Fast macro-scale transmission imaging of microvascular networks using KESM

David Mayerich; Jaerock Kwon; Chul Sung; Louise Abbott; John Keyser; Yoonsuck Choe

doi:10.1364/BOE.2.002888

Fast macro-scale transmission imaging of microvascular networks using KESM

David Mayerich, Jaerock Kwon, Chul Sung, Louise Abbott, John Keyser, and Yoonsuck Choe

Biomedical Optics Express
Vol. 2,
Issue 10,
pp. 2888-2896
(2011)
•doi: 10.1364/BOE.2.002888

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David Mayerich, Jaerock Kwon, Chul Sung, Louise Abbott, John Keyser, and Yoonsuck Choe, "Fast macro-scale transmission imaging of microvascular networks using KESM," Biomed. Opt. Express 2, 2888-2896 (2011)

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Abstract

Accurate microvascular morphometric information has significant implications in several fields, including the quantification of angiogenesis in cancer research, understanding the immune response for neural prosthetics, and predicting the nature of blood flow as it relates to stroke. We report imaging of the whole mouse brain microvascular system at resolutions sufficient to perform accurate morphometry. Imaging was performed using Knife-Edge Scanning Microscopy (KESM) and is the first example of this technique that can be directly applied to clinical research. We are able to achieve ≈ 0.7μm resolution laterally with 1μm depth resolution using serial sectioning. No alignment was necessary and contrast was sufficient to allow segmentation and measurement of vessels.

