Abstract

Cardiac remodeling following myocardial infarction (MI) involves structural and functional alterations in the infarcted and remote viable myocardium that can ultimately lead to heart failure. The underlying mechanisms are not fully understood and, following our previous study of the autofluorescence lifetime and diffuse reflectance signatures of the myocardium in vivo at 16 weeks post MI in rats [Biomed. Opt. Express 6(2), 324 (2015)], we here present data obtained at 1, 2 and 4 weeks post myocardial infarction that help follow the temporal progression of these changes. Our results demonstrate that both structural and metabolic changes in the heart can be monitored from the earliest time points following MI using label-free optical readouts, not only in the region of infarction but also in the remote non-infarcted myocardium. Changes in the autofluorescence intensity and lifetime parameters associated with collagen type I autofluorescence were indicative of progressive collagen deposition in tissue that was most pronounced at earlier time points and in the region of infarction. In addition to significant collagen deposition in infarcted and non-infarcted myocardium, we also report changes in the autofluorescence parameters associated with reduced nicotinamide adenine (phosphate) dinucleotide (NAD(P)H) and flavin adenine dinucleotide (FAD), which we associate with metabolic alterations throughout the heart. Parallel measurements of the diffuse reflectance spectra indicated an increased contribution of reduced cytochrome c. Our findings suggest that combining time-resolved spectrofluorometry and diffuse reflectance spectroscopy could provide a useful means to monitor cardiac function in vivo at the time of surgery.

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2018 (1)

2017 (3)

W. Lewis, J. P. Padilla-Martinez, A. Ortega-Martinez, and W. Franco, “Changes in endogenous UV fluorescence and biomechanical stiffness of bovine articular cartilage after collagenase digestion are strongly correlated,” J. Biophotonics 10(8), 1018–1025 (2017).
[PubMed]

F. Poulon, H. Mehidine, M. Juchaux, P. Varlet, B. Devaux, J. Pallud, and D. Abi Haidar, “Optical properties, spectral, and lifetime measurements of central nervous system tumors in humans,” Sci. Rep. 7(1), 13995 (2017).
[Crossref] [PubMed]

J. Bec, J. E. Phipps, D. Gorpas, D. Ma, H. Fatakdawala, K. B. Margulies, J. A. Southard, and L. Marcu, “In vivo label-free structural and biochemical imaging of coronary arteries using an integrated ultrasound and multispectral fluorescence lifetime catheter system,” Sci. Rep. 7(1), 8960 (2017).
[PubMed]

2016 (1)

S. R. Kantelhardt, D. Kalasauskas, K. König, E. Kim, M. Weinigel, A. Uchugonova, and A. Giese, “In vivo multiphoton tomography and fluorescence lifetime imaging of human brain tumor tissue,” J. Neurooncol. 127(3), 473–482 (2016).
[Crossref] [PubMed]

2015 (2)

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]

T. L. Nguyen, J. A. K. Phan, L. Hee, D. A. Moses, J. Otton, O. D. Terreblanche, J. Xiong, U. Premawardhana, R. Rajaratnam, C. P. Juergens, H. R. Dimitri, J. K. French, D. A. Richards, and L. Thomas, “High-sensitivity troponin T predicts infarct scar characteristics and adverse left ventricular function by cardiac magnetic resonance imaging early after reperfused acute myocardial infarction,” Am. Heart J. 170(4), 715–725 (2015).
[Crossref] [PubMed]

2014 (1)

A. C. Croce and G. Bottiroli, “Autofluorescence spectroscopy and imaging: a tool for biomedical research and diagnosis,” Eur. J. Histochem. 58(4), 2461 (2014).
[Crossref] [PubMed]

2013 (4)

I. Stefanon, M. Valero-Muñoz, A. A. Fernandes, R. F. Ribeiro, C. Rodríguez, M. Miana, J. Martínez-González, J. S. Spalenza, V. Lahera, P. F. Vassallo, and V. Cachofeiro, “Left and right ventricle late remodeling following myocardial infarction in rats,” PLoS One 8(5), e64986 (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]

Y. Sun, J. E. Phipps, J. Meier, N. Hatami, B. Poirier, D. S. Elson, D. G. Farwell, and L. Marcu, “Endoscopic fluorescence lifetime imaging for in vivo intraoperative diagnosis of oral carcinoma,” Microsc. Microanal. 19(4), 791–798 (2013).
[Crossref] [PubMed]

H. B. Manning, M. B. Nickdel, K. Yamamoto, J. L. Lagarto, D. J. Kelly, C. B. Talbot, G. Kennedy, J. Dudhia, J. Lever, C. Dunsby, P. French, and Y. Itoh, “Detection of cartilage matrix degradation by autofluorescence lifetime,” Matrix Biol. 32(1), 32–38 (2013).
[Crossref] [PubMed]

2012 (4)

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

L. Marcu, “Fluorescence lifetime techniques in medical applications,” Ann. Biomed. Eng. 40(2), 304–331 (2012).
[Crossref] [PubMed]

A. R. Lyon, V. O. Nikolaev, M. Miragoli, M. B. Sikkel, H. Paur, L. Benard, J.-S. Hulot, E. Kohlbrenner, R. J. Hajjar, N. S. Peters, Y. E. Korchev, K. T. Macleod, S. E. Harding, and J. Gorelik, “Plasticity of surface structures and β(2)-adrenergic receptor localization in failing ventricular cardiomyocytes during recovery from heart failure,” Circ Heart Fail 5(3), 357–365 (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]

2009 (3)

A. R. Lyon, K. T. MacLeod, Y. Zhang, E. Garcia, G. K. Kanda, M. J. Lab, Y. E. Korchev, S. E. Harding, and J. Gorelik, “Loss of T-tubules and other changes to surface topography in ventricular myocytes from failing human and rat heart,” Proc. Natl. Acad. Sci. U.S.A. 106(16), 6854–6859 (2009).
[Crossref] [PubMed]

P. Uehlinger, T. Gabrecht, T. Glanzmann, J.-P. Ballini, A. Radu, S. Andrejevic, P. Monnier, and G. Wagnières, “In vivo time-resolved spectroscopy of the human bronchial early cancer autofluorescence,” J. Biomed. Opt. 14(2), 024011 (2009).
[Crossref] [PubMed]

