Abstract

We developed a linear ultrasound array-based real-time photoacoustic imaging system with a compact coaxial excitation handheld photoacoustic imaging probe for guiding sentinel lymph node (SLN) needle biopsy. Compared with previous studies, our system and probe have the following advantages: (1) the imaging probe is quite compact and user-friendly; (2) laser illumination and ultrasonic detection are achieved coaxially, enabling high signal-to-noise ratio; and (3) GPU-based image reconstruction enables real-time imaging and displaying at a frame rate of 20 Hz. With the system and probe, clear visualization of the SLN at the depth of 2 cm (~human SLN depth) was demonstrated on a living rat. A fine needle was pushed towards the SLN based on the guidance of real-time photoacoustic imaging. The proposed photoacoustic imaging system and probe was shown to have great potential to be used in clinics for guiding SLN needle biopsy, which may reduce the high morbidity rate related to the current gold standard clinical SLN biopsy procedure.

© 2018 Optical Society of America

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2017 (2)

K. Sivasubramanian, V. Periyasamy, and M. Pramanik, “Non-invasive sentinel lymph node mapping and needle guidance using clinical handheld photoacoustic imaging system in small animal,” J. Biophotonics 10, 1–10 (2017).
[PubMed]

K. Sivasubramanian, V. Periyasamy, and M. Pramanik, “Hand-held clinical photoacoustic imaging system for real-time non-invasive small animal imaging,” J. Vis. Exp. 128(128), e56649 (2017).
[PubMed]

2016 (3)

J. Kim, S. Park, Y. Jung, S. Chang, J. Park, Y. Zhang, J. F. Lovell, and C. Kim, “Programmable real-time clinical photoacoustic and ultrasound imaging system,” Sci. Rep. 6(1), 35137 (2016).
[Crossref] [PubMed]

K. Sivasubramanian and M. Pramanik, “High frame rate photoacoustic imaging at 7000 frames per second using clinical ultrasound system,” Biomed. Opt. Express 7(2), 312–323 (2016).
[Crossref] [PubMed]

K. Sivasubramanian, V. Periyasamy, K. K. Wen, and M. Pramanik, “Optimizing light delivery through fiber bundle in photoacoustic imaging with clinical ultrasound system: Monte Carlo simulation and experimental validation,” J. Biomed. Opt. 22(4), 041008 (2016).
[Crossref] [PubMed]

2015 (1)

Y. Zhou, G. Li, L. Zhu, C. Li, L. A. Cornelius, and L. V. Wang, “Handheld photoacoustic probe to detect both melanoma depth and volume at high speed in vivo,” J. Biophotonics 8(11-12), 961–967 (2015).
[Crossref] [PubMed]

2014 (1)

2013 (4)

S. L. Jacques, “Optical properties of biological tissues: a review,” Phys. Med. Biol. 58(11), R37–R61 (2013).
[Crossref] [PubMed]

T. Wang and Y. Jing, “Transcranial ultrasound imaging with speed of sound-based phase correction: a numerical study,” Phys. Med. Biol. 58(19), 6663–6681 (2013).
[Crossref] [PubMed]

L. G. Montilla, R. Olafsson, D. R. Bauer, and R. S. Witte, “Real-time photoacoustic and ultrasound imaging: a simple solution for clinical ultrasound systems with linear arrays,” Phys. Med. Biol. 58(1), N1–N12 (2013).
[Crossref] [PubMed]

A. Needles, A. Heinmiller, J. Sun, C. Theodoropoulos, D. Bates, D. Hirson, M. Yin, and F. S. Foster, “Development and initial application of a fully integrated photoacoustic micro-ultrasound system,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60(5), 888–897 (2013).
[Crossref] [PubMed]

2012 (1)

L. V. Wang and S. Hu, “Photoacoustic tomography: in vivo imaging from organelles to organs,” Science 335(6075), 1458–1462 (2012).
[Crossref] [PubMed]

2011 (2)

P. Beard, “Biomedical photoacoustic imaging,” Interface Focus 1(4), 602–631 (2011).
[Crossref] [PubMed]

M. Hutteman, H. S. Choi, J. S. Mieog, J. R. van der Vorst, Y. Ashitate, P. J. Kuppen, M. C. van Groningen, C. W. Löwik, V. T. Smit, C. J. van de Velde, J. V. Frangioni, and A. L. Vahrmeijer, “Clinical translation of ex vivo sentinel lymph node mapping for colorectal cancer using invisible near-infrared fluorescence light,” Ann. Surg. Oncol. 18(4), 1006–1014 (2011).
[Crossref] [PubMed]

2010 (2)

C. Kim, T. N. Erpelding, K. Maslov, L. Jankovic, W. J. Akers, L. Song, S. Achilefu, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Handheld array-based photoacoustic probe for guiding needle biopsy of sentinel lymph nodes,” J. Biomed. Opt. 15(4), 046010 (2010).
[Crossref] [PubMed]

T. N. Erpelding, C. Kim, M. Pramanik, L. Jankovic, K. Maslov, Z. Guo, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Sentinel lymph nodes in the rat: noninvasive photoacoustic and US imaging with a clinical US system,” Radiology 256(1), 102–110 (2010).
[Crossref] [PubMed]

2009 (1)

L. V. Wang, “Multiscale photoacoustic microscopy and computed tomography,” Nat. Photonics 3(9), 503–509 (2009).
[Crossref] [PubMed]

2008 (2)

R. G. Kolkman, P. J. Brands, W. Steenbergen, and T. G. van Leeuwen, “Real-time in vivo photoacoustic and ultrasound imaging,” J. Biomed. Opt. 13(5), 050510 (2008).
[Crossref] [PubMed]

L. Song, K. Maslov, R. Bitton, K. K. Shung, and L. V. Wang, “Fast 3-D dark-field reflection-mode photoacoustic microscopy in vivo with a 30-MHz ultrasound linear array,” J. Biomed. Opt. 13(5), 054028 (2008).
[Crossref] [PubMed]

2007 (1)

M. S. Hassouna and A. A. Farag, “Multi-stencils fast marching methods: A highly accurate solution to the eikonal equation on cartesian domains,” IEEE Trans. Pattern Anal. Mach. Intell. 29(9), 1563–1574 (2007).
[Crossref] [PubMed]

2005 (2)

M. Xu and L. V. Wang, “Universal back-projection algorithm for photoacoustic computed tomography,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 71(1), 016706 (2005).
[Crossref] [PubMed]

A. D. Purushotham, S. Upponi, M. B. Klevesath, L. Bobrow, K. Millar, J. P. Myles, and S. W. Duffy, “Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial,” J. Clin. Oncol. 23(19), 4312–4321 (2005).
[Crossref] [PubMed]

