Abstract

Cardiovascular disease typically is associated with dysfunction of the coronary vasculature and microvasculature. The study of cardiovascular disease typically involves imaging of the large coronary vessels and quantification of cardiac blood perfusion. These methods, however, are not well suited for imaging of the cardiac microvasculature. We used the optical histology method, which combines chemical optical clearing and optical imaging, to create high-resolution, wide-field maps of the cardiac microvasculature in ventral slices of mouse heart. We have demonstrated the ability of the optical histology method to enable wide-field visualization of the cardiac microvasculature in high-resolution and anticipate that optical histology may have significant impact in studying cardiovascular disease.

© 2013 Optical Society of America

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2013 (5)

A. S. Go, D. Mozaffarian, V. L. Roger, E. J. Benjamin, J. D. Berry, W. B. Borden, D. M. Bravata, S. Dai, E. S. Ford, C. S. Fox, S. Franco, H. J. Fullerton, C. Gillespie, S. M. Hailpern, J. A. Heit, V. J. Howard, M. D. Huffman, B. M. Kissela, S. J. Kittner, D. T. Lackland, J. H. Lichtman, L. D. Lisabeth, D. Magid, G. M. Marcus, A. Marelli, D. B. Matchar, D. K. McGuire, E. R. Mohler, C. S. Moy, M. E. Mussolino, G. Nichol, N. P. Paynter, P. J. Schreiner, P. D. Sorlie, J. Stein, T. N. Turan, S. S. Virani, N. D. Wong, D. Woo, M. B. Turner, and American Heart Association Statistics Committee and Stroke Statistics Subcommittee, “Heart disease and stroke statistics--2013 update: a report from the American Heart Association,” Circulation 127(1), e6–e245 (2013).
[Crossref] [PubMed]

J. Nam, I. Onitsuka, J. Hatch, Y. Uchida, S. Ray, S. Huang, W. Li, H. Zang, P. Ruiz-Lozano, and Y. S. Mukouyama, “Coronary veins determine the pattern of sympathetic innervation in the developing heart,” Development 140(7), 1475–1485 (2013).
[Crossref] [PubMed]

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]

A. J. Moy, M. P. Wiersma, and B. Choi, “Optical histology: a method to visualize microvasculature in thick tissue sections of mouse brain,” PLoS ONE 8(1), e53753 (2013).
[Crossref] [PubMed]

R. K. Jain, L. L. Munn, and D. Fukumura, “Measuring angiogenesis and hemodynamics in mice,” Cold Spring Harb Protoc 2013(4), 354–358 (2013).
[Crossref] [PubMed]

2012 (4)

S. Lee, C. Vinegoni, P. F. Feruglio, L. Fexon, R. Gorbatov, M. Pivoravov, A. Sbarbati, M. Nahrendorf, and R. Weissleder, “Real-time in vivo imaging of the beating mouse heart at microscopic resolution,” Nat Commun 3, 1054 (2012).
[Crossref] [PubMed]

Y. S. Mukouyama, J. James, J. Nam, and Y. Uchida, “Whole-mount confocal microscopy for vascular branching morphogenesis,” Methods Mol. Biol. 843, 69–78 (2012).
[Crossref] [PubMed]

J. Herrmann, J. C. Kaski, and A. Lerman, “Coronary microvascular dysfunction in the clinical setting: from mystery to reality,” Eur. Heart J. 33(22), 2771–2782 (2012).
[Crossref] [PubMed]

H. M. Arthur, P. Campbell, P. J. Harvey, M. McGillion, P. Oh, E. Woodburn, and C. Hodgson, “Women, cardiac syndrome X, and microvascular heart disease,” Can. J. Cardiol. 28(2Suppl), S42–S49 (2012).
[Crossref] [PubMed]

2011 (4)

F. Leuschner and M. Nahrendorf, “Molecular imaging of coronary atherosclerosis and myocardial infarction: considerations for the bench and perspectives for the clinic,” Circ. Res. 108(5), 593–606 (2011).
[Crossref] [PubMed]

I. Y. Chen and J. C. Wu, “Cardiovascular molecular imaging: focus on clinical translation,” Circulation 123(4), 425–443 (2011).
[Crossref] [PubMed]

G. M. Kazanskaia, A. M. Volkov, T. M. D’iakonitsa, and A. M. Karas’kova, “Ultrastructure of coronary microvessels in conditions of heart reperfusion following prolonged ischemia while applying various methods of artificial hypothermia,” Tsitologiia 53(12), 968–977 (2011).
[PubMed]

S. M. White, S. C. George, and B. Choi, “Automated computation of functional vascular density using laser speckle imaging in a rodent window chamber model,” Microvasc. Res. 82(1), 92–95 (2011).
[Crossref] [PubMed]

2010 (2)

G. A. Lanza and F. Crea, “Primary coronary microvascular dysfunction: clinical presentation, pathophysiology, and management,” Circulation 121(21), 2317–2325 (2010).
[Crossref] [PubMed]

T. H. Schindler, H. R. Schelbert, A. Quercioli, and V. Dilsizian, “Cardiac PET imaging for the detection and monitoring of coronary artery disease and microvascular health,” JACC Cardiovasc. Imaging 3(6), 623–640 (2010).
[Crossref] [PubMed]

2009 (1)

R. Nijveldt, M. B. Hofman, A. Hirsch, A. M. Beek, V. A. Umans, P. R. Algra, J. J. Piek, and A. C. van Rossum, “Assessment of microvascular obstruction and prediction of short-term remodeling after acute myocardial infarction: cardiac MR imaging study,” Radiology 250(2), 363–370 (2009).
[Crossref] [PubMed]

2008 (4)

Y. Li, Y. Song, L. Zhao, G. Gaidosh, A. M. Laties, and R. Wen, “Direct labeling and visualization of blood vessels with lipophilic carbocyanine dye DiI,” Nat. Protoc. 3(11), 1703–1708 (2008).
[Crossref] [PubMed]

