Abstract

Photoacoustic imaging has emerged as a promising technique to improve preclinical and clinical imaging by providing users with label-free optical contrast of tissue. Here, we present a proof-of-concept study for noninvasive in vivo murine lipid imaging using 1210 nm light to investigate differences in periaortic fat among mice of different gender, genotypes, and maturation. Acquired lipid signals suggest that adult male apoE−/− mice have greater periaortic fat accumulation compared to adolescent males, apoE−/− females, and wild-type mice. These results demonstrate the potential of photoacoustic tomography for studying vascular pathophysiology and improving the diagnosis of lipid-based diseases.

© 2017 Optical Society of America

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References

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  1. G. Vernon, A. Baranova, and Z. M. Younossi, “Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults,” Aliment. Pharmacol. Ther. 34(3), 274–285 (2011).
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  2. A. J. Lucas, “Atherosclerosis,” Nature 407, 233–241 (2000).
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    [Crossref] [PubMed]
  4. G. S. Sangha and C. J. Goergen, “Photoacoustic tomography: applications for atherosclerosis imaging,” J. Opt. 18(8), 084005 (2016).
    [Crossref]
  5. H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-free bond-selective imaging by listening to vibrationally excited molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  7. R. Li, E. Phillips, P. Wang, C. J. Goergen, and J. X. Cheng, “Label-free in vivo imaging of peripheral nerve by multispectral photoacoustic tomography,” J. Biophotonics 9(1-2), 124–128 (2016).
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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2016 (2)

G. S. Sangha and C. J. Goergen, “Photoacoustic tomography: applications for atherosclerosis imaging,” J. Opt. 18(8), 084005 (2016).
[Crossref]

R. Li, E. Phillips, P. Wang, C. J. Goergen, and J. X. Cheng, “Label-free in vivo imaging of peripheral nerve by multispectral photoacoustic tomography,” J. Biophotonics 9(1-2), 124–128 (2016).
[Crossref] [PubMed]

2015 (2)

F. W. Damen, A. R. Adelsperger, K. E. Wilson, and C. J. Goergen, “Comparison of traditional and integrated digital anesthetic vaporizers,” J. Am. Assoc. Lab. Anim. Sci. 54(6), 756–762 (2015).
[PubMed]

E. H. Phillips, A. A. Yrineo, H. D. Schroeder, K. E. Wilson, J.-X. Cheng, and C. J. Goergen, “Morphological and biomechanical differences in the elastase and AngII apoE rodent models of abdominal aortic aneurysms,” BioMed research international 2015, 1–12 (2015).

2012 (1)

T. J. Allen, A. Hall, A. P. Dhillon, J. S. Owen, and P. C. Beard, “Spectroscopic photoacoustic imaging of lipid-rich plaques in the human aorta in the 740 to 1400 nm wavelength range,” J. Biomed. Opt. 17(6), 061209 (2012).
[Crossref] [PubMed]

2011 (5)

P. Iozzo, “Myocardial, perivascular, and epicardial fat,” Diabetes Care 34(Suppl 2), S371–S379 (2011).
[Crossref] [PubMed]

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-free bond-selective imaging by listening to vibrationally excited molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
[Crossref] [PubMed]

G. Vernon, A. Baranova, and Z. M. Younossi, “Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults,” Aliment. Pharmacol. Ther. 34(3), 274–285 (2011).
[Crossref] [PubMed]

C. J. Goergen, J. Azuma, K. N. Barr, L. Magdefessel, D. Y. Kallop, A. Gogineni, A. Grewall, R. M. Weimer, A. J. Connolly, R. L. Dalman, C. A. Taylor, P. S. Tsao, and J. M. Greve, “Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms,” Arterioscler. Thromb. Vasc. Biol. 31(2), 270–279 (2011).
[Crossref] [PubMed]

C. M. Alvarado, J. A. Diaz, A. E. Hawley, S. K. Wrobleski, R. E. Sigler, and D. D. Myers., “Male mice have increased thrombotic potential: sex differences in a mouse model of venous thrombosis,” Thromb. Res. 127(5), 478–486 (2011).
[Crossref] [PubMed]

2010 (2)

C. J. Goergen, K. N. Barr, D. T. Huynh, J. R. Eastham-Anderson, G. Choi, M. Hedehus, R. L. Dalman, A. J. Connolly, C. A. Taylor, P. S. Tsao, and J. M. Greve, “In vivo quantification of murine aortic cyclic strain, motion, and curvature: implications for abdominal aortic aneurysm growth,” J. Magn. Reson. Imaging 32(4), 847–858 (2010).
[Crossref] [PubMed]

