Abstract

We investigate the potential of an instrument combining time-resolved spectrofluorometry and diffuse reflectance spectroscopy to measure structural and metabolic changes in cardiac tissue in vivo in a 16 week post-myocardial infarction heart failure model in rats. In the scar region, we observed changes in the fluorescence signal that can be explained by increased collagen content, which is in good agreement with histology. In areas remote from the scar tissue, we measured changes in the fluorescence signal (p < 0.001) that cannot be explained by differences in collagen content and we attribute this to altered metabolism within the myocardium. A linear discriminant analysis algorithm was applied to the measurements to predict the tissue disease state. When we combine all measurements, our results reveal high diagnostic accuracy in the infarcted area (100%) and border zone (94.44%) as well as in remote regions from the scar (> 77%). Overall, our results demonstrate the potential of our instrument to characterize structural and metabolic changes in a failing heart in vivo without using exogenous labels.

© 2015 Optical Society of America

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2014 (1)

2013 (5)

V. Caorsi, C. Toepfer, M. B. Sikkel, A. R. Lyon, K. MacLeod, and M. A. Ferenczi, “Non-linear optical microscopy sheds light on cardiovascular disease,” PLoS ONE 8(2), e56136 (2013).
[Crossref] [PubMed]

M. S. Islam, M. Honma, T. Nakabayashi, M. Kinjo, and N. Ohta, “pH Dependence of the Fluorescence Lifetime of FAD in Solution and in Cells,” Int. J. Mol. Sci. 14(1), 1952–1963 (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]

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]

Y. Pu, J. Xue, W. Wang, B. Xu, Y. Gu, R. Tang, E. Ackerstaff, J. A. Koutcher, S. Achilefu, and R. R. Alfano, “Native fluorescence spectroscopy reveals spectral differences among prostate cancer cell lines with different risk levels,” J. Biomed. Opt. 18(8), 087002 (2013).
[Crossref] [PubMed]

2012 (7)

J. Park, P. Pande, S. Shrestha, F. Clubb, B. E. Applegate, and J. A. Jo, “Biochemical characterization of atherosclerotic plaques by endogenous multispectral fluorescence lifetime imaging microscopy,” Atherosclerosis 220(2), 394–401 (2012).
[Crossref] [PubMed]

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

R. Kumarswamy, A. R. Lyon, I. Volkmann, A. M. Mills, J. Bretthauer, A. Pahuja, C. Geers-Knörr, T. Kraft, R. J. Hajjar, K. T. Macleod, S. E. Harding, and T. Thum, “SERCA2a gene therapy restores microRNA-1 expression in heart failure via an Akt/FoxO3A-dependent pathway,” Eur. Heart J. 33(9), 1067–1075 (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]

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

V. Lutz, M. Sattler, S. Gallinat, H. Wenck, R. Poertner, and F. Fischer, “Impact of collagen crosslinking on the second harmonic generation signal and the fluorescence lifetime of collagen autofluorescence,” Skin Res. Technol. 18(2), 168–179 (2012).
[Crossref] [PubMed]

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. De Beule, M. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. 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]

2011 (7)

M. A. Bennet, P. R. Richardson, J. Arlt, A. McCarthy, G. S. Buller, and A. C. Jones, “Optically trapped microsensors for microfluidic temperature measurement by fluorescence lifetime imaging microscopy,” Lab Chip 11(22), 3821–3828 (2011).
[Crossref] [PubMed]

A. R. Lyon, M. L. Bannister, T. Collins, E. Pearce, A. H. Sepehripour, S. S. Dubb, E. Garcia, P. O’Gara, L. Liang, E. Kohlbrenner, R. J. Hajjar, N. S. Peters, P. A. Poole-Wilson, K. T. Macleod, and S. E. Harding, “SERCA2a gene transfer decreases sarcoplasmic reticulum calcium leak and reduces ventricular arrhythmias in a model of chronic heart failure,” Circ Arrhythm Electrophysiol 4(3), 362–372 (2011).
[Crossref] [PubMed]

J. E. Phipps, N. Hatami, Z. S. Galis, J. D. Baker, M. C. Fishbein, and L. Marcu, “A fluorescence lifetime spectroscopy study of matrix metalloproteinases-2 and -9 in human atherosclerotic plaque,” J. Biophotonics 4(9), 650–658 (2011).
[PubMed]

J. Venius, S. Bagdonas, E. Žurauskas, and R. Rotomskis, “Time-resolved fluorescence spectroscopy of the heart tissues,” Lith. J. Phys. 51(4), 370–376 (2011).
[Crossref]