2004 (1)

T. Schulze, A. Bembenek, and P. M. Schlag, “Sentinel lymph node biopsy progress in surgical treatment of cancer,” Langenbecks Arch. Surg. 389(6), 532–550 (2004).
[Crossref] [PubMed]

2002 (3)

J. Bonnema and C. J. van de Velde, “Sentinel lymph node biopsy in breast cancer,” Ann. Oncol. 13(10), 1531–1537 (2002).
[Crossref] [PubMed]

R. von Knobloch, J. Weber, Z. Varga, H. Feiber, A. Heidenreich, and R. Hofmann, “Bilateral fine-needle administered local anaesthetic nerve block for pain control during TRUS-guided multi-core prostate biopsy: a prospective randomised trial,” Eur. Urol. 41(5), 508–514 (2002).
[Crossref] [PubMed]

S. Krishnamurthy, N. Sneige, D. G. Bedi, B. S. Edieken, B. D. Fornage, H. M. Kuerer, S. E. Singletary, and K. K. Hunt, “Role of ultrasound-guided fine-needle aspiration of indeterminate and suspicious axillary lymph nodes in the initial staging of breast carcinoma,” Cancer 95(5), 982–988 (2002).
[Crossref] [PubMed]

2001 (1)

G. Mariani, L. Moresco, G. Viale, G. Villa, M. Bagnasco, G. Canavese, J. Buscombe, H. W. Strauss, and G. Paganelli, “Radioguided sentinel lymph node biopsy in breast cancer surgery,” J. Nucl. Med. 42(8), 1198–1215 (2001).
[PubMed]

1994 (1)

A. E. Giuliano, D. M. Kirgan, J. M. Guenther, and D. L. Morton, “Lymphatic mapping and sentinel lymphadenectomy for breast cancer,” Ann. Surg. 220(3), 391–401 (1994).
[Crossref] [PubMed]

1987 (1)

B. D. Fornage, M. J. Faroux, and A. Simatos, “Breast masses: US-guided fine-needle aspiration biopsy,” Radiology 162(2), 409–414 (1987).
[Crossref] [PubMed]

Achilefu, S.

C. Kim, T. N. Erpelding, K. Maslov, L. Jankovic, W. J. Akers, L. Song, S. Achilefu, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Handheld array-based photoacoustic probe for guiding needle biopsy of sentinel lymph nodes,” J. Biomed. Opt. 15(4), 046010 (2010).
[Crossref] [PubMed]

Akers, W. J.

C. Kim, T. N. Erpelding, K. Maslov, L. Jankovic, W. J. Akers, L. Song, S. Achilefu, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Handheld array-based photoacoustic probe for guiding needle biopsy of sentinel lymph nodes,” J. Biomed. Opt. 15(4), 046010 (2010).
[Crossref] [PubMed]

Ashitate, Y.

M. Hutteman, H. S. Choi, J. S. Mieog, J. R. van der Vorst, Y. Ashitate, P. J. Kuppen, M. C. van Groningen, C. W. Löwik, V. T. Smit, C. J. van de Velde, J. V. Frangioni, and A. L. Vahrmeijer, “Clinical translation of ex vivo sentinel lymph node mapping for colorectal cancer using invisible near-infrared fluorescence light,” Ann. Surg. Oncol. 18(4), 1006–1014 (2011).
[Crossref] [PubMed]

Bagnasco, M.

G. Mariani, L. Moresco, G. Viale, G. Villa, M. Bagnasco, G. Canavese, J. Buscombe, H. W. Strauss, and G. Paganelli, “Radioguided sentinel lymph node biopsy in breast cancer surgery,” J. Nucl. Med. 42(8), 1198–1215 (2001).
[PubMed]

Bates, D.

A. Needles, A. Heinmiller, J. Sun, C. Theodoropoulos, D. Bates, D. Hirson, M. Yin, and F. S. Foster, “Development and initial application of a fully integrated photoacoustic micro-ultrasound system,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60(5), 888–897 (2013).
[Crossref] [PubMed]

Bauer, D. R.

L. G. Montilla, R. Olafsson, D. R. Bauer, and R. S. Witte, “Real-time photoacoustic and ultrasound imaging: a simple solution for clinical ultrasound systems with linear arrays,” Phys. Med. Biol. 58(1), N1–N12 (2013).
[Crossref] [PubMed]

Beard, P.

P. Beard, “Biomedical photoacoustic imaging,” Interface Focus 1(4), 602–631 (2011).
[Crossref] [PubMed]

Bedi, D. G.

S. Krishnamurthy, N. Sneige, D. G. Bedi, B. S. Edieken, B. D. Fornage, H. M. Kuerer, S. E. Singletary, and K. K. Hunt, “Role of ultrasound-guided fine-needle aspiration of indeterminate and suspicious axillary lymph nodes in the initial staging of breast carcinoma,” Cancer 95(5), 982–988 (2002).
[Crossref] [PubMed]

Bembenek, A.

T. Schulze, A. Bembenek, and P. M. Schlag, “Sentinel lymph node biopsy progress in surgical treatment of cancer,” Langenbecks Arch. Surg. 389(6), 532–550 (2004).
[Crossref] [PubMed]

Bitton, R.

L. Song, K. Maslov, R. Bitton, K. K. Shung, and L. V. Wang, “Fast 3-D dark-field reflection-mode photoacoustic microscopy in vivo with a 30-MHz ultrasound linear array,” J. Biomed. Opt. 13(5), 054028 (2008).
[Crossref] [PubMed]

Bobrow, L.

A. D. Purushotham, S. Upponi, M. B. Klevesath, L. Bobrow, K. Millar, J. P. Myles, and S. W. Duffy, “Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial,” J. Clin. Oncol. 23(19), 4312–4321 (2005).
[Crossref] [PubMed]

Bonnema, J.

J. Bonnema and C. J. van de Velde, “Sentinel lymph node biopsy in breast cancer,” Ann. Oncol. 13(10), 1531–1537 (2002).
[Crossref] [PubMed]

Brands, P.

Brands, P. J.

R. G. Kolkman, P. J. Brands, W. Steenbergen, and T. G. van Leeuwen, “Real-time in vivo photoacoustic and ultrasound imaging,” J. Biomed. Opt. 13(5), 050510 (2008).
[Crossref] [PubMed]

Buscombe, J.

G. Mariani, L. Moresco, G. Viale, G. Villa, M. Bagnasco, G. Canavese, J. Buscombe, H. W. Strauss, and G. Paganelli, “Radioguided sentinel lymph node biopsy in breast cancer surgery,” J. Nucl. Med. 42(8), 1198–1215 (2001).
[PubMed]

Canavese, G.

