2013 (4)

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical metabolic imaging identifies glycolytic levels, subtypes, and early-treatment response in breast cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

M. A. Yaseen, S. Sakadžić, W. Wu, W. Becker, K. A. Kasischke, and D. A. Boas, “In vivo imaging of cerebral energy metabolism with two-photon fluorescence lifetime microscopy of NADH,” Biomed. Opt. Express 4(2), 307–321 (2013).
[Crossref] [PubMed]

M. G. Rosca and C. L. Hoppel, “Mitochondrial dysfunction in heart failure,” Heart Fail. Rev. 18(5), 607–622 (2013).
[Crossref] [PubMed]

T. Doenst, T. D. Nguyen, and E. D. Abel, “Cardiac metabolism in heart failure: implications beyond ATP production,” Circ. Res. 113(6), 709–724 (2013).
[Crossref] [PubMed]

2012 (1)

S. K. White, D. M. Sado, A. S. Flett, and J. C. Moon, “Characterising the myocardial interstitial space: the clinical relevance of non-invasive imaging,” Heart 98(10), 773–779 (2012).
[Crossref] [PubMed]

2010 (1)

Y. Ti, P. Chen, and W.-C. Lin, “In vivo characterization of myocardial infarction using fluorescence and diffuse reflectance spectroscopy,” J. Biomed. Opt. 15(3), 037009 (2010).
[Crossref] [PubMed]

2008 (2)

E. Gussakovsky, O. Jilkina, Y. Yang, and V. Kupriyanov, “Hemoglobin plus myoglobin concentrations and near infrared light pathlength in phantom and pig hearts determined by diffuse reflectance spectroscopy,” Anal. Biochem. 382(2), 107–115 (2008).
[Crossref] [PubMed]

E. Häggblad, T. Lindbergh, M. G. D. Karlsson, H. Casimir-Ahn, E. G. Salerud, and T. Strömberg, “Myocardial tissue oxygenation estimated with calibrated diffuse reflectance spectroscopy during coronary artery bypass grafting,” J. Biomed. Opt. 13(5), 054030 (2008).
[Crossref] [PubMed]

2007 (3)

S. Neubauer, “The failing heart--an engine out of fuel,” N. Engl. J. Med. 356(11), 1140–1151 (2007).
[Crossref] [PubMed]

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[Crossref] [PubMed]

A. Mayevsky and G. G. Rogatsky, “Mitochondrial function in vivo evaluated by NADH fluorescence: from animal models to human studies,” Am. J. Physiol. Cell Physiol. 292(2), C615–C640 (2007).
[Crossref] [PubMed]

2005 (2)

W. C. Stanley, F. A. Recchia, and G. D. Lopaschuk, “Myocardial substrate metabolism in the normal and failing heart,” Physiol. Rev. 85(3), 1093–1129 (2005).
[Crossref] [PubMed]

D. Chorvat, J. Kirchnerova, M. Cagalinec, J. Smolka, A. Mateasik, and A. Chorvatova, “Spectral unmixing of flavin autofluorescence components in cardiac myocytes,” Biophys. J. 89(6), L55–L57 (2005).
[Crossref] [PubMed]

2002 (2)

S. Huang, A. A. Heikal, and W. W. Webb, “Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein,” Biophys. J. 82(5), 2811–2825 (2002).
[Crossref] [PubMed]

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res. 62(3), 682–687 (2002).
[PubMed]

2001 (2)

J. P. Headrick, J. Peart, B. Hack, A. Flood, and G. P. Matherne, “Functional properties and responses to ischaemia-reperfusion in Langendorff perfused mouse heart,” Exp. Physiol. 86(6), 703–716 (2001).
[Crossref] [PubMed]

J. Tong, Y. Cao, Y. Hotta, N. Ishikawa, H. Nishimaki, K. Masuda, C. L. Yang, K. Kasai, and G. Itoh, “Cardiomyocyte Apoptosis Induced in Langendorff Preparation of Isolated Guinea-Pig Heart Perfused with Krebs-Henseleit Solution Deprived of Glucose, with and without Oxygen Supply,” Basic Appl. Myol. 11(3), 143–150 (2001).

2000 (3)

L. Marcu, D. Cohena, J. I. Maarek, W. S. Grundfesta, T. Development, and C. M. C. L. Angeles, “Characterization of Type I, II, III, IV, and V collagens by time-resolved laser-induced fluorescence spectroscopy,” Proc. SPIE 3917, 93–101 (2000).
[Crossref]

F. J. Sutherland and D. J. Hearse, “The isolated blood and perfusion fluid perfused heart,” Pharmacol. Res. 41(6), 613–627 (2000).
[Crossref] [PubMed]

Y. Sun and K. T. Weber, “Infarct scar: a dynamic tissue,” Cardiovasc. Res. 46(2), 250–256 (2000).
[Crossref] [PubMed]

1999 (1)

A. E. Arai, C. E. Kasserra, P. R. Territo, A. H. Gandjbakhche, and R. S. Balaban, “Myocardial oxygenation in vivo: optical spectroscopy of cytoplasmic myoglobin and mitochondrial cytochromes,” Am. J. Physiol. 277(2 Pt 2), H683–H697 (1999).
[PubMed]

1998 (1)

B. R. Masters, P. T. C. So, and E. Gratton, “Optical biopsy of in vivo human skin: Multi-photon excitation microscopy,” Lasers Med. Sci. 13(3), 196–203 (1998).
[Crossref]

1997 (1)

K. A. Schenkman, D. R. Marble, D. H. Burns, and E. O. Feigl, “Myoglobin oxygen dissociation by multiwavelength spectroscopy,” J. Appl. Physiol. 82(1), 86–92 (1997).
[Crossref] [PubMed]

1995 (1)

A. Pradhan, P. Pal, G. Durocher, L. Villeneuve, A. Balassy, F. Babai, L. Gaboury, and L. Blanchard, “Steady state and time-resolved fluorescence properties of metastatic and non-metastatic malignant cells from different species,” J. Photochem. Photobiol. B 31(3), 101–112 (1995).
[Crossref] [PubMed]

1994 (1)

K. Koenig, H. Schneckenburger, J. Hemmer, B. J. Tromberg, and R. W. Steiner, “In-vivo fluorescence detection and imaging of porphyrin-producing bacteria in the human skin and in the oral cavity for diagnosis of acne vulgaris, caries, and squamous cell carcinoma,” Proc. SPIE 2135, 129–138 (1994).
[Crossref]

1992 (2)

H. Schneckenburger and K. Konig, “Fluorescence decay kinetics and imaging of NAD(P)H and flavins as metabolic indicators,” Opt. Eng. 31(7), 1447–1451 (1992).
[Crossref]

J. R. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. L. Johnson, “Fluorescence lifetime imaging of free and protein-bound NADH,” Proc. Natl. Acad. Sci. U.S.A. 89(4), 1271–1275 (1992).
[Crossref] [PubMed]

1990 (1)

T. J. Biscoe and M. R. Duchen, “Responses of type I cells dissociated from the rabbit carotid body to hypoxia,” J. Physiol. 428(1), 39–59 (1990).
[Crossref] [PubMed]

1989 (4)

T. Fukushima, R. V. Decker, W. M. Anderson, and H. O. Spivey, “Substrate channeling of NADH and binding of dehydrogenases to complex I,” J. Biol. Chem. 264(28), 16483–16488 (1989).
[PubMed]