J. W. Verjans, D. Lovhaug, N. Narula, A. D. Petrov, B. Indrevoll, E. Bjurgert, T. B. Krasieva, L. B. Petersen, G. M. Kindberg, M. Solbakken, A. Cuthbertson, M. A. Vannan, C. P. Reutelingsperger, B. J. Tromberg, L. Hofstra, and J. Narula, “Noninvasive imaging of angiotensin receptors after myocardial infarction,” JACC Cardiovasc. Imaging 1(3), 354–362 (2008).
[Crossref] [PubMed]

A. R. Pries, H. Habazettl, G. Ambrosio, P. R. Hansen, J. C. Kaski, V. Schächinger, H. Tillmanns, G. Vassalli, I. Tritto, M. Weis, C. de Wit, and R. Bugiardini, “A review of methods for assessment of coronary microvascular disease in both clinical and experimental settings,” Cardiovasc. Res. 80(2), 165–174 (2008).
[Crossref] [PubMed]

J. A. Scherschel and M. Rubart, “Cardiovascular imaging using two-photon microscopy,” Microsc. Microanal. 14(6), 492–506 (2008).
[Crossref] [PubMed]

2007 (1)

P. G. Camici and F. Crea, “Coronary microvascular dysfunction,” N. Engl. J. Med. 356(8), 830–840 (2007).
[Crossref] [PubMed]

2006 (2)

A. C. Lardo, M. A. Cordeiro, C. Silva, L. C. Amado, R. T. George, A. P. Saliaris, K. H. Schuleri, V. R. Fernandes, M. Zviman, S. Nazarian, H. R. Halperin, K. C. Wu, J. M. Hare, and J. A. Lima, “Contrast-enhanced multidetector computed tomography viability imaging after myocardial infarction: characterization of myocyte death, microvascular obstruction, and chronic scar,” Circulation 113(3), 394–404 (2006).
[Crossref] [PubMed]

J. C. Russell and S. D. Proctor, “Small animal models of cardiovascular disease: tools for the study of the roles of metabolic syndrome, dyslipidemia, and atherosclerosis,” Cardiovasc. Pathol. 15(6), 318–330 (2006).
[Crossref] [PubMed]

2005 (1)

D. J. Ravnic, X. Jiang, T. Wolloscheck, J. P. Pratt, H. Huss, S. J. Mentzer, and M. A. Konerding, “Vessel painting of the microcirculation using fluorescent lipophilic tracers,” Microvasc. Res. 70(1-2), 90–96 (2005).
[Crossref] [PubMed]

2002 (3)

C. A. Molyneux, M. C. Glyn, and B. J. Ward, “Oxidative stress and cardiac microvascular structure in ischemia and reperfusion: the protective effect of antioxidant vitamins,” Microvasc. Res. 64(2), 265–277 (2002).
[Crossref] [PubMed]

J. R. Panting, P. D. Gatehouse, G. Z. Yang, F. Grothues, D. N. Firmin, P. Collins, and D. J. Pennell, “Abnormal subendocardial perfusion in cardiac syndrome X detected by cardiovascular magnetic resonance imaging,” N. Engl. J. Med. 346(25), 1948–1953 (2002).
[Crossref] [PubMed]

J. C. Kaski, “Overview of gender aspects of cardiac syndrome X,” Cardiovasc. Res. 53(3), 620–626 (2002).
[Crossref] [PubMed]

2001 (2)

S. E. Reis, R. Holubkov, A. J. Conrad Smith, S. F. Kelsey, B. L. Sharaf, N. Reichek, W. J. Rogers, C. N. Merz, G. Sopko, C. J. Pepine, and WISE Investigators, “Coronary microvascular dysfunction is highly prevalent in women with chest pain in the absence of coronary artery disease: results from the NHLBI WISE study,” Am. Heart J. 141(5), 735–741 (2001).
[Crossref] [PubMed]

K. Rakusan, N. Cicutti, and F. Kolar, “Cardiac function, microvascular structure, and capillary hematocrit in hearts of polycythemic rats,” Am. J. Physiol. Heart Circ. Physiol. 281(6), H2425–H2431 (2001).
[PubMed]

1998 (1)

K. Wei, A. R. Jayaweera, S. Firoozan, A. Linka, D. M. Skyba, and S. Kaul, “Quantification of myocardial blood flow with ultrasound-induced destruction of microbubbles administered as a constant venous infusion,” Circulation 97(5), 473–483 (1998).
[Crossref] [PubMed]

1992 (1)

D. Eitzman, Z. al-Aouar, H. L. Kanter, J. vom Dahl, M. Kirsh, G. M. Deeb, and M. Schwaiger, “Clinical outcome of patients with advanced coronary artery disease after viability studies with positron emission tomography,” J. Am. Coll. Cardiol. 20(3), 559–565 (1992).
[Crossref] [PubMed]

1991 (2)

S. E. Nissen, J. C. Gurley, C. L. Grines, D. C. Booth, R. McClure, M. Berk, C. Fischer, and A. N. DeMaria, “Intravascular ultrasound assessment of lumen size and wall morphology in normal subjects and patients with coronary artery disease,” Circulation 84(3), 1087–1099 (1991).
[Crossref] [PubMed]

J. M. Tobis, J. Mallery, D. Mahon, K. Lehmann, P. Zalesky, J. Griffith, J. Gessert, M. Moriuchi, M. McRae, and M. L. Dwyer, “Intravascular ultrasound imaging of human coronary arteries in vivo. Analysis of tissue characterizations with comparison to in vitro histological specimens,” Circulation 83(3), 913–926 (1991).
[Crossref] [PubMed]

1990 (1)