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References

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Publication

S. E. Ungersma, G. Pacheco, C. Ho, S. F. Yee, J. Ross, N. van Bruggen, F. V. Peale, S. Ross, and R. A. Carano, “Vessel imaging with viable tumor analysis for quantification of tumor angiogenesis,” Magnetic Resonance in Medicine 63, 1637–1647 (2010).
[Crossref] [PubMed]
A. R. Pries, A. J. M. Cornelissen, A. A. Sloot, M. Hinkeldey, M. R. Dreher, M. Hpfner, M. W. Dewhirst, and T. W. Secomb, “Structural adaptation and heterogeneity of normal and tumor microvascular networks,” PLoS Computational Biology 5, e1000394 (2009).
[Crossref] [PubMed]
A. B. Schwartz, X. T. Cui, D. J. Weber, and D. W. Moran, “Brain-Controlled interfaces: Movement restoration with neural prosthetics,” Neuron 52, 205–220 (2006).
[Crossref] [PubMed]
P. Blinder, A. Y. Shih, C. Rafie, and D. Kleinfeld, “Topological basis for the robust distribution of blood to rodent neocortex,” Proceedings of the National Academy of Sciences 107, 12670 –12675 (2010).
[Crossref]
B. R. Shepherd, H. Y. Chen, C. M. Smith, G. Gruionu, S. K. Williams, and J. B. Hoying, “Rapid perfusion and network remodeling in a microvascular construct after implantation,” Arteriosclerosis, Thrombosis, Vascular Biology 24, 898 –904 (2004).
[Crossref]
F. Cassot, F. Lauwers, S. Lorthois, P. Puwanarajah, V. Cances-Lauwers, and H. Duvernoy, “Branching patterns for arterioles and venules of the human cerebral cortex,” Brain Research 1313, 62–78 (2010).
[Crossref]
F. Lauwers, F. Cassot, V. Lauwers-Cances, P. Puwanarajah, and H. Duvernoy, “Morphometry of the human cerebral cortex microcirculation: General characteristics and space-related profiles,” NeuroImage 39, 936–948 (2008).
[Crossref]
P. S. Tsai, B. Friedman, A. Ifarraguerri, B. D. Thompson, V. Lev-Ram, C. B. Schaer, Q. Xiong, R. Y. Tsien, J. A. Squier, and D. Kleinfeld, “All-Optical histology using ultrashort laser pulses,” Neuron 39, 27–41 (2003).
[Crossref] [PubMed]
S. Heinzer, T. Krucker, M. Stampanoni, R. Abela, E. P. Meyer, A. Schuler, P. Schneider, and R. Muller, “Hierarchical microimaging for multiscale analysis of large vascular networks,” NeuroImage 32, 626–636 (2006).
[Crossref] [PubMed]
T. Krucker, A. Lang, and E. P. Meyer, “New polyurethane-based material for vascular corrosion casting with improved physical and imaging characteristics,” Microscopy research and technique 69, 138–147 (2006).
[Crossref] [PubMed]
Y. Choe, D. Han, P. Huang, J. Keyser, J. Kwon, D. Mayerich, and L. Abbott, “Complete submicrometer scans of mouse brain microstructure: Neurons and vasculatures,” in “2009 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2009). Program No. 389.10. Online.
D. Mayerich, J. Kwon, Y. Choe, L. Abbott, and J. Keyser, “Constructing high resolution microvascular models,” in “Third Workshop on Microscopic Image Analysis with Applications in Biology,” (2008).
A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-Optical sectioning tomography to obtain a High-Resolution atlas of the mouse brain,” Science 330, 1404 –1408 (2010).
[Crossref] [PubMed]
F. Cassot, F. Lauwers, C. Fouard, S. Prohaska, and V. Lauwers-Cances, “A novel Three-Dimensional Computer-Assisted method for a quantitative study of microvascular networks of the human cerebral cortex,” Microcirculation 13, 1–18 (2006).
[Crossref] [PubMed]
S. Akita, N. Tamai, A. Myoui, M. Nishikawa, T. Kaito, K. Takaoka, and H. Yoshikawa, “Capillary vessel network integration by inserting a vascular pedicle enhances bone formation in Tissue-Engineered bone using interconnected porous hydroxyapatite ceramics,” Tissue Engineering 10, 789–795 (2004).
[Crossref] [PubMed]
E. M. Renkin, S. D. Gray, and L. R. Dodd, “Filling of microcirculation in skeletal muscles during timed india ink perfusion,” American Journal of Physiology - Heart and Circulatory Physiology 241, H174 –H186 (1981).
L. C. Abbott and C. Sotelo, “Ultrastructural analysis of catecholaminergic innervation in weaver and normal mouse cerebellar cortices,” The Journal of Comparative Neurology 426, 316–329 (2000).
[Crossref] [PubMed]
D. Mayerich, L. C. Abbott, and B. H. McCormick, “Knife-Edge scanning microscopy for imaging and reconstruction of Three-Dimensional anatomical structures of the mouse brain,” Journal of Microscopy 231, 134–143 (2008).
[Crossref] [PubMed]
K. D. Micheva and S. J. Smith, “Array tomography: A new tool for imaging the molecular architecture and ultrastructure of neural circuits,” Neuron 55, 25–36 (2007).
[Crossref] [PubMed]
M. Wiercigroch and E. Budak, “Sources of nonlinearities, chatter generation and suppression in metal cutting,” Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences 359, 663–693 (2001).
[Crossref]
D. Mayerich, B. H. McCormick, and J. Keyser, “Noise and artifact removal in Knife-Edge scanning microscopy,” Proceedings of the 4th IEEE International Symposium on Biomedical Imaging: From Nano to Macro pp. 556–559 (2007).
[Crossref]
X. He, E. Kischell, M. Rioult, and T. J. Holmes, “Three-Dimensional thinning algorithm that peels the outmost layer with application to neuron tracing,” Journal of Computer-Assisted Microscopy 10, 123–135 (1998).
[Crossref]
T. C. Lee, R. L. Kashyap, and C. N. Chu, “Building skeleton models via 3-D medial surface/axis thinning algorithms,” Graphical Models and Image Processing 56, 462–478 (1994).
[Crossref]
T. S. Yoo, Insight into Images: Principles and Practice for Segmentation, Registration, and Image Analysis (A K Peters/CRC Press, 2004), 1st ed.
[Crossref]
J. A. Sethian, Level Set Methods and Fast Marching Methods: Evolving Interfaces in Computational Geometry, Fluid Mechanics, Computer Vision, and Materials Science (Cambridge University Press, 1999).
C. Sung, J. R. Chung, D. Mayerich, J. Kwon, D. Miller, T. Huffman, J. Keyser, L. Abbott, and Y. Choe, “Knife-edge scanning microscope brain atlas: A submicrometer-resolution web-based mouse brain atlas,” in “2011 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2011). Program No. 328.05. Online.