M. Ranji, M. Matsubara, B. G. Leshnower, R. H. Hinmon, D. L. Jaggard, B. Chance, R. C. Gorman, J. H. Gorman Iii, R. C. Gorman, and J. H. Gorman, “Quantifying acute myocardial injury using ratiometric fluorometry,” IEEE Trans. Biomed. Eng. 56(5), 1556–1563 (2009).
[PubMed]

2008 (2)

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]

H. B. Manning, G. T. Kennedy, D. M. Owen, D. M. Grant, A. I. Magee, M. A. A. Neil, Y. Itoh, C. Dunsby, and P. M. W. French, “A compact, multidimensional spectrofluorometer exploiting supercontinuum generation,” J. Biophotonics 1(6), 494–505 (2008).
[Crossref] [PubMed]

2007 (2)

M. C. Skala, K. M. Riching, D. K. Bird, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, P. J. Keely, and N. Ramanujam, “In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia,” J. Biomed. Opt. 12(2), 024014 (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]

2003 (2)

P. J. Tadrous, J. Siegel, P. M. French, S. Shousha, N. Lalani, and G. W. H. Stamp, “Fluorescence lifetime imaging of unstained tissues: early results in human breast cancer,” J. Pathol. 199(3), 309–317 (2003).
[Crossref] [PubMed]

B. I. Jugdutt, “Ventricular remodeling after infarction and the extracellular collagen matrix: when is enough enough?” Circulation 108(11), 1395–1403 (2003).
[Crossref] [PubMed]

2001 (2)

W. M. Blankesteijn, E. Creemers, E. Lutgens, J. P. Cleutjens, M. J. Daemen, and J. F. Smits, “Dynamics of cardiac wound healing following myocardial infarction: observations in genetically altered mice,” Acta Physiol. Scand. 173(1), 75–82 (2001).
[Crossref] [PubMed]

D. Baykut, M. M. Gebhard, H. Bölükoglu, K. Kadipasaoglu, S. Hennes, O. H. Frazier, and A. Krian, “Online detection of myocardial ischemia by near infrared spectroscopy with a fiberoptic catheter,” Thorac. Cardiovasc. Surg. 49(3), 162–166 (2001).
[Crossref] [PubMed]

2000 (2)

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

J. N. Cohn, R. Ferrari, and N. Sharpe, “Cardiac remodeling--concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. Behalf of an International Forum on Cardiac Remodeling,” J. Am. Coll. Cardiol. 35(3), 569–582 (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), H683–H697 (1999).
[PubMed]

1998 (2)

M.-A. Mycek, K. T. Schomacker, and N. S. Nishioka, “Colonic polyp differentiation using time-resolved autofluorescence spectroscopy,” Gastrointest. Endosc. 48(4), 390–394 (1998).
[Crossref] [PubMed]

G. A. Wagnières, W. M. Star, and B. C. Wilson, “In vivo fluorescence spectroscopy and imaging for oncological applications,” Photochem. Photobiol. 68(5), 603–632 (1998).
[Crossref] [PubMed]

1997 (1)

A. F. Maes, M. Borgers, W. Flameng, J. L. Nuyts, F. van de Werf, J. J. Ausma, P. Sergeant, and L. A. Mortelmans, “Assessment of myocardial viability in chronic coronary artery disease using technetium-99m sestamibi SPECT. Correlation with histologic and positron emission tomographic studies and functional follow-up,” J. Am. Coll. Cardiol. 29(1), 62–68 (1997).
[Crossref] [PubMed]

1996 (1)

R. S. Balaban, V. K. Mootha, and A. Arai, “Spectroscopic determination of cytochrome c oxidase content in tissues containing myoglobin or hemoglobin,” Anal. Biochem. 237(2), 274–278 (1996).
[Crossref] [PubMed]

1995 (2)

J. P. Cleutjens, M. J. Verluyten, J. F. Smiths, and M. J. Daemen, “Collagen remodeling after myocardial infarction in the rat heart,” Am. J. Pathol. 147(2), 325–338 (1995).
[PubMed]

R. W. Burt, O. W. Perkins, B. E. Oppenheim, D. S. Schauwecker, L. Stein, H. N. Wellman, and R. M. Witt, “Direct comparison of fluorine-18-FDG SPECT, fluorine-18-FDG PET and rest thallium-201 SPECT for detection of myocardial viability,” J. Nucl. Med. 36(2), 176–179 (1995).
[PubMed]

1990 (1)

M. A. Pfeffer and E. Braunwald, “Ventricular remodeling after myocardial infarction. Experimental observations and clinical implications,” Circulation 81(4), 1161–1172 (1990).
[Crossref] [PubMed]

1982 (1)

J. S. Hochman and B. H. Bulkley, “Expansion of acute myocardial infarction: an experimental study,” Circulation 65(7), 1446–1450 (1982).
[Crossref] [PubMed]

1981 (1)

L. W. Eaton and B. H. Bulkley, “Expansion of acute myocardial infarction: its relationship to infarct morphology in a canine model,” Circ. Res. 49(1), 80–88 (1981).
[Crossref] [PubMed]

1962 (1)

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

1959 (1)

E. Margoliash and N. Frohwirt, “Spectrum of horse-heart cytochrome c,” Biochem. J. 71(3), 570–572 (1959).
[Crossref] [PubMed]

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]

Abi Haidar, D.

F. Poulon, H. Mehidine, M. Juchaux, P. Varlet, B. Devaux, J. Pallud, and D. Abi Haidar, “Optical properties, spectral, and lifetime measurements of central nervous system tumors in humans,” Sci. Rep. 7(1), 13995 (2017).
[Crossref] [PubMed]

Andersson-Engels, S.

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

Andrejevic, S.

P. Uehlinger, T. Gabrecht, T. Glanzmann, J.-P. Ballini, A. Radu, S. Andrejevic, P. Monnier, and G. Wagnières, “In vivo time-resolved spectroscopy of the human bronchial early cancer autofluorescence,” J. Biomed. Opt. 14(2), 024011 (2009).
[Crossref] [PubMed]

Arai, A.

R. S. Balaban, V. K. Mootha, and A. Arai, “Spectroscopic determination of cytochrome c oxidase content in tissues containing myoglobin or hemoglobin,” Anal. Biochem. 237(2), 274–278 (1996).
[Crossref] [PubMed]

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), H683–H697 (1999).
[PubMed]

Ausma, J. J.

