Abstract

Cutaneous blood flow accounts for approximately 5% of cardiac output in human and plays a key role in a number of a physiological and pathological processes. We show for the first time a multi-modal photoacoustic tomography (PAT), optical coherence tomography (OCT) and OCT angiography system with an articulated probe to extract human cutaneous vasculature in vivo in various skin regions. OCT angiography supplements the microvasculature which PAT alone is unable to provide. Co-registered volumes for vessel network is further embedded in the morphologic image provided by OCT. This multi-modal system is therefore demonstrated as a valuable tool for comprehensive non-invasive human skin vasculature and morphology imaging in vivo.

© 2016 Optical Society of America

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References

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2016 (2)

L. Themstrup, J. Welzel, S. Ciardo, R. Kaestle, M. Ulrich, J. Holmes, R. Whitehead, E. C. Sattler, N. Kindermann, G. Pellacani, and G. B. E. Jemec, “Validation of Dynamic optical coherence tomography for non-invasive, in vivo microcirculation imaging of the skin,” Microvasc. Res. 107, 97–105 (2016).
[Crossref] [PubMed]

Z. Chen, M. Liu, M. Minneman, L. Ginner, E. Hoover, H. Sattmann, J. Ensher, M. Bonesi, W. Drexler, and R. A. Leitgeb, “Phase-stable swept source OCT angiography in human skin using an akinetic source,” Biomed. Opt. Express 7(8), 3032–3048 (2016).
[Crossref]

2015 (4)

A. Lozzi, A. Agrawal, A. Boretsky, C. G. Welle, and D. X. Hammer, “Image quality metrics for optical coherence angiography,” Biomed. Opt. Express 6(7), 2435–2447 (2015).
[Crossref] [PubMed]

U. Baran, Y. Li, W. J. Choi, G. Kalkan, and R. K. Wang, “High resolution imaging of acne lesion development and scarring in human facial skin using OCT-based microangiography,” Lasers Surg. Med. 47(3), 231–238 (2015).
[Crossref] [PubMed]

B. Zabihian, J. Weingast, M. Liu, E. Zhang, P. Beard, H. Pehamberger, W. Drexler, and B. Hermann, “In vivo dual-modality photoacoustic and optical coherence tomography imaging of human dermatological pathologies,” Biomed. Opt. Express 6(9), 3163–3178 (2015).
[Crossref] [PubMed]

C. Errico, J. Pierre, S. Pezet, Y. Desailly, Z. Lenkei, O. Couture, and M. Tanter, “Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging,” Nature 527(7579), 499–502 (2015).
[Crossref] [PubMed]

2014 (5)

S. Eriksson, J. Nilsson, and C. Sturesson, “Non-invasive imaging of microcirculation: a technology review,” Med. Devices (Auckl.) 7, 445–452 (2014).
[PubMed]

S. H. Geyer, M. M. Nöhammer, M. Mathä, L. Reissig, I. E. Tinhofer, and W. J. Weninger, “High-Resolution Episcopic Microscopy (HREM): A Tool For Visualizing Skin Biopsies,” Microsc. Microanal. 20(5), 1356–1364 (2014).
[Crossref] [PubMed]

W. Drexler, M. Liu, A. Kumar, T. Kamali, A. Unterhuber, and R. A. Leitgeb, “Optical coherence tomography today: speed, contrast, and multimodality,” J. Biomed. Opt. 19(7), 071412 (2014).
[Crossref] [PubMed]

M. Liu, B. Maurer, B. Hermann, B. Zabihian, M. G. Sandrian, A. Unterhuber, B. Baumann, E. Z. Zhang, P. C. Beard, W. J. Weninger, and W. Drexler, “Dual modality optical coherence and whole-body photoacoustic tomography imaging of chick embryos in multiple development stages,” Biomed. Opt. Express 5(9), 3150–3159 (2014).
[Crossref] [PubMed]

W. J. Choi, R. Reif, S. Yousefi, and R. K. Wang, “Improved microcirculation imaging of human skin in vivo using optical microangiography with a correlation mapping mask,” J. Biomed. Opt. 19(3), 036010 (2014).
[Crossref] [PubMed]

2013 (2)

2012 (2)

2010 (2)

B. E. Treeby and B. T. Cox, “k-Wave: MATLAB toolbox for the simulation and reconstruction of photoacoustic wave fields,” J. Biomed. Opt. 15(2), 021314 (2010).
[Crossref] [PubMed]

A. Alex, B. Považay, B. Hofer, S. Popov, C. Glittenberg, S. Binder, and W. Drexler, “Multispectral in vivo three-dimensional optical coherence tomography of human skin,” J. Biomed. Opt. 15(2), 026025 (2010).
[Crossref] [PubMed]

2008 (1)

2006 (1)

H. Ding, J. Q. Lu, W. A. Wooden, P. J. Kragel, and X. H. Hu, “Refractive indices of human skin tissues at eight wavelengths and estimated dispersion relations between 300 and 1600 nm,” Phys. Med. Biol. 51(6), 1479–1489 (2006).
[Crossref] [PubMed]