K. M. Flegal, M. D. Carroll, C. L. Ogden, and L. R. Curtin, “Prevalence and trends in obesity among US adults, 1999-2008,” JAMA 303(3), 235–241 (2010).
[Crossref] [PubMed]

2000 (1)

A. J. Lucas, “Atherosclerosis,” Nature 407, 233–241 (2000).

1994 (1)

Y. Nakashima, A. S. Plump, E. W. Raines, J. L. Breslow, and R. Ross, “ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree,” Arterioscler. Thromb. 14(1), 133–140 (1994).
[Crossref] [PubMed]

Adelsperger, A. R.

F. W. Damen, A. R. Adelsperger, K. E. Wilson, and C. J. Goergen, “Comparison of traditional and integrated digital anesthetic vaporizers,” J. Am. Assoc. Lab. Anim. Sci. 54(6), 756–762 (2015).
[PubMed]

Allen, T. J.

T. J. Allen, A. Hall, A. P. Dhillon, J. S. Owen, and P. C. Beard, “Spectroscopic photoacoustic imaging of lipid-rich plaques in the human aorta in the 740 to 1400 nm wavelength range,” J. Biomed. Opt. 17(6), 061209 (2012).
[Crossref] [PubMed]

Alvarado, C. M.

C. M. Alvarado, J. A. Diaz, A. E. Hawley, S. K. Wrobleski, R. E. Sigler, and D. D. Myers., “Male mice have increased thrombotic potential: sex differences in a mouse model of venous thrombosis,” Thromb. Res. 127(5), 478–486 (2011).
[Crossref] [PubMed]

Azuma, J.

C. J. Goergen, J. Azuma, K. N. Barr, L. Magdefessel, D. Y. Kallop, A. Gogineni, A. Grewall, R. M. Weimer, A. J. Connolly, R. L. Dalman, C. A. Taylor, P. S. Tsao, and J. M. Greve, “Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms,” Arterioscler. Thromb. Vasc. Biol. 31(2), 270–279 (2011).
[Crossref] [PubMed]

Baranova, A.

G. Vernon, A. Baranova, and Z. M. Younossi, “Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults,” Aliment. Pharmacol. Ther. 34(3), 274–285 (2011).
[Crossref] [PubMed]

Barr, K. N.

C. J. Goergen, J. Azuma, K. N. Barr, L. Magdefessel, D. Y. Kallop, A. Gogineni, A. Grewall, R. M. Weimer, A. J. Connolly, R. L. Dalman, C. A. Taylor, P. S. Tsao, and J. M. Greve, “Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms,” Arterioscler. Thromb. Vasc. Biol. 31(2), 270–279 (2011).
[Crossref] [PubMed]

C. J. Goergen, K. N. Barr, D. T. Huynh, J. R. Eastham-Anderson, G. Choi, M. Hedehus, R. L. Dalman, A. J. Connolly, C. A. Taylor, P. S. Tsao, and J. M. Greve, “In vivo quantification of murine aortic cyclic strain, motion, and curvature: implications for abdominal aortic aneurysm growth,” J. Magn. Reson. Imaging 32(4), 847–858 (2010).
[Crossref] [PubMed]

Beard, P. C.

T. J. Allen, A. Hall, A. P. Dhillon, J. S. Owen, and P. C. Beard, “Spectroscopic photoacoustic imaging of lipid-rich plaques in the human aorta in the 740 to 1400 nm wavelength range,” J. Biomed. Opt. 17(6), 061209 (2012).
[Crossref] [PubMed]

Breslow, J. L.

Y. Nakashima, A. S. Plump, E. W. Raines, J. L. Breslow, and R. Ross, “ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree,” Arterioscler. Thromb. 14(1), 133–140 (1994).
[Crossref] [PubMed]

Carroll, M. D.

K. M. Flegal, M. D. Carroll, C. L. Ogden, and L. R. Curtin, “Prevalence and trends in obesity among US adults, 1999-2008,” JAMA 303(3), 235–241 (2010).
[Crossref] [PubMed]

Chai, N.

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-free bond-selective imaging by listening to vibrationally excited molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
[Crossref] [PubMed]

Cheng, J. X.

R. Li, E. Phillips, P. Wang, C. J. Goergen, and J. X. Cheng, “Label-free in vivo imaging of peripheral nerve by multispectral photoacoustic tomography,” J. Biophotonics 9(1-2), 124–128 (2016).
[Crossref] [PubMed]

Cheng, J.-X.