J. A. Palero, A. N. Bader, H. S. de Bruijn, A. der Ploeg van den Heuvel, H. J. C. M. Sterenborg, and H. C. Gerritsen, “In vivo monitoring of protein-bound and free NADH during ischemia by nonlinear spectral imaging microscopy,” Biomed. Opt. Express 2(5), 1030–1039 (2011).
[Crossref] [PubMed]

C. B. Talbot, R. Patalay, I. Munro, S. Warren, F. Ratto, P. Matteini, R. Pini, H. G. Breunig, K. König, A. C. Chu, G. W. Stamp, M. A. Neil, P. M. French, and C. Dunsby, “Application of ultrafast gold luminescence to measuring the instrument response function for multispectral multiphoton fluorescence lifetime imaging,” Opt. Express 19(15), 13848–13861 (2011).
[Crossref] [PubMed]

T. Lindbergh, E. Häggblad, H. Ahn, E. Göran Salerud, M. Larsson, and T. Strömberg, “Improved model for myocardial diffuse reflectance spectra by including mitochondrial cytochrome aa3, methemoglobin, and inhomogenously distributed RBC,” J. Biophotonics 4(4), 268–276 (2011).
[Crossref] [PubMed]

2010 (4)

V. O. Nikolaev, A. Moshkov, A. R. Lyon, M. Miragoli, P. Novak, H. Paur, M. J. Lohse, Y. E. Korchev, S. E. Harding, and J. Gorelik, “Beta2-adrenergic receptor redistribution in heart failure changes cAMP compartmentation,” Science 327(5973), 1653–1657 (2010).
[Crossref] [PubMed]

D. Cardinale, A. Colombo, G. Lamantia, N. Colombo, M. Civelli, G. De Giacomi, M. Rubino, F. Veglia, C. Fiorentini, and C. M. Cipolla, “Anthracycline-induced cardiomyopathy: clinical relevance and response to pharmacologic therapy,” J. Am. Coll. Cardiol. 55(3), 213–220 (2010).
[Crossref] [PubMed]

L. Marcu, “Fluorescence lifetime in cardiovascular diagnostics,” J. Biomed. Opt. 15(1), 011106 (2010).
[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]

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]

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

J. A. Jo and L. Marcu, “Laguerre-based method for analysis of time-resolved fluorescence data: application to in-vivo characterization and diagnosis of atherosclerotic lesions,” J. Biomed. Opt. 11, 1–22 (2009).

2008 (2)

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. French, “A compact, multidimensional spectrofluorometer exploiting supercontinuum generation,” J. Biophotonics 1(6), 494–505 (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 (5)

M. Chandra, J. Scheiman, D. Heidt, D. Simeone, B. McKenna, and M.-A. Mycek, “Probing pancreatic disease using tissue optical spectroscopy,” J. Biomed. Opt. 12(6), 060501 (2007).
[Crossref] [PubMed]

P. A. A. De Beule, C. Dunsby, N. P. Galletly, G. W. Stamp, A. C. Chu, U. Anand, P. Anand, C. D. Benham, A. Naylor, and P. M. French, “A hyperspectral fluorescence lifetime probe for skin cancer diagnosis,” Rev. Sci. Instrum. 78(12), 123101 (2007).
[Crossref] [PubMed]

A. Mayevsky and B. Chance, “Oxidation-reduction states of NADH in vivo: from animals to clinical use,” Mitochondrion 7(5), 330–339 (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]

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]

2006 (4)

G. Zonios and A. Dimou, “Modeling diffuse reflectance from semi-infinite turbid media: application to the study of skin optical properties,” Opt. Express 14(19), 8661–8674 (2006).
[Crossref] [PubMed]

D. Chorvat and A. Chorvatova, “Spectrally resolved time-correlated single photon counting: a novel approach for characterization of endogenous fluorescence in isolated cardiac myocytes,” Eur. Biophys. J. 36(1), 73–83 (2006).
[Crossref] [PubMed]

L. H. Opie, P. J. Commerford, B. J. Gersh, M. A. Pfeffer, and N. England, “Controversies in cardiology,” The Lancet 4, 367 (2006).