2003 (3)

D. F. Fiorentino, “Cutaneous vasculitis,” J. Am. Acad. Dermatol. 48(3), 311–344 (2003).
[Crossref] [PubMed]

D. M. McDonald and P. L. Choyke, “Imaging of angiogenesis: from microscope to clinic,” Nat. Med. 9(6), 713–725 (2003).
[Crossref] [PubMed]

D. Cosgrove, “Angiogenesis imaging--ultrasound,” Br. J. Radiol. 76(suppl_1), S43–S49 (2003).
[Crossref] [PubMed]

2002 (1)

M. Bhushan, H. S. Young, P. E. C. Brenchley, and C. E. M. Griffiths, “Recent advances in cutaneous angiogenesis,” Br. J. Dermatol. 147(3), 418–425 (2002).
[Crossref] [PubMed]

Agrawal, A.

Alex, A.

C. Blatter, J. Weingast, A. Alex, B. Grajciar, W. Wieser, W. Drexler, R. Huber, and R. A. Leitgeb, “In situ structural and microangiographic assessment of human skin lesions with high-speed OCT,” Biomed. Opt. Express 3(10), 2636–2646 (2012).
[Crossref] [PubMed]

A. Alex, B. Považay, B. Hofer, S. Popov, C. Glittenberg, S. Binder, and W. Drexler, “Multispectral in vivo three-dimensional optical coherence tomography of human skin,” J. Biomed. Opt. 15(2), 026025 (2010).
[Crossref] [PubMed]

Baran, U.

U. Baran, Y. Li, W. J. Choi, G. Kalkan, and R. K. Wang, “High resolution imaging of acne lesion development and scarring in human facial skin using OCT-based microangiography,” Lasers Surg. Med. 47(3), 231–238 (2015).
[Crossref] [PubMed]

Baumann, B.

Beard, P.

Beard, P. C.

Bhushan, M.

M. Bhushan, H. S. Young, P. E. C. Brenchley, and C. E. M. Griffiths, “Recent advances in cutaneous angiogenesis,” Br. J. Dermatol. 147(3), 418–425 (2002).
[Crossref] [PubMed]

Binder, S.

A. Alex, B. Považay, B. Hofer, S. Popov, C. Glittenberg, S. Binder, and W. Drexler, “Multispectral in vivo three-dimensional optical coherence tomography of human skin,” J. Biomed. Opt. 15(2), 026025 (2010).
[Crossref] [PubMed]

Blatter, C.

Bonesi, M.

Boretsky, A.

Brenchley, P. E. C.

M. Bhushan, H. S. Young, P. E. C. Brenchley, and C. E. M. Griffiths, “Recent advances in cutaneous angiogenesis,” Br. J. Dermatol. 147(3), 418–425 (2002).
[Crossref] [PubMed]

Chen, Z.

Choi, W. J.

U. Baran, Y. Li, W. J. Choi, G. Kalkan, and R. K. Wang, “High resolution imaging of acne lesion development and scarring in human facial skin using OCT-based microangiography,” Lasers Surg. Med. 47(3), 231–238 (2015).
[Crossref] [PubMed]

W. J. Choi, R. Reif, S. Yousefi, and R. K. Wang, “Improved microcirculation imaging of human skin in vivo using optical microangiography with a correlation mapping mask,” J. Biomed. Opt. 19(3), 036010 (2014).
[Crossref] [PubMed]

Choyke, P. L.

D. M. McDonald and P. L. Choyke, “Imaging of angiogenesis: from microscope to clinic,” Nat. Med. 9(6), 713–725 (2003).
[Crossref] [PubMed]

Ciardo, S.

L. Themstrup, J. Welzel, S. Ciardo, R. Kaestle, M. Ulrich, J. Holmes, R. Whitehead, E. C. Sattler, N. Kindermann, G. Pellacani, and G. B. E. Jemec, “Validation of Dynamic optical coherence tomography for non-invasive, in vivo microcirculation imaging of the skin,” Microvasc. Res. 107, 97–105 (2016).
[Crossref] [PubMed]

Cosgrove, D.

D. Cosgrove, “Angiogenesis imaging--ultrasound,” Br. J. Radiol. 76(suppl_1), S43–S49 (2003).
[Crossref] [PubMed]

Couture, O.

C. Errico, J. Pierre, S. Pezet, Y. Desailly, Z. Lenkei, O. Couture, and M. Tanter, “Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging,” Nature 527(7579), 499–502 (2015).
[Crossref] [PubMed]

Cox, B. T.

B. E. Treeby and B. T. Cox, “k-Wave: MATLAB toolbox for the simulation and reconstruction of photoacoustic wave fields,” J. Biomed. Opt. 15(2), 021314 (2010).
[Crossref] [PubMed]

Desailly, Y.

C. Errico, J. Pierre, S. Pezet, Y. Desailly, Z. Lenkei, O. Couture, and M. Tanter, “Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging,” Nature 527(7579), 499–502 (2015).
[Crossref] [PubMed]

Ding, H.