B. N. Potkin, A. L. Bartorelli, J. M. Gessert, R. F. Neville, Y. Almagor, W. C. Roberts, and M. B. Leon, “Coronary artery imaging with intravascular high-frequency ultrasound,” Circulation 81(5), 1575–1585 (1990).
[Crossref] [PubMed]

1988 (2)

E. A. Zerhouni, D. M. Parish, W. J. Rogers, A. Yang, and E. P. Shapiro, “Human heart: tagging with MR imaging--a method for noninvasive assessment of myocardial motion,” Radiology 169(1), 59–63 (1988).
[PubMed]

J. E. Brush, R. O. Cannon, W. H. Schenke, R. O. Bonow, M. B. Leon, B. J. Maron, and S. E. Epstein, “Angina due to coronary microvascular disease in hypertensive patients without left ventricular hypertrophy,” N. Engl. J. Med. 319(20), 1302–1307 (1988).
[Crossref] [PubMed]

1986 (1)

K. L. Gould, R. A. Goldstein, N. A. Mullani, R. L. Kirkeeide, W. H. Wong, T. J. Tewson, M. S. Berridge, L. A. Bolomey, R. K. Hartz, R. W. Smalling, F. Fuentes, and A. Nishikawa, “Noninvasive assessment of coronary stenoses by myocardial perfusion imaging during pharmacologic coronary vasodilation. VIII. Clinical feasibility of positron cardiac imaging without a cyclotron using generator-produced rubidium-82,” J. Am. Coll. Cardiol. 7(4), 775–789 (1986).
[Crossref] [PubMed]

1982 (1)

E. M. Geltman, D. Biello, M. J. Welch, M. M. Ter-Pogossian, R. Roberts, and B. E. Sobel, “Characterization of nontransmural myocardial infarction by positron-emission tomography,” Circulation 65(4), 747–755 (1982).
[Crossref] [PubMed]

1966 (1)

W. L. Proudfit, E. K. Shirey, and F. M. Sones., “Selective cine coronary arteriography. Correlation with clinical findings in 1,000 patients,” Circulation 33(6), 901–910 (1966).
[Crossref] [PubMed]

al-Aouar, Z.

D. Eitzman, Z. al-Aouar, H. L. Kanter, J. vom Dahl, M. Kirsh, G. M. Deeb, and M. Schwaiger, “Clinical outcome of patients with advanced coronary artery disease after viability studies with positron emission tomography,” J. Am. Coll. Cardiol. 20(3), 559–565 (1992).
[Crossref] [PubMed]

Algra, P. R.

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J. Herrmann, J. C. Kaski, and A. Lerman, “Coronary microvascular dysfunction in the clinical setting: from mystery to reality,” Eur. Heart J. 33(22), 2771–2782 (2012).
[Crossref] [PubMed]

A. R. Pries, H. Habazettl, G. Ambrosio, P. R. Hansen, J. C. Kaski, V. Schächinger, H. Tillmanns, G. Vassalli, I. Tritto, M. Weis, C. de Wit, and R. Bugiardini, “A review of methods for assessment of coronary microvascular disease in both clinical and experimental settings,” Cardiovasc. Res. 80(2), 165–174 (2008).
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J. C. Kaski, “Overview of gender aspects of cardiac syndrome X,” Cardiovasc. Res. 53(3), 620–626 (2002).
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K. Wei, A. R. Jayaweera, S. Firoozan, A. Linka, D. M. Skyba, and S. Kaul, “Quantification of myocardial blood flow with ultrasound-induced destruction of microbubbles administered as a constant venous infusion,” Circulation 97(5), 473–483 (1998).
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G. M. Kazanskaia, A. M. Volkov, T. M. D’iakonitsa, and A. M. Karas’kova, “Ultrastructure of coronary microvessels in conditions of heart reperfusion following prolonged ischemia while applying various methods of artificial hypothermia,” Tsitologiia 53(12), 968–977 (2011).
[PubMed]

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S. E. Reis, R. Holubkov, A. J. Conrad Smith, S. F. Kelsey, B. L. Sharaf, N. Reichek, W. J. Rogers, C. N. Merz, G. Sopko, C. J. Pepine, and WISE Investigators, “Coronary microvascular dysfunction is highly prevalent in women with chest pain in the absence of coronary artery disease: results from the NHLBI WISE study,” Am. Heart J. 141(5), 735–741 (2001).
[Crossref] [PubMed]

Kindberg, G. M.

J. W. Verjans, D. Lovhaug, N. Narula, A. D. Petrov, B. Indrevoll, E. Bjurgert, T. B. Krasieva, L. B. Petersen, G. M. Kindberg, M. Solbakken, A. Cuthbertson, M. A. Vannan, C. P. Reutelingsperger, B. J. Tromberg, L. Hofstra, and J. Narula, “Noninvasive imaging of angiotensin receptors after myocardial infarction,” JACC Cardiovasc. Imaging 1(3), 354–362 (2008).
[Crossref] [PubMed]

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K. L. Gould, R. A. Goldstein, N. A. Mullani, R. L. Kirkeeide, W. H. Wong, T. J. Tewson, M. S. Berridge, L. A. Bolomey, R. K. Hartz, R. W. Smalling, F. Fuentes, and A. Nishikawa, “Noninvasive assessment of coronary stenoses by myocardial perfusion imaging during pharmacologic coronary vasodilation. VIII. Clinical feasibility of positron cardiac imaging without a cyclotron using generator-produced rubidium-82,” J. Am. Coll. Cardiol. 7(4), 775–789 (1986).
[Crossref] [PubMed]

Kirsh, M.