N. F. Voelkel, R. A. Quaife, L. A. Leinwand, R. J. Barst, M. D. McGoon, D. R. Meldrum, J. Dupuis, C. S. Long, L. J. Rubin, F. W. Smart, Y. J. Suzuki, M. Gladwin, E. M. Denholm, and D. B. Gail, “Right ventricular function and failure: report of a National Heart, Lung, and Blood Institute working group on cellular and molecular mechanisms of right heart failure,” Circulation 114(17), 1883–1891 (2006).
[Crossref] [PubMed]

2005 (2)

H. D. Vishwasrao, A. A. Heikal, K. A. Kasischke, and W. W. Webb, “Conformational dependence of intracellular NADH on metabolic state revealed by associated fluorescence anisotropy,” J. Biol. Chem. 280(26), 25119–25126 (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]

2004 (3)

K. Konig, K. Schenke-layland, I. Riemann, and U. A. Stock, “Multiphoton autofluorescence imaging of intratissue elastic fibers,” Biomaterials 26, 495–500 (2004).

A. Mayevsky, T. Manor, E. Pevzner, A. Deutsch, R. Etziony, N. Dekel, and A. Jaronkin, “Tissue spectroscope: a novel in vivo approach to real time monitoring of tissue vitality,” J. Biomed. Opt. 9(5), 1028–1045 (2004).
[Crossref] [PubMed]

P. Ashjian, A. Elbarbary, P. Zuk, D. A. DeUgarte, P. Benhaim, L. Marcu, and M. H. Hedrick, “Noninvasive in situ evaluation of osteogenic differentiation by time-resolved laser-induced fluorescence spectroscopy,” Tissue Eng. 10(3-4), 411–420 (2004).
[Crossref] [PubMed]

2003 (2)

J. Swartling, S. Pålsson, P. Platonov, S. B. Olsson, and S. Andersson-Engels, “Changes in tissue optical properties due to radio-frequency ablation of myocardium,” Med. Biol. Eng. Comput. 41(4), 403–409 (2003).
[Crossref] [PubMed]

H.-J. Lin, P. Herman, and J. R. Lakowicz, “Fluorescence lifetime-resolved pH imaging of living cells,” Cytometry A 52(2), 77–89 (2003).
[Crossref] [PubMed]

2002 (1)

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]

2001 (2)

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]

L. Marcu, M. C. Fishbein, J.-M. I. Maarek, and W. S. Grundfest, “Discrimination of Human Coronary Artery Atherosclerotic Lipid-Rich Lesions by Time-Resolved Laser-Induced Fluorescence Spectroscopy,” Arterioscler. Thromb. Vasc. Biol. 21(7), 1244–1250 (2001).
[Crossref] [PubMed]

2000 (1)

S. M. Weis, J. L. Emery, K. D. Becker, D. J. McBride, J. H. Omens, and A. D. McCulloch, “Myocardial Mechanics and Collagen Structure in the Osteogenesis Imperfecta Murine (oim),” Circ. Res. 87(8), 663–669 (2000).
[Crossref] [PubMed]

1999 (3)

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]

T. Glanzmann, J.-P. Ballini, H. van den Bergh, and G. Wagnières, “Time-resolved spectrofluorometer for clinical tissue characterization during endoscopy,” Rev. Sci. Instrum. 70(10), 4067 (1999).
[Crossref]

K. A. Schenkman, D. R. M. Arble, D. H. Burns, and E. O. Feigl, “Optical spectroscopic method for in vivo measurement of cardiac myoglobin oxygen saturation,” Appl. Spectros. 53, 332(1999).

1998 (1)

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]

1997 (3)

K. Carlsson and A. Liljeborg, “Confocal fluorescence microscopy using spectral and lifetime information to simultaneously record four fluorophores with high channel separation,” J. Microscopy 185, 37–46 (1997).

H. C. Gerritsen, R. Sanders, A. Draaijer, C. Ince, and Y. K. Levine, “Fluorescence lifetime imaging of oxygen in living cells,” J. Fluoresc. 7(1), 11–15 (1997).
[Crossref]

Y. H. Li, J. C. Yue, and G. P. Cai, “Fluorescence characterization of type I collagen from normal and silicotic rats and its quenching dynamics induced by hypocrellin B,” Biopolymers 42(2), 219–226 (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 (2)

R. Sanders, H. C. Gerritsen, A. Draaijer, P. M. Houpt, and Y. K. Levine, “Confocal fluorescence lifetime imaging of free calcium in single cells,” J. Fluoresc. 4(4), 291–294 (1994).
[Crossref] [PubMed]

P. Whittaker, R. A. Kloner, D. R. Boughner, and J. G. Pickering, “Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light,” Basic Res. Cardiol. 89(5), 397–410 (1994).
[Crossref] [PubMed]