H. Ding, J. Q. Lu, W. A. Wooden, P. J. Kragel, and X. H. Hu, “Refractive indices of human skin tissues at eight wavelengths and estimated dispersion relations between 300 and 1600 nm,” Phys. Med. Biol. 51(6), 1479–1489 (2006).
[Crossref] [PubMed]

Drexler, W.

Z. Chen, M. Liu, M. Minneman, L. Ginner, E. Hoover, H. Sattmann, J. Ensher, M. Bonesi, W. Drexler, and R. A. Leitgeb, “Phase-stable swept source OCT angiography in human skin using an akinetic source,” Biomed. Opt. Express 7(8), 3032–3048 (2016).
[Crossref]

B. Zabihian, J. Weingast, M. Liu, E. Zhang, P. Beard, H. Pehamberger, W. Drexler, and B. Hermann, “In vivo dual-modality photoacoustic and optical coherence tomography imaging of human dermatological pathologies,” Biomed. Opt. Express 6(9), 3163–3178 (2015).
[Crossref] [PubMed]

M. Liu, B. Maurer, B. Hermann, B. Zabihian, M. G. Sandrian, A. Unterhuber, B. Baumann, E. Z. Zhang, P. C. Beard, W. J. Weninger, and W. Drexler, “Dual modality optical coherence and whole-body photoacoustic tomography imaging of chick embryos in multiple development stages,” Biomed. Opt. Express 5(9), 3150–3159 (2014).
[Crossref] [PubMed]

W. Drexler, M. Liu, A. Kumar, T. Kamali, A. Unterhuber, and R. A. Leitgeb, “Optical coherence tomography today: speed, contrast, and multimodality,” J. Biomed. Opt. 19(7), 071412 (2014).
[Crossref] [PubMed]

M. Liu, N. Schmitner, M. G. Sandrian, B. Zabihian, B. Hermann, W. Salvenmoser, D. Meyer, and W. Drexler, “In vivo three dimensional dual wavelength photoacoustic tomography imaging of the far red fluorescent protein E2-Crimson expressed in adult zebrafish,” Biomed. Opt. Express 4(10), 1846–1855 (2013).
[Crossref] [PubMed]

C. Blatter, J. Weingast, A. Alex, B. Grajciar, W. Wieser, W. Drexler, R. Huber, and R. A. Leitgeb, “In situ structural and microangiographic assessment of human skin lesions with high-speed OCT,” Biomed. Opt. Express 3(10), 2636–2646 (2012).
[Crossref] [PubMed]

A. Alex, B. Považay, B. Hofer, S. Popov, C. Glittenberg, S. Binder, and W. Drexler, “Multispectral in vivo three-dimensional optical coherence tomography of human skin,” J. Biomed. Opt. 15(2), 026025 (2010).
[Crossref] [PubMed]

Eliceiri, K. W.

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

Ensher, J.

Eriksson, S.

S. Eriksson, J. Nilsson, and C. Sturesson, “Non-invasive imaging of microcirculation: a technology review,” Med. Devices (Auckl.) 7, 445–452 (2014).
[PubMed]

Errico, C.

C. Errico, J. Pierre, S. Pezet, Y. Desailly, Z. Lenkei, O. Couture, and M. Tanter, “Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging,” Nature 527(7579), 499–502 (2015).
[Crossref] [PubMed]

Fiorentino, D. F.

D. F. Fiorentino, “Cutaneous vasculitis,” J. Am. Acad. Dermatol. 48(3), 311–344 (2003).
[Crossref] [PubMed]

Geyer, S. H.

S. H. Geyer, M. M. Nöhammer, M. Mathä, L. Reissig, I. E. Tinhofer, and W. J. Weninger, “High-Resolution Episcopic Microscopy (HREM): A Tool For Visualizing Skin Biopsies,” Microsc. Microanal. 20(5), 1356–1364 (2014).
[Crossref] [PubMed]

S. H. Geyer, M. M. Nöhammer, I. E. Tinhofer, and W. J. Weninger, “The dermal arteries of the human thumb pad,” J. Anat. 223(6), 603–609 (2013).
[Crossref] [PubMed]

Ginner, L.

Glittenberg, C.

A. Alex, B. Považay, B. Hofer, S. Popov, C. Glittenberg, S. Binder, and W. Drexler, “Multispectral in vivo three-dimensional optical coherence tomography of human skin,” J. Biomed. Opt. 15(2), 026025 (2010).
[Crossref] [PubMed]

Grajciar, B.

Griffiths, C. E. M.

M. Bhushan, H. S. Young, P. E. C. Brenchley, and C. E. M. Griffiths, “Recent advances in cutaneous angiogenesis,” Br. J. Dermatol. 147(3), 418–425 (2002).
[Crossref] [PubMed]

Hammer, D. X.

Hermann, B.

Hofer, B.

A. Alex, B. Považay, B. Hofer, S. Popov, C. Glittenberg, S. Binder, and W. Drexler, “Multispectral in vivo three-dimensional optical coherence tomography of human skin,” J. Biomed. Opt. 15(2), 026025 (2010).
[Crossref] [PubMed]

Holmes, J.