D. Eitzman, Z. al-Aouar, H. L. Kanter, J. vom Dahl, M. Kirsh, G. M. Deeb, and M. Schwaiger, “Clinical outcome of patients with advanced coronary artery disease after viability studies with positron emission tomography,” J. Am. Coll. Cardiol. 20(3), 559–565 (1992).
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A. S. Go, D. Mozaffarian, V. L. Roger, E. J. Benjamin, J. D. Berry, W. B. Borden, D. M. Bravata, S. Dai, E. S. Ford, C. S. Fox, S. Franco, H. J. Fullerton, C. Gillespie, S. M. Hailpern, J. A. Heit, V. J. Howard, M. D. Huffman, B. M. Kissela, S. J. Kittner, D. T. Lackland, J. H. Lichtman, L. D. Lisabeth, D. Magid, G. M. Marcus, A. Marelli, D. B. Matchar, D. K. McGuire, E. R. Mohler, C. S. Moy, M. E. Mussolino, G. Nichol, N. P. Paynter, P. J. Schreiner, P. D. Sorlie, J. Stein, T. N. Turan, S. S. Virani, N. D. Wong, D. Woo, M. B. Turner, and American Heart Association Statistics Committee and Stroke Statistics Subcommittee, “Heart disease and stroke statistics--2013 update: a report from the American Heart Association,” Circulation 127(1), e6–e245 (2013).
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A. S. Go, D. Mozaffarian, V. L. Roger, E. J. Benjamin, J. D. Berry, W. B. Borden, D. M. Bravata, S. Dai, E. S. Ford, C. S. Fox, S. Franco, H. J. Fullerton, C. Gillespie, S. M. Hailpern, J. A. Heit, V. J. Howard, M. D. Huffman, B. M. Kissela, S. J. Kittner, D. T. Lackland, J. H. Lichtman, L. D. Lisabeth, D. Magid, G. M. Marcus, A. Marelli, D. B. Matchar, D. K. McGuire, E. R. Mohler, C. S. Moy, M. E. Mussolino, G. Nichol, N. P. Paynter, P. J. Schreiner, P. D. Sorlie, J. Stein, T. N. Turan, S. S. Virani, N. D. Wong, D. Woo, M. B. Turner, and American Heart Association Statistics Committee and Stroke Statistics Subcommittee, “Heart disease and stroke statistics--2013 update: a report from the American Heart Association,” Circulation 127(1), e6–e245 (2013).
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K. Rakusan, N. Cicutti, and F. Kolar, “Cardiac function, microvascular structure, and capillary hematocrit in hearts of polycythemic rats,” Am. J. Physiol. Heart Circ. Physiol. 281(6), H2425–H2431 (2001).
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Konerding, M. A.

D. J. Ravnic, X. Jiang, T. Wolloscheck, J. P. Pratt, H. Huss, S. J. Mentzer, and M. A. Konerding, “Vessel painting of the microcirculation using fluorescent lipophilic tracers,” Microvasc. Res. 70(1-2), 90–96 (2005).
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A. C. Lardo, M. A. Cordeiro, C. Silva, L. C. Amado, R. T. George, A. P. Saliaris, K. H. Schuleri, V. R. Fernandes, M. Zviman, S. Nazarian, H. R. Halperin, K. C. Wu, J. M. Hare, and J. A. Lima, “Contrast-enhanced multidetector computed tomography viability imaging after myocardial infarction: characterization of myocyte death, microvascular obstruction, and chronic scar,” Circulation 113(3), 394–404 (2006).
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B. N. Potkin, A. L. Bartorelli, J. M. Gessert, R. F. Neville, Y. Almagor, W. C. Roberts, and M. B. Leon, “Coronary artery imaging with intravascular high-frequency ultrasound,” Circulation 81(5), 1575–1585 (1990).
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A. S. Go, D. Mozaffarian, V. L. Roger, E. J. Benjamin, J. D. Berry, W. B. Borden, D. M. Bravata, S. Dai, E. S. Ford, C. S. Fox, S. Franco, H. J. Fullerton, C. Gillespie, S. M. Hailpern, J. A. Heit, V. J. Howard, M. D. Huffman, B. M. Kissela, S. J. Kittner, D. T. Lackland, J. H. Lichtman, L. D. Lisabeth, D. Magid, G. M. Marcus, A. Marelli, D. B. Matchar, D. K. McGuire, E. R. Mohler, C. S. Moy, M. E. Mussolino, G. Nichol, N. P. Paynter, P. J. Schreiner, P. D. Sorlie, J. Stein, T. N. Turan, S. S. Virani, N. D. Wong, D. Woo, M. B. Turner, and American Heart Association Statistics Committee and Stroke Statistics Subcommittee, “Heart disease and stroke statistics--2013 update: a report from the American Heart Association,” Circulation 127(1), e6–e245 (2013).
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R. Nijveldt, M. B. Hofman, A. Hirsch, A. M. Beek, V. A. Umans, P. R. Algra, J. J. Piek, and A. C. van Rossum, “Assessment of microvascular obstruction and prediction of short-term remodeling after acute myocardial infarction: cardiac MR imaging study,” Radiology 250(2), 363–370 (2009).
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K. L. Gould, R. A. Goldstein, N. A. Mullani, R. L. Kirkeeide, W. H. Wong, T. J. Tewson, M. S. Berridge, L. A. Bolomey, R. K. Hartz, R. W. Smalling, F. Fuentes, and A. Nishikawa, “Noninvasive assessment of coronary stenoses by myocardial perfusion imaging during pharmacologic coronary vasodilation. VIII. Clinical feasibility of positron cardiac imaging without a cyclotron using generator-produced rubidium-82,” J. Am. Coll. Cardiol. 7(4), 775–789 (1986).
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S. E. Nissen, J. C. Gurley, C. L. Grines, D. C. Booth, R. McClure, M. Berk, C. Fischer, and A. N. DeMaria, “Intravascular ultrasound assessment of lumen size and wall morphology in normal subjects and patients with coronary artery disease,” Circulation 84(3), 1087–1099 (1991).
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H. M. Arthur, P. Campbell, P. J. Harvey, M. McGillion, P. Oh, E. Woodburn, and C. Hodgson, “Women, cardiac syndrome X, and microvascular heart disease,” Can. J. Cardiol. 28(2Suppl), S42–S49 (2012).
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J. Nam, I. Onitsuka, J. Hatch, Y. Uchida, S. Ray, S. Huang, W. Li, H. Zang, P. Ruiz-Lozano, and Y. S. Mukouyama, “Coronary veins determine the pattern of sympathetic innervation in the developing heart,” Development 140(7), 1475–1485 (2013).
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J. R. Panting, P. D. Gatehouse, G. Z. Yang, F. Grothues, D. N. Firmin, P. Collins, and D. J. Pennell, “Abnormal subendocardial perfusion in cardiac syndrome X detected by cardiovascular magnetic resonance imaging,” N. Engl. J. Med. 346(25), 1948–1953 (2002).
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E. A. Zerhouni, D. M. Parish, W. J. Rogers, A. Yang, and E. P. Shapiro, “Human heart: tagging with MR imaging--a method for noninvasive assessment of myocardial motion,” Radiology 169(1), 59–63 (1988).
[PubMed]