E. H. Phillips, A. A. Yrineo, H. D. Schroeder, K. E. Wilson, J.-X. Cheng, and C. J. Goergen, “Morphological and biomechanical differences in the elastase and AngII apoE rodent models of abdominal aortic aneurysms,” BioMed research international 2015, 1–12 (2015).

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-free bond-selective imaging by listening to vibrationally excited molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
[Crossref] [PubMed]

Choi, G.

C. J. Goergen, K. N. Barr, D. T. Huynh, J. R. Eastham-Anderson, G. Choi, M. Hedehus, R. L. Dalman, A. J. Connolly, C. A. Taylor, P. S. Tsao, and J. M. Greve, “In vivo quantification of murine aortic cyclic strain, motion, and curvature: implications for abdominal aortic aneurysm growth,” J. Magn. Reson. Imaging 32(4), 847–858 (2010).
[Crossref] [PubMed]

Connolly, A. J.

C. J. Goergen, J. Azuma, K. N. Barr, L. Magdefessel, D. Y. Kallop, A. Gogineni, A. Grewall, R. M. Weimer, A. J. Connolly, R. L. Dalman, C. A. Taylor, P. S. Tsao, and J. M. Greve, “Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms,” Arterioscler. Thromb. Vasc. Biol. 31(2), 270–279 (2011).
[Crossref] [PubMed]

C. J. Goergen, K. N. Barr, D. T. Huynh, J. R. Eastham-Anderson, G. Choi, M. Hedehus, R. L. Dalman, A. J. Connolly, C. A. Taylor, P. S. Tsao, and J. M. Greve, “In vivo quantification of murine aortic cyclic strain, motion, and curvature: implications for abdominal aortic aneurysm growth,” J. Magn. Reson. Imaging 32(4), 847–858 (2010).
[Crossref] [PubMed]

Curtin, L. R.

K. M. Flegal, M. D. Carroll, C. L. Ogden, and L. R. Curtin, “Prevalence and trends in obesity among US adults, 1999-2008,” JAMA 303(3), 235–241 (2010).
[Crossref] [PubMed]

Dalman, R. L.

C. J. Goergen, J. Azuma, K. N. Barr, L. Magdefessel, D. Y. Kallop, A. Gogineni, A. Grewall, R. M. Weimer, A. J. Connolly, R. L. Dalman, C. A. Taylor, P. S. Tsao, and J. M. Greve, “Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms,” Arterioscler. Thromb. Vasc. Biol. 31(2), 270–279 (2011).
[Crossref] [PubMed]

C. J. Goergen, K. N. Barr, D. T. Huynh, J. R. Eastham-Anderson, G. Choi, M. Hedehus, R. L. Dalman, A. J. Connolly, C. A. Taylor, P. S. Tsao, and J. M. Greve, “In vivo quantification of murine aortic cyclic strain, motion, and curvature: implications for abdominal aortic aneurysm growth,” J. Magn. Reson. Imaging 32(4), 847–858 (2010).
[Crossref] [PubMed]

Damen, F. W.

F. W. Damen, A. R. Adelsperger, K. E. Wilson, and C. J. Goergen, “Comparison of traditional and integrated digital anesthetic vaporizers,” J. Am. Assoc. Lab. Anim. Sci. 54(6), 756–762 (2015).
[PubMed]

Dhillon, A. P.

T. J. Allen, A. Hall, A. P. Dhillon, J. S. Owen, and P. C. Beard, “Spectroscopic photoacoustic imaging of lipid-rich plaques in the human aorta in the 740 to 1400 nm wavelength range,” J. Biomed. Opt. 17(6), 061209 (2012).
[Crossref] [PubMed]

Diaz, J. A.

C. M. Alvarado, J. A. Diaz, A. E. Hawley, S. K. Wrobleski, R. E. Sigler, and D. D. Myers., “Male mice have increased thrombotic potential: sex differences in a mouse model of venous thrombosis,” Thromb. Res. 127(5), 478–486 (2011).
[Crossref] [PubMed]

Dou, W.

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-free bond-selective imaging by listening to vibrationally excited molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
[Crossref] [PubMed]

Eastham-Anderson, J. R.

C. J. Goergen, K. N. Barr, D. T. Huynh, J. R. Eastham-Anderson, G. Choi, M. Hedehus, R. L. Dalman, A. J. Connolly, C. A. Taylor, P. S. Tsao, and J. M. Greve, “In vivo quantification of murine aortic cyclic strain, motion, and curvature: implications for abdominal aortic aneurysm growth,” J. Magn. Reson. Imaging 32(4), 847–858 (2010).
[Crossref] [PubMed]

Flegal, K. M.