L. Themstrup, J. Welzel, S. Ciardo, R. Kaestle, M. Ulrich, J. Holmes, R. Whitehead, E. C. Sattler, N. Kindermann, G. Pellacani, and G. B. E. Jemec, “Validation of Dynamic optical coherence tomography for non-invasive, in vivo microcirculation imaging of the skin,” Microvasc. Res. 107, 97–105 (2016).
[Crossref] [PubMed]

Hoover, E.

Hu, X. H.

H. Ding, J. Q. Lu, W. A. Wooden, P. J. Kragel, and X. H. Hu, “Refractive indices of human skin tissues at eight wavelengths and estimated dispersion relations between 300 and 1600 nm,” Phys. Med. Biol. 51(6), 1479–1489 (2006).
[Crossref] [PubMed]

Huber, R.

Jemec, G. B. E.

L. Themstrup, J. Welzel, S. Ciardo, R. Kaestle, M. Ulrich, J. Holmes, R. Whitehead, E. C. Sattler, N. Kindermann, G. Pellacani, and G. B. E. Jemec, “Validation of Dynamic optical coherence tomography for non-invasive, in vivo microcirculation imaging of the skin,” Microvasc. Res. 107, 97–105 (2016).
[Crossref] [PubMed]

Kaestle, R.

L. Themstrup, J. Welzel, S. Ciardo, R. Kaestle, M. Ulrich, J. Holmes, R. Whitehead, E. C. Sattler, N. Kindermann, G. Pellacani, and G. B. E. Jemec, “Validation of Dynamic optical coherence tomography for non-invasive, in vivo microcirculation imaging of the skin,” Microvasc. Res. 107, 97–105 (2016).
[Crossref] [PubMed]

Kalkan, G.

U. Baran, Y. Li, W. J. Choi, G. Kalkan, and R. K. Wang, “High resolution imaging of acne lesion development and scarring in human facial skin using OCT-based microangiography,” Lasers Surg. Med. 47(3), 231–238 (2015).
[Crossref] [PubMed]

Kamali, T.

W. Drexler, M. Liu, A. Kumar, T. Kamali, A. Unterhuber, and R. A. Leitgeb, “Optical coherence tomography today: speed, contrast, and multimodality,” J. Biomed. Opt. 19(7), 071412 (2014).
[Crossref] [PubMed]

Kindermann, N.

L. Themstrup, J. Welzel, S. Ciardo, R. Kaestle, M. Ulrich, J. Holmes, R. Whitehead, E. C. Sattler, N. Kindermann, G. Pellacani, and G. B. E. Jemec, “Validation of Dynamic optical coherence tomography for non-invasive, in vivo microcirculation imaging of the skin,” Microvasc. Res. 107, 97–105 (2016).
[Crossref] [PubMed]

Kragel, P. J.

H. Ding, J. Q. Lu, W. A. Wooden, P. J. Kragel, and X. H. Hu, “Refractive indices of human skin tissues at eight wavelengths and estimated dispersion relations between 300 and 1600 nm,” Phys. Med. Biol. 51(6), 1479–1489 (2006).
[Crossref] [PubMed]

Kumar, A.

W. Drexler, M. Liu, A. Kumar, T. Kamali, A. Unterhuber, and R. A. Leitgeb, “Optical coherence tomography today: speed, contrast, and multimodality,” J. Biomed. Opt. 19(7), 071412 (2014).
[Crossref] [PubMed]

Laufer, J.

Leitgeb, R. A.

Lenkei, Z.

C. Errico, J. Pierre, S. Pezet, Y. Desailly, Z. Lenkei, O. Couture, and M. Tanter, “Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging,” Nature 527(7579), 499–502 (2015).
[Crossref] [PubMed]

Li, Y.

U. Baran, Y. Li, W. J. Choi, G. Kalkan, and R. K. Wang, “High resolution imaging of acne lesion development and scarring in human facial skin using OCT-based microangiography,” Lasers Surg. Med. 47(3), 231–238 (2015).
[Crossref] [PubMed]

Liu, M.

Lozzi, A.

Lu, J. Q.

H. Ding, J. Q. Lu, W. A. Wooden, P. J. Kragel, and X. H. Hu, “Refractive indices of human skin tissues at eight wavelengths and estimated dispersion relations between 300 and 1600 nm,” Phys. Med. Biol. 51(6), 1479–1489 (2006).
[Crossref] [PubMed]

Mathä, M.

S. H. Geyer, M. M. Nöhammer, M. Mathä, L. Reissig, I. E. Tinhofer, and W. J. Weninger, “High-Resolution Episcopic Microscopy (HREM): A Tool For Visualizing Skin Biopsies,” Microsc. Microanal. 20(5), 1356–1364 (2014).
[Crossref] [PubMed]

Maurer, B.

McDonald, D. M.

D. M. McDonald and P. L. Choyke, “Imaging of angiogenesis: from microscope to clinic,” Nat. Med. 9(6), 713–725 (2003).
[Crossref] [PubMed]

Meyer, D.