D. M. Jameson, V. Thomas, and D. M. Zhou, “Time-resolved fluorescence studies on NADH bound to mitochondrial malate dehydrogenase,” Biochim. Biophys. Acta 994(2), 187–190 (1989).
[Crossref] [PubMed]

J. Eng, R. M. Lynch, and R. S. Balaban, “Nicotinamide adenine dinucleotide fluorescence spectroscopy and imaging of isolated cardiac myocytes,” Biophys. J. 55(4), 621–630 (1989).
[Crossref] [PubMed]

K. T. Weber, “Cardiac interstitium in health and disease: the fibrillar collagen network,” J. Am. Coll. Cardiol. 13(7), 1637–1652 (1989).
[Crossref] [PubMed]

1981 (1)

D. R. Saunders and H. S. Wiggins, “Conservation of mannitol, lactulose, and raffinose by the human colon,” Am. J. Physiol. 241(5), G397–G402 (1981).
[PubMed]

1979 (1)

T. Torikata, L. S. Forster, R. E. Johnson, and J. A. Rupley, “Lifetimes and NADH quenching of tryptophan fluorescence in pig heart cytoplasmic malate dehydrogenase,” J. Biol. Chem. 254(9), 3516–3520 (1979).
[PubMed]

1969 (1)

S. M. Nasrallah and F. L. Iber, “Mannitol absorption and metabolism in man,” Am. J. Med. Sci. 258(2), 80–88 (1969).
[Crossref] [PubMed]

1962 (2)

T. E. King, R. L. Howard, D. F. Wilson, and J. C. Li, “The Partition of Flavins in the Heart Muscle Preparation and Heart Mitochondria,” J. Biol. Chem. 237(9), 2941–2946 (1962).
[PubMed]

B. Chance, P. Cohen, F. Jobsis, and B. Schoener, “Intracellular oxidation-reduction states in vivo,” Science 137(3529), 499–508 (1962).
[Crossref] [PubMed]

1958 (1)

B. Chance and H. Baltscheffsky, “Respiratory enzymes in oxidative phosphorylation. vii. binding of intramitochondrial reduced pyridine nucleotide,” J. Biol. Chem. 233(3), 736–739 (1958).
[PubMed]

1957 (1)

L. N. M. Duysens and J. Amesz, “Fluorescence spectrophotometry of reduced phosphopyridine nucleotide in intact cells in the near-ultraviolet and visible region,” Biochim. Biophys. Acta 24(1), 19–26 (1957).
[Crossref] [PubMed]

1954 (1)

A. N. Wick, T. N. Morita, and L. Joseph, “The oxidation of mannitol,” Proc. Soc. Exp. Biol. Med. 85(1), 188–190 (1954).
[Crossref] [PubMed]

1949 (1)

O. A. Bessey, O. H. Lowry, and R. H. Love, “The fluorometric measurement of the nucleotides of riboflavin and their concentration in tissues,” J. Biol. Chem. 180(2), 755–769 (1949).
[PubMed]

1937 (1)

R. Hober and J. Hober, “Experiments on the absorption of organic solutes in the small intestine of rats,” J. Cell. Comp. Physiol. 10(4), 401–422 (1937).
[Crossref]

Abel, E. D.

T. Doenst, T. D. Nguyen, and E. D. Abel, “Cardiac metabolism in heart failure: implications beyond ATP production,” Circ. Res. 113(6), 709–724 (2013).
[Crossref] [PubMed]

Amesz, J.

L. N. M. Duysens and J. Amesz, “Fluorescence spectrophotometry of reduced phosphopyridine nucleotide in intact cells in the near-ultraviolet and visible region,” Biochim. Biophys. Acta 24(1), 19–26 (1957).
[Crossref] [PubMed]

Anderson, W. M.

T. Fukushima, R. V. Decker, W. M. Anderson, and H. O. Spivey, “Substrate channeling of NADH and binding of dehydrogenases to complex I,” J. Biol. Chem. 264(28), 16483–16488 (1989).
[PubMed]

Angeles, C. M. C. L.

L. Marcu, D. Cohena, J. I. Maarek, W. S. Grundfesta, T. Development, and C. M. C. L. Angeles, “Characterization of Type I, II, III, IV, and V collagens by time-resolved laser-induced fluorescence spectroscopy,” Proc. SPIE 3917, 93–101 (2000).
[Crossref]

Arai, A. E.

A. E. Arai, C. E. Kasserra, P. R. Territo, A. H. Gandjbakhche, and R. S. Balaban, “Myocardial oxygenation in vivo: optical spectroscopy of cytoplasmic myoglobin and mitochondrial cytochromes,” Am. J. Physiol. 277(2 Pt 2), H683–H697 (1999).
[PubMed]

Arteaga, C. L.

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical metabolic imaging identifies glycolytic levels, subtypes, and early-treatment response in breast cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

Babai, F.

A. Pradhan, P. Pal, G. Durocher, L. Villeneuve, A. Balassy, F. Babai, L. Gaboury, and L. Blanchard, “Steady state and time-resolved fluorescence properties of metastatic and non-metastatic malignant cells from different species,” J. Photochem. Photobiol. B 31(3), 101–112 (1995).
[Crossref] [PubMed]

Badizadegan, K.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res. 62(3), 682–687 (2002).
[PubMed]

Bain, A. J.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5(1), 3936 (2014).
[Crossref] [PubMed]

Balaban, R. S.

A. E. Arai, C. E. Kasserra, P. R. Territo, A. H. Gandjbakhche, and R. S. Balaban, “Myocardial oxygenation in vivo: optical spectroscopy of cytoplasmic myoglobin and mitochondrial cytochromes,” Am. J. Physiol. 277(2 Pt 2), H683–H697 (1999).
[PubMed]

J. Eng, R. M. Lynch, and R. S. Balaban, “Nicotinamide adenine dinucleotide fluorescence spectroscopy and imaging of isolated cardiac myocytes,” Biophys. J. 55(4), 621–630 (1989).
[Crossref] [PubMed]

Balassy, A.

A. Pradhan, P. Pal, G. Durocher, L. Villeneuve, A. Balassy, F. Babai, L. Gaboury, and L. Blanchard, “Steady state and time-resolved fluorescence properties of metastatic and non-metastatic malignant cells from different species,” J. Photochem. Photobiol. B 31(3), 101–112 (1995).
[Crossref] [PubMed]

Baltscheffsky, H.

B. Chance and H. Baltscheffsky, “Respiratory enzymes in oxidative phosphorylation. vii. binding of intramitochondrial reduced pyridine nucleotide,” J. Biol. Chem. 233(3), 736–739 (1958).
[PubMed]

Bär, K. J.

S. Jentsch, D. Schweitzer, K. U. Schmidtke, S. Peters, J. Dawczynski, K. J. Bär, and M. Hammer, “Retinal fluorescence lifetime imaging ophthalmoscopy measures depend on the severity of Alzheimer’s disease,” Acta Ophthalmol. 93(4), e241–e247 (2015).
[Crossref] [PubMed]

Becker, W.

Bessey, O. A.

O. A. Bessey, O. H. Lowry, and R. H. Love, “The fluorometric measurement of the nucleotides of riboflavin and their concentration in tissues,” J. Biol. Chem. 180(2), 755–769 (1949).
[PubMed]

Biscoe, T. J.

T. J. Biscoe and M. R. Duchen, “Responses of type I cells dissociated from the rabbit carotid body to hypoxia,” J. Physiol. 428(1), 39–59 (1990).
[Crossref] [PubMed]

Blacker, T. S.