2010 (4)

S. E. Ungersma, G. Pacheco, C. Ho, S. F. Yee, J. Ross, N. van Bruggen, F. V. Peale, S. Ross, and R. A. Carano, “Vessel imaging with viable tumor analysis for quantification of tumor angiogenesis,” Magnetic Resonance in Medicine 63, 1637–1647 (2010).
[Crossref] [PubMed]

P. Blinder, A. Y. Shih, C. Rafie, and D. Kleinfeld, “Topological basis for the robust distribution of blood to rodent neocortex,” Proceedings of the National Academy of Sciences 107, 12670 –12675 (2010).
[Crossref]

F. Cassot, F. Lauwers, S. Lorthois, P. Puwanarajah, V. Cances-Lauwers, and H. Duvernoy, “Branching patterns for arterioles and venules of the human cerebral cortex,” Brain Research 1313, 62–78 (2010).
[Crossref]

A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-Optical sectioning tomography to obtain a High-Resolution atlas of the mouse brain,” Science 330, 1404 –1408 (2010).
[Crossref] [PubMed]

2009 (1)

A. R. Pries, A. J. M. Cornelissen, A. A. Sloot, M. Hinkeldey, M. R. Dreher, M. Hpfner, M. W. Dewhirst, and T. W. Secomb, “Structural adaptation and heterogeneity of normal and tumor microvascular networks,” PLoS Computational Biology 5, e1000394 (2009).
[Crossref] [PubMed]

2008 (2)

F. Lauwers, F. Cassot, V. Lauwers-Cances, P. Puwanarajah, and H. Duvernoy, “Morphometry of the human cerebral cortex microcirculation: General characteristics and space-related profiles,” NeuroImage 39, 936–948 (2008).
[Crossref]

D. Mayerich, L. C. Abbott, and B. H. McCormick, “Knife-Edge scanning microscopy for imaging and reconstruction of Three-Dimensional anatomical structures of the mouse brain,” Journal of Microscopy 231, 134–143 (2008).
[Crossref] [PubMed]

2007 (1)

K. D. Micheva and S. J. Smith, “Array tomography: A new tool for imaging the molecular architecture and ultrastructure of neural circuits,” Neuron 55, 25–36 (2007).
[Crossref] [PubMed]

2006 (4)

F. Cassot, F. Lauwers, C. Fouard, S. Prohaska, and V. Lauwers-Cances, “A novel Three-Dimensional Computer-Assisted method for a quantitative study of microvascular networks of the human cerebral cortex,” Microcirculation 13, 1–18 (2006).
[Crossref] [PubMed]

S. Heinzer, T. Krucker, M. Stampanoni, R. Abela, E. P. Meyer, A. Schuler, P. Schneider, and R. Muller, “Hierarchical microimaging for multiscale analysis of large vascular networks,” NeuroImage 32, 626–636 (2006).
[Crossref] [PubMed]

T. Krucker, A. Lang, and E. P. Meyer, “New polyurethane-based material for vascular corrosion casting with improved physical and imaging characteristics,” Microscopy research and technique 69, 138–147 (2006).
[Crossref] [PubMed]

A. B. Schwartz, X. T. Cui, D. J. Weber, and D. W. Moran, “Brain-Controlled interfaces: Movement restoration with neural prosthetics,” Neuron 52, 205–220 (2006).
[Crossref] [PubMed]

2004 (2)

