Abstract

Novel diagnostic tools with the ability to monitor variations in biochemical composition and provide benchmark indicators of vascular tissue maturation are needed to create functional tissue replacements. We investigated the ability of fiber-based, label-free multispectral fluorescent lifetime imaging (FLIm) to quantify the anatomical variations in biochemical composition of native carotid arteries and validated these results against biochemical assays. FLIm-derived parameters in spectral band 415–455 nm correlated with tissue collagen content (R2 = 0.64) and cell number (R2 = 0.61) and in spectral band 465–553 nm strongly correlated with elastin content (R2 = 0.89). These results suggest that FLIm holds great potential for assessing vascular tissue maturation and functional properties based on tissue autofluorescence.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2018 (2)

B. E. Sherlock, J. N. Harvestine, D. Mitra, A. Haudenschild, J. Hu, K. A. Athanasiou, J. K. Leach, and L. Marcu, “Nondestructive assessment of collagen hydrogel cross-linking using time-resolved autofluorescence imaging,” J. Biomed. Opt. 23, 1–9 (2018).
[Crossref] [PubMed]

A. Alfonso-Garcia, J. Shklover, B. E. Sherlock, A. Panitch, L. G. Griffiths, and L. Marcu, “Fiber-based fluorescence lifetime imaging of recellularization processes on vascular tissue constructs,” J. Biophotonics 2018, e201700391 (2018).
[Crossref] [PubMed]

2017 (2)

M. Dettin, A. Zamuner, F. Naso, A. Monteleone, M. Spina, and G. Gerosa, “Natural scaffolds for regenerative medicine: Direct determination of detergents entrapped in decellularized heart valves,” Biomed. Res. Int. 2017, 9274135 (2017).

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. Reports 7, 8690(2017).

2016 (6)

T. C. Rothuizen, F. F. R. Damanik, T. Lavrijsen, M. J. T. Visser, J. F. Hamming, R. A. Lalai, J. M. G. J. Duijs, A. J. van Zonneveld, I. E. Hoefer, C. A. van Blitterswijk, T. J. Rabelink, L. Moroni, and J. I. Rotmans, “Development and evaluation of in vivo tissue engineered blood vessels in a porcine model,” Biomaterials. 75, 82–90 (2016).
[Crossref]

D. Gorpas, D. Ma, J. Bec, D. R. Yankelevich, and L. Marcu, “Real-time visualization of tissue surface biochemical features derived from fluorescence lifetime measurements,” IEEE Trans. Med. Imaging 35, 1802–1811 (2016).
[Crossref] [PubMed]

S. Shrestha, M. J. Serafino, J. Rico-Jimenez, J. Park, X. Chen, S. Zhaorigetu, B. L. Walton, J. A. Jo, and B. E. Applegate, “Multimodal optical coherence tomography and fluorescence lifetime imaging with interleaved excitation sources for simultaneous endogenous and exogenous fluorescence,” Biomed. Opt. Express 7, 3184 (2016).
[Crossref] [PubMed]

Y. Cao, J. Hui, A. Kole, P. Wang, Q. Yu, W. Chen, M. Sturek, and J. X. Cheng, “High-sensitivity intravascular photoacoustic imaging of lipid-laden plaque with a collinear catheter design,” Sci. Rep. 6, 1–8 (2016).

T. C. Rothuizen, F. F. R. Damanik, T. Lavrijsen, M. J. T. Visser, J. F. Hamming, R. A. Lalai, J. M. G. J. Duijs, A. J. van Zonneveld, I. E. Hoefer, C. A. van Blitterswijk, T. J. Rabelink, L. Moroni, and J. I. Rotmans, “Development and evaluation of in vivo tissue engineered blood vessels in a porcine model,” Biomaterials. 75, 82–90 (2016).
[Crossref]

A. Ozcelikkale and B. Han, “Thermal destabilization of collagen matrix hierarchical structure by freeze/thaw,” PLoS ONE 11, 146660 (2016).
[Crossref] [PubMed]

2015 (5)

J. F. Gillooly, A. Hein, and R. Damiani, “Nuclear DNA Content Varies with Cell Size across Human Cell Types,” Cold Spring Harb. Perspect. Biol. 7, 1–28 (2015).
[Crossref]

S. Ranjit, A. Dvornikov, M. Stakic, S.-H. Hong, M. Levi, R. M. Evans, and E. Gratton, “Imaging Fibrosis and Separating Collagens using Second Harmonic Generation and Phasor Approach to Fluorescence Lifetime Imaging,” Sci. Reports 5, 13378 (2015).
[Crossref]

G. S. Mintz, “Intravascular imaging of coronary calcification and its clinical implications,” JACC: Cardiovasc. Imaging 8, 461–471 (2015).