T. S. Blacker and M. R. Duchen, “Investigating mitochondrial redox state using NADH and NADPH autofluorescence,” Free Radic. Biol. Med. 100, 53–65 (2016).
[Crossref] [PubMed]

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5(1), 3936 (2014).
[Crossref] [PubMed]

Blanchard, L.

A. Pradhan, P. Pal, G. Durocher, L. Villeneuve, A. Balassy, F. Babai, L. Gaboury, and L. Blanchard, “Steady state and time-resolved fluorescence properties of metastatic and non-metastatic malignant cells from different species,” J. Photochem. Photobiol. B 31(3), 101–112 (1995).
[Crossref] [PubMed]

Boas, D. A.

Boone, C. W.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res. 62(3), 682–687 (2002).
[PubMed]

Burns, D. H.

K. A. Schenkman, D. R. Marble, D. H. Burns, and E. O. Feigl, “Myoglobin oxygen dissociation by multiwavelength spectroscopy,” J. Appl. Physiol. 82(1), 86–92 (1997).
[Crossref] [PubMed]

Cagalinec, M.

D. Chorvat, J. Kirchnerova, M. Cagalinec, J. Smolka, A. Mateasik, and A. Chorvatova, “Spectral unmixing of flavin autofluorescence components in cardiac myocytes,” Biophys. J. 89(6), L55–L57 (2005).
[Crossref] [PubMed]

Camara, A. K. S.

M. F. la Cour, S. Mehrvar, J. S. Heisner, M. M. Motlagh, M. Medhora, M. Ranji, and A. K. S. Camara, “Optical metabolic imaging of irradiated rat heart exposed to ischemia-reperfusion injury,” J. Biomed. Opt. 23(1), 1–9 (2018).
[Crossref] [PubMed]

Cao, Y.

J. Tong, Y. Cao, Y. Hotta, N. Ishikawa, H. Nishimaki, K. Masuda, C. L. Yang, K. Kasai, and G. Itoh, “Cardiomyocyte Apoptosis Induced in Langendorff Preparation of Isolated Guinea-Pig Heart Perfused with Krebs-Henseleit Solution Deprived of Glucose, with and without Oxygen Supply,” Basic Appl. Myol. 11(3), 143–150 (2001).

Carr-Locke, D. L.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res. 62(3), 682–687 (2002).
[PubMed]

Casimir-Ahn, H.

E. Häggblad, T. Lindbergh, M. G. D. Karlsson, H. Casimir-Ahn, E. G. Salerud, and T. Strömberg, “Myocardial tissue oxygenation estimated with calibrated diffuse reflectance spectroscopy during coronary artery bypass grafting,” J. Biomed. Opt. 13(5), 054030 (2008).
[Crossref] [PubMed]

Chance, B.

B. Chance, P. Cohen, F. Jobsis, and B. Schoener, “Intracellular oxidation-reduction states in vivo,” Science 137(3529), 499–508 (1962).
[Crossref] [PubMed]

B. Chance and H. Baltscheffsky, “Respiratory enzymes in oxidative phosphorylation. vii. binding of intramitochondrial reduced pyridine nucleotide,” J. Biol. Chem. 233(3), 736–739 (1958).
[PubMed]

Chen, P.

Y. Ti, P. Chen, and W.-C. Lin, “In vivo characterization of myocardial infarction using fluorescence and diffuse reflectance spectroscopy,” J. Biomed. Opt. 15(3), 037009 (2010).
[Crossref] [PubMed]

Chorvat, D.

D. Chorvat, J. Kirchnerova, M. Cagalinec, J. Smolka, A. Mateasik, and A. Chorvatova, “Spectral unmixing of flavin autofluorescence components in cardiac myocytes,” Biophys. J. 89(6), L55–L57 (2005).
[Crossref] [PubMed]

Chorvatova, A.

D. Chorvat, J. Kirchnerova, M. Cagalinec, J. Smolka, A. Mateasik, and A. Chorvatova, “Spectral unmixing of flavin autofluorescence components in cardiac myocytes,” Biophys. J. 89(6), L55–L57 (2005).
[Crossref] [PubMed]

Cohen, P.

B. Chance, P. Cohen, F. Jobsis, and B. Schoener, “Intracellular oxidation-reduction states in vivo,” Science 137(3529), 499–508 (1962).
[Crossref] [PubMed]

Cohena, D.

L. Marcu, D. Cohena, J. I. Maarek, W. S. Grundfesta, T. Development, and C. M. C. L. Angeles, “Characterization of Type I, II, III, IV, and V collagens by time-resolved laser-induced fluorescence spectroscopy,” Proc. SPIE 3917, 93–101 (2000).
[Crossref]

Cook, R. S.

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical metabolic imaging identifies glycolytic levels, subtypes, and early-treatment response in breast cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

Crum, C. P.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res. 62(3), 682–687 (2002).
[PubMed]

Dasari, R. R.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res. 62(3), 682–687 (2002).
[PubMed]

Dawczynski, J.

S. Jentsch, D. Schweitzer, K. U. Schmidtke, S. Peters, J. Dawczynski, K. J. Bär, and M. Hammer, “Retinal fluorescence lifetime imaging ophthalmoscopy measures depend on the severity of Alzheimer’s disease,” Acta Ophthalmol. 93(4), e241–e247 (2015).
[Crossref] [PubMed]

Decker, R. V.

T. Fukushima, R. V. Decker, W. M. Anderson, and H. O. Spivey, “Substrate channeling of NADH and binding of dehydrogenases to complex I,” J. Biol. Chem. 264(28), 16483–16488 (1989).
[PubMed]

Development, T.

L. Marcu, D. Cohena, J. I. Maarek, W. S. Grundfesta, T. Development, and C. M. C. L. Angeles, “Characterization of Type I, II, III, IV, and V collagens by time-resolved laser-induced fluorescence spectroscopy,” Proc. SPIE 3917, 93–101 (2000).
[Crossref]

Doenst, T.

T. Doenst, T. D. Nguyen, and E. D. Abel, “Cardiac metabolism in heart failure: implications beyond ATP production,” Circ. Res. 113(6), 709–724 (2013).
[Crossref] [PubMed]

Duchen, M. R.

T. S. Blacker and M. R. Duchen, “Investigating mitochondrial redox state using NADH and NADPH autofluorescence,” Free Radic. Biol. Med. 100, 53–65 (2016).
[Crossref] [PubMed]

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5(1), 3936 (2014).
[Crossref] [PubMed]

T. J. Biscoe and M. R. Duchen, “Responses of type I cells dissociated from the rabbit carotid body to hypoxia,” J. Physiol. 428(1), 39–59 (1990).
[Crossref] [PubMed]

Dunsby, C.

Durocher, G.

A. Pradhan, P. Pal, G. Durocher, L. Villeneuve, A. Balassy, F. Babai, L. Gaboury, and L. Blanchard, “Steady state and time-resolved fluorescence properties of metastatic and non-metastatic malignant cells from different species,” J. Photochem. Photobiol. B 31(3), 101–112 (1995).
[Crossref] [PubMed]

Duysens, L. N. M.

L. N. M. Duysens and J. Amesz, “Fluorescence spectrophotometry of reduced phosphopyridine nucleotide in intact cells in the near-ultraviolet and visible region,” Biochim. Biophys. Acta 24(1), 19–26 (1957).
[Crossref] [PubMed]

Dyer, B. T.