B. R. Shepherd, H. Y. Chen, C. M. Smith, G. Gruionu, S. K. Williams, and J. B. Hoying, “Rapid perfusion and network remodeling in a microvascular construct after implantation,” Arteriosclerosis, Thrombosis, Vascular Biology 24, 898 –904 (2004).
[Crossref]

S. Akita, N. Tamai, A. Myoui, M. Nishikawa, T. Kaito, K. Takaoka, and H. Yoshikawa, “Capillary vessel network integration by inserting a vascular pedicle enhances bone formation in Tissue-Engineered bone using interconnected porous hydroxyapatite ceramics,” Tissue Engineering 10, 789–795 (2004).
[Crossref] [PubMed]

2003 (1)

P. S. Tsai, B. Friedman, A. Ifarraguerri, B. D. Thompson, V. Lev-Ram, C. B. Schaer, Q. Xiong, R. Y. Tsien, J. A. Squier, and D. Kleinfeld, “All-Optical histology using ultrashort laser pulses,” Neuron 39, 27–41 (2003).
[Crossref] [PubMed]

2001 (1)

M. Wiercigroch and E. Budak, “Sources of nonlinearities, chatter generation and suppression in metal cutting,” Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences 359, 663–693 (2001).
[Crossref]

2000 (1)

L. C. Abbott and C. Sotelo, “Ultrastructural analysis of catecholaminergic innervation in weaver and normal mouse cerebellar cortices,” The Journal of Comparative Neurology 426, 316–329 (2000).
[Crossref] [PubMed]

1998 (1)

X. He, E. Kischell, M. Rioult, and T. J. Holmes, “Three-Dimensional thinning algorithm that peels the outmost layer with application to neuron tracing,” Journal of Computer-Assisted Microscopy 10, 123–135 (1998).
[Crossref]

1994 (1)

T. C. Lee, R. L. Kashyap, and C. N. Chu, “Building skeleton models via 3-D medial surface/axis thinning algorithms,” Graphical Models and Image Processing 56, 462–478 (1994).
[Crossref]

1981 (1)

E. M. Renkin, S. D. Gray, and L. R. Dodd, “Filling of microcirculation in skeletal muscles during timed india ink perfusion,” American Journal of Physiology - Heart and Circulatory Physiology 241, H174 –H186 (1981).

Abbott, L.

Y. Choe, D. Han, P. Huang, J. Keyser, J. Kwon, D. Mayerich, and L. Abbott, “Complete submicrometer scans of mouse brain microstructure: Neurons and vasculatures,” in “2009 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2009). Program No. 389.10. Online.

D. Mayerich, J. Kwon, Y. Choe, L. Abbott, and J. Keyser, “Constructing high resolution microvascular models,” in “Third Workshop on Microscopic Image Analysis with Applications in Biology,” (2008).

C. Sung, J. R. Chung, D. Mayerich, J. Kwon, D. Miller, T. Huffman, J. Keyser, L. Abbott, and Y. Choe, “Knife-edge scanning microscope brain atlas: A submicrometer-resolution web-based mouse brain atlas,” in “2011 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2011). Program No. 328.05. Online.

Abbott, L. C.

Abela, R.

Akita, S.

Blinder, P.

Budak, E.

Cances-Lauwers, V.

Carano, R. A.

Cassot, F.

Chen, H. Y.

Choe, Y.

Chu, C. N.

T. C. Lee, R. L. Kashyap, and C. N. Chu, “Building skeleton models via 3-D medial surface/axis thinning algorithms,” Graphical Models and Image Processing 56, 462–478 (1994).
[Crossref]

Chung, J. R.

Cornelissen, A. J. M.

Cui, X. T.

A. B. Schwartz, X. T. Cui, D. J. Weber, and D. W. Moran, “Brain-Controlled interfaces: Movement restoration with neural prosthetics,” Neuron 52, 205–220 (2006).
[Crossref] [PubMed]

Dewhirst, M. W.

Dodd, L. R.