T. Ma, M. Yu, Z. Chen, C. Fei, K. K. Shung, and Q. Zhou, “Multi-Frequency Intravascular Ultrasound,” IEEE Transactions on Ultrason. Ferroelectr. Freq. Control. 62, 97–107 (2015).
[Crossref]

D. Gorpas, H. Fatakdawala, J. Bec, D. Ma, D. R. Yankelevich, J. Qi, and L. Marcu, “Fluorescence lifetime imaging and intravascular ultrasound: co-registration study using ex vivo human coronaries,” IEEE Trans Med Imaging 34, 156–166 (2015).
[Crossref]

2014 (5)

D. Ma, J. Bec, D. R. Yankelevich, D. Gorpas, H. Fatakdawala, and L. Marcu, “Rotational multispectral fluorescence lifetime imaging and intravascular ultrasound: bimodal system for intravascular applications,” J. Biomed. Opt. 19, 066004 (2014).
[Crossref] [PubMed]

D. D. Cissell, J. C. Hu, L. G. Griffiths, and K. A. Athanasiou, “Antigen removal for the production of biomechanically functional, xenogeneic tissue grafts,” J. Biomech. 47, 1987–1996 (2014).
[Crossref]

H. Y. Tuan-Mu, C. H. Yu, and J. J. Hu, “On the decellularization of fresh or frozen human umbilical arteries: implications for small-diameter tissue engineered vascular grafts,” Ann. Biomed. Eng. 42, 1305–1318 (2014).
[Crossref] [PubMed]

D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instruments 85, 034303 (2014).
[Crossref]

S. A. O’Leary, B. J. Doyle, and T. M. McGloughlin, “The impact of long term freezing on the mechanical properties of porcine aortic tissue,” J. Mech. Behav. Biomed. Mater. 37, 165–173 (2014).
[Crossref] [PubMed]

2013 (1)

M. L. Wong, J. L. Wong, K. A. Athanasiou, and L. G. Griffiths, “Stepwise solubilization-based antigen removal for xenogeneic scaffold generation in tissue engineering,” Acta Biomater. 9, 6492–6501 (2013).
[Crossref] [PubMed]

2012 (5)

P. Kochová, J. Kuncová, J. Švíglerová, R. Cimrman, M. Miklíková, V. Liška, and Z. Tonar, “The contribution of vascular smooth muscle, elastin and collagen on the passive mechanics of porcine carotid arteries,” Physiol. Meas. 33, 1335–1351 (2012).
[Crossref] [PubMed]

S. Liang, A. Saidi, J. Jing, G. Liu, J. Li, J. Zhang, C. Sun, J. Narula, and Z. Chen, “Intravascular atherosclerotic imaging with combined fluorescence and optical coherence tomography probe based on a double-clad fiber combiner,” J. Biomed. Opt. 17, 0705011 (2012).
[Crossref]

J. Bec, H. Xie, D. R. Yankelevich, F. Zhou, Y. Sun, N. Ghata, R. Aldredge, and L. Marcu, “Design, construction, and validation of a rotary multifunctional intravascular diagnostic catheter combining multispectral fluorescence lifetime imaging and intravascular ultrasound,” J. Biomed. Opt. 17, 106012 (2012).
[Crossref] [PubMed]

W. Becker, “Fluorescence lifetime imaging - techniques and applications,” J. Microsc. 247, 119–136 (2012).
[Crossref] [PubMed]

K. P. Quinn, E. Bellas, N. Fourligas, K. Lee, D. L. Kaplan, and I. Georgakoudi, “Characterization of metabolic changes associated with the functional development of 3D engineered tissues by non-invasive, dynamic measurement of individual cell redox ratios,” Biomaterials 33, 5341–5348 (2012).
[Crossref] [PubMed]

2011 (7)

Y. Sun, Y. Sun, D. Stephens, H. Xie, J. Phipps, R. Saroufeem, J. Southard, D. S. Elson, and L. Marcu, “Dynamic tissue analysis using time- and wavelength-resolved fluorescence spectroscopy for atherosclerosis diagnosis,” Opt. Express 19, 3890–3901 (2011).
[Crossref] [PubMed]

J. Phipps, Y. Sun, R. Saroufeem, N. Hatami, M. C. Fishbein, and L. Marcu, “Fluorescence lifetime imaging for the characterization of the biochemical composition of atherosclerotic plaques,” J. Biomed. Opt. 16, 096018 (2011).
[Crossref] [PubMed]

D. Sindram, K. Martin, J. P. Meadows, A. S. Prabhu, J. J. Heath, I. H. McKillop, and D. A. Iannitti, “Collagen–elastin ratio predicts burst pressure of arterial seals created using a bipolar vessel sealing device in a porcine model,” Surg. Endosc. 25, 2604–2612 (2011).
[Crossref] [PubMed]

F. R. Nowrozani and B. Zareiyan, “A microscopic study of the external carotid artery transitional zone of the adult male dog,” J. Appl. Animal Res. 39, 406–411 (2011).
[Crossref]

A. García, E. Peña, A. Laborda, F. Lostalé, M. A. De Gregorio, M. Doblaré, and M. A. Martínez, “Experimental study and constitutive modelling of the passive mechanical properties of the porcine carotid artery and its relation to histological analysis: Implications in animal cardiovascular device trials,” Med. Eng. Phys. 33, 665–676 (2011).
[Crossref] [PubMed]

D. Sindram, K. Martin, J. P. Meadows, A. S. Prabhu, J. J. Heath, I. H. McKillop, and D. A. Iannitti, “Collagen-elastin ratio predicts burst pressure of arterial seals created using a bipolar vessel sealing device in a porcine model,” Surg. Endosc. Other Interv. Tech. 25, 2604–2612 (2011).
[Crossref]

P. Pande and J. A. Jo, “Automated analysis of fluorescence lifetime imaging microscopy (FLIM) data based on the laguerre deconvolution method,” IEEE Transactions on Biomed. Eng. 58, 172–181 (2011).
[Crossref]

2010 (1)

R. T. Venkatasubramanian, W. F. Wolkers, M. M. Shenoi, V. H. Barocas, D. Lafontaine, C. L. Soule, P. A. Iaizzo, and J. C. Bischof, “Freeze-thaw induced biomechanical changes in arteries: Role of collagen matrix and smooth muscle cells,” Annals Biomed. Eng. 38, 694–706 (2010).
[Crossref]