Eickhoff, J.

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[Crossref] [PubMed]

Eliceiri, K. W.

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[Crossref] [PubMed]

Eng, J.

J. Eng, R. M. Lynch, and R. S. Balaban, “Nicotinamide adenine dinucleotide fluorescence spectroscopy and imaging of isolated cardiac myocytes,” Biophys. J. 55(4), 621–630 (1989).
[Crossref] [PubMed]

Feigl, E. O.

K. A. Schenkman, D. R. Marble, D. H. Burns, and E. O. Feigl, “Myoglobin oxygen dissociation by multiwavelength spectroscopy,” J. Appl. Physiol. 82(1), 86–92 (1997).
[Crossref] [PubMed]

Feld, M. S.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res. 62(3), 682–687 (2002).
[PubMed]

Flett, A. S.

S. K. White, D. M. Sado, A. S. Flett, and J. C. Moon, “Characterising the myocardial interstitial space: the clinical relevance of non-invasive imaging,” Heart 98(10), 773–779 (2012).
[Crossref] [PubMed]

Flood, A.

J. P. Headrick, J. Peart, B. Hack, A. Flood, and G. P. Matherne, “Functional properties and responses to ischaemia-reperfusion in Langendorff perfused mouse heart,” Exp. Physiol. 86(6), 703–716 (2001).
[Crossref] [PubMed]

Forster, L. S.

T. Torikata, L. S. Forster, R. E. Johnson, and J. A. Rupley, “Lifetimes and NADH quenching of tryptophan fluorescence in pig heart cytoplasmic malate dehydrogenase,” J. Biol. Chem. 254(9), 3516–3520 (1979).
[PubMed]

French, P. M. W.

Fukushima, T.

T. Fukushima, R. V. Decker, W. M. Anderson, and H. O. Spivey, “Substrate channeling of NADH and binding of dehydrogenases to complex I,” J. Biol. Chem. 264(28), 16483–16488 (1989).
[PubMed]

Gaboury, L.

A. Pradhan, P. Pal, G. Durocher, L. Villeneuve, A. Balassy, F. Babai, L. Gaboury, and L. Blanchard, “Steady state and time-resolved fluorescence properties of metastatic and non-metastatic malignant cells from different species,” J. Photochem. Photobiol. B 31(3), 101–112 (1995).
[Crossref] [PubMed]

Galagudza, M.

G. Papayan, N. Petrishchev, and M. Galagudza, “Autofluorescence spectroscopy for NADH and flavoproteins redox state monitoring in the isolated rat heart subjected to ischemia-reperfusion,” Photodiagn. Photodyn. Ther. 11(3), 400–408 (2014).
[Crossref] [PubMed]

Gale, J. E.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5(1), 3936 (2014).
[Crossref] [PubMed]

Gandjbakhche, A. H.

A. E. Arai, C. E. Kasserra, P. R. Territo, A. H. Gandjbakhche, and R. S. Balaban, “Myocardial oxygenation in vivo: optical spectroscopy of cytoplasmic myoglobin and mitochondrial cytochromes,” Am. J. Physiol. 277(2 Pt 2), H683–H697 (1999).
[PubMed]

Gendron-Fitzpatrick, A.

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[Crossref] [PubMed]

Georgakoudi, I.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res. 62(3), 682–687 (2002).
[PubMed]

Gratton, E.

B. R. Masters, P. T. C. So, and E. Gratton, “Optical biopsy of in vivo human skin: Multi-photon excitation microscopy,” Lasers Med. Sci. 13(3), 196–203 (1998).
[Crossref]

Grundfesta, W. S.

L. Marcu, D. Cohena, J. I. Maarek, W. S. Grundfesta, T. Development, and C. M. C. L. Angeles, “Characterization of Type I, II, III, IV, and V collagens by time-resolved laser-induced fluorescence spectroscopy,” Proc. SPIE 3917, 93–101 (2000).
[Crossref]

Gussakovsky, E.

E. Gussakovsky, O. Jilkina, Y. Yang, and V. Kupriyanov, “Hemoglobin plus myoglobin concentrations and near infrared light pathlength in phantom and pig hearts determined by diffuse reflectance spectroscopy,” Anal. Biochem. 382(2), 107–115 (2008).
[Crossref] [PubMed]

Hack, B.

J. P. Headrick, J. Peart, B. Hack, A. Flood, and G. P. Matherne, “Functional properties and responses to ischaemia-reperfusion in Langendorff perfused mouse heart,” Exp. Physiol. 86(6), 703–716 (2001).
[Crossref] [PubMed]

Häggblad, E.

E. Häggblad, T. Lindbergh, M. G. D. Karlsson, H. Casimir-Ahn, E. G. Salerud, and T. Strömberg, “Myocardial tissue oxygenation estimated with calibrated diffuse reflectance spectroscopy during coronary artery bypass grafting,” J. Biomed. Opt. 13(5), 054030 (2008).
[Crossref] [PubMed]

Hammer, M.

S. Jentsch, D. Schweitzer, K. U. Schmidtke, S. Peters, J. Dawczynski, K. J. Bär, and M. Hammer, “Retinal fluorescence lifetime imaging ophthalmoscopy measures depend on the severity of Alzheimer’s disease,” Acta Ophthalmol. 93(4), e241–e247 (2015).
[Crossref] [PubMed]

Headrick, J. P.

J. P. Headrick, J. Peart, B. Hack, A. Flood, and G. P. Matherne, “Functional properties and responses to ischaemia-reperfusion in Langendorff perfused mouse heart,” Exp. Physiol. 86(6), 703–716 (2001).
[Crossref] [PubMed]

Hearse, D. J.

F. J. Sutherland and D. J. Hearse, “The isolated blood and perfusion fluid perfused heart,” Pharmacol. Res. 41(6), 613–627 (2000).
[Crossref] [PubMed]

Heikal, A. A.

S. Huang, A. A. Heikal, and W. W. Webb, “Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein,” Biophys. J. 82(5), 2811–2825 (2002).
[Crossref] [PubMed]

Heisner, J. S.

M. F. la Cour, S. Mehrvar, J. S. Heisner, M. M. Motlagh, M. Medhora, M. Ranji, and A. K. S. Camara, “Optical metabolic imaging of irradiated rat heart exposed to ischemia-reperfusion injury,” J. Biomed. Opt. 23(1), 1–9 (2018).
[Crossref] [PubMed]

Helmes, M.

R. C. I. Wüst, M. Helmes, and G. J. M. Stienen, “Rapid changes in NADH and flavin autofluorescence in rat cardiac trabeculae reveal large mitochondrial complex II reserve capacity,” J. Physiol. 593(8), 1829–1840 (2015).
[Crossref] [PubMed]

Hemmer, J.

K. Koenig, H. Schneckenburger, J. Hemmer, B. J. Tromberg, and R. W. Steiner, “In-vivo fluorescence detection and imaging of porphyrin-producing bacteria in the human skin and in the oral cavity for diagnosis of acne vulgaris, caries, and squamous cell carcinoma,” Proc. SPIE 2135, 129–138 (1994).
[Crossref]

Hicks, D. J.

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical metabolic imaging identifies glycolytic levels, subtypes, and early-treatment response in breast cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

Hober, J.

R. Hober and J. Hober, “Experiments on the absorption of organic solutes in the small intestine of rats,” J. Cell. Comp. Physiol. 10(4), 401–422 (1937).
[Crossref]

Hober, R.