Dreher, M. R.

Duvernoy, H.

Fouard, C.

Friedman, B.

Gong, H.

Gray, S. D.

Gruionu, G.

Han, D.

He, X.

Heinzer, S.

Hinkeldey, M.

Ho, C.

Holmes, T. J.

Hoying, J. B.

Hpfner, M.

Huang, P.

Huffman, T.

Ifarraguerri, A.

Kaito, T.

Kashyap, R. L.

T. C. Lee, R. L. Kashyap, and C. N. Chu, “Building skeleton models via 3-D medial surface/axis thinning algorithms,” Graphical Models and Image Processing 56, 462–478 (1994).
[Crossref]

Keyser, J.

D. Mayerich, B. H. McCormick, and J. Keyser, “Noise and artifact removal in Knife-Edge scanning microscopy,” Proceedings of the 4th IEEE International Symposium on Biomedical Imaging: From Nano to Macro pp. 556–559 (2007).
[Crossref]

Kischell, E.

Kleinfeld, D.

Krucker, T.

Kwon, J.

Lang, A.

Lauwers, F.

Lauwers-Cances, V.

Lee, T. C.

T. C. Lee, R. L. Kashyap, and C. N. Chu, “Building skeleton models via 3-D medial surface/axis thinning algorithms,” Graphical Models and Image Processing 56, 462–478 (1994).
[Crossref]

Lev-Ram, V.

Li, A.

Liu, Q.

Lorthois, S.

Luo, Q.

Mayerich, D.

McCormick, B. H.

Meyer, E. P.

Micheva, K. D.

K. D. Micheva and S. J. Smith, “Array tomography: A new tool for imaging the molecular architecture and ultrastructure of neural circuits,” Neuron 55, 25–36 (2007).
[Crossref] [PubMed]

Miller, D.

Moran, D. W.

A. B. Schwartz, X. T. Cui, D. J. Weber, and D. W. Moran, “Brain-Controlled interfaces: Movement restoration with neural prosthetics,” Neuron 52, 205–220 (2006).
[Crossref] [PubMed]

Muller, R.

Myoui, A.

Nishikawa, M.

Pacheco, G.

Peale, F. V.

Pries, A. R.

Prohaska, S.

Puwanarajah, P.

Rafie, C.

Renkin, E. M.

Rioult, M.

Ross, J.

Ross, S.

Schaer, C. B.

Schneider, P.

Schuler, A.

Schwartz, A. B.

A. B. Schwartz, X. T. Cui, D. J. Weber, and D. W. Moran, “Brain-Controlled interfaces: Movement restoration with neural prosthetics,” Neuron 52, 205–220 (2006).
[Crossref] [PubMed]

Secomb, T. W.

Sethian, J. A.

J. A. Sethian, Level Set Methods and Fast Marching Methods: Evolving Interfaces in Computational Geometry, Fluid Mechanics, Computer Vision, and Materials Science (Cambridge University Press, 1999).

Shepherd, B. R.

Shih, A. Y.

Sloot, A. A.

Smith, C. M.

Smith, S. J.

K. D. Micheva and S. J. Smith, “Array tomography: A new tool for imaging the molecular architecture and ultrastructure of neural circuits,” Neuron 55, 25–36 (2007).
[Crossref] [PubMed]

Sotelo, C.

Squier, J. A.

Stampanoni, M.

Sung, C.

Takaoka, K.

Tamai, N.

Thompson, B. D.

Tsai, P. S.

Tsien, R. Y.

Ungersma, S. E.

van Bruggen, N.

Wang, Q.

Weber, D. J.

A. B. Schwartz, X. T. Cui, D. J. Weber, and D. W. Moran, “Brain-Controlled interfaces: Movement restoration with neural prosthetics,” Neuron 52, 205–220 (2006).
[Crossref] [PubMed]

Wiercigroch, M.

Williams, S. K.

Wu, J.

Xiong, Q.

Yan, C.

Yee, S. F.