1992 (1)

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]

1991 (1)

J. Y. Yager, R. M. Brucklacher, and R. C. Vannucci, “Cerebral oxidative metabolism and redox state during hypoxia-ischemia and early recovery in immature rats,” Am. J. Physiol. 261(4 Pt 2), H1102–H1108 (1991).
[PubMed]

1989 (2)

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]

1987 (1)

A. P. Koretsky, L. A. Katz, and R. S. Balaban, “Determination of pyridine nucleotide fluorescence from the perfused heart using an internal standard,” Am. J. Physiol. 253(4 Pt 2), H856–H862 (1987).
[PubMed]

1985 (1)

H. F. Weisman, D. E. Bush, J. A. Mannisi, and B. H. Bulkley, “Global cardiac remodeling after acute myocardial infarction: A study in the rat model,” J. Am. Coll. Cardiol. 5(6), 1355–1362 (1985).
[Crossref] [PubMed]

1979 (1)

S. Roth and I. Freund, “Second harmonic generation in collagen,” J. Chem. Phys. 70(4), 1637 (1979).
[Crossref]

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).
[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]

Achilefu, S.

Y. Pu, J. Xue, W. Wang, B. Xu, Y. Gu, R. Tang, E. Ackerstaff, J. A. Koutcher, S. Achilefu, and R. R. Alfano, “Native fluorescence spectroscopy reveals spectral differences among prostate cancer cell lines with different risk levels,” J. Biomed. Opt. 18(8), 087002 (2013).
[Crossref] [PubMed]

Ackerstaff, E.

Y. Pu, J. Xue, W. Wang, B. Xu, Y. Gu, R. Tang, E. Ackerstaff, J. A. Koutcher, S. Achilefu, and R. R. Alfano, “Native fluorescence spectroscopy reveals spectral differences among prostate cancer cell lines with different risk levels,” J. Biomed. Opt. 18(8), 087002 (2013).
[Crossref] [PubMed]

Ahn, H.

T. Lindbergh, E. Häggblad, H. Ahn, E. Göran Salerud, M. Larsson, and T. Strömberg, “Improved model for myocardial diffuse reflectance spectra by including mitochondrial cytochrome aa3, methemoglobin, and inhomogenously distributed RBC,” J. Biophotonics 4(4), 268–276 (2011).
[Crossref] [PubMed]

Alfano, R. R.

Y. Pu, J. Xue, W. Wang, B. Xu, Y. Gu, R. Tang, E. Ackerstaff, J. A. Koutcher, S. Achilefu, and R. R. Alfano, “Native fluorescence spectroscopy reveals spectral differences among prostate cancer cell lines with different risk levels,” J. Biomed. Opt. 18(8), 087002 (2013).
[Crossref] [PubMed]

Anand, P.

P. A. A. De Beule, C. Dunsby, N. P. Galletly, G. W. Stamp, A. C. Chu, U. Anand, P. Anand, C. D. Benham, A. Naylor, and P. M. French, “A hyperspectral fluorescence lifetime probe for skin cancer diagnosis,” Rev. Sci. Instrum. 78(12), 123101 (2007).
[Crossref] [PubMed]

Anand, U.

P. A. A. De Beule, C. Dunsby, N. P. Galletly, G. W. Stamp, A. C. Chu, U. Anand, P. Anand, C. D. Benham, A. Naylor, and P. M. French, “A hyperspectral fluorescence lifetime probe for skin cancer diagnosis,” Rev. Sci. Instrum. 78(12), 123101 (2007).
[Crossref] [PubMed]

Andersson-Engels, S.

A. J. Thompson, S. Coda, M. B. Sørensen, G. Kennedy, R. Patalay, U. Waitong-Brämming, P. A. De Beule, M. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. 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]

J. Swartling, S. Pålsson, P. Platonov, S. B. Olsson, and S. Andersson-Engels, “Changes in tissue optical properties due to radio-frequency ablation of myocardium,” Med. Biol. Eng. Comput. 41(4), 403–409 (2003).
[Crossref] [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,” 3917, 93–101 (2000).

Applegate, B. E.

J. Park, P. Pande, S. Shrestha, F. Clubb, B. E. Applegate, and J. A. Jo, “Biochemical characterization of atherosclerotic plaques by endogenous multispectral fluorescence lifetime imaging microscopy,” Atherosclerosis 220(2), 394–401 (2012).
[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 Pt 2), H683–H697 (1999).
[PubMed]

Arble, D. R. M.