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A. S. Go, D. Mozaffarian, V. L. Roger, E. J. Benjamin, J. D. Berry, W. B. Borden, D. M. Bravata, S. Dai, E. S. Ford, C. S. Fox, S. Franco, H. J. Fullerton, C. Gillespie, S. M. Hailpern, J. A. Heit, V. J. Howard, M. D. Huffman, B. M. Kissela, S. J. Kittner, D. T. Lackland, J. H. Lichtman, L. D. Lisabeth, D. Magid, G. M. Marcus, A. Marelli, D. B. Matchar, D. K. McGuire, E. R. Mohler, C. S. Moy, M. E. Mussolino, G. Nichol, N. P. Paynter, P. J. Schreiner, P. D. Sorlie, J. Stein, T. N. Turan, S. S. Virani, N. D. Wong, D. Woo, M. B. Turner, and American Heart Association Statistics Committee and Stroke Statistics Subcommittee, “Heart disease and stroke statistics--2013 update: a report from the American Heart Association,” Circulation 127(1), e6–e245 (2013).
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J. R. Panting, P. D. Gatehouse, G. Z. Yang, F. Grothues, D. N. Firmin, P. Collins, and D. J. Pennell, “Abnormal subendocardial perfusion in cardiac syndrome X detected by cardiovascular magnetic resonance imaging,” N. Engl. J. Med. 346(25), 1948–1953 (2002).
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S. E. Reis, R. Holubkov, A. J. Conrad Smith, S. F. Kelsey, B. L. Sharaf, N. Reichek, W. J. Rogers, C. N. Merz, G. Sopko, C. J. Pepine, and WISE Investigators, “Coronary microvascular dysfunction is highly prevalent in women with chest pain in the absence of coronary artery disease: results from the NHLBI WISE study,” Am. Heart J. 141(5), 735–741 (2001).
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J. W. Verjans, D. Lovhaug, N. Narula, A. D. Petrov, B. Indrevoll, E. Bjurgert, T. B. Krasieva, L. B. Petersen, G. M. Kindberg, M. Solbakken, A. Cuthbertson, M. A. Vannan, C. P. Reutelingsperger, B. J. Tromberg, L. Hofstra, and J. Narula, “Noninvasive imaging of angiotensin receptors after myocardial infarction,” JACC Cardiovasc. Imaging 1(3), 354–362 (2008).
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J. W. Verjans, D. Lovhaug, N. Narula, A. D. Petrov, B. Indrevoll, E. Bjurgert, T. B. Krasieva, L. B. Petersen, G. M. Kindberg, M. Solbakken, A. Cuthbertson, M. A. Vannan, C. P. Reutelingsperger, B. J. Tromberg, L. Hofstra, and J. Narula, “Noninvasive imaging of angiotensin receptors after myocardial infarction,” JACC Cardiovasc. Imaging 1(3), 354–362 (2008).
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R. Nijveldt, M. B. Hofman, A. Hirsch, A. M. Beek, V. A. Umans, P. R. Algra, J. J. Piek, and A. C. van Rossum, “Assessment of microvascular obstruction and prediction of short-term remodeling after acute myocardial infarction: cardiac MR imaging study,” Radiology 250(2), 363–370 (2009).
[Crossref] [PubMed]

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S. Lee, C. Vinegoni, P. F. Feruglio, L. Fexon, R. Gorbatov, M. Pivoravov, A. Sbarbati, M. Nahrendorf, and R. Weissleder, “Real-time in vivo imaging of the beating mouse heart at microscopic resolution,” Nat Commun 3, 1054 (2012).
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B. N. Potkin, A. L. Bartorelli, J. M. Gessert, R. F. Neville, Y. Almagor, W. C. Roberts, and M. B. Leon, “Coronary artery imaging with intravascular high-frequency ultrasound,” Circulation 81(5), 1575–1585 (1990).
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D. J. Ravnic, X. Jiang, T. Wolloscheck, J. P. Pratt, H. Huss, S. J. Mentzer, and M. A. Konerding, “Vessel painting of the microcirculation using fluorescent lipophilic tracers,” Microvasc. Res. 70(1-2), 90–96 (2005).
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A. R. Pries, H. Habazettl, G. Ambrosio, P. R. Hansen, J. C. Kaski, V. Schächinger, H. Tillmanns, G. Vassalli, I. Tritto, M. Weis, C. de Wit, and R. Bugiardini, “A review of methods for assessment of coronary microvascular disease in both clinical and experimental settings,” Cardiovasc. Res. 80(2), 165–174 (2008).
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Proctor, S. D.

J. C. Russell and S. D. Proctor, “Small animal models of cardiovascular disease: tools for the study of the roles of metabolic syndrome, dyslipidemia, and atherosclerosis,” Cardiovasc. Pathol. 15(6), 318–330 (2006).
[Crossref] [PubMed]

Proudfit, W. L.