R. Hober and J. Hober, “Experiments on the absorption of organic solutes in the small intestine of rats,” J. Cell. Comp. Physiol. 10(4), 401–422 (1937).
[Crossref]

Hoppel, C. L.

M. G. Rosca and C. L. Hoppel, “Mitochondrial dysfunction in heart failure,” Heart Fail. Rev. 18(5), 607–622 (2013).
[Crossref] [PubMed]

Hotta, Y.

J. Tong, Y. Cao, Y. Hotta, N. Ishikawa, H. Nishimaki, K. Masuda, C. L. Yang, K. Kasai, and G. Itoh, “Cardiomyocyte Apoptosis Induced in Langendorff Preparation of Isolated Guinea-Pig Heart Perfused with Krebs-Henseleit Solution Deprived of Glucose, with and without Oxygen Supply,” Basic Appl. Myol. 11(3), 143–150 (2001).

Howard, R. L.

T. E. King, R. L. Howard, D. F. Wilson, and J. C. Li, “The Partition of Flavins in the Heart Muscle Preparation and Heart Mitochondria,” J. Biol. Chem. 237(9), 2941–2946 (1962).
[PubMed]

Huang, S.

S. Huang, A. A. Heikal, and W. W. Webb, “Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein,” Biophys. J. 82(5), 2811–2825 (2002).
[Crossref] [PubMed]

Iber, F. L.

S. M. Nasrallah and F. L. Iber, “Mannitol absorption and metabolism in man,” Am. J. Med. Sci. 258(2), 80–88 (1969).
[Crossref] [PubMed]

Ishikawa, N.

J. Tong, Y. Cao, Y. Hotta, N. Ishikawa, H. Nishimaki, K. Masuda, C. L. Yang, K. Kasai, and G. Itoh, “Cardiomyocyte Apoptosis Induced in Langendorff Preparation of Isolated Guinea-Pig Heart Perfused with Krebs-Henseleit Solution Deprived of Glucose, with and without Oxygen Supply,” Basic Appl. Myol. 11(3), 143–150 (2001).

Itoh, G.

J. Tong, Y. Cao, Y. Hotta, N. Ishikawa, H. Nishimaki, K. Masuda, C. L. Yang, K. Kasai, and G. Itoh, “Cardiomyocyte Apoptosis Induced in Langendorff Preparation of Isolated Guinea-Pig Heart Perfused with Krebs-Henseleit Solution Deprived of Glucose, with and without Oxygen Supply,” Basic Appl. Myol. 11(3), 143–150 (2001).

Jacobson, B. C.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res. 62(3), 682–687 (2002).
[PubMed]

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D. M. Jameson, V. Thomas, and D. M. Zhou, “Time-resolved fluorescence studies on NADH bound to mitochondrial malate dehydrogenase,” Biochim. Biophys. Acta 994(2), 187–190 (1989).
[Crossref] [PubMed]

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S. Jentsch, D. Schweitzer, K. U. Schmidtke, S. Peters, J. Dawczynski, K. J. Bär, and M. Hammer, “Retinal fluorescence lifetime imaging ophthalmoscopy measures depend on the severity of Alzheimer’s disease,” Acta Ophthalmol. 93(4), e241–e247 (2015).
[Crossref] [PubMed]

Jilkina, O.

E. Gussakovsky, O. Jilkina, Y. Yang, and V. Kupriyanov, “Hemoglobin plus myoglobin concentrations and near infrared light pathlength in phantom and pig hearts determined by diffuse reflectance spectroscopy,” Anal. Biochem. 382(2), 107–115 (2008).
[Crossref] [PubMed]

Jobsis, F.

B. Chance, P. Cohen, F. Jobsis, and B. Schoener, “Intracellular oxidation-reduction states in vivo,” Science 137(3529), 499–508 (1962).
[Crossref] [PubMed]

Johnson, M. L.

J. R. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. L. Johnson, “Fluorescence lifetime imaging of free and protein-bound NADH,” Proc. Natl. Acad. Sci. U.S.A. 89(4), 1271–1275 (1992).
[Crossref] [PubMed]

Johnson, R. E.

T. Torikata, L. S. Forster, R. E. Johnson, and J. A. Rupley, “Lifetimes and NADH quenching of tryptophan fluorescence in pig heart cytoplasmic malate dehydrogenase,” J. Biol. Chem. 254(9), 3516–3520 (1979).
[PubMed]

Joseph, L.

A. N. Wick, T. N. Morita, and L. Joseph, “The oxidation of mannitol,” Proc. Soc. Exp. Biol. Med. 85(1), 188–190 (1954).
[Crossref] [PubMed]

Karlsson, M. G. D.

E. Häggblad, T. Lindbergh, M. G. D. Karlsson, H. Casimir-Ahn, E. G. Salerud, and T. Strömberg, “Myocardial tissue oxygenation estimated with calibrated diffuse reflectance spectroscopy during coronary artery bypass grafting,” J. Biomed. Opt. 13(5), 054030 (2008).
[Crossref] [PubMed]

Kasai, K.

J. Tong, Y. Cao, Y. Hotta, N. Ishikawa, H. Nishimaki, K. Masuda, C. L. Yang, K. Kasai, and G. Itoh, “Cardiomyocyte Apoptosis Induced in Langendorff Preparation of Isolated Guinea-Pig Heart Perfused with Krebs-Henseleit Solution Deprived of Glucose, with and without Oxygen Supply,” Basic Appl. Myol. 11(3), 143–150 (2001).

Kasischke, K. A.

Kasserra, C. E.

A. E. Arai, C. E. Kasserra, P. R. Territo, A. H. Gandjbakhche, and R. S. Balaban, “Myocardial oxygenation in vivo: optical spectroscopy of cytoplasmic myoglobin and mitochondrial cytochromes,” Am. J. Physiol. 277(2 Pt 2), H683–H697 (1999).
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T. E. King, R. L. Howard, D. F. Wilson, and J. C. Li, “The Partition of Flavins in the Heart Muscle Preparation and Heart Mitochondria,” J. Biol. Chem. 237(9), 2941–2946 (1962).
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D. Chorvat, J. Kirchnerova, M. Cagalinec, J. Smolka, A. Mateasik, and A. Chorvatova, “Spectral unmixing of flavin autofluorescence components in cardiac myocytes,” Biophys. J. 89(6), L55–L57 (2005).
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Koenig, K.

K. Koenig, H. Schneckenburger, J. Hemmer, B. J. Tromberg, and R. W. Steiner, “In-vivo fluorescence detection and imaging of porphyrin-producing bacteria in the human skin and in the oral cavity for diagnosis of acne vulgaris, caries, and squamous cell carcinoma,” Proc. SPIE 2135, 129–138 (1994).
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Konig, K.

H. Schneckenburger and K. Konig, “Fluorescence decay kinetics and imaging of NAD(P)H and flavins as metabolic indicators,” Opt. Eng. 31(7), 1447–1451 (1992).
[Crossref]

K. Konig, K. Schenke-layland, I. Riemann, and U. A. Stock, “Multiphoton autofluorescence imaging of intratissue elastic fibers,” Biomaterials26(1), 495–500 (2004).

Kupriyanov, V.

E. Gussakovsky, O. Jilkina, Y. Yang, and V. Kupriyanov, “Hemoglobin plus myoglobin concentrations and near infrared light pathlength in phantom and pig hearts determined by diffuse reflectance spectroscopy,” Anal. Biochem. 382(2), 107–115 (2008).
[Crossref] [PubMed]

la Cour, M. F.