G. Mariani, L. Moresco, G. Viale, G. Villa, M. Bagnasco, G. Canavese, J. Buscombe, H. W. Strauss, and G. Paganelli, “Radioguided sentinel lymph node biopsy in breast cancer surgery,” J. Nucl. Med. 42(8), 1198–1215 (2001).
[PubMed]

Chang, S.

J. Kim, S. Park, Y. Jung, S. Chang, J. Park, Y. Zhang, J. F. Lovell, and C. Kim, “Programmable real-time clinical photoacoustic and ultrasound imaging system,” Sci. Rep. 6(1), 35137 (2016).
[Crossref] [PubMed]

Choi, H. S.

M. Hutteman, H. S. Choi, J. S. Mieog, J. R. van der Vorst, Y. Ashitate, P. J. Kuppen, M. C. van Groningen, C. W. Löwik, V. T. Smit, C. J. van de Velde, J. V. Frangioni, and A. L. Vahrmeijer, “Clinical translation of ex vivo sentinel lymph node mapping for colorectal cancer using invisible near-infrared fluorescence light,” Ann. Surg. Oncol. 18(4), 1006–1014 (2011).
[Crossref] [PubMed]

Cornelius, L. A.

Y. Zhou, G. Li, L. Zhu, C. Li, L. A. Cornelius, and L. V. Wang, “Handheld photoacoustic probe to detect both melanoma depth and volume at high speed in vivo,” J. Biophotonics 8(11-12), 961–967 (2015).
[Crossref] [PubMed]

Daoudi, K.

Duffy, S. W.

A. D. Purushotham, S. Upponi, M. B. Klevesath, L. Bobrow, K. Millar, J. P. Myles, and S. W. Duffy, “Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial,” J. Clin. Oncol. 23(19), 4312–4321 (2005).
[Crossref] [PubMed]

Edieken, B. S.

S. Krishnamurthy, N. Sneige, D. G. Bedi, B. S. Edieken, B. D. Fornage, H. M. Kuerer, S. E. Singletary, and K. K. Hunt, “Role of ultrasound-guided fine-needle aspiration of indeterminate and suspicious axillary lymph nodes in the initial staging of breast carcinoma,” Cancer 95(5), 982–988 (2002).
[Crossref] [PubMed]

Erpelding, T. N.

C. Kim, T. N. Erpelding, K. Maslov, L. Jankovic, W. J. Akers, L. Song, S. Achilefu, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Handheld array-based photoacoustic probe for guiding needle biopsy of sentinel lymph nodes,” J. Biomed. Opt. 15(4), 046010 (2010).
[Crossref] [PubMed]

T. N. Erpelding, C. Kim, M. Pramanik, L. Jankovic, K. Maslov, Z. Guo, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Sentinel lymph nodes in the rat: noninvasive photoacoustic and US imaging with a clinical US system,” Radiology 256(1), 102–110 (2010).
[Crossref] [PubMed]

Farag, A. A.

M. S. Hassouna and A. A. Farag, “Multi-stencils fast marching methods: A highly accurate solution to the eikonal equation on cartesian domains,” IEEE Trans. Pattern Anal. Mach. Intell. 29(9), 1563–1574 (2007).
[Crossref] [PubMed]

Faroux, M. J.

B. D. Fornage, M. J. Faroux, and A. Simatos, “Breast masses: US-guided fine-needle aspiration biopsy,” Radiology 162(2), 409–414 (1987).
[Crossref] [PubMed]

Feiber, H.

R. von Knobloch, J. Weber, Z. Varga, H. Feiber, A. Heidenreich, and R. Hofmann, “Bilateral fine-needle administered local anaesthetic nerve block for pain control during TRUS-guided multi-core prostate biopsy: a prospective randomised trial,” Eur. Urol. 41(5), 508–514 (2002).
[Crossref] [PubMed]

Fornage, B. D.

S. Krishnamurthy, N. Sneige, D. G. Bedi, B. S. Edieken, B. D. Fornage, H. M. Kuerer, S. E. Singletary, and K. K. Hunt, “Role of ultrasound-guided fine-needle aspiration of indeterminate and suspicious axillary lymph nodes in the initial staging of breast carcinoma,” Cancer 95(5), 982–988 (2002).
[Crossref] [PubMed]

B. D. Fornage, M. J. Faroux, and A. Simatos, “Breast masses: US-guided fine-needle aspiration biopsy,” Radiology 162(2), 409–414 (1987).
[Crossref] [PubMed]

Foster, F. S.

A. Needles, A. Heinmiller, J. Sun, C. Theodoropoulos, D. Bates, D. Hirson, M. Yin, and F. S. Foster, “Development and initial application of a fully integrated photoacoustic micro-ultrasound system,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60(5), 888–897 (2013).
[Crossref] [PubMed]

Frangioni, J. V.

M. Hutteman, H. S. Choi, J. S. Mieog, J. R. van der Vorst, Y. Ashitate, P. J. Kuppen, M. C. van Groningen, C. W. Löwik, V. T. Smit, C. J. van de Velde, J. V. Frangioni, and A. L. Vahrmeijer, “Clinical translation of ex vivo sentinel lymph node mapping for colorectal cancer using invisible near-infrared fluorescence light,” Ann. Surg. Oncol. 18(4), 1006–1014 (2011).
[Crossref] [PubMed]

Giuliano, A. E.

A. E. Giuliano, D. M. Kirgan, J. M. Guenther, and D. L. Morton, “Lymphatic mapping and sentinel lymphadenectomy for breast cancer,” Ann. Surg. 220(3), 391–401 (1994).
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Guenther, J. M.

A. E. Giuliano, D. M. Kirgan, J. M. Guenther, and D. L. Morton, “Lymphatic mapping and sentinel lymphadenectomy for breast cancer,” Ann. Surg. 220(3), 391–401 (1994).
[Crossref] [PubMed]

Guo, Z.

T. N. Erpelding, C. Kim, M. Pramanik, L. Jankovic, K. Maslov, Z. Guo, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Sentinel lymph nodes in the rat: noninvasive photoacoustic and US imaging with a clinical US system,” Radiology 256(1), 102–110 (2010).
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Hassouna, M. S.

M. S. Hassouna and A. A. Farag, “Multi-stencils fast marching methods: A highly accurate solution to the eikonal equation on cartesian domains,” IEEE Trans. Pattern Anal. Mach. Intell. 29(9), 1563–1574 (2007).
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Heidenreich, A.

R. von Knobloch, J. Weber, Z. Varga, H. Feiber, A. Heidenreich, and R. Hofmann, “Bilateral fine-needle administered local anaesthetic nerve block for pain control during TRUS-guided multi-core prostate biopsy: a prospective randomised trial,” Eur. Urol. 41(5), 508–514 (2002).
[Crossref] [PubMed]

Heinmiller, A.