2009 (1)

J. E. Wagenseil and R. P. Mecham, “Vascular Extracellular Matrix and Arterial Mechanics,” Physiol. Rev. 89, 957–989 (2009).
[Crossref] [PubMed]

2007 (1)

S. L. Dahl, C. Rhim, Y. C. Song, and L. E. Niklason, “Mechanical Properties and Compositions of Tissue Engineered and Native Arteries,” Annals Biomed. Eng. 35, 348–355 (2007).
[Crossref]

2005 (1)

S. Roy, P. Silacci, and N. Stergiopulos, “Biomechanical proprieties of decellularized porcine common carotid arteries Sylvain,” Am. J. Physiol. Hear. Circ. Physiol. 289, H1567–H1576 (2005).
[Crossref]

2002 (1)

I. Georgakoudi, B. C. Jacobson, M. G. Mu, E. E. Sheets, K. Badizadegan, D. L. Carr-locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. V. Dam, and M. S. Feld, “NAD(P)H and Collagen as in Vivo Quantitative Fluorescent Biomarkers of Epithelial Precancerous Changes,” Cancer Res. 62, 682–687 (2002).
[PubMed]

2001 (1)

G. E. Kochiadakis, S. I. Chrysostomakis, M. D. Kalebubas, G. M. Filippidis, I. G. Zacharakis, T. G. Papazoglou, and P. E. Vardas, “The role of laser-induced fluorescence in myocardial tissue characterization: an experimental in vitro study,” Chest. 120, 233–239 (2001).
[Crossref] [PubMed]

2000 (3)

J. M. Maarek, L. Marcu, W. J. Snyder, and W. S. Grundfest, “Time-resolved fluorescence spectra of arterial fluorescent compounds: reconstruction with the Laguerre expansion technique,” Photochem. Photobiol. 71, 178–187 (2000).
[Crossref] [PubMed]

L. Marcu, “Characterization of type I, II, III, IV, and V collagens by time-resolved laser-induced fluorescence spectroscopy,” Proc. SPIE 3917, 93–101 (2000).
[Crossref]

J. Kim, M. Lee, J. H. Yang, and J. H. Choy, “Photophysical Properties of Hemicyanine Dyes Intercalated in Na -Fluorine Mica,” J. Phys. Chem. A 104, 1388–1392 (2000).
[Crossref]

1999 (1)

K. Dowling, M. J. Dayel, S. C. W. Hyde, P. M. W. French, M. J. Lever, J. D. Hares, and A. K. L. Dymoke-bradshaw, “High resolution time-domain fluorescence lifetime imaging for biomedical applications,” J. Mod. Opt. 46, 199–209 (1999).
[Crossref]

1998 (2)

G. a. Wagnieres, W. M. Star, and B. C. Wilson, “ln Vivo Fluorescence Spectroscopy and Imaging for Oncological Applications,” Photochem. Photobiol. 68, 603–632 (1998).
[Crossref]

A. Sillen and Y. Engelborghs, “The Correct Use of "Average" Fluorescence Parameters,” Photochem. Photobiol 67, 475–486 (1998).

1991 (1)

S. Andersson-Engels, J. Johansson, K. Svanberg, and S. Svanberg, “Fluorescence imaging and point measurements of tissue: applications to the demarcation of malignant tumors and atherosclerotic lesions from normal tissue,” Photochem. Photobiol. 53, 807–814 (1991).
[Crossref] [PubMed]

Aldredge, R.

J. Bec, H. Xie, D. R. Yankelevich, F. Zhou, Y. Sun, N. Ghata, R. Aldredge, and L. Marcu, “Design, construction, and validation of a rotary multifunctional intravascular diagnostic catheter combining multispectral fluorescence lifetime imaging and intravascular ultrasound,” J. Biomed. Opt. 17, 106012 (2012).
[Crossref] [PubMed]

Alfonso-Garcia, A.

A. Alfonso-Garcia, J. Shklover, B. E. Sherlock, A. Panitch, L. G. Griffiths, and L. Marcu, “Fiber-based fluorescence lifetime imaging of recellularization processes on vascular tissue constructs,” J. Biophotonics 2018, e201700391 (2018).
[Crossref] [PubMed]

Andersson-Engels, S.

S. Andersson-Engels, J. Johansson, K. Svanberg, and S. Svanberg, “Fluorescence imaging and point measurements of tissue: applications to the demarcation of malignant tumors and atherosclerotic lesions from normal tissue,” Photochem. Photobiol. 53, 807–814 (1991).
[Crossref] [PubMed]

Applegate, B. E.

Athanasiou, K. A.

B. E. Sherlock, J. N. Harvestine, D. Mitra, A. Haudenschild, J. Hu, K. A. Athanasiou, J. K. Leach, and L. Marcu, “Nondestructive assessment of collagen hydrogel cross-linking using time-resolved autofluorescence imaging,” J. Biomed. Opt. 23, 1–9 (2018).
[Crossref] [PubMed]

D. D. Cissell, J. C. Hu, L. G. Griffiths, and K. A. Athanasiou, “Antigen removal for the production of biomechanically functional, xenogeneic tissue grafts,” J. Biomech. 47, 1987–1996 (2014).
[Crossref]

M. L. Wong, J. L. Wong, K. A. Athanasiou, and L. G. Griffiths, “Stepwise solubilization-based antigen removal for xenogeneic scaffold generation in tissue engineering,” Acta Biomater. 9, 6492–6501 (2013).
[Crossref] [PubMed]

Badizadegan, K.