Minneman, M.

Nilsson, J.

S. Eriksson, J. Nilsson, and C. Sturesson, “Non-invasive imaging of microcirculation: a technology review,” Med. Devices (Auckl.) 7, 445–452 (2014).
[PubMed]

Nöhammer, M. M.

S. H. Geyer, M. M. Nöhammer, M. Mathä, L. Reissig, I. E. Tinhofer, and W. J. Weninger, “High-Resolution Episcopic Microscopy (HREM): A Tool For Visualizing Skin Biopsies,” Microsc. Microanal. 20(5), 1356–1364 (2014).
[Crossref] [PubMed]

S. H. Geyer, M. M. Nöhammer, I. E. Tinhofer, and W. J. Weninger, “The dermal arteries of the human thumb pad,” J. Anat. 223(6), 603–609 (2013).
[Crossref] [PubMed]

Pehamberger, H.

Pellacani, G.

L. Themstrup, J. Welzel, S. Ciardo, R. Kaestle, M. Ulrich, J. Holmes, R. Whitehead, E. C. Sattler, N. Kindermann, G. Pellacani, and G. B. E. Jemec, “Validation of Dynamic optical coherence tomography for non-invasive, in vivo microcirculation imaging of the skin,” Microvasc. Res. 107, 97–105 (2016).
[Crossref] [PubMed]

Pezet, S.

C. Errico, J. Pierre, S. Pezet, Y. Desailly, Z. Lenkei, O. Couture, and M. Tanter, “Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging,” Nature 527(7579), 499–502 (2015).
[Crossref] [PubMed]

Pierre, J.

C. Errico, J. Pierre, S. Pezet, Y. Desailly, Z. Lenkei, O. Couture, and M. Tanter, “Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging,” Nature 527(7579), 499–502 (2015).
[Crossref] [PubMed]

Popov, S.

A. Alex, B. Považay, B. Hofer, S. Popov, C. Glittenberg, S. Binder, and W. Drexler, “Multispectral in vivo three-dimensional optical coherence tomography of human skin,” J. Biomed. Opt. 15(2), 026025 (2010).
[Crossref] [PubMed]

Považay, B.

A. Alex, B. Považay, B. Hofer, S. Popov, C. Glittenberg, S. Binder, and W. Drexler, “Multispectral in vivo three-dimensional optical coherence tomography of human skin,” J. Biomed. Opt. 15(2), 026025 (2010).
[Crossref] [PubMed]

Rasband, W. S.

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

Reif, R.

W. J. Choi, R. Reif, S. Yousefi, and R. K. Wang, “Improved microcirculation imaging of human skin in vivo using optical microangiography with a correlation mapping mask,” J. Biomed. Opt. 19(3), 036010 (2014).
[Crossref] [PubMed]

Reissig, L.

S. H. Geyer, M. M. Nöhammer, M. Mathä, L. Reissig, I. E. Tinhofer, and W. J. Weninger, “High-Resolution Episcopic Microscopy (HREM): A Tool For Visualizing Skin Biopsies,” Microsc. Microanal. 20(5), 1356–1364 (2014).
[Crossref] [PubMed]

Salvenmoser, W.

Sandrian, M. G.

Sattler, E. C.

L. Themstrup, J. Welzel, S. Ciardo, R. Kaestle, M. Ulrich, J. Holmes, R. Whitehead, E. C. Sattler, N. Kindermann, G. Pellacani, and G. B. E. Jemec, “Validation of Dynamic optical coherence tomography for non-invasive, in vivo microcirculation imaging of the skin,” Microvasc. Res. 107, 97–105 (2016).
[Crossref] [PubMed]

Sattmann, H.

Schmitner, N.

Schneider, C. A.

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

Sturesson, C.

S. Eriksson, J. Nilsson, and C. Sturesson, “Non-invasive imaging of microcirculation: a technology review,” Med. Devices (Auckl.) 7, 445–452 (2014).
[PubMed]

Tanter, M.

C. Errico, J. Pierre, S. Pezet, Y. Desailly, Z. Lenkei, O. Couture, and M. Tanter, “Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging,” Nature 527(7579), 499–502 (2015).
[Crossref] [PubMed]

Themstrup, L.

L. Themstrup, J. Welzel, S. Ciardo, R. Kaestle, M. Ulrich, J. Holmes, R. Whitehead, E. C. Sattler, N. Kindermann, G. Pellacani, and G. B. E. Jemec, “Validation of Dynamic optical coherence tomography for non-invasive, in vivo microcirculation imaging of the skin,” Microvasc. Res. 107, 97–105 (2016).
[Crossref] [PubMed]

Tinhofer, I. E.

S. H. Geyer, M. M. Nöhammer, M. Mathä, L. Reissig, I. E. Tinhofer, and W. J. Weninger, “High-Resolution Episcopic Microscopy (HREM): A Tool For Visualizing Skin Biopsies,” Microsc. Microanal. 20(5), 1356–1364 (2014).
[Crossref] [PubMed]

S. H. Geyer, M. M. Nöhammer, I. E. Tinhofer, and W. J. Weninger, “The dermal arteries of the human thumb pad,” J. Anat. 223(6), 603–609 (2013).
[Crossref] [PubMed]

Treeby, B. E.