Yoo, T. S.

T. S. Yoo, Insight into Images: Principles and Practice for Segmentation, Registration, and Image Analysis (A K Peters/CRC Press, 2004), 1st ed.
[Crossref]

Yoshikawa, H.

Zeng, S.

Zhang, B.

American Journal of Physiology - Heart and Circulatory Physiology (1)

Arteriosclerosis, Thrombosis, Vascular Biology (1)

Brain Research (1)

Graphical Models and Image Processing (1)

T. C. Lee, R. L. Kashyap, and C. N. Chu, “Building skeleton models via 3-D medial surface/axis thinning algorithms,” Graphical Models and Image Processing 56, 462–478 (1994).
[Crossref]

Journal of Computer-Assisted Microscopy (1)

Journal of Microscopy (1)

Magnetic Resonance in Medicine (1)

Microcirculation (1)

Microscopy research and technique (1)

NeuroImage (2)

Neuron (3)

A. B. Schwartz, X. T. Cui, D. J. Weber, and D. W. Moran, “Brain-Controlled interfaces: Movement restoration with neural prosthetics,” Neuron 52, 205–220 (2006).
[Crossref] [PubMed]

K. D. Micheva and S. J. Smith, “Array tomography: A new tool for imaging the molecular architecture and ultrastructure of neural circuits,” Neuron 55, 25–36 (2007).
[Crossref] [PubMed]

Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences (1)

PLoS Computational Biology (1)

Proceedings of the National Academy of Sciences (1)

Science (1)

The Journal of Comparative Neurology (1)

Tissue Engineering (1)

Other (6)

T. S. Yoo, Insight into Images: Principles and Practice for Segmentation, Registration, and Image Analysis (A K Peters/CRC Press, 2004), 1st ed.
[Crossref]

J. A. Sethian, Level Set Methods and Fast Marching Methods: Evolving Interfaces in Computational Geometry, Fluid Mechanics, Computer Vision, and Materials Science (Cambridge University Press, 1999).

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Fig. 1

Knife-edge scanning microscopy. Serial sections are concurrently cut and imaged under water (a–b). Imaging is performed in transmission mode by sending illumination through a diamond cutting tool. Image capture is synchronized with stage position and performed using a line-scan camera. Illumination is provided using a mercury vapor short arc lamp to send light to the knife through a liquid-optic light guide (0.55NA, η = 1.65). Geometric angles of the refracted light are shown for each interface (c). Total internal reflection (TIR) within the diamond knife at the diamond/water interface results in light scattering and emission through the knife tip when the incident angle is less than the critical angle (33.3°) for a diamond knife (η = 2.42) immersed in water (η = 1.33) (d). The density of illumination around the knife is estimated using a first-order Monte Carlo simulation (e–f). The amount of scattering is determined by the NA of the light guide. Light intensity is shown as a factor of input intensity using the associated color map. Imaging is performed using time-delayed integation (TDI) as the tissue moves along the 35° bevel at the knife tip. Using TDI increases the SNR and increases the amount of scattered illumination used to construct the final image.

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Fig. 2

(a) Single coronal KESM section of the mouse cerebellum and mid-brain and closeup showing a (b) 500μm and (c) 200μm view of the same section. (d) A single tissue cross-section at any depth z is composed of several adjacent sections with a width that falls within the objective FOV.

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Fig. 3

Visualization of the whole-brain vascular data set. The whole downsampled brain is shown (a–b) along with cross-sections composed of ≈ 200 slices (c–f). Scale bars = 2mm. (g) Close-up of an anterior coronal section through the cortex. Features labeled are (1) surface of the lateral ventricles, (2) Pericallosal artery, and (3) the cortical surface with descending microvessels. (h–i) Close-up of a volume reconstruction of the labeled region. Color value indicates estimated vessel radius computed by performing a distance transform on the medial axis.

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Equations (2)

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F = \frac{2 Δ x}{π r}

| \nabla u (x) | = F (x)