A. F. Maes, M. Borgers, W. Flameng, J. L. Nuyts, F. van de Werf, J. J. Ausma, P. Sergeant, and L. A. Mortelmans, “Assessment of myocardial viability in chronic coronary artery disease using technetium-99m sestamibi SPECT. Correlation with histologic and positron emission tomographic studies and functional follow-up,” J. Am. Coll. Cardiol. 29(1), 62–68 (1997).
[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), H683–H697 (1999).
[PubMed]

R. S. Balaban, V. K. Mootha, and A. Arai, “Spectroscopic determination of cytochrome c oxidase content in tissues containing myoglobin or hemoglobin,” Anal. Biochem. 237(2), 274–278 (1996).
[Crossref] [PubMed]

Ballini, J.-P.

P. Uehlinger, T. Gabrecht, T. Glanzmann, J.-P. Ballini, A. Radu, S. Andrejevic, P. Monnier, and G. Wagnières, “In vivo time-resolved spectroscopy of the human bronchial early cancer autofluorescence,” J. Biomed. Opt. 14(2), 024011 (2009).
[Crossref] [PubMed]

Baykut, D.

D. Baykut, M. M. Gebhard, H. Bölükoglu, K. Kadipasaoglu, S. Hennes, O. H. Frazier, and A. Krian, “Online detection of myocardial ischemia by near infrared spectroscopy with a fiberoptic catheter,” Thorac. Cardiovasc. Surg. 49(3), 162–166 (2001).
[Crossref] [PubMed]

Bec, J.

J. Bec, J. E. Phipps, D. Gorpas, D. Ma, H. Fatakdawala, K. B. Margulies, J. A. Southard, and L. Marcu, “In vivo label-free structural and biochemical imaging of coronary arteries using an integrated ultrasound and multispectral fluorescence lifetime catheter system,” Sci. Rep. 7(1), 8960 (2017).
[PubMed]

Benard, L.

A. R. Lyon, V. O. Nikolaev, M. Miragoli, M. B. Sikkel, H. Paur, L. Benard, J.-S. Hulot, E. Kohlbrenner, R. J. Hajjar, N. S. Peters, Y. E. Korchev, K. T. Macleod, S. E. Harding, and J. Gorelik, “Plasticity of surface structures and β(2)-adrenergic receptor localization in failing ventricular cardiomyocytes during recovery from heart failure,” Circ Heart Fail 5(3), 357–365 (2012).
[Crossref] [PubMed]

Bendsøe, N.

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

Bird, D. K.

M. C. Skala, K. M. Riching, D. K. Bird, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, P. J. Keely, and N. Ramanujam, “In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia,” J. Biomed. Opt. 12(2), 024014 (2007).
[Crossref] [PubMed]

Blankesteijn, W. M.

W. M. Blankesteijn, E. Creemers, E. Lutgens, J. P. Cleutjens, M. J. Daemen, and J. F. Smits, “Dynamics of cardiac wound healing following myocardial infarction: observations in genetically altered mice,” Acta Physiol. Scand. 173(1), 75–82 (2001).
[Crossref] [PubMed]

Bölükoglu, H.

D. Baykut, M. M. Gebhard, H. Bölükoglu, K. Kadipasaoglu, S. Hennes, O. H. Frazier, and A. Krian, “Online detection of myocardial ischemia by near infrared spectroscopy with a fiberoptic catheter,” Thorac. Cardiovasc. Surg. 49(3), 162–166 (2001).
[Crossref] [PubMed]

Borgers, M.

A. F. Maes, M. Borgers, W. Flameng, J. L. Nuyts, F. van de Werf, J. J. Ausma, P. Sergeant, and L. A. Mortelmans, “Assessment of myocardial viability in chronic coronary artery disease using technetium-99m sestamibi SPECT. Correlation with histologic and positron emission tomographic studies and functional follow-up,” J. Am. Coll. Cardiol. 29(1), 62–68 (1997).
[Crossref] [PubMed]

Bottiroli, G.

A. C. Croce and G. Bottiroli, “Autofluorescence spectroscopy and imaging: a tool for biomedical research and diagnosis,” Eur. J. Histochem. 58(4), 2461 (2014).
[Crossref] [PubMed]

Braunwald, E.

M. A. Pfeffer and E. Braunwald, “Ventricular remodeling after myocardial infarction. Experimental observations and clinical implications,” Circulation 81(4), 1161–1172 (1990).
[Crossref] [PubMed]

Bulkley, B. H.

J. S. Hochman and B. H. Bulkley, “Expansion of acute myocardial infarction: an experimental study,” Circulation 65(7), 1446–1450 (1982).
[Crossref] [PubMed]

L. W. Eaton and B. H. Bulkley, “Expansion of acute myocardial infarction: its relationship to infarct morphology in a canine model,” Circ. Res. 49(1), 80–88 (1981).
[Crossref] [PubMed]

Burt, R. W.

R. W. Burt, O. W. Perkins, B. E. Oppenheim, D. S. Schauwecker, L. Stein, H. N. Wellman, and R. M. Witt, “Direct comparison of fluorine-18-FDG SPECT, fluorine-18-FDG PET and rest thallium-201 SPECT for detection of myocardial viability,” J. Nucl. Med. 36(2), 176–179 (1995).
[PubMed]

Cachofeiro, V.

I. Stefanon, M. Valero-Muñoz, A. A. Fernandes, R. F. Ribeiro, C. Rodríguez, M. Miana, J. Martínez-González, J. S. Spalenza, V. Lahera, P. F. Vassallo, and V. Cachofeiro, “Left and right ventricle late remodeling following myocardial infarction in rats,” PLoS One 8(5), e64986 (2013).
[Crossref] [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.

M. Ranji, M. Matsubara, B. G. Leshnower, R. H. Hinmon, D. L. Jaggard, B. Chance, R. C. Gorman, J. H. Gorman Iii, R. C. Gorman, and J. H. Gorman, “Quantifying acute myocardial injury using ratiometric fluorometry,” IEEE Trans. Biomed. Eng. 56(5), 1556–1563 (2009).
[PubMed]

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

Cleutjens, J. P.

W. M. Blankesteijn, E. Creemers, E. Lutgens, J. P. Cleutjens, M. J. Daemen, and J. F. Smits, “Dynamics of cardiac wound healing following myocardial infarction: observations in genetically altered mice,” Acta Physiol. Scand. 173(1), 75–82 (2001).
[Crossref] [PubMed]

J. P. Cleutjens, M. J. Verluyten, J. F. Smiths, and M. J. Daemen, “Collagen remodeling after myocardial infarction in the rat heart,” Am. J. Pathol. 147(2), 325–338 (1995).
[PubMed]

Coda, S.