K. A. Schenkman, D. R. M. Arble, D. H. Burns, and E. O. Feigl, “Optical spectroscopic method for in vivo measurement of cardiac myoglobin oxygen saturation,” Appl. Spectros. 53, 332(1999).

Arganda-Carreras, I.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods 9(7), 676–682 (2012).
[Crossref] [PubMed]

Arlt, J.

M. A. Bennet, P. R. Richardson, J. Arlt, A. McCarthy, G. S. Buller, and A. C. Jones, “Optically trapped microsensors for microfluidic temperature measurement by fluorescence lifetime imaging microscopy,” Lab Chip 11(22), 3821–3828 (2011).
[Crossref] [PubMed]

Ashjian, P.

P. Ashjian, A. Elbarbary, P. Zuk, D. A. DeUgarte, P. Benhaim, L. Marcu, and M. H. Hedrick, “Noninvasive in situ evaluation of osteogenic differentiation by time-resolved laser-induced fluorescence spectroscopy,” Tissue Eng. 10(3-4), 411–420 (2004).
[Crossref] [PubMed]

Ayaru, L.

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]

Bader, A. N.

Bagdonas, S.

J. Venius, S. Bagdonas, E. Žurauskas, and R. Rotomskis, “Time-resolved fluorescence spectroscopy of the heart tissues,” Lith. J. Phys. 51(4), 370–376 (2011).
[Crossref]

Baker, J. D.

J. E. Phipps, N. Hatami, Z. S. Galis, J. D. Baker, M. C. Fishbein, and L. Marcu, “A fluorescence lifetime spectroscopy study of matrix metalloproteinases-2 and -9 in human atherosclerotic plaque,” J. Biophotonics 4(9), 650–658 (2011).
[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]

A. P. Koretsky, L. A. Katz, and R. S. Balaban, “Determination of pyridine nucleotide fluorescence from the perfused heart using an internal standard,” Am. J. Physiol. 253(4 Pt 2), H856–H862 (1987).
[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]

Ballini, J.-P.

T. Glanzmann, J.-P. Ballini, H. van den Bergh, and G. Wagnières, “Time-resolved spectrofluorometer for clinical tissue characterization during endoscopy,” Rev. Sci. Instrum. 70(10), 4067 (1999).
[Crossref]

Bannister, M. L.

A. R. Lyon, M. L. Bannister, T. Collins, E. Pearce, A. H. Sepehripour, S. S. Dubb, E. Garcia, P. O’Gara, L. Liang, E. Kohlbrenner, R. J. Hajjar, N. S. Peters, P. A. Poole-Wilson, K. T. Macleod, and S. E. Harding, “SERCA2a gene transfer decreases sarcoplasmic reticulum calcium leak and reduces ventricular arrhythmias in a model of chronic heart failure,” Circ Arrhythm Electrophysiol 4(3), 362–372 (2011).
[Crossref] [PubMed]

Bansi, D. S.

Barst, R. J.

N. F. Voelkel, R. A. Quaife, L. A. Leinwand, R. J. Barst, M. D. McGoon, D. R. Meldrum, J. Dupuis, C. S. Long, L. J. Rubin, F. W. Smart, Y. J. Suzuki, M. Gladwin, E. M. Denholm, and D. B. Gail, “Right ventricular function and failure: report of a National Heart, Lung, and Blood Institute working group on cellular and molecular mechanisms of right heart failure,” Circulation 114(17), 1883–1891 (2006).
[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]

Becker, K. D.

S. M. Weis, J. L. Emery, K. D. Becker, D. J. McBride, J. H. Omens, and A. D. McCulloch, “Myocardial Mechanics and Collagen Structure in the Osteogenesis Imperfecta Murine (oim),” Circ. Res. 87(8), 663–669 (2000).
[Crossref] [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. De Beule, M. A. Neil, S. Andersson-Engels, N. Bendsøe, P. M. 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]

Benhaim, P.

P. Ashjian, A. Elbarbary, P. Zuk, D. A. DeUgarte, P. Benhaim, L. Marcu, and M. H. Hedrick, “Noninvasive in situ evaluation of osteogenic differentiation by time-resolved laser-induced fluorescence spectroscopy,” Tissue Eng. 10(3-4), 411–420 (2004).
[Crossref] [PubMed]

Benham, C. D.

P. A. A. De Beule, C. Dunsby, N. P. Galletly, G. W. Stamp, A. C. Chu, U. Anand, P. Anand, C. D. Benham, A. Naylor, and P. M. French, “A hyperspectral fluorescence lifetime probe for skin cancer diagnosis,” Rev. Sci. Instrum. 78(12), 123101 (2007).
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Bennet, M. A.