M. F. la Cour, S. Mehrvar, J. S. Heisner, M. M. Motlagh, M. Medhora, M. Ranji, and A. K. S. Camara, “Optical metabolic imaging of irradiated rat heart exposed to ischemia-reperfusion injury,” J. Biomed. Opt. 23(1), 1–9 (2018).
[Crossref] [PubMed]

Lafontant, A.

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical metabolic imaging identifies glycolytic levels, subtypes, and early-treatment response in breast cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

Lagarto, J.

Lakowicz, J. R.

J. R. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. L. Johnson, “Fluorescence lifetime imaging of free and protein-bound NADH,” Proc. Natl. Acad. Sci. U.S.A. 89(4), 1271–1275 (1992).
[Crossref] [PubMed]

Li, J. C.

T. E. King, R. L. Howard, D. F. Wilson, and J. C. Li, “The Partition of Flavins in the Heart Muscle Preparation and Heart Mitochondria,” J. Biol. Chem. 237(9), 2941–2946 (1962).
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Y. Ti, P. Chen, and W.-C. Lin, “In vivo characterization of myocardial infarction using fluorescence and diffuse reflectance spectroscopy,” J. Biomed. Opt. 15(3), 037009 (2010).
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Lindbergh, T.

E. Häggblad, T. Lindbergh, M. G. D. Karlsson, H. Casimir-Ahn, E. G. Salerud, and T. Strömberg, “Myocardial tissue oxygenation estimated with calibrated diffuse reflectance spectroscopy during coronary artery bypass grafting,” J. Biomed. Opt. 13(5), 054030 (2008).
[Crossref] [PubMed]

Lopaschuk, G. D.

W. C. Stanley, F. A. Recchia, and G. D. Lopaschuk, “Myocardial substrate metabolism in the normal and failing heart,” Physiol. Rev. 85(3), 1093–1129 (2005).
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O. A. Bessey, O. H. Lowry, and R. H. Love, “The fluorometric measurement of the nucleotides of riboflavin and their concentration in tissues,” J. Biol. Chem. 180(2), 755–769 (1949).
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J. Eng, R. M. Lynch, and R. S. Balaban, “Nicotinamide adenine dinucleotide fluorescence spectroscopy and imaging of isolated cardiac myocytes,” Biophys. J. 55(4), 621–630 (1989).
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Maarek, J. I.

L. Marcu, D. Cohena, J. I. Maarek, W. S. Grundfesta, T. Development, and C. M. C. L. Angeles, “Characterization of Type I, II, III, IV, and V collagens by time-resolved laser-induced fluorescence spectroscopy,” Proc. SPIE 3917, 93–101 (2000).
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T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5(1), 3936 (2014).
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Manning, H. C.

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical metabolic imaging identifies glycolytic levels, subtypes, and early-treatment response in breast cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

Marble, D. R.

K. A. Schenkman, D. R. Marble, D. H. Burns, and E. O. Feigl, “Myoglobin oxygen dissociation by multiwavelength spectroscopy,” J. Appl. Physiol. 82(1), 86–92 (1997).
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L. Marcu, D. Cohena, J. I. Maarek, W. S. Grundfesta, T. Development, and C. M. C. L. Angeles, “Characterization of Type I, II, III, IV, and V collagens by time-resolved laser-induced fluorescence spectroscopy,” Proc. SPIE 3917, 93–101 (2000).
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Masters, B. R.

B. R. Masters, P. T. C. So, and E. Gratton, “Optical biopsy of in vivo human skin: Multi-photon excitation microscopy,” Lasers Med. Sci. 13(3), 196–203 (1998).
[Crossref]

Masuda, K.

J. Tong, Y. Cao, Y. Hotta, N. Ishikawa, H. Nishimaki, K. Masuda, C. L. Yang, K. Kasai, and G. Itoh, “Cardiomyocyte Apoptosis Induced in Langendorff Preparation of Isolated Guinea-Pig Heart Perfused with Krebs-Henseleit Solution Deprived of Glucose, with and without Oxygen Supply,” Basic Appl. Myol. 11(3), 143–150 (2001).

Mateasik, A.

D. Chorvat, J. Kirchnerova, M. Cagalinec, J. Smolka, A. Mateasik, and A. Chorvatova, “Spectral unmixing of flavin autofluorescence components in cardiac myocytes,” Biophys. J. 89(6), L55–L57 (2005).
[Crossref] [PubMed]

Matherne, G. P.

J. P. Headrick, J. Peart, B. Hack, A. Flood, and G. P. Matherne, “Functional properties and responses to ischaemia-reperfusion in Langendorff perfused mouse heart,” Exp. Physiol. 86(6), 703–716 (2001).
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A. Mayevsky and G. G. Rogatsky, “Mitochondrial function in vivo evaluated by NADH fluorescence: from animal models to human studies,” Am. J. Physiol. Cell Physiol. 292(2), C615–C640 (2007).
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Medhora, M.

M. F. la Cour, S. Mehrvar, J. S. Heisner, M. M. Motlagh, M. Medhora, M. Ranji, and A. K. S. Camara, “Optical metabolic imaging of irradiated rat heart exposed to ischemia-reperfusion injury,” J. Biomed. Opt. 23(1), 1–9 (2018).
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Mehrvar, S.

M. F. la Cour, S. Mehrvar, J. S. Heisner, M. M. Motlagh, M. Medhora, M. Ranji, and A. K. S. Camara, “Optical metabolic imaging of irradiated rat heart exposed to ischemia-reperfusion injury,” J. Biomed. Opt. 23(1), 1–9 (2018).
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Moon, J. C.

S. K. White, D. M. Sado, A. S. Flett, and J. C. Moon, “Characterising the myocardial interstitial space: the clinical relevance of non-invasive imaging,” Heart 98(10), 773–779 (2012).
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Morita, T. N.

A. N. Wick, T. N. Morita, and L. Joseph, “The oxidation of mannitol,” Proc. Soc. Exp. Biol. Med. 85(1), 188–190 (1954).
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Motlagh, M. M.

M. F. la Cour, S. Mehrvar, J. S. Heisner, M. M. Motlagh, M. Medhora, M. Ranji, and A. K. S. Camara, “Optical metabolic imaging of irradiated rat heart exposed to ischemia-reperfusion injury,” J. Biomed. Opt. 23(1), 1–9 (2018).
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Müller, M. G.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res. 62(3), 682–687 (2002).
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T. Doenst, T. D. Nguyen, and E. D. Abel, “Cardiac metabolism in heart failure: implications beyond ATP production,” Circ. Res. 113(6), 709–724 (2013).
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Nishimaki, H.

J. Tong, Y. Cao, Y. Hotta, N. Ishikawa, H. Nishimaki, K. Masuda, C. L. Yang, K. Kasai, and G. Itoh, “Cardiomyocyte Apoptosis Induced in Langendorff Preparation of Isolated Guinea-Pig Heart Perfused with Krebs-Henseleit Solution Deprived of Glucose, with and without Oxygen Supply,” Basic Appl. Myol. 11(3), 143–150 (2001).

Nowaczyk, K.

J. R. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. L. Johnson, “Fluorescence lifetime imaging of free and protein-bound NADH,” Proc. Natl. Acad. Sci. U.S.A. 89(4), 1271–1275 (1992).
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Pal, P.