B. E. Treeby and B. T. Cox, “k-Wave: MATLAB toolbox for the simulation and reconstruction of photoacoustic wave fields,” J. Biomed. Opt. 15(2), 021314 (2010).
[Crossref] [PubMed]

Ulrich, M.

L. Themstrup, J. Welzel, S. Ciardo, R. Kaestle, M. Ulrich, J. Holmes, R. Whitehead, E. C. Sattler, N. Kindermann, G. Pellacani, and G. B. E. Jemec, “Validation of Dynamic optical coherence tomography for non-invasive, in vivo microcirculation imaging of the skin,” Microvasc. Res. 107, 97–105 (2016).
[Crossref] [PubMed]

Unterhuber, A.

Wang, R. K.

U. Baran, Y. Li, W. J. Choi, G. Kalkan, and R. K. Wang, “High resolution imaging of acne lesion development and scarring in human facial skin using OCT-based microangiography,” Lasers Surg. Med. 47(3), 231–238 (2015).
[Crossref] [PubMed]

W. J. Choi, R. Reif, S. Yousefi, and R. K. Wang, “Improved microcirculation imaging of human skin in vivo using optical microangiography with a correlation mapping mask,” J. Biomed. Opt. 19(3), 036010 (2014).
[Crossref] [PubMed]

Weingast, J.

Welle, C. G.

Welzel, J.

L. Themstrup, J. Welzel, S. Ciardo, R. Kaestle, M. Ulrich, J. Holmes, R. Whitehead, E. C. Sattler, N. Kindermann, G. Pellacani, and G. B. E. Jemec, “Validation of Dynamic optical coherence tomography for non-invasive, in vivo microcirculation imaging of the skin,” Microvasc. Res. 107, 97–105 (2016).
[Crossref] [PubMed]

Weninger, W. J.

S. H. Geyer, M. M. Nöhammer, M. Mathä, L. Reissig, I. E. Tinhofer, and W. J. Weninger, “High-Resolution Episcopic Microscopy (HREM): A Tool For Visualizing Skin Biopsies,” Microsc. Microanal. 20(5), 1356–1364 (2014).
[Crossref] [PubMed]

M. Liu, B. Maurer, B. Hermann, B. Zabihian, M. G. Sandrian, A. Unterhuber, B. Baumann, E. Z. Zhang, P. C. Beard, W. J. Weninger, and W. Drexler, “Dual modality optical coherence and whole-body photoacoustic tomography imaging of chick embryos in multiple development stages,” Biomed. Opt. Express 5(9), 3150–3159 (2014).
[Crossref] [PubMed]

S. H. Geyer, M. M. Nöhammer, I. E. Tinhofer, and W. J. Weninger, “The dermal arteries of the human thumb pad,” J. Anat. 223(6), 603–609 (2013).
[Crossref] [PubMed]

Whitehead, R.

L. Themstrup, J. Welzel, S. Ciardo, R. Kaestle, M. Ulrich, J. Holmes, R. Whitehead, E. C. Sattler, N. Kindermann, G. Pellacani, and G. B. E. Jemec, “Validation of Dynamic optical coherence tomography for non-invasive, in vivo microcirculation imaging of the skin,” Microvasc. Res. 107, 97–105 (2016).
[Crossref] [PubMed]

Wieser, W.

Wooden, W. A.

H. Ding, J. Q. Lu, W. A. Wooden, P. J. Kragel, and X. H. Hu, “Refractive indices of human skin tissues at eight wavelengths and estimated dispersion relations between 300 and 1600 nm,” Phys. Med. Biol. 51(6), 1479–1489 (2006).
[Crossref] [PubMed]

Young, H. S.

M. Bhushan, H. S. Young, P. E. C. Brenchley, and C. E. M. Griffiths, “Recent advances in cutaneous angiogenesis,” Br. J. Dermatol. 147(3), 418–425 (2002).
[Crossref] [PubMed]

Yousefi, S.

W. J. Choi, R. Reif, S. Yousefi, and R. K. Wang, “Improved microcirculation imaging of human skin in vivo using optical microangiography with a correlation mapping mask,” J. Biomed. Opt. 19(3), 036010 (2014).
[Crossref] [PubMed]

Zabihian, B.

Zhang, E.

Zhang, E. Z.