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[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]

Cohn, J. N.

J. N. Cohn, R. Ferrari, and N. Sharpe, “Cardiac remodeling--concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. Behalf of an International Forum on Cardiac Remodeling,” J. Am. Coll. Cardiol. 35(3), 569–582 (2000).
[Crossref] [PubMed]

Creemers, E.

W. M. Blankesteijn, E. Creemers, E. Lutgens, J. P. Cleutjens, M. J. Daemen, and J. F. Smits, “Dynamics of cardiac wound healing following myocardial infarction: observations in genetically altered mice,” Acta Physiol. Scand. 173(1), 75–82 (2001).
[Crossref] [PubMed]

Croce, A. C.

A. C. Croce and G. Bottiroli, “Autofluorescence spectroscopy and imaging: a tool for biomedical research and diagnosis,” Eur. J. Histochem. 58(4), 2461 (2014).
[Crossref] [PubMed]

Daemen, M. J.

W. M. Blankesteijn, E. Creemers, E. Lutgens, J. P. Cleutjens, M. J. Daemen, and J. F. Smits, “Dynamics of cardiac wound healing following myocardial infarction: observations in genetically altered mice,” Acta Physiol. Scand. 173(1), 75–82 (2001).
[Crossref] [PubMed]

J. P. Cleutjens, M. J. Verluyten, J. F. Smiths, and M. J. Daemen, “Collagen remodeling after myocardial infarction in the rat heart,” Am. J. Pathol. 147(2), 325–338 (1995).
[PubMed]

De Beule, P. A. A.

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

Devaux, B.

F. Poulon, H. Mehidine, M. Juchaux, P. Varlet, B. Devaux, J. Pallud, and D. Abi Haidar, “Optical properties, spectral, and lifetime measurements of central nervous system tumors in humans,” Sci. Rep. 7(1), 13995 (2017).
[Crossref] [PubMed]

Dimitri, H. R.

T. L. Nguyen, J. A. K. Phan, L. Hee, D. A. Moses, J. Otton, O. D. Terreblanche, J. Xiong, U. Premawardhana, R. Rajaratnam, C. P. Juergens, H. R. Dimitri, J. K. French, D. A. Richards, and L. Thomas, “High-sensitivity troponin T predicts infarct scar characteristics and adverse left ventricular function by cardiac magnetic resonance imaging early after reperfused acute myocardial infarction,” Am. Heart J. 170(4), 715–725 (2015).
[Crossref] [PubMed]

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]

Dudhia, J.

H. B. Manning, M. B. Nickdel, K. Yamamoto, J. L. Lagarto, D. J. Kelly, C. B. Talbot, G. Kennedy, J. Dudhia, J. Lever, C. Dunsby, P. French, and Y. Itoh, “Detection of cartilage matrix degradation by autofluorescence lifetime,” Matrix Biol. 32(1), 32–38 (2013).
[Crossref] [PubMed]

Dunsby, C.

J. L. Lagarto, B. T. Dyer, C. B. Talbot, N. S. Peters, P. M. W. French, A. R. Lyon, and C. Dunsby, “Characterization of NAD(P)H and FAD autofluorescence signatures in a Langendorff isolated-perfused rat heart model,” Biomed. Opt. Express 9(10), 4961–4978 (2018).
[Crossref] [PubMed]

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]

H. B. Manning, M. B. Nickdel, K. Yamamoto, J. L. Lagarto, D. J. Kelly, C. B. Talbot, G. Kennedy, J. Dudhia, J. Lever, C. Dunsby, P. French, and Y. Itoh, “Detection of cartilage matrix degradation by autofluorescence lifetime,” Matrix Biol. 32(1), 32–38 (2013).
[Crossref] [PubMed]

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

H. B. Manning, G. T. Kennedy, D. M. Owen, D. M. Grant, A. I. Magee, M. A. A. Neil, Y. Itoh, C. Dunsby, and P. M. W. French, “A compact, multidimensional spectrofluorometer exploiting supercontinuum generation,” J. Biophotonics 1(6), 494–505 (2008).
[Crossref] [PubMed]

Dyer, B. T.

Eaton, L. W.

L. W. Eaton and B. H. Bulkley, “Expansion of acute myocardial infarction: its relationship to infarct morphology in a canine model,” Circ. Res. 49(1), 80–88 (1981).
[Crossref] [PubMed]

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]

M. C. Skala, K. M. Riching, D. K. Bird, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, P. J. Keely, and N. Ramanujam, “In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia,” J. Biomed. Opt. 12(2), 024014 (2007).
[Crossref] [PubMed]

Eliceiri, K. W.

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

M. C. Skala, K. M. Riching, D. K. Bird, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, P. J. Keely, and N. Ramanujam, “In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia,” J. Biomed. Opt. 12(2), 024014 (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]

Elson, D. S.

Y. Sun, J. E. Phipps, J. Meier, N. Hatami, B. Poirier, D. S. Elson, D. G. Farwell, and L. Marcu, “Endoscopic fluorescence lifetime imaging for in vivo intraoperative diagnosis of oral carcinoma,” Microsc. Microanal. 19(4), 791–798 (2013).
[Crossref] [PubMed]

Farwell, D. G.

Y. Sun, J. E. Phipps, J. Meier, N. Hatami, B. Poirier, D. S. Elson, D. G. Farwell, and L. Marcu, “Endoscopic fluorescence lifetime imaging for in vivo intraoperative diagnosis of oral carcinoma,” Microsc. Microanal. 19(4), 791–798 (2013).
[Crossref] [PubMed]

Fatakdawala, H.

J. Bec, J. E. Phipps, D. Gorpas, D. Ma, H. Fatakdawala, K. B. Margulies, J. A. Southard, and L. Marcu, “In vivo label-free structural and biochemical imaging of coronary arteries using an integrated ultrasound and multispectral fluorescence lifetime catheter system,” Sci. Rep. 7(1), 8960 (2017).
[PubMed]

Fernandes, A. A.