K. M. Flegal, M. D. Carroll, C. L. Ogden, and L. R. Curtin, “Prevalence and trends in obesity among US adults, 1999-2008,” JAMA 303(3), 235–241 (2010).
[Crossref] [PubMed]

Goergen, C. J.

R. Li, E. Phillips, P. Wang, C. J. Goergen, and J. X. Cheng, “Label-free in vivo imaging of peripheral nerve by multispectral photoacoustic tomography,” J. Biophotonics 9(1-2), 124–128 (2016).
[Crossref] [PubMed]

G. S. Sangha and C. J. Goergen, “Photoacoustic tomography: applications for atherosclerosis imaging,” J. Opt. 18(8), 084005 (2016).
[Crossref]

F. W. Damen, A. R. Adelsperger, K. E. Wilson, and C. J. Goergen, “Comparison of traditional and integrated digital anesthetic vaporizers,” J. Am. Assoc. Lab. Anim. Sci. 54(6), 756–762 (2015).
[PubMed]

E. H. Phillips, A. A. Yrineo, H. D. Schroeder, K. E. Wilson, J.-X. Cheng, and C. J. Goergen, “Morphological and biomechanical differences in the elastase and AngII apoE rodent models of abdominal aortic aneurysms,” BioMed research international 2015, 1–12 (2015).

C. J. Goergen, J. Azuma, K. N. Barr, L. Magdefessel, D. Y. Kallop, A. Gogineni, A. Grewall, R. M. Weimer, A. J. Connolly, R. L. Dalman, C. A. Taylor, P. S. Tsao, and J. M. Greve, “Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms,” Arterioscler. Thromb. Vasc. Biol. 31(2), 270–279 (2011).
[Crossref] [PubMed]

C. J. Goergen, K. N. Barr, D. T. Huynh, J. R. Eastham-Anderson, G. Choi, M. Hedehus, R. L. Dalman, A. J. Connolly, C. A. Taylor, P. S. Tsao, and J. M. Greve, “In vivo quantification of murine aortic cyclic strain, motion, and curvature: implications for abdominal aortic aneurysm growth,” J. Magn. Reson. Imaging 32(4), 847–858 (2010).
[Crossref] [PubMed]

Gogineni, A.

C. J. Goergen, J. Azuma, K. N. Barr, L. Magdefessel, D. Y. Kallop, A. Gogineni, A. Grewall, R. M. Weimer, A. J. Connolly, R. L. Dalman, C. A. Taylor, P. S. Tsao, and J. M. Greve, “Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms,” Arterioscler. Thromb. Vasc. Biol. 31(2), 270–279 (2011).
[Crossref] [PubMed]

Greve, J. M.

C. J. Goergen, J. Azuma, K. N. Barr, L. Magdefessel, D. Y. Kallop, A. Gogineni, A. Grewall, R. M. Weimer, A. J. Connolly, R. L. Dalman, C. A. Taylor, P. S. Tsao, and J. M. Greve, “Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms,” Arterioscler. Thromb. Vasc. Biol. 31(2), 270–279 (2011).
[Crossref] [PubMed]

C. J. Goergen, K. N. Barr, D. T. Huynh, J. R. Eastham-Anderson, G. Choi, M. Hedehus, R. L. Dalman, A. J. Connolly, C. A. Taylor, P. S. Tsao, and J. M. Greve, “In vivo quantification of murine aortic cyclic strain, motion, and curvature: implications for abdominal aortic aneurysm growth,” J. Magn. Reson. Imaging 32(4), 847–858 (2010).
[Crossref] [PubMed]

Grewall, A.

C. J. Goergen, J. Azuma, K. N. Barr, L. Magdefessel, D. Y. Kallop, A. Gogineni, A. Grewall, R. M. Weimer, A. J. Connolly, R. L. Dalman, C. A. Taylor, P. S. Tsao, and J. M. Greve, “Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms,” Arterioscler. Thromb. Vasc. Biol. 31(2), 270–279 (2011).
[Crossref] [PubMed]

Hall, A.

T. J. Allen, A. Hall, A. P. Dhillon, J. S. Owen, and P. C. Beard, “Spectroscopic photoacoustic imaging of lipid-rich plaques in the human aorta in the 740 to 1400 nm wavelength range,” J. Biomed. Opt. 17(6), 061209 (2012).
[Crossref] [PubMed]

Hawley, A. E.