Appl. Opt. (1)

Biomed. Opt. Express (6)

C. Blatter, J. Weingast, A. Alex, B. Grajciar, W. Wieser, W. Drexler, R. Huber, and R. A. Leitgeb, “In situ structural and microangiographic assessment of human skin lesions with high-speed OCT,” Biomed. Opt. Express 3(10), 2636–2646 (2012).
[Crossref] [PubMed]

M. Liu, N. Schmitner, M. G. Sandrian, B. Zabihian, B. Hermann, W. Salvenmoser, D. Meyer, and W. Drexler, “In vivo three dimensional dual wavelength photoacoustic tomography imaging of the far red fluorescent protein E2-Crimson expressed in adult zebrafish,” Biomed. Opt. Express 4(10), 1846–1855 (2013).
[Crossref] [PubMed]

M. Liu, B. Maurer, B. Hermann, B. Zabihian, M. G. Sandrian, A. Unterhuber, B. Baumann, E. Z. Zhang, P. C. Beard, W. J. Weninger, and W. Drexler, “Dual modality optical coherence and whole-body photoacoustic tomography imaging of chick embryos in multiple development stages,” Biomed. Opt. Express 5(9), 3150–3159 (2014).
[Crossref] [PubMed]

A. Lozzi, A. Agrawal, A. Boretsky, C. G. Welle, and D. X. Hammer, “Image quality metrics for optical coherence angiography,” Biomed. Opt. Express 6(7), 2435–2447 (2015).
[Crossref] [PubMed]

B. Zabihian, J. Weingast, M. Liu, E. Zhang, P. Beard, H. Pehamberger, W. Drexler, and B. Hermann, “In vivo dual-modality photoacoustic and optical coherence tomography imaging of human dermatological pathologies,” Biomed. Opt. Express 6(9), 3163–3178 (2015).
[Crossref] [PubMed]

Z. Chen, M. Liu, M. Minneman, L. Ginner, E. Hoover, H. Sattmann, J. Ensher, M. Bonesi, W. Drexler, and R. A. Leitgeb, “Phase-stable swept source OCT angiography in human skin using an akinetic source,” Biomed. Opt. Express 7(8), 3032–3048 (2016).
[Crossref]

Br. J. Dermatol. (1)

M. Bhushan, H. S. Young, P. E. C. Brenchley, and C. E. M. Griffiths, “Recent advances in cutaneous angiogenesis,” Br. J. Dermatol. 147(3), 418–425 (2002).
[Crossref] [PubMed]

Br. J. Radiol. (1)

D. Cosgrove, “Angiogenesis imaging--ultrasound,” Br. J. Radiol. 76(suppl_1), S43–S49 (2003).
[Crossref] [PubMed]

J. Am. Acad. Dermatol. (1)

D. F. Fiorentino, “Cutaneous vasculitis,” J. Am. Acad. Dermatol. 48(3), 311–344 (2003).
[Crossref] [PubMed]

J. Anat. (1)

S. H. Geyer, M. M. Nöhammer, I. E. Tinhofer, and W. J. Weninger, “The dermal arteries of the human thumb pad,” J. Anat. 223(6), 603–609 (2013).
[Crossref] [PubMed]

J. Biomed. Opt. (4)

A. Alex, B. Považay, B. Hofer, S. Popov, C. Glittenberg, S. Binder, and W. Drexler, “Multispectral in vivo three-dimensional optical coherence tomography of human skin,” J. Biomed. Opt. 15(2), 026025 (2010).
[Crossref] [PubMed]

W. J. Choi, R. Reif, S. Yousefi, and R. K. Wang, “Improved microcirculation imaging of human skin in vivo using optical microangiography with a correlation mapping mask,” J. Biomed. Opt. 19(3), 036010 (2014).
[Crossref] [PubMed]

W. Drexler, M. Liu, A. Kumar, T. Kamali, A. Unterhuber, and R. A. Leitgeb, “Optical coherence tomography today: speed, contrast, and multimodality,” J. Biomed. Opt. 19(7), 071412 (2014).
[Crossref] [PubMed]

B. E. Treeby and B. T. Cox, “k-Wave: MATLAB toolbox for the simulation and reconstruction of photoacoustic wave fields,” J. Biomed. Opt. 15(2), 021314 (2010).
[Crossref] [PubMed]

Lasers Surg. Med. (1)

U. Baran, Y. Li, W. J. Choi, G. Kalkan, and R. K. Wang, “High resolution imaging of acne lesion development and scarring in human facial skin using OCT-based microangiography,” Lasers Surg. Med. 47(3), 231–238 (2015).
[Crossref] [PubMed]

Med. Devices (Auckl.) (1)

S. Eriksson, J. Nilsson, and C. Sturesson, “Non-invasive imaging of microcirculation: a technology review,” Med. Devices (Auckl.) 7, 445–452 (2014).
[PubMed]

Microsc. Microanal. (1)

S. H. Geyer, M. M. Nöhammer, M. Mathä, L. Reissig, I. E. Tinhofer, and W. J. Weninger, “High-Resolution Episcopic Microscopy (HREM): A Tool For Visualizing Skin Biopsies,” Microsc. Microanal. 20(5), 1356–1364 (2014).
[Crossref] [PubMed]

Microvasc. Res. (1)

L. Themstrup, J. Welzel, S. Ciardo, R. Kaestle, M. Ulrich, J. Holmes, R. Whitehead, E. C. Sattler, N. Kindermann, G. Pellacani, and G. B. E. Jemec, “Validation of Dynamic optical coherence tomography for non-invasive, in vivo microcirculation imaging of the skin,” Microvasc. Res. 107, 97–105 (2016).
[Crossref] [PubMed]