A. Pradhan, P. Pal, G. Durocher, L. Villeneuve, A. Balassy, F. Babai, L. Gaboury, and L. Blanchard, “Steady state and time-resolved fluorescence properties of metastatic and non-metastatic malignant cells from different species,” J. Photochem. Photobiol. B 31(3), 101–112 (1995).
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Papayan, G.

G. Papayan, N. Petrishchev, and M. Galagudza, “Autofluorescence spectroscopy for NADH and flavoproteins redox state monitoring in the isolated rat heart subjected to ischemia-reperfusion,” Photodiagn. Photodyn. Ther. 11(3), 400–408 (2014).
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Peart, J.

J. P. Headrick, J. Peart, B. Hack, A. Flood, and G. P. Matherne, “Functional properties and responses to ischaemia-reperfusion in Langendorff perfused mouse heart,” Exp. Physiol. 86(6), 703–716 (2001).
[Crossref] [PubMed]

Peters, N. S.

Peters, S.

S. Jentsch, D. Schweitzer, K. U. Schmidtke, S. Peters, J. Dawczynski, K. J. Bär, and M. Hammer, “Retinal fluorescence lifetime imaging ophthalmoscopy measures depend on the severity of Alzheimer’s disease,” Acta Ophthalmol. 93(4), e241–e247 (2015).
[Crossref] [PubMed]

Petrishchev, N.

G. Papayan, N. Petrishchev, and M. Galagudza, “Autofluorescence spectroscopy for NADH and flavoproteins redox state monitoring in the isolated rat heart subjected to ischemia-reperfusion,” Photodiagn. Photodyn. Ther. 11(3), 400–408 (2014).
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Pradhan, A.

A. Pradhan, P. Pal, G. Durocher, L. Villeneuve, A. Balassy, F. Babai, L. Gaboury, and L. Blanchard, “Steady state and time-resolved fluorescence properties of metastatic and non-metastatic malignant cells from different species,” J. Photochem. Photobiol. B 31(3), 101–112 (1995).
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Ramanujam, N.

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[Crossref] [PubMed]

Ranji, M.

M. F. la Cour, S. Mehrvar, J. S. Heisner, M. M. Motlagh, M. Medhora, M. Ranji, and A. K. S. Camara, “Optical metabolic imaging of irradiated rat heart exposed to ischemia-reperfusion injury,” J. Biomed. Opt. 23(1), 1–9 (2018).
[Crossref] [PubMed]

Recchia, F. A.

W. C. Stanley, F. A. Recchia, and G. D. Lopaschuk, “Myocardial substrate metabolism in the normal and failing heart,” Physiol. Rev. 85(3), 1093–1129 (2005).
[Crossref] [PubMed]

Riching, K. M.

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[Crossref] [PubMed]

Riemann, I.

K. Konig, K. Schenke-layland, I. Riemann, and U. A. Stock, “Multiphoton autofluorescence imaging of intratissue elastic fibers,” Biomaterials26(1), 495–500 (2004).

Rogatsky, G. G.

A. Mayevsky and G. G. Rogatsky, “Mitochondrial function in vivo evaluated by NADH fluorescence: from animal models to human studies,” Am. J. Physiol. Cell Physiol. 292(2), C615–C640 (2007).
[Crossref] [PubMed]

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M. G. Rosca and C. L. Hoppel, “Mitochondrial dysfunction in heart failure,” Heart Fail. Rev. 18(5), 607–622 (2013).
[Crossref] [PubMed]

Rupley, J. A.

T. Torikata, L. S. Forster, R. E. Johnson, and J. A. Rupley, “Lifetimes and NADH quenching of tryptophan fluorescence in pig heart cytoplasmic malate dehydrogenase,” J. Biol. Chem. 254(9), 3516–3520 (1979).
[PubMed]

Sado, D. M.

S. K. White, D. M. Sado, A. S. Flett, and J. C. Moon, “Characterising the myocardial interstitial space: the clinical relevance of non-invasive imaging,” Heart 98(10), 773–779 (2012).
[Crossref] [PubMed]

Sakadžic, S.

Salerud, E. G.

E. Häggblad, T. Lindbergh, M. G. D. Karlsson, H. Casimir-Ahn, E. G. Salerud, and T. Strömberg, “Myocardial tissue oxygenation estimated with calibrated diffuse reflectance spectroscopy during coronary artery bypass grafting,” J. Biomed. Opt. 13(5), 054030 (2008).
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D. R. Saunders and H. S. Wiggins, “Conservation of mannitol, lactulose, and raffinose by the human colon,” Am. J. Physiol. 241(5), G397–G402 (1981).
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K. Konig, K. Schenke-layland, I. Riemann, and U. A. Stock, “Multiphoton autofluorescence imaging of intratissue elastic fibers,” Biomaterials26(1), 495–500 (2004).

Schenkman, K. A.

K. A. Schenkman, D. R. Marble, D. H. Burns, and E. O. Feigl, “Myoglobin oxygen dissociation by multiwavelength spectroscopy,” J. Appl. Physiol. 82(1), 86–92 (1997).
[Crossref] [PubMed]

Schmidtke, K. U.

S. Jentsch, D. Schweitzer, K. U. Schmidtke, S. Peters, J. Dawczynski, K. J. Bär, and M. Hammer, “Retinal fluorescence lifetime imaging ophthalmoscopy measures depend on the severity of Alzheimer’s disease,” Acta Ophthalmol. 93(4), e241–e247 (2015).
[Crossref] [PubMed]

Schneckenburger, H.

K. Koenig, H. Schneckenburger, J. Hemmer, B. J. Tromberg, and R. W. Steiner, “In-vivo fluorescence detection and imaging of porphyrin-producing bacteria in the human skin and in the oral cavity for diagnosis of acne vulgaris, caries, and squamous cell carcinoma,” Proc. SPIE 2135, 129–138 (1994).
[Crossref]

H. Schneckenburger and K. Konig, “Fluorescence decay kinetics and imaging of NAD(P)H and flavins as metabolic indicators,” Opt. Eng. 31(7), 1447–1451 (1992).
[Crossref]

Schoener, B.

B. Chance, P. Cohen, F. Jobsis, and B. Schoener, “Intracellular oxidation-reduction states in vivo,” Science 137(3529), 499–508 (1962).
[Crossref] [PubMed]

Schweitzer, D.

S. Jentsch, D. Schweitzer, K. U. Schmidtke, S. Peters, J. Dawczynski, K. J. Bär, and M. Hammer, “Retinal fluorescence lifetime imaging ophthalmoscopy measures depend on the severity of Alzheimer’s disease,” Acta Ophthalmol. 93(4), e241–e247 (2015).
[Crossref] [PubMed]

Sheets, E. E.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res. 62(3), 682–687 (2002).
[PubMed]

Sikkel, M. B.

Skala, M. C.

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical metabolic imaging identifies glycolytic levels, subtypes, and early-treatment response in breast cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[Crossref] [PubMed]

Smolka, J.

D. Chorvat, J. Kirchnerova, M. Cagalinec, J. Smolka, A. Mateasik, and A. Chorvatova, “Spectral unmixing of flavin autofluorescence components in cardiac myocytes,” Biophys. J. 89(6), L55–L57 (2005).
[Crossref] [PubMed]

So, P. T. C.

B. R. Masters, P. T. C. So, and E. Gratton, “Optical biopsy of in vivo human skin: Multi-photon excitation microscopy,” Lasers Med. Sci. 13(3), 196–203 (1998).
[Crossref]

Spivey, H. O.