C. M. Alvarado, J. A. Diaz, A. E. Hawley, S. K. Wrobleski, R. E. Sigler, and D. D. Myers., “Male mice have increased thrombotic potential: sex differences in a mouse model of venous thrombosis,” Thromb. Res. 127(5), 478–486 (2011).
[Crossref] [PubMed]

Hedehus, M.

C. J. Goergen, K. N. Barr, D. T. Huynh, J. R. Eastham-Anderson, G. Choi, M. Hedehus, R. L. Dalman, A. J. Connolly, C. A. Taylor, P. S. Tsao, and J. M. Greve, “In vivo quantification of murine aortic cyclic strain, motion, and curvature: implications for abdominal aortic aneurysm growth,” J. Magn. Reson. Imaging 32(4), 847–858 (2010).
[Crossref] [PubMed]

Hu, S.

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-free bond-selective imaging by listening to vibrationally excited molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
[Crossref] [PubMed]

Huynh, D. T.

C. J. Goergen, K. N. Barr, D. T. Huynh, J. R. Eastham-Anderson, G. Choi, M. Hedehus, R. L. Dalman, A. J. Connolly, C. A. Taylor, P. S. Tsao, and J. M. Greve, “In vivo quantification of murine aortic cyclic strain, motion, and curvature: implications for abdominal aortic aneurysm growth,” J. Magn. Reson. Imaging 32(4), 847–858 (2010).
[Crossref] [PubMed]

Iozzo, P.

P. Iozzo, “Myocardial, perivascular, and epicardial fat,” Diabetes Care 34(Suppl 2), S371–S379 (2011).
[Crossref] [PubMed]

Kallop, D. Y.

C. J. Goergen, J. Azuma, K. N. Barr, L. Magdefessel, D. Y. Kallop, A. Gogineni, A. Grewall, R. M. Weimer, A. J. Connolly, R. L. Dalman, C. A. Taylor, P. S. Tsao, and J. M. Greve, “Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms,” Arterioscler. Thromb. Vasc. Biol. 31(2), 270–279 (2011).
[Crossref] [PubMed]

Li, R.

R. Li, E. Phillips, P. Wang, C. J. Goergen, and J. X. Cheng, “Label-free in vivo imaging of peripheral nerve by multispectral photoacoustic tomography,” J. Biophotonics 9(1-2), 124–128 (2016).
[Crossref] [PubMed]

Lucas, A. J.

A. J. Lucas, “Atherosclerosis,” Nature 407, 233–241 (2000).

Lucht, R.

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-free bond-selective imaging by listening to vibrationally excited molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
[Crossref] [PubMed]

Magdefessel, L.

C. J. Goergen, J. Azuma, K. N. Barr, L. Magdefessel, D. Y. Kallop, A. Gogineni, A. Grewall, R. M. Weimer, A. J. Connolly, R. L. Dalman, C. A. Taylor, P. S. Tsao, and J. M. Greve, “Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms,” Arterioscler. Thromb. Vasc. Biol. 31(2), 270–279 (2011).
[Crossref] [PubMed]

Myers, D. D.

C. M. Alvarado, J. A. Diaz, A. E. Hawley, S. K. Wrobleski, R. E. Sigler, and D. D. Myers., “Male mice have increased thrombotic potential: sex differences in a mouse model of venous thrombosis,” Thromb. Res. 127(5), 478–486 (2011).
[Crossref] [PubMed]

Nakashima, Y.

Y. Nakashima, A. S. Plump, E. W. Raines, J. L. Breslow, and R. Ross, “ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree,” Arterioscler. Thromb. 14(1), 133–140 (1994).
[Crossref] [PubMed]

Ogden, C. L.

K. M. Flegal, M. D. Carroll, C. L. Ogden, and L. R. Curtin, “Prevalence and trends in obesity among US adults, 1999-2008,” JAMA 303(3), 235–241 (2010).
[Crossref] [PubMed]

Owen, J. S.

T. J. Allen, A. Hall, A. P. Dhillon, J. S. Owen, and P. C. Beard, “Spectroscopic photoacoustic imaging of lipid-rich plaques in the human aorta in the 740 to 1400 nm wavelength range,” J. Biomed. Opt. 17(6), 061209 (2012).
[Crossref] [PubMed]

Phillips, E.

R. Li, E. Phillips, P. Wang, C. J. Goergen, and J. X. Cheng, “Label-free in vivo imaging of peripheral nerve by multispectral photoacoustic tomography,” J. Biophotonics 9(1-2), 124–128 (2016).
[Crossref] [PubMed]

Phillips, E. H.