I. Stefanon, M. Valero-Muñoz, A. A. Fernandes, R. F. Ribeiro, C. Rodríguez, M. Miana, J. Martínez-González, J. S. Spalenza, V. Lahera, P. F. Vassallo, and V. Cachofeiro, “Left and right ventricle late remodeling following myocardial infarction in rats,” PLoS One 8(5), e64986 (2013).
[Crossref] [PubMed]

Ferrari, R.

J. N. Cohn, R. Ferrari, and N. Sharpe, “Cardiac remodeling--concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. Behalf of an International Forum on Cardiac Remodeling,” J. Am. Coll. Cardiol. 35(3), 569–582 (2000).
[Crossref] [PubMed]

Flameng, W.

A. F. Maes, M. Borgers, W. Flameng, J. L. Nuyts, F. van de Werf, J. J. Ausma, P. Sergeant, and L. A. Mortelmans, “Assessment of myocardial viability in chronic coronary artery disease using technetium-99m sestamibi SPECT. Correlation with histologic and positron emission tomographic studies and functional follow-up,” J. Am. Coll. Cardiol. 29(1), 62–68 (1997).
[Crossref] [PubMed]

Franco, W.

W. Lewis, J. P. Padilla-Martinez, A. Ortega-Martinez, and W. Franco, “Changes in endogenous UV fluorescence and biomechanical stiffness of bovine articular cartilage after collagenase digestion are strongly correlated,” J. Biophotonics 10(8), 1018–1025 (2017).
[PubMed]

Frazier, O. H.

D. Baykut, M. M. Gebhard, H. Bölükoglu, K. Kadipasaoglu, S. Hennes, O. H. Frazier, and A. Krian, “Online detection of myocardial ischemia by near infrared spectroscopy with a fiberoptic catheter,” Thorac. Cardiovasc. Surg. 49(3), 162–166 (2001).
[Crossref] [PubMed]

French, J. K.

T. L. Nguyen, J. A. K. Phan, L. Hee, D. A. Moses, J. Otton, O. D. Terreblanche, J. Xiong, U. Premawardhana, R. Rajaratnam, C. P. Juergens, H. R. Dimitri, J. K. French, D. A. Richards, and L. Thomas, “High-sensitivity troponin T predicts infarct scar characteristics and adverse left ventricular function by cardiac magnetic resonance imaging early after reperfused acute myocardial infarction,” Am. Heart J. 170(4), 715–725 (2015).
[Crossref] [PubMed]

French, P.

H. B. Manning, M. B. Nickdel, K. Yamamoto, J. L. Lagarto, D. J. Kelly, C. B. Talbot, G. Kennedy, J. Dudhia, J. Lever, C. Dunsby, P. French, and Y. Itoh, “Detection of cartilage matrix degradation by autofluorescence lifetime,” Matrix Biol. 32(1), 32–38 (2013).
[Crossref] [PubMed]

French, P. M.

P. J. Tadrous, J. Siegel, P. M. French, S. Shousha, N. Lalani, and G. W. H. Stamp, “Fluorescence lifetime imaging of unstained tissues: early results in human breast cancer,” J. Pathol. 199(3), 309–317 (2003).
[Crossref] [PubMed]

French, P. M. W.

J. L. Lagarto, B. T. Dyer, C. B. Talbot, N. S. Peters, P. M. W. French, A. R. Lyon, and C. Dunsby, “Characterization of NAD(P)H and FAD autofluorescence signatures in a Langendorff isolated-perfused rat heart model,” Biomed. Opt. Express 9(10), 4961–4978 (2018).
[Crossref] [PubMed]

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]

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

H. B. Manning, G. T. Kennedy, D. M. Owen, D. M. Grant, A. I. Magee, M. A. A. Neil, Y. Itoh, C. Dunsby, and P. M. W. French, “A compact, multidimensional spectrofluorometer exploiting supercontinuum generation,” J. Biophotonics 1(6), 494–505 (2008).
[Crossref] [PubMed]

Frohwirt, N.

E. Margoliash and N. Frohwirt, “Spectrum of horse-heart cytochrome c,” Biochem. J. 71(3), 570–572 (1959).
[Crossref] [PubMed]

Gabrecht, T.

P. Uehlinger, T. Gabrecht, T. Glanzmann, J.-P. Ballini, A. Radu, S. Andrejevic, P. Monnier, and G. Wagnières, “In vivo time-resolved spectroscopy of the human bronchial early cancer autofluorescence,” J. Biomed. Opt. 14(2), 024011 (2009).
[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), H683–H697 (1999).
[PubMed]

Garcia, E.

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A. R. Lyon, K. T. MacLeod, Y. Zhang, E. Garcia, G. K. Kanda, M. J. Lab, Y. E. Korchev, S. E. Harding, and J. Gorelik, “Loss of T-tubules and other changes to surface topography in ventricular myocytes from failing human and rat heart,” Proc. Natl. Acad. Sci. U.S.A. 106(16), 6854–6859 (2009).
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H. B. Manning, G. T. Kennedy, D. M. Owen, D. M. Grant, A. I. Magee, M. A. A. Neil, Y. Itoh, C. Dunsby, and P. M. W. French, “A compact, multidimensional spectrofluorometer exploiting supercontinuum generation,” J. Biophotonics 1(6), 494–505 (2008).
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M. Ranji, M. Matsubara, B. G. Leshnower, R. H. Hinmon, D. L. Jaggard, B. Chance, R. C. Gorman, J. H. Gorman Iii, R. C. Gorman, and J. H. Gorman, “Quantifying acute myocardial injury using ratiometric fluorometry,” IEEE Trans. Biomed. Eng. 56(5), 1556–1563 (2009).
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D. Baykut, M. M. Gebhard, H. Bölükoglu, K. Kadipasaoglu, S. Hennes, O. H. Frazier, and A. Krian, “Online detection of myocardial ischemia by near infrared spectroscopy with a fiberoptic catheter,” Thorac. Cardiovasc. Surg. 49(3), 162–166 (2001).
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A. R. Lyon, K. T. MacLeod, Y. Zhang, E. Garcia, G. K. Kanda, M. J. Lab, Y. E. Korchev, S. E. Harding, and J. Gorelik, “Loss of T-tubules and other changes to surface topography in ventricular myocytes from failing human and rat heart,” Proc. Natl. Acad. Sci. U.S.A. 106(16), 6854–6859 (2009).
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A. R. Lyon, K. T. MacLeod, Y. Zhang, E. Garcia, G. K. Kanda, M. J. Lab, Y. E. Korchev, S. E. Harding, and J. Gorelik, “Loss of T-tubules and other changes to surface topography in ventricular myocytes from failing human and rat heart,” Proc. Natl. Acad. Sci. U.S.A. 106(16), 6854–6859 (2009).
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J. Bec, J. E. Phipps, D. Gorpas, D. Ma, H. Fatakdawala, K. B. Margulies, J. A. Southard, and L. Marcu, “In vivo label-free structural and biochemical imaging of coronary arteries using an integrated ultrasound and multispectral fluorescence lifetime catheter system,” Sci. Rep. 7(1), 8960 (2017).
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H. B. Manning, G. T. Kennedy, D. M. Owen, D. M. Grant, A. I. Magee, M. A. A. Neil, Y. Itoh, C. Dunsby, and P. M. W. French, “A compact, multidimensional spectrofluorometer exploiting supercontinuum generation,” J. Biophotonics 1(6), 494–505 (2008).
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I. Stefanon, M. Valero-Muñoz, A. A. Fernandes, R. F. Ribeiro, C. Rodríguez, M. Miana, J. Martínez-González, J. S. Spalenza, V. Lahera, P. F. Vassallo, and V. Cachofeiro, “Left and right ventricle late remodeling following myocardial infarction in rats,” PLoS One 8(5), e64986 (2013).
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Stein, L.