I. Georgakoudi, B. C. Jacobson, M. G. Mu, E. E. Sheets, K. Badizadegan, D. L. Carr-locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. V. Dam, and M. S. Feld, “NAD(P)H and Collagen as in Vivo Quantitative Fluorescent Biomarkers of Epithelial Precancerous Changes,” Cancer Res. 62, 682–687 (2002).
[PubMed]

Barocas, V. H.

R. T. Venkatasubramanian, W. F. Wolkers, M. M. Shenoi, V. H. Barocas, D. Lafontaine, C. L. Soule, P. A. Iaizzo, and J. C. Bischof, “Freeze-thaw induced biomechanical changes in arteries: Role of collagen matrix and smooth muscle cells,” Annals Biomed. Eng. 38, 694–706 (2010).
[Crossref]

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. Reports 7, 8690(2017).

D. Gorpas, D. Ma, J. Bec, D. R. Yankelevich, and L. Marcu, “Real-time visualization of tissue surface biochemical features derived from fluorescence lifetime measurements,” IEEE Trans. Med. Imaging 35, 1802–1811 (2016).
[Crossref] [PubMed]

D. Gorpas, H. Fatakdawala, J. Bec, D. Ma, D. R. Yankelevich, J. Qi, and L. Marcu, “Fluorescence lifetime imaging and intravascular ultrasound: co-registration study using ex vivo human coronaries,” IEEE Trans Med Imaging 34, 156–166 (2015).
[Crossref]

D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instruments 85, 034303 (2014).
[Crossref]

D. Ma, J. Bec, D. R. Yankelevich, D. Gorpas, H. Fatakdawala, and L. Marcu, “Rotational multispectral fluorescence lifetime imaging and intravascular ultrasound: bimodal system for intravascular applications,” J. Biomed. Opt. 19, 066004 (2014).
[Crossref] [PubMed]

J. Bec, H. Xie, D. R. Yankelevich, F. Zhou, Y. Sun, N. Ghata, R. Aldredge, and L. Marcu, “Design, construction, and validation of a rotary multifunctional intravascular diagnostic catheter combining multispectral fluorescence lifetime imaging and intravascular ultrasound,” J. Biomed. Opt. 17, 106012 (2012).
[Crossref] [PubMed]

Becker, W.

W. Becker, “Fluorescence lifetime imaging - techniques and applications,” J. Microsc. 247, 119–136 (2012).
[Crossref] [PubMed]

Bellas, E.

K. P. Quinn, E. Bellas, N. Fourligas, K. Lee, D. L. Kaplan, and I. Georgakoudi, “Characterization of metabolic changes associated with the functional development of 3D engineered tissues by non-invasive, dynamic measurement of individual cell redox ratios,” Biomaterials 33, 5341–5348 (2012).
[Crossref] [PubMed]

Bischof, J. C.

R. T. Venkatasubramanian, W. F. Wolkers, M. M. Shenoi, V. H. Barocas, D. Lafontaine, C. L. Soule, P. A. Iaizzo, and J. C. Bischof, “Freeze-thaw induced biomechanical changes in arteries: Role of collagen matrix and smooth muscle cells,” Annals Biomed. Eng. 38, 694–706 (2010).
[Crossref]

Boone, C. W.

I. Georgakoudi, B. C. Jacobson, M. G. Mu, E. E. Sheets, K. Badizadegan, D. L. Carr-locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. V. Dam, and M. S. Feld, “NAD(P)H and Collagen as in Vivo Quantitative Fluorescent Biomarkers of Epithelial Precancerous Changes,” Cancer Res. 62, 682–687 (2002).
[PubMed]

Cao, Y.

Y. Cao, J. Hui, A. Kole, P. Wang, Q. Yu, W. Chen, M. Sturek, and J. X. Cheng, “High-sensitivity intravascular photoacoustic imaging of lipid-laden plaque with a collinear catheter design,” Sci. Rep. 6, 1–8 (2016).

Carr-locke, D. L.

I. Georgakoudi, B. C. Jacobson, M. G. Mu, E. E. Sheets, K. Badizadegan, D. L. Carr-locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. V. Dam, and M. S. Feld, “NAD(P)H and Collagen as in Vivo Quantitative Fluorescent Biomarkers of Epithelial Precancerous Changes,” Cancer Res. 62, 682–687 (2002).
[PubMed]

Chen, W.

Y. Cao, J. Hui, A. Kole, P. Wang, Q. Yu, W. Chen, M. Sturek, and J. X. Cheng, “High-sensitivity intravascular photoacoustic imaging of lipid-laden plaque with a collinear catheter design,” Sci. Rep. 6, 1–8 (2016).

Chen, X.

Chen, Z.

T. Ma, M. Yu, Z. Chen, C. Fei, K. K. Shung, and Q. Zhou, “Multi-Frequency Intravascular Ultrasound,” IEEE Transactions on Ultrason. Ferroelectr. Freq. Control. 62, 97–107 (2015).
[Crossref]

S. Liang, A. Saidi, J. Jing, G. Liu, J. Li, J. Zhang, C. Sun, J. Narula, and Z. Chen, “Intravascular atherosclerotic imaging with combined fluorescence and optical coherence tomography probe based on a double-clad fiber combiner,” J. Biomed. Opt. 17, 0705011 (2012).
[Crossref]

Cheng, J. X.

Y. Cao, J. Hui, A. Kole, P. Wang, Q. Yu, W. Chen, M. Sturek, and J. X. Cheng, “High-sensitivity intravascular photoacoustic imaging of lipid-laden plaque with a collinear catheter design,” Sci. Rep. 6, 1–8 (2016).