W. L. Proudfit, E. K. Shirey, and F. M. Sones., “Selective cine coronary arteriography. Correlation with clinical findings in 1,000 patients,” Circulation 33(6), 901–910 (1966).
[Crossref] [PubMed]

Quercioli, A.

T. H. Schindler, H. R. Schelbert, A. Quercioli, and V. Dilsizian, “Cardiac PET imaging for the detection and monitoring of coronary artery disease and microvascular health,” JACC Cardiovasc. Imaging 3(6), 623–640 (2010).
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K. Rakusan, N. Cicutti, and F. Kolar, “Cardiac function, microvascular structure, and capillary hematocrit in hearts of polycythemic rats,” Am. J. Physiol. Heart Circ. Physiol. 281(6), H2425–H2431 (2001).
[PubMed]

Ravnic, D. J.

D. J. Ravnic, X. Jiang, T. Wolloscheck, J. P. Pratt, H. Huss, S. J. Mentzer, and M. A. Konerding, “Vessel painting of the microcirculation using fluorescent lipophilic tracers,” Microvasc. Res. 70(1-2), 90–96 (2005).
[Crossref] [PubMed]

Ray, S.

J. Nam, I. Onitsuka, J. Hatch, Y. Uchida, S. Ray, S. Huang, W. Li, H. Zang, P. Ruiz-Lozano, and Y. S. Mukouyama, “Coronary veins determine the pattern of sympathetic innervation in the developing heart,” Development 140(7), 1475–1485 (2013).
[Crossref] [PubMed]

Reichek, N.

S. E. Reis, R. Holubkov, A. J. Conrad Smith, S. F. Kelsey, B. L. Sharaf, N. Reichek, W. J. Rogers, C. N. Merz, G. Sopko, C. J. Pepine, and WISE Investigators, “Coronary microvascular dysfunction is highly prevalent in women with chest pain in the absence of coronary artery disease: results from the NHLBI WISE study,” Am. Heart J. 141(5), 735–741 (2001).
[Crossref] [PubMed]

Reis, S. E.

S. E. Reis, R. Holubkov, A. J. Conrad Smith, S. F. Kelsey, B. L. Sharaf, N. Reichek, W. J. Rogers, C. N. Merz, G. Sopko, C. J. Pepine, and WISE Investigators, “Coronary microvascular dysfunction is highly prevalent in women with chest pain in the absence of coronary artery disease: results from the NHLBI WISE study,” Am. Heart J. 141(5), 735–741 (2001).
[Crossref] [PubMed]

Reutelingsperger, C. P.

J. W. Verjans, D. Lovhaug, N. Narula, A. D. Petrov, B. Indrevoll, E. Bjurgert, T. B. Krasieva, L. B. Petersen, G. M. Kindberg, M. Solbakken, A. Cuthbertson, M. A. Vannan, C. P. Reutelingsperger, B. J. Tromberg, L. Hofstra, and J. Narula, “Noninvasive imaging of angiotensin receptors after myocardial infarction,” JACC Cardiovasc. Imaging 1(3), 354–362 (2008).
[Crossref] [PubMed]

Roberts, R.

E. M. Geltman, D. Biello, M. J. Welch, M. M. Ter-Pogossian, R. Roberts, and B. E. Sobel, “Characterization of nontransmural myocardial infarction by positron-emission tomography,” Circulation 65(4), 747–755 (1982).
[Crossref] [PubMed]

Roberts, W. C.

B. N. Potkin, A. L. Bartorelli, J. M. Gessert, R. F. Neville, Y. Almagor, W. C. Roberts, and M. B. Leon, “Coronary artery imaging with intravascular high-frequency ultrasound,” Circulation 81(5), 1575–1585 (1990).
[Crossref] [PubMed]

Roger, V. L.

A. S. Go, D. Mozaffarian, V. L. Roger, E. J. Benjamin, J. D. Berry, W. B. Borden, D. M. Bravata, S. Dai, E. S. Ford, C. S. Fox, S. Franco, H. J. Fullerton, C. Gillespie, S. M. Hailpern, J. A. Heit, V. J. Howard, M. D. Huffman, B. M. Kissela, S. J. Kittner, D. T. Lackland, J. H. Lichtman, L. D. Lisabeth, D. Magid, G. M. Marcus, A. Marelli, D. B. Matchar, D. K. McGuire, E. R. Mohler, C. S. Moy, M. E. Mussolino, G. Nichol, N. P. Paynter, P. J. Schreiner, P. D. Sorlie, J. Stein, T. N. Turan, S. S. Virani, N. D. Wong, D. Woo, M. B. Turner, and American Heart Association Statistics Committee and Stroke Statistics Subcommittee, “Heart disease and stroke statistics--2013 update: a report from the American Heart Association,” Circulation 127(1), e6–e245 (2013).
[Crossref] [PubMed]

Rogers, W. J.

S. E. Reis, R. Holubkov, A. J. Conrad Smith, S. F. Kelsey, B. L. Sharaf, N. Reichek, W. J. Rogers, C. N. Merz, G. Sopko, C. J. Pepine, and WISE Investigators, “Coronary microvascular dysfunction is highly prevalent in women with chest pain in the absence of coronary artery disease: results from the NHLBI WISE study,” Am. Heart J. 141(5), 735–741 (2001).
[Crossref] [PubMed]

E. A. Zerhouni, D. M. Parish, W. J. Rogers, A. Yang, and E. P. Shapiro, “Human heart: tagging with MR imaging--a method for noninvasive assessment of myocardial motion,” Radiology 169(1), 59–63 (1988).
[PubMed]

Rubart, M.

J. A. Scherschel and M. Rubart, “Cardiovascular imaging using two-photon microscopy,” Microsc. Microanal. 14(6), 492–506 (2008).
[Crossref] [PubMed]

Ruiz-Lozano, P.