A. Needles, A. Heinmiller, J. Sun, C. Theodoropoulos, D. Bates, D. Hirson, M. Yin, and F. S. Foster, “Development and initial application of a fully integrated photoacoustic micro-ultrasound system,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60(5), 888–897 (2013).
[Crossref] [PubMed]

Hirson, D.

A. Needles, A. Heinmiller, J. Sun, C. Theodoropoulos, D. Bates, D. Hirson, M. Yin, and F. S. Foster, “Development and initial application of a fully integrated photoacoustic micro-ultrasound system,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60(5), 888–897 (2013).
[Crossref] [PubMed]

Hofmann, R.

R. von Knobloch, J. Weber, Z. Varga, H. Feiber, A. Heidenreich, and R. Hofmann, “Bilateral fine-needle administered local anaesthetic nerve block for pain control during TRUS-guided multi-core prostate biopsy: a prospective randomised trial,” Eur. Urol. 41(5), 508–514 (2002).
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Hu, S.

L. V. Wang and S. Hu, “Photoacoustic tomography: in vivo imaging from organelles to organs,” Science 335(6075), 1458–1462 (2012).
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Hunt, K. K.

S. Krishnamurthy, N. Sneige, D. G. Bedi, B. S. Edieken, B. D. Fornage, H. M. Kuerer, S. E. Singletary, and K. K. Hunt, “Role of ultrasound-guided fine-needle aspiration of indeterminate and suspicious axillary lymph nodes in the initial staging of breast carcinoma,” Cancer 95(5), 982–988 (2002).
[Crossref] [PubMed]

Hutteman, M.

M. Hutteman, H. S. Choi, J. S. Mieog, J. R. van der Vorst, Y. Ashitate, P. J. Kuppen, M. C. van Groningen, C. W. Löwik, V. T. Smit, C. J. van de Velde, J. V. Frangioni, and A. L. Vahrmeijer, “Clinical translation of ex vivo sentinel lymph node mapping for colorectal cancer using invisible near-infrared fluorescence light,” Ann. Surg. Oncol. 18(4), 1006–1014 (2011).
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S. L. Jacques, “Optical properties of biological tissues: a review,” Phys. Med. Biol. 58(11), R37–R61 (2013).
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Jankovic, L.

T. N. Erpelding, C. Kim, M. Pramanik, L. Jankovic, K. Maslov, Z. Guo, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Sentinel lymph nodes in the rat: noninvasive photoacoustic and US imaging with a clinical US system,” Radiology 256(1), 102–110 (2010).
[Crossref] [PubMed]

C. Kim, T. N. Erpelding, K. Maslov, L. Jankovic, W. J. Akers, L. Song, S. Achilefu, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Handheld array-based photoacoustic probe for guiding needle biopsy of sentinel lymph nodes,” J. Biomed. Opt. 15(4), 046010 (2010).
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Jing, Y.

T. Wang and Y. Jing, “Transcranial ultrasound imaging with speed of sound-based phase correction: a numerical study,” Phys. Med. Biol. 58(19), 6663–6681 (2013).
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Jung, Y.

J. Kim, S. Park, Y. Jung, S. Chang, J. Park, Y. Zhang, J. F. Lovell, and C. Kim, “Programmable real-time clinical photoacoustic and ultrasound imaging system,” Sci. Rep. 6(1), 35137 (2016).
[Crossref] [PubMed]

Kim, C.

J. Kim, S. Park, Y. Jung, S. Chang, J. Park, Y. Zhang, J. F. Lovell, and C. Kim, “Programmable real-time clinical photoacoustic and ultrasound imaging system,” Sci. Rep. 6(1), 35137 (2016).
[Crossref] [PubMed]

T. N. Erpelding, C. Kim, M. Pramanik, L. Jankovic, K. Maslov, Z. Guo, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Sentinel lymph nodes in the rat: noninvasive photoacoustic and US imaging with a clinical US system,” Radiology 256(1), 102–110 (2010).
[Crossref] [PubMed]

C. Kim, T. N. Erpelding, K. Maslov, L. Jankovic, W. J. Akers, L. Song, S. Achilefu, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Handheld array-based photoacoustic probe for guiding needle biopsy of sentinel lymph nodes,” J. Biomed. Opt. 15(4), 046010 (2010).
[Crossref] [PubMed]

Kim, J.

J. Kim, S. Park, Y. Jung, S. Chang, J. Park, Y. Zhang, J. F. Lovell, and C. Kim, “Programmable real-time clinical photoacoustic and ultrasound imaging system,” Sci. Rep. 6(1), 35137 (2016).
[Crossref] [PubMed]

Kirgan, D. M.

A. E. Giuliano, D. M. Kirgan, J. M. Guenther, and D. L. Morton, “Lymphatic mapping and sentinel lymphadenectomy for breast cancer,” Ann. Surg. 220(3), 391–401 (1994).
[Crossref] [PubMed]

Klevesath, M. B.

A. D. Purushotham, S. Upponi, M. B. Klevesath, L. Bobrow, K. Millar, J. P. Myles, and S. W. Duffy, “Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial,” J. Clin. Oncol. 23(19), 4312–4321 (2005).
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Kohl, A.

Kolkman, R. G.

R. G. Kolkman, P. J. Brands, W. Steenbergen, and T. G. van Leeuwen, “Real-time in vivo photoacoustic and ultrasound imaging,” J. Biomed. Opt. 13(5), 050510 (2008).
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Krishnamurthy, S.

S. Krishnamurthy, N. Sneige, D. G. Bedi, B. S. Edieken, B. D. Fornage, H. M. Kuerer, S. E. Singletary, and K. K. Hunt, “Role of ultrasound-guided fine-needle aspiration of indeterminate and suspicious axillary lymph nodes in the initial staging of breast carcinoma,” Cancer 95(5), 982–988 (2002).
[Crossref] [PubMed]

Kuerer, H. M.

S. Krishnamurthy, N. Sneige, D. G. Bedi, B. S. Edieken, B. D. Fornage, H. M. Kuerer, S. E. Singletary, and K. K. Hunt, “Role of ultrasound-guided fine-needle aspiration of indeterminate and suspicious axillary lymph nodes in the initial staging of breast carcinoma,” Cancer 95(5), 982–988 (2002).
[Crossref] [PubMed]

Kuppen, P. J.

M. Hutteman, H. S. Choi, J. S. Mieog, J. R. van der Vorst, Y. Ashitate, P. J. Kuppen, M. C. van Groningen, C. W. Löwik, V. T. Smit, C. J. van de Velde, J. V. Frangioni, and A. L. Vahrmeijer, “Clinical translation of ex vivo sentinel lymph node mapping for colorectal cancer using invisible near-infrared fluorescence light,” Ann. Surg. Oncol. 18(4), 1006–1014 (2011).
[Crossref] [PubMed]

Li, C.