Choy, J. H.

J. Kim, M. Lee, J. H. Yang, and J. H. Choy, “Photophysical Properties of Hemicyanine Dyes Intercalated in Na -Fluorine Mica,” J. Phys. Chem. A 104, 1388–1392 (2000).
[Crossref]

Chrysostomakis, S. I.

G. E. Kochiadakis, S. I. Chrysostomakis, M. D. Kalebubas, G. M. Filippidis, I. G. Zacharakis, T. G. Papazoglou, and P. E. Vardas, “The role of laser-induced fluorescence in myocardial tissue characterization: an experimental in vitro study,” Chest. 120, 233–239 (2001).
[Crossref] [PubMed]

Cimrman, R.

P. Kochová, J. Kuncová, J. Švíglerová, R. Cimrman, M. Miklíková, V. Liška, and Z. Tonar, “The contribution of vascular smooth muscle, elastin and collagen on the passive mechanics of porcine carotid arteries,” Physiol. Meas. 33, 1335–1351 (2012).
[Crossref] [PubMed]

Cissell, D. D.

D. D. Cissell, J. C. Hu, L. G. Griffiths, and K. A. Athanasiou, “Antigen removal for the production of biomechanically functional, xenogeneic tissue grafts,” J. Biomech. 47, 1987–1996 (2014).
[Crossref]

Crum, C. P.

I. Georgakoudi, B. C. Jacobson, M. G. Mu, E. E. Sheets, K. Badizadegan, D. L. Carr-locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. V. Dam, and M. S. Feld, “NAD(P)H and Collagen as in Vivo Quantitative Fluorescent Biomarkers of Epithelial Precancerous Changes,” Cancer Res. 62, 682–687 (2002).
[PubMed]

Dahl, S. L.

S. L. Dahl, C. Rhim, Y. C. Song, and L. E. Niklason, “Mechanical Properties and Compositions of Tissue Engineered and Native Arteries,” Annals Biomed. Eng. 35, 348–355 (2007).
[Crossref]

Dam, J. V.

I. Georgakoudi, B. C. Jacobson, M. G. Mu, E. E. Sheets, K. Badizadegan, D. L. Carr-locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. V. Dam, and M. S. Feld, “NAD(P)H and Collagen as in Vivo Quantitative Fluorescent Biomarkers of Epithelial Precancerous Changes,” Cancer Res. 62, 682–687 (2002).
[PubMed]

Damanik, F. F. R.

T. C. Rothuizen, F. F. R. Damanik, T. Lavrijsen, M. J. T. Visser, J. F. Hamming, R. A. Lalai, J. M. G. J. Duijs, A. J. van Zonneveld, I. E. Hoefer, C. A. van Blitterswijk, T. J. Rabelink, L. Moroni, and J. I. Rotmans, “Development and evaluation of in vivo tissue engineered blood vessels in a porcine model,” Biomaterials. 75, 82–90 (2016).
[Crossref]

T. C. Rothuizen, F. F. R. Damanik, T. Lavrijsen, M. J. T. Visser, J. F. Hamming, R. A. Lalai, J. M. G. J. Duijs, A. J. van Zonneveld, I. E. Hoefer, C. A. van Blitterswijk, T. J. Rabelink, L. Moroni, and J. I. Rotmans, “Development and evaluation of in vivo tissue engineered blood vessels in a porcine model,” Biomaterials. 75, 82–90 (2016).
[Crossref]

Damiani, R.

J. F. Gillooly, A. Hein, and R. Damiani, “Nuclear DNA Content Varies with Cell Size across Human Cell Types,” Cold Spring Harb. Perspect. Biol. 7, 1–28 (2015).
[Crossref]

Dasari, R. R.

I. Georgakoudi, B. C. Jacobson, M. G. Mu, E. E. Sheets, K. Badizadegan, D. L. Carr-locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. V. Dam, and M. S. Feld, “NAD(P)H and Collagen as in Vivo Quantitative Fluorescent Biomarkers of Epithelial Precancerous Changes,” Cancer Res. 62, 682–687 (2002).
[PubMed]

Dayel, M. J.

K. Dowling, M. J. Dayel, S. C. W. Hyde, P. M. W. French, M. J. Lever, J. D. Hares, and A. K. L. Dymoke-bradshaw, “High resolution time-domain fluorescence lifetime imaging for biomedical applications,” J. Mod. Opt. 46, 199–209 (1999).
[Crossref]

De Gregorio, M. A.

A. García, E. Peña, A. Laborda, F. Lostalé, M. A. De Gregorio, M. Doblaré, and M. A. Martínez, “Experimental study and constitutive modelling of the passive mechanical properties of the porcine carotid artery and its relation to histological analysis: Implications in animal cardiovascular device trials,” Med. Eng. Phys. 33, 665–676 (2011).
[Crossref] [PubMed]

De Lahunta, A.

H. E. Evans and A. De Lahunta, Miller’s Anatomy of the Dog-E-Book(Elsevier Health Sciences2013).

Dettin, M.

M. Dettin, A. Zamuner, F. Naso, A. Monteleone, M. Spina, and G. Gerosa, “Natural scaffolds for regenerative medicine: Direct determination of detergents entrapped in decellularized heart valves,” Biomed. Res. Int. 2017, 9274135 (2017).

Doblaré, M.