R. W. Burt, O. W. Perkins, B. E. Oppenheim, D. S. Schauwecker, L. Stein, H. N. Wellman, and R. M. Witt, “Direct comparison of fluorine-18-FDG SPECT, fluorine-18-FDG PET and rest thallium-201 SPECT for detection of myocardial viability,” J. Nucl. Med. 36(2), 176–179 (1995).
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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, J. E. Phipps, J. Meier, N. Hatami, B. Poirier, D. S. Elson, D. G. Farwell, and L. Marcu, “Endoscopic fluorescence lifetime imaging for in vivo intraoperative diagnosis of oral carcinoma,” Microsc. Microanal. 19(4), 791–798 (2013).
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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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A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
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P. J. Tadrous, J. Siegel, P. M. French, S. Shousha, N. Lalani, and G. W. H. Stamp, “Fluorescence lifetime imaging of unstained tissues: early results in human breast cancer,” J. Pathol. 199(3), 309–317 (2003).
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Talbot, C.

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J. L. Lagarto, B. T. Dyer, C. B. Talbot, N. S. Peters, P. M. W. French, A. R. Lyon, and C. Dunsby, “Characterization of NAD(P)H and FAD autofluorescence signatures in a Langendorff isolated-perfused rat heart model,” Biomed. Opt. Express 9(10), 4961–4978 (2018).
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H. B. Manning, M. B. Nickdel, K. Yamamoto, J. L. Lagarto, D. J. Kelly, C. B. Talbot, G. Kennedy, J. Dudhia, J. Lever, C. Dunsby, P. French, and Y. Itoh, “Detection of cartilage matrix degradation by autofluorescence lifetime,” Matrix Biol. 32(1), 32–38 (2013).
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T. L. Nguyen, J. A. K. Phan, L. Hee, D. A. Moses, J. Otton, O. D. Terreblanche, J. Xiong, U. Premawardhana, R. Rajaratnam, C. P. Juergens, H. R. Dimitri, J. K. French, D. A. Richards, and L. Thomas, “High-sensitivity troponin T predicts infarct scar characteristics and adverse left ventricular function by cardiac magnetic resonance imaging early after reperfused acute myocardial infarction,” Am. Heart J. 170(4), 715–725 (2015).
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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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S. R. Kantelhardt, D. Kalasauskas, K. König, E. Kim, M. Weinigel, A. Uchugonova, and A. Giese, “In vivo multiphoton tomography and fluorescence lifetime imaging of human brain tumor tissue,” J. Neurooncol. 127(3), 473–482 (2016).
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P. Uehlinger, T. Gabrecht, T. Glanzmann, J.-P. Ballini, A. Radu, S. Andrejevic, P. Monnier, and G. Wagnières, “In vivo time-resolved spectroscopy of the human bronchial early cancer autofluorescence,” J. Biomed. Opt. 14(2), 024011 (2009).
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A. F. Maes, M. Borgers, W. Flameng, J. L. Nuyts, F. van de Werf, J. J. Ausma, P. Sergeant, and L. A. Mortelmans, “Assessment of myocardial viability in chronic coronary artery disease using technetium-99m sestamibi SPECT. Correlation with histologic and positron emission tomographic studies and functional follow-up,” J. Am. Coll. Cardiol. 29(1), 62–68 (1997).
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F. Poulon, H. Mehidine, M. Juchaux, P. Varlet, B. Devaux, J. Pallud, and D. Abi Haidar, “Optical properties, spectral, and lifetime measurements of central nervous system tumors in humans,” Sci. Rep. 7(1), 13995 (2017).
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Vassallo, P. F.

I. Stefanon, M. Valero-Muñoz, A. A. Fernandes, R. F. Ribeiro, C. Rodríguez, M. Miana, J. Martínez-González, J. S. Spalenza, V. Lahera, P. F. Vassallo, and V. Cachofeiro, “Left and right ventricle late remodeling following myocardial infarction in rats,” PLoS One 8(5), e64986 (2013).
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J. P. Cleutjens, M. J. Verluyten, J. F. Smiths, and M. J. Daemen, “Collagen remodeling after myocardial infarction in the rat heart,” Am. J. Pathol. 147(2), 325–338 (1995).
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P. Uehlinger, T. Gabrecht, T. Glanzmann, J.-P. Ballini, A. Radu, S. Andrejevic, P. Monnier, and G. Wagnières, “In vivo time-resolved spectroscopy of the human bronchial early cancer autofluorescence,” J. Biomed. Opt. 14(2), 024011 (2009).
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G. A. Wagnières, W. M. Star, and B. C. Wilson, “In vivo fluorescence spectroscopy and imaging for oncological applications,” Photochem. Photobiol. 68(5), 603–632 (1998).
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A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
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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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S. R. Kantelhardt, D. Kalasauskas, K. König, E. Kim, M. Weinigel, A. Uchugonova, and A. Giese, “In vivo multiphoton tomography and fluorescence lifetime imaging of human brain tumor tissue,” J. Neurooncol. 127(3), 473–482 (2016).
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R. W. Burt, O. W. Perkins, B. E. Oppenheim, D. S. Schauwecker, L. Stein, H. N. Wellman, and R. M. Witt, “Direct comparison of fluorine-18-FDG SPECT, fluorine-18-FDG PET and rest thallium-201 SPECT for detection of myocardial viability,” J. Nucl. Med. 36(2), 176–179 (1995).
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White, J. G.