E. H. Phillips, A. A. Yrineo, H. D. Schroeder, K. E. Wilson, J.-X. Cheng, and C. J. Goergen, “Morphological and biomechanical differences in the elastase and AngII apoE rodent models of abdominal aortic aneurysms,” BioMed research international 2015, 1–12 (2015).

Plump, A. S.

Y. Nakashima, A. S. Plump, E. W. Raines, J. L. Breslow, and R. Ross, “ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree,” Arterioscler. Thromb. 14(1), 133–140 (1994).
[Crossref] [PubMed]

Raines, E. W.

Y. Nakashima, A. S. Plump, E. W. Raines, J. L. Breslow, and R. Ross, “ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree,” Arterioscler. Thromb. 14(1), 133–140 (1994).
[Crossref] [PubMed]

Ross, R.

Y. Nakashima, A. S. Plump, E. W. Raines, J. L. Breslow, and R. Ross, “ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree,” Arterioscler. Thromb. 14(1), 133–140 (1994).
[Crossref] [PubMed]

Sangha, G. S.

G. S. Sangha and C. J. Goergen, “Photoacoustic tomography: applications for atherosclerosis imaging,” J. Opt. 18(8), 084005 (2016).
[Crossref]

Schroeder, H. D.

E. H. Phillips, A. A. Yrineo, H. D. Schroeder, K. E. Wilson, J.-X. Cheng, and C. J. Goergen, “Morphological and biomechanical differences in the elastase and AngII apoE rodent models of abdominal aortic aneurysms,” BioMed research international 2015, 1–12 (2015).

Sigler, R. E.

C. M. Alvarado, J. A. Diaz, A. E. Hawley, S. K. Wrobleski, R. E. Sigler, and D. D. Myers., “Male mice have increased thrombotic potential: sex differences in a mouse model of venous thrombosis,” Thromb. Res. 127(5), 478–486 (2011).
[Crossref] [PubMed]

Sturek, M.

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-free bond-selective imaging by listening to vibrationally excited molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
[Crossref] [PubMed]

Taylor, C. A.

C. J. Goergen, J. Azuma, K. N. Barr, L. Magdefessel, D. Y. Kallop, A. Gogineni, A. Grewall, R. M. Weimer, A. J. Connolly, R. L. Dalman, C. A. Taylor, P. S. Tsao, and J. M. Greve, “Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms,” Arterioscler. Thromb. Vasc. Biol. 31(2), 270–279 (2011).
[Crossref] [PubMed]

C. J. Goergen, K. N. Barr, D. T. Huynh, J. R. Eastham-Anderson, G. Choi, M. Hedehus, R. L. Dalman, A. J. Connolly, C. A. Taylor, P. S. Tsao, and J. M. Greve, “In vivo quantification of murine aortic cyclic strain, motion, and curvature: implications for abdominal aortic aneurysm growth,” J. Magn. Reson. Imaging 32(4), 847–858 (2010).
[Crossref] [PubMed]

Tsao, P. S.

C. J. Goergen, J. Azuma, K. N. Barr, L. Magdefessel, D. Y. Kallop, A. Gogineni, A. Grewall, R. M. Weimer, A. J. Connolly, R. L. Dalman, C. A. Taylor, P. S. Tsao, and J. M. Greve, “Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms,” Arterioscler. Thromb. Vasc. Biol. 31(2), 270–279 (2011).
[Crossref] [PubMed]

C. J. Goergen, K. N. Barr, D. T. Huynh, J. R. Eastham-Anderson, G. Choi, M. Hedehus, R. L. Dalman, A. J. Connolly, C. A. Taylor, P. S. Tsao, and J. M. Greve, “In vivo quantification of murine aortic cyclic strain, motion, and curvature: implications for abdominal aortic aneurysm growth,” J. Magn. Reson. Imaging 32(4), 847–858 (2010).
[Crossref] [PubMed]

Umulis, D.

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-free bond-selective imaging by listening to vibrationally excited molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
[Crossref] [PubMed]

Vernon, G.

G. Vernon, A. Baranova, and Z. M. Younossi, “Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults,” Aliment. Pharmacol. Ther. 34(3), 274–285 (2011).
[Crossref] [PubMed]

Wang, H.-W.

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-free bond-selective imaging by listening to vibrationally excited molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
[Crossref] [PubMed]

Wang, L. V.

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-free bond-selective imaging by listening to vibrationally excited molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
[Crossref] [PubMed]

Wang, P.