A. García, E. Peña, A. Laborda, F. Lostalé, M. A. De Gregorio, M. Doblaré, and M. A. Martínez, “Experimental study and constitutive modelling of the passive mechanical properties of the porcine carotid artery and its relation to histological analysis: Implications in animal cardiovascular device trials,” Med. Eng. Phys. 33, 665–676 (2011).
[Crossref] [PubMed]

Dowling, K.

K. Dowling, M. J. Dayel, S. C. W. Hyde, P. M. W. French, M. J. Lever, J. D. Hares, and A. K. L. Dymoke-bradshaw, “High resolution time-domain fluorescence lifetime imaging for biomedical applications,” J. Mod. Opt. 46, 199–209 (1999).
[Crossref]

Doyle, B. J.

S. A. O’Leary, B. J. Doyle, and T. M. McGloughlin, “The impact of long term freezing on the mechanical properties of porcine aortic tissue,” J. Mech. Behav. Biomed. Mater. 37, 165–173 (2014).
[Crossref] [PubMed]

Duijs, J. M. G. J.

T. C. Rothuizen, F. F. R. Damanik, T. Lavrijsen, M. J. T. Visser, J. F. Hamming, R. A. Lalai, J. M. G. J. Duijs, A. J. van Zonneveld, I. E. Hoefer, C. A. van Blitterswijk, T. J. Rabelink, L. Moroni, and J. I. Rotmans, “Development and evaluation of in vivo tissue engineered blood vessels in a porcine model,” Biomaterials. 75, 82–90 (2016).
[Crossref]

T. C. Rothuizen, F. F. R. Damanik, T. Lavrijsen, M. J. T. Visser, J. F. Hamming, R. A. Lalai, J. M. G. J. Duijs, A. J. van Zonneveld, I. E. Hoefer, C. A. van Blitterswijk, T. J. Rabelink, L. Moroni, and J. I. Rotmans, “Development and evaluation of in vivo tissue engineered blood vessels in a porcine model,” Biomaterials. 75, 82–90 (2016).
[Crossref]

Dvornikov, A.

S. Ranjit, A. Dvornikov, M. Stakic, S.-H. Hong, M. Levi, R. M. Evans, and E. Gratton, “Imaging Fibrosis and Separating Collagens using Second Harmonic Generation and Phasor Approach to Fluorescence Lifetime Imaging,” Sci. Reports 5, 13378 (2015).
[Crossref]

Dymoke-bradshaw, A. K. L.

K. Dowling, M. J. Dayel, S. C. W. Hyde, P. M. W. French, M. J. Lever, J. D. Hares, and A. K. L. Dymoke-bradshaw, “High resolution time-domain fluorescence lifetime imaging for biomedical applications,” J. Mod. Opt. 46, 199–209 (1999).
[Crossref]

Elson, D. S.

D. R. Yankelevich, D. Ma, J. Liu, Y. Sun, Y. Sun, J. Bec, D. S. Elson, and L. Marcu, “Design and evaluation of a device for fast multispectral time-resolved fluorescence spectroscopy and imaging,” Rev. Sci. Instruments 85, 034303 (2014).
[Crossref]

Y. Sun, Y. Sun, D. Stephens, H. Xie, J. Phipps, R. Saroufeem, J. Southard, D. S. Elson, and L. Marcu, “Dynamic tissue analysis using time- and wavelength-resolved fluorescence spectroscopy for atherosclerosis diagnosis,” Opt. Express 19, 3890–3901 (2011).
[Crossref] [PubMed]

L. Marcu, P. M. French, and D. S. Elson, Fluorescence Lifetime Spectroscopy and Imaging: Principles and Applications in Biomedical Diagnostics(CRC Press, 2014).
[Crossref]

Engelborghs, Y.

A. Sillen and Y. Engelborghs, “The Correct Use of "Average" Fluorescence Parameters,” Photochem. Photobiol 67, 475–486 (1998).

Evans, H. E.

H. E. Evans and A. De Lahunta, Miller’s Anatomy of the Dog-E-Book(Elsevier Health Sciences2013).

Evans, R. M.

S. Ranjit, A. Dvornikov, M. Stakic, S.-H. Hong, M. Levi, R. M. Evans, and E. Gratton, “Imaging Fibrosis and Separating Collagens using Second Harmonic Generation and Phasor Approach to Fluorescence Lifetime Imaging,” Sci. Reports 5, 13378 (2015).
[Crossref]

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. Reports 7, 8690(2017).

D. Gorpas, H. Fatakdawala, J. Bec, D. Ma, D. R. Yankelevich, J. Qi, and L. Marcu, “Fluorescence lifetime imaging and intravascular ultrasound: co-registration study using ex vivo human coronaries,” IEEE Trans Med Imaging 34, 156–166 (2015).
[Crossref]

D. Ma, J. Bec, D. R. Yankelevich, D. Gorpas, H. Fatakdawala, and L. Marcu, “Rotational multispectral fluorescence lifetime imaging and intravascular ultrasound: bimodal system for intravascular applications,” J. Biomed. Opt. 19, 066004 (2014).
[Crossref] [PubMed]

Fei, C.

T. Ma, M. Yu, Z. Chen, C. Fei, K. K. Shung, and Q. Zhou, “Multi-Frequency Intravascular Ultrasound,” IEEE Transactions on Ultrason. Ferroelectr. Freq. Control. 62, 97–107 (2015).
[Crossref]

Feld, M. S.

I. Georgakoudi, B. C. Jacobson, M. G. Mu, E. E. Sheets, K. Badizadegan, D. L. Carr-locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. V. Dam, and M. S. Feld, “NAD(P)H and Collagen as in Vivo Quantitative Fluorescent Biomarkers of Epithelial Precancerous Changes,” Cancer Res. 62, 682–687 (2002).
[PubMed]

Filippidis, G. M.