Y. Zhou, G. Li, L. Zhu, C. Li, L. A. Cornelius, and L. V. Wang, “Handheld photoacoustic probe to detect both melanoma depth and volume at high speed in vivo,” J. Biophotonics 8(11-12), 961–967 (2015).
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Li, G.

Y. Zhou, G. Li, L. Zhu, C. Li, L. A. Cornelius, and L. V. Wang, “Handheld photoacoustic probe to detect both melanoma depth and volume at high speed in vivo,” J. Biophotonics 8(11-12), 961–967 (2015).
[Crossref] [PubMed]

Lovell, J. F.

J. Kim, S. Park, Y. Jung, S. Chang, J. Park, Y. Zhang, J. F. Lovell, and C. Kim, “Programmable real-time clinical photoacoustic and ultrasound imaging system,” Sci. Rep. 6(1), 35137 (2016).
[Crossref] [PubMed]

Löwik, C. W.

M. Hutteman, H. S. Choi, J. S. Mieog, J. R. van der Vorst, Y. Ashitate, P. J. Kuppen, M. C. van Groningen, C. W. Löwik, V. T. Smit, C. J. van de Velde, J. V. Frangioni, and A. L. Vahrmeijer, “Clinical translation of ex vivo sentinel lymph node mapping for colorectal cancer using invisible near-infrared fluorescence light,” Ann. Surg. Oncol. 18(4), 1006–1014 (2011).
[Crossref] [PubMed]

Margenthaler, J. A.

C. Kim, T. N. Erpelding, K. Maslov, L. Jankovic, W. J. Akers, L. Song, S. Achilefu, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Handheld array-based photoacoustic probe for guiding needle biopsy of sentinel lymph nodes,” J. Biomed. Opt. 15(4), 046010 (2010).
[Crossref] [PubMed]

T. N. Erpelding, C. Kim, M. Pramanik, L. Jankovic, K. Maslov, Z. Guo, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Sentinel lymph nodes in the rat: noninvasive photoacoustic and US imaging with a clinical US system,” Radiology 256(1), 102–110 (2010).
[Crossref] [PubMed]

Mariani, G.

G. Mariani, L. Moresco, G. Viale, G. Villa, M. Bagnasco, G. Canavese, J. Buscombe, H. W. Strauss, and G. Paganelli, “Radioguided sentinel lymph node biopsy in breast cancer surgery,” J. Nucl. Med. 42(8), 1198–1215 (2001).
[PubMed]

Maslov, K.

C. Kim, T. N. Erpelding, K. Maslov, L. Jankovic, W. J. Akers, L. Song, S. Achilefu, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Handheld array-based photoacoustic probe for guiding needle biopsy of sentinel lymph nodes,” J. Biomed. Opt. 15(4), 046010 (2010).
[Crossref] [PubMed]

T. N. Erpelding, C. Kim, M. Pramanik, L. Jankovic, K. Maslov, Z. Guo, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Sentinel lymph nodes in the rat: noninvasive photoacoustic and US imaging with a clinical US system,” Radiology 256(1), 102–110 (2010).
[Crossref] [PubMed]

L. Song, K. Maslov, R. Bitton, K. K. Shung, and L. V. Wang, “Fast 3-D dark-field reflection-mode photoacoustic microscopy in vivo with a 30-MHz ultrasound linear array,” J. Biomed. Opt. 13(5), 054028 (2008).
[Crossref] [PubMed]

Mieog, J. S.

M. Hutteman, H. S. Choi, J. S. Mieog, J. R. van der Vorst, Y. Ashitate, P. J. Kuppen, M. C. van Groningen, C. W. Löwik, V. T. Smit, C. J. van de Velde, J. V. Frangioni, and A. L. Vahrmeijer, “Clinical translation of ex vivo sentinel lymph node mapping for colorectal cancer using invisible near-infrared fluorescence light,” Ann. Surg. Oncol. 18(4), 1006–1014 (2011).
[Crossref] [PubMed]

Millar, K.

A. D. Purushotham, S. Upponi, M. B. Klevesath, L. Bobrow, K. Millar, J. P. Myles, and S. W. Duffy, “Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial,” J. Clin. Oncol. 23(19), 4312–4321 (2005).
[Crossref] [PubMed]

Montilla, L. G.

L. G. Montilla, R. Olafsson, D. R. Bauer, and R. S. Witte, “Real-time photoacoustic and ultrasound imaging: a simple solution for clinical ultrasound systems with linear arrays,” Phys. Med. Biol. 58(1), N1–N12 (2013).
[Crossref] [PubMed]

Moresco, L.

G. Mariani, L. Moresco, G. Viale, G. Villa, M. Bagnasco, G. Canavese, J. Buscombe, H. W. Strauss, and G. Paganelli, “Radioguided sentinel lymph node biopsy in breast cancer surgery,” J. Nucl. Med. 42(8), 1198–1215 (2001).
[PubMed]

Morton, D. L.

A. E. Giuliano, D. M. Kirgan, J. M. Guenther, and D. L. Morton, “Lymphatic mapping and sentinel lymphadenectomy for breast cancer,” Ann. Surg. 220(3), 391–401 (1994).
[Crossref] [PubMed]

Myles, J. P.

A. D. Purushotham, S. Upponi, M. B. Klevesath, L. Bobrow, K. Millar, J. P. Myles, and S. W. Duffy, “Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial,” J. Clin. Oncol. 23(19), 4312–4321 (2005).
[Crossref] [PubMed]

Needles, A.

A. Needles, A. Heinmiller, J. Sun, C. Theodoropoulos, D. Bates, D. Hirson, M. Yin, and F. S. Foster, “Development and initial application of a fully integrated photoacoustic micro-ultrasound system,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60(5), 888–897 (2013).
[Crossref] [PubMed]

Olafsson, R.

L. G. Montilla, R. Olafsson, D. R. Bauer, and R. S. Witte, “Real-time photoacoustic and ultrasound imaging: a simple solution for clinical ultrasound systems with linear arrays,” Phys. Med. Biol. 58(1), N1–N12 (2013).
[Crossref] [PubMed]

Paganelli, G.

G. Mariani, L. Moresco, G. Viale, G. Villa, M. Bagnasco, G. Canavese, J. Buscombe, H. W. Strauss, and G. Paganelli, “Radioguided sentinel lymph node biopsy in breast cancer surgery,” J. Nucl. Med. 42(8), 1198–1215 (2001).
[PubMed]

Park, J.