R. Li, E. Phillips, P. Wang, C. J. Goergen, and J. X. Cheng, “Label-free in vivo imaging of peripheral nerve by multispectral photoacoustic tomography,” J. Biophotonics 9(1-2), 124–128 (2016).
[Crossref] [PubMed]

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-free bond-selective imaging by listening to vibrationally excited molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
[Crossref] [PubMed]

Weimer, R. M.

C. J. Goergen, J. Azuma, K. N. Barr, L. Magdefessel, D. Y. Kallop, A. Gogineni, A. Grewall, R. M. Weimer, A. J. Connolly, R. L. Dalman, C. A. Taylor, P. S. Tsao, and J. M. Greve, “Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms,” Arterioscler. Thromb. Vasc. Biol. 31(2), 270–279 (2011).
[Crossref] [PubMed]

Wilson, K. E.

E. H. Phillips, A. A. Yrineo, H. D. Schroeder, K. E. Wilson, J.-X. Cheng, and C. J. Goergen, “Morphological and biomechanical differences in the elastase and AngII apoE rodent models of abdominal aortic aneurysms,” BioMed research international 2015, 1–12 (2015).

F. W. Damen, A. R. Adelsperger, K. E. Wilson, and C. J. Goergen, “Comparison of traditional and integrated digital anesthetic vaporizers,” J. Am. Assoc. Lab. Anim. Sci. 54(6), 756–762 (2015).
[PubMed]

Wrobleski, S. K.

C. M. Alvarado, J. A. Diaz, A. E. Hawley, S. K. Wrobleski, R. E. Sigler, and D. D. Myers., “Male mice have increased thrombotic potential: sex differences in a mouse model of venous thrombosis,” Thromb. Res. 127(5), 478–486 (2011).
[Crossref] [PubMed]

Younossi, Z. M.

G. Vernon, A. Baranova, and Z. M. Younossi, “Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults,” Aliment. Pharmacol. Ther. 34(3), 274–285 (2011).
[Crossref] [PubMed]

Yrineo, A. A.

E. H. Phillips, A. A. Yrineo, H. D. Schroeder, K. E. Wilson, J.-X. Cheng, and C. J. Goergen, “Morphological and biomechanical differences in the elastase and AngII apoE rodent models of abdominal aortic aneurysms,” BioMed research international 2015, 1–12 (2015).

Aliment. Pharmacol. Ther. (1)

G. Vernon, A. Baranova, and Z. M. Younossi, “Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults,” Aliment. Pharmacol. Ther. 34(3), 274–285 (2011).
[Crossref] [PubMed]

Arterioscler. Thromb. (1)

Y. Nakashima, A. S. Plump, E. W. Raines, J. L. Breslow, and R. Ross, “ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree,” Arterioscler. Thromb. 14(1), 133–140 (1994).
[Crossref] [PubMed]

Arterioscler. Thromb. Vasc. Biol. (1)

C. J. Goergen, J. Azuma, K. N. Barr, L. Magdefessel, D. Y. Kallop, A. Gogineni, A. Grewall, R. M. Weimer, A. J. Connolly, R. L. Dalman, C. A. Taylor, P. S. Tsao, and J. M. Greve, “Influences of aortic motion and curvature on vessel expansion in murine experimental aneurysms,” Arterioscler. Thromb. Vasc. Biol. 31(2), 270–279 (2011).
[Crossref] [PubMed]

BioMed research international (1)

E. H. Phillips, A. A. Yrineo, H. D. Schroeder, K. E. Wilson, J.-X. Cheng, and C. J. Goergen, “Morphological and biomechanical differences in the elastase and AngII apoE rodent models of abdominal aortic aneurysms,” BioMed research international 2015, 1–12 (2015).

Diabetes Care (1)

P. Iozzo, “Myocardial, perivascular, and epicardial fat,” Diabetes Care 34(Suppl 2), S371–S379 (2011).
[Crossref] [PubMed]

J. Am. Assoc. Lab. Anim. Sci. (1)

F. W. Damen, A. R. Adelsperger, K. E. Wilson, and C. J. Goergen, “Comparison of traditional and integrated digital anesthetic vaporizers,” J. Am. Assoc. Lab. Anim. Sci. 54(6), 756–762 (2015).
[PubMed]

J. Biomed. Opt. (1)

T. J. Allen, A. Hall, A. P. Dhillon, J. S. Owen, and P. C. Beard, “Spectroscopic photoacoustic imaging of lipid-rich plaques in the human aorta in the 740 to 1400 nm wavelength range,” J. Biomed. Opt. 17(6), 061209 (2012).
[Crossref] [PubMed]