J. Nam, I. Onitsuka, J. Hatch, Y. Uchida, S. Ray, S. Huang, W. Li, H. Zang, P. Ruiz-Lozano, and Y. S. Mukouyama, “Coronary veins determine the pattern of sympathetic innervation in the developing heart,” Development 140(7), 1475–1485 (2013).
[Crossref] [PubMed]

Russell, J. C.

J. C. Russell and S. D. Proctor, “Small animal models of cardiovascular disease: tools for the study of the roles of metabolic syndrome, dyslipidemia, and atherosclerosis,” Cardiovasc. Pathol. 15(6), 318–330 (2006).
[Crossref] [PubMed]

Saliaris, A. P.

A. C. Lardo, M. A. Cordeiro, C. Silva, L. C. Amado, R. T. George, A. P. Saliaris, K. H. Schuleri, V. R. Fernandes, M. Zviman, S. Nazarian, H. R. Halperin, K. C. Wu, J. M. Hare, and J. A. Lima, “Contrast-enhanced multidetector computed tomography viability imaging after myocardial infarction: characterization of myocyte death, microvascular obstruction, and chronic scar,” Circulation 113(3), 394–404 (2006).
[Crossref] [PubMed]

Sbarbati, A.

S. Lee, C. Vinegoni, P. F. Feruglio, L. Fexon, R. Gorbatov, M. Pivoravov, A. Sbarbati, M. Nahrendorf, and R. Weissleder, “Real-time in vivo imaging of the beating mouse heart at microscopic resolution,” Nat Commun 3, 1054 (2012).
[Crossref] [PubMed]

Schächinger, V.

A. R. Pries, H. Habazettl, G. Ambrosio, P. R. Hansen, J. C. Kaski, V. Schächinger, H. Tillmanns, G. Vassalli, I. Tritto, M. Weis, C. de Wit, and R. Bugiardini, “A review of methods for assessment of coronary microvascular disease in both clinical and experimental settings,” Cardiovasc. Res. 80(2), 165–174 (2008).
[Crossref] [PubMed]

Schelbert, H. R.

T. H. Schindler, H. R. Schelbert, A. Quercioli, and V. Dilsizian, “Cardiac PET imaging for the detection and monitoring of coronary artery disease and microvascular health,” JACC Cardiovasc. Imaging 3(6), 623–640 (2010).
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J. E. Brush, R. O. Cannon, W. H. Schenke, R. O. Bonow, M. B. Leon, B. J. Maron, and S. E. Epstein, “Angina due to coronary microvascular disease in hypertensive patients without left ventricular hypertrophy,” N. Engl. J. Med. 319(20), 1302–1307 (1988).
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Scherschel, J. A.

J. A. Scherschel and M. Rubart, “Cardiovascular imaging using two-photon microscopy,” Microsc. Microanal. 14(6), 492–506 (2008).
[Crossref] [PubMed]

Schindler, T. H.

T. H. Schindler, H. R. Schelbert, A. Quercioli, and V. Dilsizian, “Cardiac PET imaging for the detection and monitoring of coronary artery disease and microvascular health,” JACC Cardiovasc. Imaging 3(6), 623–640 (2010).
[Crossref] [PubMed]

Schreiner, P. J.

A. S. Go, D. Mozaffarian, V. L. Roger, E. J. Benjamin, J. D. Berry, W. B. Borden, D. M. Bravata, S. Dai, E. S. Ford, C. S. Fox, S. Franco, H. J. Fullerton, C. Gillespie, S. M. Hailpern, J. A. Heit, V. J. Howard, M. D. Huffman, B. M. Kissela, S. J. Kittner, D. T. Lackland, J. H. Lichtman, L. D. Lisabeth, D. Magid, G. M. Marcus, A. Marelli, D. B. Matchar, D. K. McGuire, E. R. Mohler, C. S. Moy, M. E. Mussolino, G. Nichol, N. P. Paynter, P. J. Schreiner, P. D. Sorlie, J. Stein, T. N. Turan, S. S. Virani, N. D. Wong, D. Woo, M. B. Turner, and American Heart Association Statistics Committee and Stroke Statistics Subcommittee, “Heart disease and stroke statistics--2013 update: a report from the American Heart Association,” Circulation 127(1), e6–e245 (2013).
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Schuleri, K. H.

A. C. Lardo, M. A. Cordeiro, C. Silva, L. C. Amado, R. T. George, A. P. Saliaris, K. H. Schuleri, V. R. Fernandes, M. Zviman, S. Nazarian, H. R. Halperin, K. C. Wu, J. M. Hare, and J. A. Lima, “Contrast-enhanced multidetector computed tomography viability imaging after myocardial infarction: characterization of myocyte death, microvascular obstruction, and chronic scar,” Circulation 113(3), 394–404 (2006).
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D. Eitzman, Z. al-Aouar, H. L. Kanter, J. vom Dahl, M. Kirsh, G. M. Deeb, and M. Schwaiger, “Clinical outcome of patients with advanced coronary artery disease after viability studies with positron emission tomography,” J. Am. Coll. Cardiol. 20(3), 559–565 (1992).
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Shapiro, E. P.

E. A. Zerhouni, D. M. Parish, W. J. Rogers, A. Yang, and E. P. Shapiro, “Human heart: tagging with MR imaging--a method for noninvasive assessment of myocardial motion,” Radiology 169(1), 59–63 (1988).
[PubMed]

Sharaf, B. L.

S. E. Reis, R. Holubkov, A. J. Conrad Smith, S. F. Kelsey, B. L. Sharaf, N. Reichek, W. J. Rogers, C. N. Merz, G. Sopko, C. J. Pepine, and WISE Investigators, “Coronary microvascular dysfunction is highly prevalent in women with chest pain in the absence of coronary artery disease: results from the NHLBI WISE study,” Am. Heart J. 141(5), 735–741 (2001).
[Crossref] [PubMed]

Shirey, E. K.