T. Fukushima, R. V. Decker, W. M. Anderson, and H. O. Spivey, “Substrate channeling of NADH and binding of dehydrogenases to complex I,” J. Biol. Chem. 264(28), 16483–16488 (1989).
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Stanley, W. C.

W. C. Stanley, F. A. Recchia, and G. D. Lopaschuk, “Myocardial substrate metabolism in the normal and failing heart,” Physiol. Rev. 85(3), 1093–1129 (2005).
[Crossref] [PubMed]

Steiner, R. W.

K. Koenig, H. Schneckenburger, J. Hemmer, B. J. Tromberg, and R. W. Steiner, “In-vivo fluorescence detection and imaging of porphyrin-producing bacteria in the human skin and in the oral cavity for diagnosis of acne vulgaris, caries, and squamous cell carcinoma,” Proc. SPIE 2135, 129–138 (1994).
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Stienen, G. J. M.

R. C. I. Wüst, M. Helmes, and G. J. M. Stienen, “Rapid changes in NADH and flavin autofluorescence in rat cardiac trabeculae reveal large mitochondrial complex II reserve capacity,” J. Physiol. 593(8), 1829–1840 (2015).
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Stock, U. A.

K. Konig, K. Schenke-layland, I. Riemann, and U. A. Stock, “Multiphoton autofluorescence imaging of intratissue elastic fibers,” Biomaterials26(1), 495–500 (2004).

Strömberg, T.

E. Häggblad, T. Lindbergh, M. G. D. Karlsson, H. Casimir-Ahn, E. G. Salerud, and T. Strömberg, “Myocardial tissue oxygenation estimated with calibrated diffuse reflectance spectroscopy during coronary artery bypass grafting,” J. Biomed. Opt. 13(5), 054030 (2008).
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Y. Sun and K. T. Weber, “Infarct scar: a dynamic tissue,” Cardiovasc. Res. 46(2), 250–256 (2000).
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F. J. Sutherland and D. J. Hearse, “The isolated blood and perfusion fluid perfused heart,” Pharmacol. Res. 41(6), 613–627 (2000).
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Szabadkai, G.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5(1), 3936 (2014).
[Crossref] [PubMed]

Szmacinski, H.

J. R. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. L. Johnson, “Fluorescence lifetime imaging of free and protein-bound NADH,” Proc. Natl. Acad. Sci. U.S.A. 89(4), 1271–1275 (1992).
[Crossref] [PubMed]

Talbot, C.

Territo, P. R.

A. E. Arai, C. E. Kasserra, P. R. Territo, A. H. Gandjbakhche, and R. S. Balaban, “Myocardial oxygenation in vivo: optical spectroscopy of cytoplasmic myoglobin and mitochondrial cytochromes,” Am. J. Physiol. 277(2 Pt 2), H683–H697 (1999).
[PubMed]

Thomas, V.

D. M. Jameson, V. Thomas, and D. M. Zhou, “Time-resolved fluorescence studies on NADH bound to mitochondrial malate dehydrogenase,” Biochim. Biophys. Acta 994(2), 187–190 (1989).
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Figures (6)

Fig. 1
Fig. 1 Schematic representation of the Langendorff experimental setup. A three-way tap was positioned immediately after the reservoirs to guarantee that only oxygenated or deoxygenation solution was delivered to the heart at a given time. Temperature of the heart was maintained at 37.5 ± 1 °C. Highlighted area in the left ventricular wall of the heart indicates the region of measurements. Black arrows indicate direction of the flow.
Fig. 2
Fig. 2 A) Representative absorbance spectra of oxygenated (blue curve) and hypoxic (red curve) cardiac tissue obtained from the Langendorff setup. The bottom curve (in green) shows the difference between the two spectra, i.e. A(baseline)-A(hypoxia). In the top panel, vertical black arrows indicate two wavelengths at which the differences between curves are maximized and the transition from + O2 to –O2 is also indicated. B) Estimated tissue oxygenation throughout the experiments calculated using the ratio of tissue absorption at 578 nm divided by the absorption at 600 nm. C) Estimated cytochrome c oxidation state estimated by the ratio of the tissue absorption at 502 nm divided by the absorption at 550 nm. Dashed vertical lines in grey indicate the switching time between oxygenated and deoxygenated Krebs solutions. Solid lines represent the mean taken over different hearts and shaded regions represent the region up to one standard deviation from the mean. Control, n = 4; hypoxia, n = 6; mannitol, n = 5.
Fig. 3
Fig. 3 Variation of autofluorescence intensity signal in channels (A) 2 and (B) 4, corresponding primarily to NAD(P)H and FAD autofluorescence, respectively. (C) Redox ratio curves calculated according to Eq. (2). Solid lines represent the mean taken over different heart and shaded regions represent up to one standard deviation from the mean. Greyed dashed lines indicate the time when the perfusion solution was changed.
Fig. 4
Fig. 4 Autofluorescence lifetime parameters measured in channel 2: (A) mean lifetime; (B) contribution of short lifetime component α1; (C) short lifetime τ1; (D) long lifetime τ2. NADH is the major fluorophore contributing to the autofluorescence signal in this channel. Decrease of short component lifetime with concomitant increase in its contribution suggests increase in free-NADH content during hypoxia. Solid lines represent the mean taken over different heart and shaded regions represent up to one standard deviation from the mean. Greyed dashed lines indicate the time when the perfusion solution was changed.
Fig. 5
Fig. 5 Autofluorescence lifetime parameters measured in channel 3: (A) mean lifetime; (B) contribution of short lifetime component α1; (C) short lifetime τ1; (D) long lifetime τ2. The autofluorescence signal in this channel emanates primarily from NADH and, to a lesser extent, FAD. Solid lines represent the mean taken over different heart and shaded regions represent up to one standard deviation from the mean. Greyed dashed lines indicate the time when the perfusion solution was changed.
Fig. 6
Fig. 6 Autofluorescence lifetime parameters measured in channel 4: (A) mean lifetime; (B) contribution of short lifetime component α1; (C) short lifetime τ1; (D) long lifetime τ2. The major contributor to the autofluorescence signal in this channel is FAD. Solid lines represent the mean taken over different heart and shaded regions represent up to one standard deviation from the mean. Greyed dashed lines indicate the time when the perfusion solution was changed.

Tables (3)

Tables Icon

Table 1 Summary of the different detection spectral channels.

Tables Icon

Table 2 Comparison of weighted mean autofluorescence lifetimes previously reported for healthy hearts in vivo [25] and in this study. In vivo measurements were realized in the anterior wall of the left ventricle.

Tables Icon

Table 3 Summary of variation of autofluorescence intensity and lifetime parameters during hypoxia and glucose-depletion measurements. Arrows indicate increase (↑) or decrease (↓) in the corresponding parameter relative to baseline measurements.

Equations (6)

Equations on this page are rendered with MathJax. Learn more.

A(λ)= log 10 ( I(λ) I 0 (λ) )
RR= I CH2 I CH2 + I CH3 NAD(P)H NAD(P)H+FAD
I(t)= a 1 e (t/ τ 1 ) + a 2 e (t/ τ 2 )
τ mean = a 1 τ 1 2 + a 2 τ 2 2 a 1 τ 1 + a 1 τ 2
α 1 = a 1 a 1 + a 2
χ 2 = k=1 n (I( t k ) I model ( t k )) 2 I( t k )

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