G. E. Kochiadakis, S. I. Chrysostomakis, M. D. Kalebubas, G. M. Filippidis, I. G. Zacharakis, T. G. Papazoglou, and P. E. Vardas, “The role of laser-induced fluorescence in myocardial tissue characterization: an experimental in vitro study,” Chest. 120, 233–239 (2001).
[Crossref] [PubMed]

Fishbein, M. C.

J. Phipps, Y. Sun, R. Saroufeem, N. Hatami, M. C. Fishbein, and L. Marcu, “Fluorescence lifetime imaging for the characterization of the biochemical composition of atherosclerotic plaques,” J. Biomed. Opt. 16, 096018 (2011).
[Crossref] [PubMed]

Fourligas, N.

K. P. Quinn, E. Bellas, N. Fourligas, K. Lee, D. L. Kaplan, and I. Georgakoudi, “Characterization of metabolic changes associated with the functional development of 3D engineered tissues by non-invasive, dynamic measurement of individual cell redox ratios,” Biomaterials 33, 5341–5348 (2012).
[Crossref] [PubMed]

French, P. M.

L. Marcu, P. M. French, and D. S. Elson, Fluorescence Lifetime Spectroscopy and Imaging: Principles and Applications in Biomedical Diagnostics(CRC Press, 2014).
[Crossref]

French, P. M. W.

K. Dowling, M. J. Dayel, S. C. W. Hyde, P. M. W. French, M. J. Lever, J. D. Hares, and A. K. L. Dymoke-bradshaw, “High resolution time-domain fluorescence lifetime imaging for biomedical applications,” J. Mod. Opt. 46, 199–209 (1999).
[Crossref]

García, A.

A. García, E. Peña, A. Laborda, F. Lostalé, M. A. De Gregorio, M. Doblaré, and M. A. Martínez, “Experimental study and constitutive modelling of the passive mechanical properties of the porcine carotid artery and its relation to histological analysis: Implications in animal cardiovascular device trials,” Med. Eng. Phys. 33, 665–676 (2011).
[Crossref] [PubMed]

Georgakoudi, I.

K. P. Quinn, E. Bellas, N. Fourligas, K. Lee, D. L. Kaplan, and I. Georgakoudi, “Characterization of metabolic changes associated with the functional development of 3D engineered tissues by non-invasive, dynamic measurement of individual cell redox ratios,” Biomaterials 33, 5341–5348 (2012).
[Crossref] [PubMed]

I. Georgakoudi, B. C. Jacobson, M. G. Mu, E. E. Sheets, K. Badizadegan, D. L. Carr-locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. V. Dam, and M. S. Feld, “NAD(P)H and Collagen as in Vivo Quantitative Fluorescent Biomarkers of Epithelial Precancerous Changes,” Cancer Res. 62, 682–687 (2002).
[PubMed]

Gerosa, G.

M. Dettin, A. Zamuner, F. Naso, A. Monteleone, M. Spina, and G. Gerosa, “Natural scaffolds for regenerative medicine: Direct determination of detergents entrapped in decellularized heart valves,” Biomed. Res. Int. 2017, 9274135 (2017).

Ghata, N.

J. Bec, H. Xie, D. R. Yankelevich, F. Zhou, Y. Sun, N. Ghata, R. Aldredge, and L. Marcu, “Design, construction, and validation of a rotary multifunctional intravascular diagnostic catheter combining multispectral fluorescence lifetime imaging and intravascular ultrasound,” J. Biomed. Opt. 17, 106012 (2012).
[Crossref] [PubMed]

Gillooly, J. F.

J. F. Gillooly, A. Hein, and R. Damiani, “Nuclear DNA Content Varies with Cell Size across Human Cell Types,” Cold Spring Harb. Perspect. Biol. 7, 1–28 (2015).
[Crossref]

Gorpas, D.

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. Reports 7, 8690(2017).

D. Gorpas, D. Ma, J. Bec, D. R. Yankelevich, and L. Marcu, “Real-time visualization of tissue surface biochemical features derived from fluorescence lifetime measurements,” IEEE Trans. Med. Imaging 35, 1802–1811 (2016).
[Crossref] [PubMed]

D. Gorpas, H. Fatakdawala, J. Bec, D. Ma, D. R. Yankelevich, J. Qi, and L. Marcu, “Fluorescence lifetime imaging and intravascular ultrasound: co-registration study using ex vivo human coronaries,” IEEE Trans Med Imaging 34, 156–166 (2015).
[Crossref]

D. Ma, J. Bec, D. R. Yankelevich, D. Gorpas, H. Fatakdawala, and L. Marcu, “Rotational multispectral fluorescence lifetime imaging and intravascular ultrasound: bimodal system for intravascular applications,” J. Biomed. Opt. 19, 066004 (2014).
[Crossref] [PubMed]

Gratton, E.

S. Ranjit, A. Dvornikov, M. Stakic, S.-H. Hong, M. Levi, R. M. Evans, and E. Gratton, “Imaging Fibrosis and Separating Collagens using Second Harmonic Generation and Phasor Approach to Fluorescence Lifetime Imaging,” Sci. Reports 5, 13378 (2015).
[Crossref]

Griffiths, L. G.