W. L. Proudfit, E. K. Shirey, and F. M. Sones., “Selective cine coronary arteriography. Correlation with clinical findings in 1,000 patients,” Circulation 33(6), 901–910 (1966).
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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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Silva, C.

A. C. Lardo, M. A. Cordeiro, C. Silva, L. C. Amado, R. T. George, A. P. Saliaris, K. H. Schuleri, V. R. Fernandes, M. Zviman, S. Nazarian, H. R. Halperin, K. C. Wu, J. M. Hare, and J. A. Lima, “Contrast-enhanced multidetector computed tomography viability imaging after myocardial infarction: characterization of myocyte death, microvascular obstruction, and chronic scar,” Circulation 113(3), 394–404 (2006).
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K. Wei, A. R. Jayaweera, S. Firoozan, A. Linka, D. M. Skyba, and S. Kaul, “Quantification of myocardial blood flow with ultrasound-induced destruction of microbubbles administered as a constant venous infusion,” Circulation 97(5), 473–483 (1998).
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Smalling, R. W.

K. L. Gould, R. A. Goldstein, N. A. Mullani, R. L. Kirkeeide, W. H. Wong, T. J. Tewson, M. S. Berridge, L. A. Bolomey, R. K. Hartz, R. W. Smalling, F. Fuentes, and A. Nishikawa, “Noninvasive assessment of coronary stenoses by myocardial perfusion imaging during pharmacologic coronary vasodilation. VIII. Clinical feasibility of positron cardiac imaging without a cyclotron using generator-produced rubidium-82,” J. Am. Coll. Cardiol. 7(4), 775–789 (1986).
[Crossref] [PubMed]

Sobel, B. E.

E. M. Geltman, D. Biello, M. J. Welch, M. M. Ter-Pogossian, R. Roberts, and B. E. Sobel, “Characterization of nontransmural myocardial infarction by positron-emission tomography,” Circulation 65(4), 747–755 (1982).
[Crossref] [PubMed]

Solbakken, M.

J. W. Verjans, D. Lovhaug, N. Narula, A. D. Petrov, B. Indrevoll, E. Bjurgert, T. B. Krasieva, L. B. Petersen, G. M. Kindberg, M. Solbakken, A. Cuthbertson, M. A. Vannan, C. P. Reutelingsperger, B. J. Tromberg, L. Hofstra, and J. Narula, “Noninvasive imaging of angiotensin receptors after myocardial infarction,” JACC Cardiovasc. Imaging 1(3), 354–362 (2008).
[Crossref] [PubMed]

Sones, F. M.

W. L. Proudfit, E. K. Shirey, and F. M. Sones., “Selective cine coronary arteriography. Correlation with clinical findings in 1,000 patients,” Circulation 33(6), 901–910 (1966).
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Y. Li, Y. Song, L. Zhao, G. Gaidosh, A. M. Laties, and R. Wen, “Direct labeling and visualization of blood vessels with lipophilic carbocyanine dye DiI,” Nat. Protoc. 3(11), 1703–1708 (2008).
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Sopko, G.

S. E. Reis, R. Holubkov, A. J. Conrad Smith, S. F. Kelsey, B. L. Sharaf, N. Reichek, W. J. Rogers, C. N. Merz, G. Sopko, C. J. Pepine, and WISE Investigators, “Coronary microvascular dysfunction is highly prevalent in women with chest pain in the absence of coronary artery disease: results from the NHLBI WISE study,” Am. Heart J. 141(5), 735–741 (2001).
[Crossref] [PubMed]

Sorlie, P. D.

A. S. Go, D. Mozaffarian, V. L. Roger, E. J. Benjamin, J. D. Berry, W. B. Borden, D. M. Bravata, S. Dai, E. S. Ford, C. S. Fox, S. Franco, H. J. Fullerton, C. Gillespie, S. M. Hailpern, J. A. Heit, V. J. Howard, M. D. Huffman, B. M. Kissela, S. J. Kittner, D. T. Lackland, J. H. Lichtman, L. D. Lisabeth, D. Magid, G. M. Marcus, A. Marelli, D. B. Matchar, D. K. McGuire, E. R. Mohler, C. S. Moy, M. E. Mussolino, G. Nichol, N. P. Paynter, P. J. Schreiner, P. D. Sorlie, J. Stein, T. N. Turan, S. S. Virani, N. D. Wong, D. Woo, M. B. Turner, and American Heart Association Statistics Committee and Stroke Statistics Subcommittee, “Heart disease and stroke statistics--2013 update: a report from the American Heart Association,” Circulation 127(1), e6–e245 (2013).
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Figures (5)

Fig. 1
Fig. 1

Epi-illumination images of mouse heart sections (left) before and (right) after optical clearing with FocusClear. These images clearly depict the increased section transparency that results from optical clearing.

Fig. 2
Fig. 2

MIP map of the cardiac microvasculature in a (a) native and (b) optically-cleared ventral heart slice. The colormap corresponds to the depth of maximum signal at each pixel, and is the same for both images. The imaging depth does not increase substantially due to the relative thinness of the tissue, however, the vascular density is much more pronounced. Region outlined in green is shown in Fig. 3.

Fig. 3
Fig. 3

Region outlined in green in Fig. 2(B) showing zoomed in view of coronary vessel and microvasculature acquired at 10x magnification. Scale bar is 100 µm.

Fig. 4
Fig. 4

MIP map of representative ventral slices of mouse heart after optical clearing.

Fig. 5
Fig. 5

Optical histology enables imaging of multiple markers of interest. Images were acquired at (a) 20x and (b) 40x magnification of mouse cardiac microvasculature labeled with DiI and nuclei counter stained with DAPI. Scale bar for (a) is 50 µm and (b) 25 μm.

Tables (1)

Tables Icon

Table 1 FVD calculations of select regions of interest of the heart slices in Fig. 2 and Fig. 4

Metrics