Nat. Med. (1)

D. M. McDonald and P. L. Choyke, “Imaging of angiogenesis: from microscope to clinic,” Nat. Med. 9(6), 713–725 (2003).
[Crossref] [PubMed]

Nat. Methods (1)

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

Nature (1)

C. Errico, J. Pierre, S. Pezet, Y. Desailly, Z. Lenkei, O. Couture, and M. Tanter, “Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging,” Nature 527(7579), 499–502 (2015).
[Crossref] [PubMed]

Phys. Med. Biol. (1)

H. Ding, J. Q. Lu, W. A. Wooden, P. J. Kragel, and X. H. Hu, “Refractive indices of human skin tissues at eight wavelengths and estimated dispersion relations between 300 and 1600 nm,” Phys. Med. Biol. 51(6), 1479–1489 (2006).
[Crossref] [PubMed]

Other (2)

W. Drexler and J. G. Fujimoto, Optical Coherence Tomography: Technology and Applications, 2nd ed. (Springer International Publishing, 2015).

S. Standring, Gray’s Anatomy, 41st ed. (Elsevier Limited, 2016).

Supplementary Material (2)

NameDescription
» Visualization 1: MP4 (9641 KB)      related to Fig. 4(e)
» Visualization 2: MP4 (10010 KB)      related to Fig. 6(d) and Fig. 6(g)

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Figures (6)

Fig. 1
Fig. 1 (a) 3D modeling of the multi-modal system’s scanning probe. (b) An exploded view of the switchable sensor holder assembly. (c) The probe in PAT scan imaging an arm. (d) The probe in PAT scan imaging a foot.
Fig. 2
Fig. 2 Schematic of the multi-modal system. The green dashed line encircles the probe. Black dashed line indicates the two workstations used for PAT and OCT. The two sub-systems share the same probe. DO: digital output; AO: analog output; Ct: counter; AI: analog input; OPO: optical parametric oscillator; DAQ: data acquisition card; Ext. Clk: external clock; R: retroreflector; C: circulator; P: polarization controllers; FM: flip mirror; DBD: dual balanced detector; PD: photodetector.
Fig. 3
Fig. 3 (a) 3D display of PAT resolved blood vessels. (b) OCT morphologic volume showing the skin creases. The inlet is a photo of the knee imaged with the dashed square indicating approximately the scanned region. (c) A slice in the dermal-epidermal junction giving PAT in green and OCT angiography in red. (d) Summation of the depth range from 403 to 452 µm for the fused PAT and OCT angiography volume. PAT in green and OCT angiography in red. (e) An MIP image of PAT showing the strong absorbing layer before reaching reticular dermis. (f) An MIP image of PAT with hue to depth projection, visualizing deeper vessels in the skin of knee. Scale bar = 1 mm.
Fig. 4
Fig. 4 (a), (b) and (c) are from the fused PAT/OCT-angiography volume with green for PAT and red for OCT angiography. (a) A slice at 164 µm measured from the surface of the skin. (b) Summation for the depth range between 353 µm and 580 µm. (c) Summation from 592 µm to 832 µm. (d) PAT MIP image in HSV coordinate with depth to hue projection showing a depth range of 3 mm from 1 mm below skin surface. (e) 3D snapshots of fused PAT/OCT and OCT angiography volume (see Visualization 1). Gray color maps OCT while red hot color map is used for blood vessels from OCT angiography and PAT. Scale bar = 1 mm.
Fig. 5
Fig. 5 (a) PAT MIP image of type III skin over a depth of 4.6 mm. (b) PAT/OCT-angiography image over a depth range of 380 µm from 540 µm below skin surface with red for OCT angiography resolved blood vessels and green for PAT signal. (c) A photo of the nevus imaged in type III skin. (d) PAT MIP image of type II skin in the arm over a depth of 4.6 mm. The hue to depth projection bar to the right of (a) and (d) means that these two figures share the same projection. (e) 3D display of (d), showing the ruptured blood vessels (inside the yellow circle) and granulation tissue caused by a wound in the arm. Scale bar = 1 mm.
Fig. 6
Fig. 6 (a), (b) and (c) are fused PAT/OCT-angiography images with PAT in the green channel and OCT angiography in the red channel. (a) A slice at 252 µm below skin surface. Capillary loops are visible following the ridges. (b) Summation over the depth range from 391 µm to 680 µm. Postcapillary venules are displayed using OCT angiography. (c) A single slice at 680 µm into skin shows where the transition zone from OCT angiography to PAT locates. (d) Whole cutaneous blood vessel network given in volumetric display by fused OCT angiography and PAT data. (e) PAT MIP image with HSV coordinate. Same pattern is observed as is given in (a) but capillary loops not distinguishable. (f) PAT MIP image in deeper region showing blood vessels located in and below reticular dermis. (g) A snapshot of the 3D volume with OCT in gray, OCT angiography and PAT in red color map (see Visualization 2). Scale bar = 1 mm.

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