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K. A. Schenkman, D. R. M. Arble, D. H. Burns, and E. O. Feigl, “Optical spectroscopic method for in vivo measurement of cardiac myoglobin oxygen saturation,” Appl. Spectros. 53, 332(1999).

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

Ferenczi, M. A.

V. Caorsi, C. Toepfer, M. B. Sikkel, A. R. Lyon, K. MacLeod, and M. A. Ferenczi, “Non-linear optical microscopy sheds light on cardiovascular disease,” PLoS ONE 8(2), e56136 (2013).
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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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Platonov, P.

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Biomed. Opt. Express (2)

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Biopolymers (1)

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Figures (9)

Fig. 1
Fig. 1 (A) Experimental layout of the single point fluorescence lifetime probe system and its optical fiber configuration at the excitation (proximal) and sample (distal) ends. Optical fiber cores are colored blue for excitation fibers, white for fibers delivering white light and collecting the diffuse reflected light and green for fibers collecting the fluorescence. (B) System mounted on a portable trolley for ease of deployment in clinical settings. (C) Distal end of the fiber-optic probe.
Fig. 2
Fig. 2 Emission spectra of endogenous fluorophores of interest excited at 375 nm and plotted to show their relation to the spectral range of the detection channels of the fluorescence lifetime point probe system. Curves are normalized to their maximum amplitude. Data measured as described in section 2.3.
Fig. 3
Fig. 3 Diagram of the heart illustrating regions of interest (ROI) for our measurements: (A) anterior view; (B) posterior view. “RV” - right ventricle; “LV posterior” - left ventricle posterior wall; “LV anterior (scar)” - left ventricle anterior wall; and “border zone” - scar border zone or septum.
Fig. 4
Fig. 4 Representative histology images from of AMC (left column) and MI-HF (right column) hearts. (A, E) RV; (B, F) LV posterior; (C, G) Border zone; (D, H) LV anterior
Fig. 5
Fig. 5 Diffuse reflectance spectra in (a) RV, (b) LV posterior, (c) Border zone, (d) LV anterior. Dashed lines indicate +/− 1 SD.
Fig. 6
Fig. 6 Absorbance spectra of key chromophores in cardiac tissue. The absorbance curves for human Hb and HbO2 were obtained from [52]. The absorbance curves for oxidized and reduced horse cytochrome C were obtained from [54]. The absorbance curves for horse Mb and MbO2 were obtained from [53]. The Hb and HbO2, Mb and MbO2 and reduced and oxidized cytochrome c pairs of curves were scaled in proportion with the largest of each curve being normalized to 1.
Fig. 7
Fig. 7 Relative contribution for each spectral detection channel for AMC and MI hearts, displayed by ROI (top row) and channel center wavelength (bottom row). Dashed lines in bottom row graphs identify the spectral range of each detection channel of the FL point probe system.
Fig. 8
Fig. 8 Autofluorescence lifetime parameters for each spectral channel, displayed by ROI.
Fig. 9
Fig. 9 Results from PCA of all spectroscopic parameters for each ROI shown as scatter plots of the scores of the first two PC for each ROI: a) RV, b) LV posterior, c) border zone and d) LV anterior. Different markers in the scatter plot identify data obtained from different specimens. Black lines show the decision lines produced by LDA analysis.

Tables (5)

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Table 3 List of spectroscopic parameters extracted from a single fluorescence lifetime measurement

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Table 4 P-value results from two-tailed Student’s t-test, for all ROI. A p-value < 0.05 was considered to be significant.

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Table 5 Fluorescence parameters ranked by Cohen’s d coefficient.

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Table 1 Collagen content calculated from representative histology images. Statistical analysis between AMC and MI hearts was computed using a two-tailed Student t-test (n = 3).

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Table 2 Results of the PCA/LDA discrimination algorithm applied for each ROI using fluorescence and diffuse reflectance parameters and combinations of these parameters.

Equations (7)

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

A( λ )= log 10 ( I( λ ) I 0 ( λ ) )
I( t )= i=1 N a i e t τ +C
τ mean =β τ 1 +( 1β ) τ 2
β= a 1 τ 1 a 1 τ 1 + a 2 τ 2
χ 2 = k=1 n ( I( t k ) I model ( t k ) ) 2 I( t k )
d= | μ 1 μ 2 | σ
σ= s 1 2 + s 2 2 2

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