J. Kim, S. Park, Y. Jung, S. Chang, J. Park, Y. Zhang, J. F. Lovell, and C. Kim, “Programmable real-time clinical photoacoustic and ultrasound imaging system,” Sci. Rep. 6(1), 35137 (2016).
[Crossref] [PubMed]

Park, S.

J. Kim, S. Park, Y. Jung, S. Chang, J. Park, Y. Zhang, J. F. Lovell, and C. Kim, “Programmable real-time clinical photoacoustic and ultrasound imaging system,” Sci. Rep. 6(1), 35137 (2016).
[Crossref] [PubMed]

Pashley, M. D.

T. N. Erpelding, C. Kim, M. Pramanik, L. Jankovic, K. Maslov, Z. Guo, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Sentinel lymph nodes in the rat: noninvasive photoacoustic and US imaging with a clinical US system,” Radiology 256(1), 102–110 (2010).
[Crossref] [PubMed]

C. Kim, T. N. Erpelding, K. Maslov, L. Jankovic, W. J. Akers, L. Song, S. Achilefu, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Handheld array-based photoacoustic probe for guiding needle biopsy of sentinel lymph nodes,” J. Biomed. Opt. 15(4), 046010 (2010).
[Crossref] [PubMed]

Periyasamy, V.

K. Sivasubramanian, V. Periyasamy, and M. Pramanik, “Hand-held clinical photoacoustic imaging system for real-time non-invasive small animal imaging,” J. Vis. Exp. 128(128), e56649 (2017).
[PubMed]

K. Sivasubramanian, V. Periyasamy, and M. Pramanik, “Non-invasive sentinel lymph node mapping and needle guidance using clinical handheld photoacoustic imaging system in small animal,” J. Biophotonics 10, 1–10 (2017).
[PubMed]

K. Sivasubramanian, V. Periyasamy, K. K. Wen, and M. Pramanik, “Optimizing light delivery through fiber bundle in photoacoustic imaging with clinical ultrasound system: Monte Carlo simulation and experimental validation,” J. Biomed. Opt. 22(4), 041008 (2016).
[Crossref] [PubMed]

Pramanik, M.

K. Sivasubramanian, V. Periyasamy, and M. Pramanik, “Non-invasive sentinel lymph node mapping and needle guidance using clinical handheld photoacoustic imaging system in small animal,” J. Biophotonics 10, 1–10 (2017).
[PubMed]

K. Sivasubramanian, V. Periyasamy, and M. Pramanik, “Hand-held clinical photoacoustic imaging system for real-time non-invasive small animal imaging,” J. Vis. Exp. 128(128), e56649 (2017).
[PubMed]

K. Sivasubramanian, V. Periyasamy, K. K. Wen, and M. Pramanik, “Optimizing light delivery through fiber bundle in photoacoustic imaging with clinical ultrasound system: Monte Carlo simulation and experimental validation,” J. Biomed. Opt. 22(4), 041008 (2016).
[Crossref] [PubMed]

K. Sivasubramanian and M. Pramanik, “High frame rate photoacoustic imaging at 7000 frames per second using clinical ultrasound system,” Biomed. Opt. Express 7(2), 312–323 (2016).
[Crossref] [PubMed]

T. N. Erpelding, C. Kim, M. Pramanik, L. Jankovic, K. Maslov, Z. Guo, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Sentinel lymph nodes in the rat: noninvasive photoacoustic and US imaging with a clinical US system,” Radiology 256(1), 102–110 (2010).
[Crossref] [PubMed]

Purushotham, A. D.

A. D. Purushotham, S. Upponi, M. B. Klevesath, L. Bobrow, K. Millar, J. P. Myles, and S. W. Duffy, “Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial,” J. Clin. Oncol. 23(19), 4312–4321 (2005).
[Crossref] [PubMed]

Rabot, O.

Schlag, P. M.

T. Schulze, A. Bembenek, and P. M. Schlag, “Sentinel lymph node biopsy progress in surgical treatment of cancer,” Langenbecks Arch. Surg. 389(6), 532–550 (2004).
[Crossref] [PubMed]

Schulze, T.

T. Schulze, A. Bembenek, and P. M. Schlag, “Sentinel lymph node biopsy progress in surgical treatment of cancer,” Langenbecks Arch. Surg. 389(6), 532–550 (2004).
[Crossref] [PubMed]

Shung, K. K.

L. Song, K. Maslov, R. Bitton, K. K. Shung, and L. V. Wang, “Fast 3-D dark-field reflection-mode photoacoustic microscopy in vivo with a 30-MHz ultrasound linear array,” J. Biomed. Opt. 13(5), 054028 (2008).
[Crossref] [PubMed]

Simatos, A.

B. D. Fornage, M. J. Faroux, and A. Simatos, “Breast masses: US-guided fine-needle aspiration biopsy,” Radiology 162(2), 409–414 (1987).
[Crossref] [PubMed]

Singletary, S. E.

S. Krishnamurthy, N. Sneige, D. G. Bedi, B. S. Edieken, B. D. Fornage, H. M. Kuerer, S. E. Singletary, and K. K. Hunt, “Role of ultrasound-guided fine-needle aspiration of indeterminate and suspicious axillary lymph nodes in the initial staging of breast carcinoma,” Cancer 95(5), 982–988 (2002).
[Crossref] [PubMed]

Sivasubramanian, K.

K. Sivasubramanian, V. Periyasamy, and M. Pramanik, “Non-invasive sentinel lymph node mapping and needle guidance using clinical handheld photoacoustic imaging system in small animal,” J. Biophotonics 10, 1–10 (2017).
[PubMed]

K. Sivasubramanian, V. Periyasamy, and M. Pramanik, “Hand-held clinical photoacoustic imaging system for real-time non-invasive small animal imaging,” J. Vis. Exp. 128(128), e56649 (2017).
[PubMed]

K. Sivasubramanian and M. Pramanik, “High frame rate photoacoustic imaging at 7000 frames per second using clinical ultrasound system,” Biomed. Opt. Express 7(2), 312–323 (2016).
[Crossref] [PubMed]

K. Sivasubramanian, V. Periyasamy, K. K. Wen, and M. Pramanik, “Optimizing light delivery through fiber bundle in photoacoustic imaging with clinical ultrasound system: Monte Carlo simulation and experimental validation,” J. Biomed. Opt. 22(4), 041008 (2016).
[Crossref] [PubMed]

Smit, V. T.

M. Hutteman, H. S. Choi, J. S. Mieog, J. R. van der Vorst, Y. Ashitate, P. J. Kuppen, M. C. van Groningen, C. W. Löwik, V. T. Smit, C. J. van de Velde, J. V. Frangioni, and A. L. Vahrmeijer, “Clinical translation of ex vivo sentinel lymph node mapping for colorectal cancer using invisible near-infrared fluorescence light,” Ann. Surg. Oncol. 18(4), 1006–1014 (2011).
[Crossref] [PubMed]

Sneige, N.