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).
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Wilson, B. C.

G. A. Wagnières, W. M. Star, and B. C. Wilson, “In vivo fluorescence spectroscopy and imaging for oncological applications,” Photochem. Photobiol. 68(5), 603–632 (1998).
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Witt, R. M.

R. W. Burt, O. W. Perkins, B. E. Oppenheim, D. S. Schauwecker, L. Stein, H. N. Wellman, and R. M. Witt, “Direct comparison of fluorine-18-FDG SPECT, fluorine-18-FDG PET and rest thallium-201 SPECT for detection of myocardial viability,” J. Nucl. Med. 36(2), 176–179 (1995).
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Xiong, J.

T. L. Nguyen, J. A. K. Phan, L. Hee, D. A. Moses, J. Otton, O. D. Terreblanche, J. Xiong, U. Premawardhana, R. Rajaratnam, C. P. Juergens, H. R. Dimitri, J. K. French, D. A. Richards, and L. Thomas, “High-sensitivity troponin T predicts infarct scar characteristics and adverse left ventricular function by cardiac magnetic resonance imaging early after reperfused acute myocardial infarction,” Am. Heart J. 170(4), 715–725 (2015).
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H. B. Manning, M. B. Nickdel, K. Yamamoto, J. L. Lagarto, D. J. Kelly, C. B. Talbot, G. Kennedy, J. Dudhia, J. Lever, C. Dunsby, P. French, and Y. Itoh, “Detection of cartilage matrix degradation by autofluorescence lifetime,” Matrix Biol. 32(1), 32–38 (2013).
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Zhang, Y.

A. R. Lyon, K. T. MacLeod, Y. Zhang, E. Garcia, G. K. Kanda, M. J. Lab, Y. E. Korchev, S. E. Harding, and J. Gorelik, “Loss of T-tubules and other changes to surface topography in ventricular myocytes from failing human and rat heart,” Proc. Natl. Acad. Sci. U.S.A. 106(16), 6854–6859 (2009).
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Acta Physiol. Scand. (1)

W. M. Blankesteijn, E. Creemers, E. Lutgens, J. P. Cleutjens, M. J. Daemen, and J. F. Smits, “Dynamics of cardiac wound healing following myocardial infarction: observations in genetically altered mice,” Acta Physiol. Scand. 173(1), 75–82 (2001).
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Am. Heart J. (1)

T. L. Nguyen, J. A. K. Phan, L. Hee, D. A. Moses, J. Otton, O. D. Terreblanche, J. Xiong, U. Premawardhana, R. Rajaratnam, C. P. Juergens, H. R. Dimitri, J. K. French, D. A. Richards, and L. Thomas, “High-sensitivity troponin T predicts infarct scar characteristics and adverse left ventricular function by cardiac magnetic resonance imaging early after reperfused acute myocardial infarction,” Am. Heart J. 170(4), 715–725 (2015).
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Am. J. Pathol. (1)

J. P. Cleutjens, M. J. Verluyten, J. F. Smiths, and M. J. Daemen, “Collagen remodeling after myocardial infarction in the rat heart,” Am. J. Pathol. 147(2), 325–338 (1995).
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Am. J. Physiol. (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), H683–H697 (1999).
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Cardiovasc. Res. (1)

Y. Sun and K. T. Weber, “Infarct scar: a dynamic tissue,” Cardiovasc. Res. 46(2), 250–256 (2000).
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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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A. C. Croce and G. Bottiroli, “Autofluorescence spectroscopy and imaging: a tool for biomedical research and diagnosis,” Eur. J. Histochem. 58(4), 2461 (2014).
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M.-A. Mycek, K. T. Schomacker, and N. S. Nishioka, “Colonic polyp differentiation using time-resolved autofluorescence spectroscopy,” Gastrointest. Endosc. 48(4), 390–394 (1998).
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M. Ranji, M. Matsubara, B. G. Leshnower, R. H. Hinmon, D. L. Jaggard, B. Chance, R. C. Gorman, J. H. Gorman Iii, R. C. Gorman, and J. H. Gorman, “Quantifying acute myocardial injury using ratiometric fluorometry,” IEEE Trans. Biomed. Eng. 56(5), 1556–1563 (2009).
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J. N. Cohn, R. Ferrari, and N. Sharpe, “Cardiac remodeling--concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. Behalf of an International Forum on Cardiac Remodeling,” J. Am. Coll. Cardiol. 35(3), 569–582 (2000).
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A. F. Maes, M. Borgers, W. Flameng, J. L. Nuyts, F. van de Werf, J. J. Ausma, P. Sergeant, and L. A. Mortelmans, “Assessment of myocardial viability in chronic coronary artery disease using technetium-99m sestamibi SPECT. Correlation with histologic and positron emission tomographic studies and functional follow-up,” J. Am. Coll. Cardiol. 29(1), 62–68 (1997).
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J. Biomed. Opt. (4)

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]

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]

P. Uehlinger, T. Gabrecht, T. Glanzmann, J.-P. Ballini, A. Radu, S. Andrejevic, P. Monnier, and G. Wagnières, “In vivo time-resolved spectroscopy of the human bronchial early cancer autofluorescence,” J. Biomed. Opt. 14(2), 024011 (2009).
[Crossref] [PubMed]

M. C. Skala, K. M. Riching, D. K. Bird, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, P. J. Keely, and N. Ramanujam, “In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia,” J. Biomed. Opt. 12(2), 024014 (2007).
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J. Biophotonics (3)

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. A. De Beule, M. A. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. W. French, K. Svanberg, and C. Dunsby, “In vivo measurements of diffuse reflectance and time-resolved autofluorescence emission spectra of basal cell carcinomas,” J. Biophotonics 5(3), 240–254 (2012).
[Crossref] [PubMed]