A. Alfonso-Garcia, J. Shklover, B. E. Sherlock, A. Panitch, L. G. Griffiths, and L. Marcu, “Fiber-based fluorescence lifetime imaging of recellularization processes on vascular tissue constructs,” J. Biophotonics 2018, e201700391 (2018).
[Crossref] [PubMed]

D. D. Cissell, J. C. Hu, L. G. Griffiths, and K. A. Athanasiou, “Antigen removal for the production of biomechanically functional, xenogeneic tissue grafts,” J. Biomech. 47, 1987–1996 (2014).
[Crossref]

M. L. Wong, J. L. Wong, K. A. Athanasiou, and L. G. Griffiths, “Stepwise solubilization-based antigen removal for xenogeneic scaffold generation in tissue engineering,” Acta Biomater. 9, 6492–6501 (2013).
[Crossref] [PubMed]

Grundfest, W. S.

J. M. Maarek, L. Marcu, W. J. Snyder, and W. S. Grundfest, “Time-resolved fluorescence spectra of arterial fluorescent compounds: reconstruction with the Laguerre expansion technique,” Photochem. Photobiol. 71, 178–187 (2000).
[Crossref] [PubMed]

Hamming, J. F.

T. C. Rothuizen, F. F. R. Damanik, T. Lavrijsen, M. J. T. Visser, J. F. Hamming, R. A. Lalai, J. M. G. J. Duijs, A. J. van Zonneveld, I. E. Hoefer, C. A. van Blitterswijk, T. J. Rabelink, L. Moroni, and J. I. Rotmans, “Development and evaluation of in vivo tissue engineered blood vessels in a porcine model,” Biomaterials. 75, 82–90 (2016).
[Crossref]

T. C. Rothuizen, F. F. R. Damanik, T. Lavrijsen, M. J. T. Visser, J. F. Hamming, R. A. Lalai, J. M. G. J. Duijs, A. J. van Zonneveld, I. E. Hoefer, C. A. van Blitterswijk, T. J. Rabelink, L. Moroni, and J. I. Rotmans, “Development and evaluation of in vivo tissue engineered blood vessels in a porcine model,” Biomaterials. 75, 82–90 (2016).
[Crossref]

Han, B.

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A. Alfonso-Garcia, J. Shklover, B. E. Sherlock, A. Panitch, L. G. Griffiths, and L. Marcu, “Fiber-based fluorescence lifetime imaging of recellularization processes on vascular tissue constructs,” J. Biophotonics 2018, e201700391 (2018).
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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. Reports 7, 8690(2017).

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M. Dettin, A. Zamuner, F. Naso, A. Monteleone, M. Spina, and G. Gerosa, “Natural scaffolds for regenerative medicine: Direct determination of detergents entrapped in decellularized heart valves,” Biomed. Res. Int. 2017, 9274135 (2017).

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S. Ranjit, A. Dvornikov, M. Stakic, S.-H. Hong, M. Levi, R. M. Evans, and E. Gratton, “Imaging Fibrosis and Separating Collagens using Second Harmonic Generation and Phasor Approach to Fluorescence Lifetime Imaging,” Sci. Reports 5, 13378 (2015).
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Figures (5)

Fig. 1
Fig. 1 (a) Schematic of sample preparation, imaging and biochemical evaluation. (b) Schematic of the FLIm system. (c) Spectral signatures of collagen and elastin, and identification of the used spectral bands, SB1: 380 – 400 nm, SB2: 415 – 455 nm, SB3: 465 – 553 nm.
Fig. 2
Fig. 2 Anatomical variations in porcine carotid artery biochemical composition. (a) Representative native porcine carotid artery shows narrowing from caudal (bottom) to cranial (top) regions. (b) Longitudinal incision to expose the lumen for imaging. (c) Representative picrosirius red staining (left) and Verhoeff-Van Gieson staining (right) staining of two different anatomical regions within the artery (caudal - bottom and cranial - top) as indicated corresponding to black squared regions (* denotes luminal side). (d) Quantification of collagen and elastin composition confirms significant anatomical variations in extracellular matrix biochemical composition.
Fig. 3
Fig. 3 FLIm analysis detects anatomical variations in porcine carotid artery. (a) Fluorescence intensity ratio (IR) images of a representative carotid artery in the three spectral bands (SB). (b) Fluorescence lifetime (LT) images of four representative carotid arteries in the three SB from three large pigs (P1–P3) and one smaller pig (P4). Average intensity ratios (c), and fluorescence lifetime (d) quantification for each spectral band in the cranial and the caudal regions of the arteries (n = 11).
Fig. 4
Fig. 4 FLIm-derived parameters are sensitive to tissue composition. Linear correlations between (a) SB3 LT and elastin content, (b) SB2 LT and collagen content, and (c) SB2 LT and cell number. (d) Multivariable linear regression model of all biochemical components against FLIm LT data.
Fig. 5
Fig. 5 Freezing alters optical properties. (a) Representative fluorescence lifetime images of a viable porcine carotid artery (viable) and after three freeze-thaw cycles at −20 °C (frozen). Quantification of the intensity ratio(b) and the fluorescence lifetime (c) in the cranial and caudal regions of the arteries before and after freezing.

Tables (3)

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Table 1 Assignation of spectral bands in the multispectral FLIm instrument.

Tables Icon

Table 2 Anatomical variation in fluorescence lifetime values of pig carotid arteries (mean ± std; matched t-test p-values; n = 11).

Tables Icon

Table 3 Effect of freezing on fluorescence lifetime in the cranial and the caudal regions of pig carotid arteries (mean ± std; matched t-test p-values; n = 3/group).

Equations (2)

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I R i = I i j = 1 3 I j , i = 1.2.3
τ a v g = 0 t I ( t ) d t 0 I ( t ) d t