S. Krishnamurthy, N. Sneige, D. G. Bedi, B. S. Edieken, B. D. Fornage, H. M. Kuerer, S. E. Singletary, and K. K. Hunt, “Role of ultrasound-guided fine-needle aspiration of indeterminate and suspicious axillary lymph nodes in the initial staging of breast carcinoma,” Cancer 95(5), 982–988 (2002).
[Crossref] [PubMed]

Song, L.

C. Kim, T. N. Erpelding, K. Maslov, L. Jankovic, W. J. Akers, L. Song, S. Achilefu, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Handheld array-based photoacoustic probe for guiding needle biopsy of sentinel lymph nodes,” J. Biomed. Opt. 15(4), 046010 (2010).
[Crossref] [PubMed]

L. Song, K. Maslov, R. Bitton, K. K. Shung, and L. V. Wang, “Fast 3-D dark-field reflection-mode photoacoustic microscopy in vivo with a 30-MHz ultrasound linear array,” J. Biomed. Opt. 13(5), 054028 (2008).
[Crossref] [PubMed]

Steenbergen, W.

Strauss, H. W.

G. Mariani, L. Moresco, G. Viale, G. Villa, M. Bagnasco, G. Canavese, J. Buscombe, H. W. Strauss, and G. Paganelli, “Radioguided sentinel lymph node biopsy in breast cancer surgery,” J. Nucl. Med. 42(8), 1198–1215 (2001).
[PubMed]

Sun, J.

A. Needles, A. Heinmiller, J. Sun, C. Theodoropoulos, D. Bates, D. Hirson, M. Yin, and F. S. Foster, “Development and initial application of a fully integrated photoacoustic micro-ultrasound system,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60(5), 888–897 (2013).
[Crossref] [PubMed]

Theodoropoulos, C.

A. Needles, A. Heinmiller, J. Sun, C. Theodoropoulos, D. Bates, D. Hirson, M. Yin, and F. S. Foster, “Development and initial application of a fully integrated photoacoustic micro-ultrasound system,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60(5), 888–897 (2013).
[Crossref] [PubMed]

Tisserand, S.

Upponi, S.

A. D. Purushotham, S. Upponi, M. B. Klevesath, L. Bobrow, K. Millar, J. P. Myles, and S. W. Duffy, “Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial,” J. Clin. Oncol. 23(19), 4312–4321 (2005).
[Crossref] [PubMed]

Vahrmeijer, A. L.

M. Hutteman, H. S. Choi, J. S. Mieog, J. R. van der Vorst, Y. Ashitate, P. J. Kuppen, M. C. van Groningen, C. W. Löwik, V. T. Smit, C. J. van de Velde, J. V. Frangioni, and A. L. Vahrmeijer, “Clinical translation of ex vivo sentinel lymph node mapping for colorectal cancer using invisible near-infrared fluorescence light,” Ann. Surg. Oncol. 18(4), 1006–1014 (2011).
[Crossref] [PubMed]

van de Velde, C. J.

M. Hutteman, H. S. Choi, J. S. Mieog, J. R. van der Vorst, Y. Ashitate, P. J. Kuppen, M. C. van Groningen, C. W. Löwik, V. T. Smit, C. J. van de Velde, J. V. Frangioni, and A. L. Vahrmeijer, “Clinical translation of ex vivo sentinel lymph node mapping for colorectal cancer using invisible near-infrared fluorescence light,” Ann. Surg. Oncol. 18(4), 1006–1014 (2011).
[Crossref] [PubMed]

J. Bonnema and C. J. van de Velde, “Sentinel lymph node biopsy in breast cancer,” Ann. Oncol. 13(10), 1531–1537 (2002).
[Crossref] [PubMed]

van den Berg, P. J.

van der Vorst, J. R.

M. Hutteman, H. S. Choi, J. S. Mieog, J. R. van der Vorst, Y. Ashitate, P. J. Kuppen, M. C. van Groningen, C. W. Löwik, V. T. Smit, C. J. van de Velde, J. V. Frangioni, and A. L. Vahrmeijer, “Clinical translation of ex vivo sentinel lymph node mapping for colorectal cancer using invisible near-infrared fluorescence light,” Ann. Surg. Oncol. 18(4), 1006–1014 (2011).
[Crossref] [PubMed]

van Groningen, M. C.

M. Hutteman, H. S. Choi, J. S. Mieog, J. R. van der Vorst, Y. Ashitate, P. J. Kuppen, M. C. van Groningen, C. W. Löwik, V. T. Smit, C. J. van de Velde, J. V. Frangioni, and A. L. Vahrmeijer, “Clinical translation of ex vivo sentinel lymph node mapping for colorectal cancer using invisible near-infrared fluorescence light,” Ann. Surg. Oncol. 18(4), 1006–1014 (2011).
[Crossref] [PubMed]

van Leeuwen, T. G.

R. G. Kolkman, P. J. Brands, W. Steenbergen, and T. G. van Leeuwen, “Real-time in vivo photoacoustic and ultrasound imaging,” J. Biomed. Opt. 13(5), 050510 (2008).
[Crossref] [PubMed]

Varga, Z.

R. von Knobloch, J. Weber, Z. Varga, H. Feiber, A. Heidenreich, and R. Hofmann, “Bilateral fine-needle administered local anaesthetic nerve block for pain control during TRUS-guided multi-core prostate biopsy: a prospective randomised trial,” Eur. Urol. 41(5), 508–514 (2002).
[Crossref] [PubMed]

Viale, G.

G. Mariani, L. Moresco, G. Viale, G. Villa, M. Bagnasco, G. Canavese, J. Buscombe, H. W. Strauss, and G. Paganelli, “Radioguided sentinel lymph node biopsy in breast cancer surgery,” J. Nucl. Med. 42(8), 1198–1215 (2001).
[PubMed]

Villa, G.

G. Mariani, L. Moresco, G. Viale, G. Villa, M. Bagnasco, G. Canavese, J. Buscombe, H. W. Strauss, and G. Paganelli, “Radioguided sentinel lymph node biopsy in breast cancer surgery,” J. Nucl. Med. 42(8), 1198–1215 (2001).
[PubMed]

von Knobloch, R.

R. von Knobloch, J. Weber, Z. Varga, H. Feiber, A. Heidenreich, and R. Hofmann, “Bilateral fine-needle administered local anaesthetic nerve block for pain control during TRUS-guided multi-core prostate biopsy: a prospective randomised trial,” Eur. Urol. 41(5), 508–514 (2002).
[Crossref] [PubMed]

Wang, L. V.