J. Biophotonics (1)

R. Li, E. Phillips, P. Wang, C. J. Goergen, and J. X. Cheng, “Label-free in vivo imaging of peripheral nerve by multispectral photoacoustic tomography,” J. Biophotonics 9(1-2), 124–128 (2016).
[Crossref] [PubMed]

J. Magn. Reson. Imaging (1)

C. J. Goergen, K. N. Barr, D. T. Huynh, J. R. Eastham-Anderson, G. Choi, M. Hedehus, R. L. Dalman, A. J. Connolly, C. A. Taylor, P. S. Tsao, and J. M. Greve, “In vivo quantification of murine aortic cyclic strain, motion, and curvature: implications for abdominal aortic aneurysm growth,” J. Magn. Reson. Imaging 32(4), 847–858 (2010).
[Crossref] [PubMed]

J. Opt. (1)

G. S. Sangha and C. J. Goergen, “Photoacoustic tomography: applications for atherosclerosis imaging,” J. Opt. 18(8), 084005 (2016).
[Crossref]

JAMA (1)

K. M. Flegal, M. D. Carroll, C. L. Ogden, and L. R. Curtin, “Prevalence and trends in obesity among US adults, 1999-2008,” JAMA 303(3), 235–241 (2010).
[Crossref] [PubMed]

Nature (1)

A. J. Lucas, “Atherosclerosis,” Nature 407, 233–241 (2000).

Phys. Rev. Lett. (1)

H.-W. Wang, N. Chai, P. Wang, S. Hu, W. Dou, D. Umulis, L. V. Wang, M. Sturek, R. Lucht, and J.-X. Cheng, “Label-free bond-selective imaging by listening to vibrationally excited molecules,” Phys. Rev. Lett. 106(23), 238106 (2011).
[Crossref] [PubMed]

Thromb. Res. (1)

C. M. Alvarado, J. A. Diaz, A. E. Hawley, S. K. Wrobleski, R. E. Sigler, and D. D. Myers., “Male mice have increased thrombotic potential: sex differences in a mouse model of venous thrombosis,” Thromb. Res. 127(5), 478–486 (2011).
[Crossref] [PubMed]

Other (1)

K. Flurkey, J. M. Currer, and D. E. Harrison, “Mouse models in aging research,” in The Mouse in Biomedical Research (Elsevier, 2007).

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Figures (5)

Fig. 1
Fig. 1

Schematic depicting PAT setup. Nd:YAG OPO laser delivered light through a fiber optic bundle to an anesthetized mouse. A 40 MHz center frequency transducer was used to acquire the resulting PAT signal. A function generator coordinated pulse excitation and image acquisition between the laser and the Vevo2100 ultrasound system. A pulse generator was used to synchronize the trigger of the laser with the ultrasound system. The ultrasound transducer face is 20x5 mm and fiber optic bundle face is 12x2 mm.

Fig. 2
Fig. 2

Ultrasound (left), lipid PAT (middle), and blood PAT (right) images of adult male apoE−/− (top) and WT (bottom) mice. Images are shown such that the animals are orientated in supine position with the head located to the left and tail is located to the right. Greater periaortic fat signal is evident in the apoE−/− mouse compared to the WT mouse. Using these images we can clearly discriminate the infrarenal aorta (red dotted outline), subcutaneous fat (white arrows), periaortic fat (orange arrows), and blood (red arrows).

Fig. 3
Fig. 3

Averaged PAT image (1210 nm) reveals subcutaneous and periaortic fat (A). Histogram of PAT pixel intensities shows peaks for background and lipid signal (B). Gray arrow represents threshold point used to create PAT mask, which is overlaid on the original PAT image to confirm thresholding accuracy (C). Plot profile analysis was used to measure periaortic thickness at multiple locations (D). Width of top peak (SV) represents subcutaneous and visceral fat and width of bottom peak (P) represents periaortic fat from one plot profile measurement (E). ORO staining on excised aorta confirms periaortic fat accumulation(F).

Fig. 4
Fig. 4

Three representative raw 1210 nm PAT and measurement images (A-C) and mean (D) image of an apoE−/− mouse. Measurements were taken in same location in all images.

Fig. 5
Fig. 5

Periaortic thickness values in apoE−/− and WT groups. Adult male apoE−/− mice have significantly higher periaortic thickness compared to other groups (p<0.05).

Tables (1)

Tables Icon

Table 1 Summary of the Characteristics for Experimental Mouse Groups

Metrics