H. B. Manning, G. T. Kennedy, D. M. Owen, D. M. Grant, A. I. Magee, M. A. A. Neil, Y. Itoh, C. Dunsby, and P. M. W. French, “A compact, multidimensional spectrofluorometer exploiting supercontinuum generation,” J. Biophotonics 1(6), 494–505 (2008).
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S. R. Kantelhardt, D. Kalasauskas, K. König, E. Kim, M. Weinigel, A. Uchugonova, and A. Giese, “In vivo multiphoton tomography and fluorescence lifetime imaging of human brain tumor tissue,” J. Neurooncol. 127(3), 473–482 (2016).
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J. Nucl. Med. (1)

R. W. Burt, O. W. Perkins, B. E. Oppenheim, D. S. Schauwecker, L. Stein, H. N. Wellman, and R. M. Witt, “Direct comparison of fluorine-18-FDG SPECT, fluorine-18-FDG PET and rest thallium-201 SPECT for detection of myocardial viability,” J. Nucl. Med. 36(2), 176–179 (1995).
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P. J. Tadrous, J. Siegel, P. M. French, S. Shousha, N. Lalani, and G. W. H. Stamp, “Fluorescence lifetime imaging of unstained tissues: early results in human breast cancer,” J. Pathol. 199(3), 309–317 (2003).
[Crossref] [PubMed]

Matrix Biol. (1)

H. B. Manning, M. B. Nickdel, K. Yamamoto, J. L. Lagarto, D. J. Kelly, C. B. Talbot, G. Kennedy, J. Dudhia, J. Lever, C. Dunsby, P. French, and Y. Itoh, “Detection of cartilage matrix degradation by autofluorescence lifetime,” Matrix Biol. 32(1), 32–38 (2013).
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Microsc. Microanal. (1)

Y. Sun, J. E. Phipps, J. Meier, N. Hatami, B. Poirier, D. S. Elson, D. G. Farwell, and L. Marcu, “Endoscopic fluorescence lifetime imaging for in vivo intraoperative diagnosis of oral carcinoma,” Microsc. Microanal. 19(4), 791–798 (2013).
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G. A. Wagnières, W. M. Star, and B. C. Wilson, “In vivo fluorescence spectroscopy and imaging for oncological applications,” Photochem. Photobiol. 68(5), 603–632 (1998).
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PLoS One (1)

I. Stefanon, M. Valero-Muñoz, A. A. Fernandes, R. F. Ribeiro, C. Rodríguez, M. Miana, J. Martínez-González, J. S. Spalenza, V. Lahera, P. F. Vassallo, and V. Cachofeiro, “Left and right ventricle late remodeling following myocardial infarction in rats,” PLoS One 8(5), e64986 (2013).
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Proc. Natl. Acad. Sci. U.S.A. (2)

A. R. Lyon, K. T. MacLeod, Y. Zhang, E. Garcia, G. K. Kanda, M. J. Lab, Y. E. Korchev, S. E. Harding, and J. Gorelik, “Loss of T-tubules and other changes to surface topography in ventricular myocytes from failing human and rat heart,” Proc. Natl. Acad. Sci. U.S.A. 106(16), 6854–6859 (2009).
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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).
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F. Poulon, H. Mehidine, M. Juchaux, P. Varlet, B. Devaux, J. Pallud, and D. Abi Haidar, “Optical properties, spectral, and lifetime measurements of central nervous system tumors in humans,” Sci. Rep. 7(1), 13995 (2017).
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Figures (9)

Fig. 1
Fig. 1 Diagram of the heart illustrating the regions of interest (ROI) studied. RV – Right ventricle; LVP – left ventricle posterior wall; LVA – left ventricle anterior wall. The region highlighted in red corresponds to the region of infarction.
Fig. 2
Fig. 2 Representative histology images of AMC (A - D) and MI hearts (E - H) stained with PSR at weeks 1 (A, E), 2 (B, F), 4 (C, G) and 16 (D, H). Arrows on the bottom row indicate region of infarction (LVA) where scar tissue was formed, and deposition of collagen is more pronounced.
Fig. 3
Fig. 3 Autofluorescence lifetime parameters (see section on Data Analysis) measured in RV at 1, 2, 4 and 16 weeks.
Fig. 4
Fig. 4 Autofluorescence lifetime parameters measured in LVP at 1, 2, 4 and 16 weeks. Differences in AMC and MI hearts are more pronounced compared to those observed for RV in all channels. In channel 4, we observe a general decrease in τ1 (all time points) and an increase in τ2 (weeks 2, 4 & 16) in MI relative to AMC hearts.
Fig. 5
Fig. 5 Autofluorescence lifetime parameters measured in LVA at 1, 2, 4 and 16 weeks. We observe a gradual increase in autofluorescence lifetime of MI hearts from week 1 to week 16, which suggests that collagen proliferation in the scar region starts immediately after MI induction. As in other regions, the lifetime component τ1 of channel 4 is shorter in MI than in AMC hearts at earlier time points. At week 16, extensive collagen proliferation leads to an increase in the fluorescence lifetime that possibly masks alterations in the fluorescence lifetime parameters caused by metabolic changes.
Fig. 6
Fig. 6 Normalized autofluorescence intensities in the RV, LVP and LVA under 372 nm excitation. Standard deviation bars are not included to avoid overcrowding the plots. Markers in each channel identify time point studied, from left (week 1) to right (week 16), as indicated in channel 1 of the right ventricle plot (left panel).
Fig. 7
Fig. 7 Normalized absorbance spectra in the RV between 500 and 600 nm for AMC (blue) and MI (red) hearts for different time points (left to right). Solid lines show average and dimmed lines show corresponding standard deviation curves.
Fig. 8
Fig. 8 Normalized absorbance spectra in the LVP between 500 and 600 nm for AMC (blue) and MI (red) hearts for different time points (left to right). Solid lines show average and dimmed lines show corresponding standard deviation curves.
Fig. 9
Fig. 9 Normalized absorbance spectra in LVP between 500 and 600 nm for AMC (blue) and MI (red) hearts for different time points (left to right). Solid lines show average and dimmed lines show corresponding standard deviation curves.

Tables (2)

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Table 1 Number of animals studied for both experimental groups at each time point

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Table 2 Heart to body weight ratio demonstrate hypertrophy of the myocardium in MI specimens. All values are presented as mean ± standard deviation, in units of g/kg. NS – not significant.

Equations (4)

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F n = I n I 1 + I 2 + I 3 .
I(t)= i=1 n α i e t τ i +C
τ mean = α 1 τ 1 2 + α 2 τ 2 2 α 1 τ 1 + α 2 τ 2
A( λ )= log 10 ( I( λ ) I 0 ( λ ) )

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