Y. Zhou, G. Li, L. Zhu, C. Li, L. A. Cornelius, and L. V. Wang, “Handheld photoacoustic probe to detect both melanoma depth and volume at high speed in vivo,” J. Biophotonics 8(11-12), 961–967 (2015).
[Crossref] [PubMed]

L. V. Wang and S. Hu, “Photoacoustic tomography: in vivo imaging from organelles to organs,” Science 335(6075), 1458–1462 (2012).
[Crossref] [PubMed]

C. Kim, T. N. Erpelding, K. Maslov, L. Jankovic, W. J. Akers, L. Song, S. Achilefu, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Handheld array-based photoacoustic probe for guiding needle biopsy of sentinel lymph nodes,” J. Biomed. Opt. 15(4), 046010 (2010).
[Crossref] [PubMed]

T. N. Erpelding, C. Kim, M. Pramanik, L. Jankovic, K. Maslov, Z. Guo, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Sentinel lymph nodes in the rat: noninvasive photoacoustic and US imaging with a clinical US system,” Radiology 256(1), 102–110 (2010).
[Crossref] [PubMed]

L. V. Wang, “Multiscale photoacoustic microscopy and computed tomography,” Nat. Photonics 3(9), 503–509 (2009).
[Crossref] [PubMed]

L. Song, K. Maslov, R. Bitton, K. K. Shung, and L. V. Wang, “Fast 3-D dark-field reflection-mode photoacoustic microscopy in vivo with a 30-MHz ultrasound linear array,” J. Biomed. Opt. 13(5), 054028 (2008).
[Crossref] [PubMed]

M. Xu and L. V. Wang, “Universal back-projection algorithm for photoacoustic computed tomography,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 71(1), 016706 (2005).
[Crossref] [PubMed]

Wang, T.

T. Wang and Y. Jing, “Transcranial ultrasound imaging with speed of sound-based phase correction: a numerical study,” Phys. Med. Biol. 58(19), 6663–6681 (2013).
[Crossref] [PubMed]

Weber, J.

R. von Knobloch, J. Weber, Z. Varga, H. Feiber, A. Heidenreich, and R. Hofmann, “Bilateral fine-needle administered local anaesthetic nerve block for pain control during TRUS-guided multi-core prostate biopsy: a prospective randomised trial,” Eur. Urol. 41(5), 508–514 (2002).
[Crossref] [PubMed]

Wen, K. K.

K. Sivasubramanian, V. Periyasamy, K. K. Wen, and M. Pramanik, “Optimizing light delivery through fiber bundle in photoacoustic imaging with clinical ultrasound system: Monte Carlo simulation and experimental validation,” J. Biomed. Opt. 22(4), 041008 (2016).
[Crossref] [PubMed]

Witte, R. S.

L. G. Montilla, R. Olafsson, D. R. Bauer, and R. S. Witte, “Real-time photoacoustic and ultrasound imaging: a simple solution for clinical ultrasound systems with linear arrays,” Phys. Med. Biol. 58(1), N1–N12 (2013).
[Crossref] [PubMed]

Xu, M.

M. Xu and L. V. Wang, “Universal back-projection algorithm for photoacoustic computed tomography,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 71(1), 016706 (2005).
[Crossref] [PubMed]

Yin, M.

A. Needles, A. Heinmiller, J. Sun, C. Theodoropoulos, D. Bates, D. Hirson, M. Yin, and F. S. Foster, “Development and initial application of a fully integrated photoacoustic micro-ultrasound system,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60(5), 888–897 (2013).
[Crossref] [PubMed]

Zhang, Y.

J. Kim, S. Park, Y. Jung, S. Chang, J. Park, Y. Zhang, J. F. Lovell, and C. Kim, “Programmable real-time clinical photoacoustic and ultrasound imaging system,” Sci. Rep. 6(1), 35137 (2016).
[Crossref] [PubMed]

Zhou, Y.

Y. Zhou, G. Li, L. Zhu, C. Li, L. A. Cornelius, and L. V. Wang, “Handheld photoacoustic probe to detect both melanoma depth and volume at high speed in vivo,” J. Biophotonics 8(11-12), 961–967 (2015).
[Crossref] [PubMed]

Zhu, L.

Y. Zhou, G. Li, L. Zhu, C. Li, L. A. Cornelius, and L. V. Wang, “Handheld photoacoustic probe to detect both melanoma depth and volume at high speed in vivo,” J. Biophotonics 8(11-12), 961–967 (2015).
[Crossref] [PubMed]

Ann. Oncol. (1)

J. Bonnema and C. J. van de Velde, “Sentinel lymph node biopsy in breast cancer,” Ann. Oncol. 13(10), 1531–1537 (2002).
[Crossref] [PubMed]

Ann. Surg. (1)

A. E. Giuliano, D. M. Kirgan, J. M. Guenther, and D. L. Morton, “Lymphatic mapping and sentinel lymphadenectomy for breast cancer,” Ann. Surg. 220(3), 391–401 (1994).
[Crossref] [PubMed]

Ann. Surg. Oncol. (1)

M. Hutteman, H. S. Choi, J. S. Mieog, J. R. van der Vorst, Y. Ashitate, P. J. Kuppen, M. C. van Groningen, C. W. Löwik, V. T. Smit, C. J. van de Velde, J. V. Frangioni, and A. L. Vahrmeijer, “Clinical translation of ex vivo sentinel lymph node mapping for colorectal cancer using invisible near-infrared fluorescence light,” Ann. Surg. Oncol. 18(4), 1006–1014 (2011).
[Crossref] [PubMed]

Biomed. Opt. Express (1)

Cancer (1)

S. Krishnamurthy, N. Sneige, D. G. Bedi, B. S. Edieken, B. D. Fornage, H. M. Kuerer, S. E. Singletary, and K. K. Hunt, “Role of ultrasound-guided fine-needle aspiration of indeterminate and suspicious axillary lymph nodes in the initial staging of breast carcinoma,” Cancer 95(5), 982–988 (2002).
[Crossref] [PubMed]

Eur. Urol. (1)

R. von Knobloch, J. Weber, Z. Varga, H. Feiber, A. Heidenreich, and R. Hofmann, “Bilateral fine-needle administered local anaesthetic nerve block for pain control during TRUS-guided multi-core prostate biopsy: a prospective randomised trial,” Eur. Urol. 41(5), 508–514 (2002).
[Crossref] [PubMed]

IEEE Trans. Pattern Anal. Mach. Intell. (1)

M. S. Hassouna and A. A. Farag, “Multi-stencils fast marching methods: A highly accurate solution to the eikonal equation on cartesian domains,” IEEE Trans. Pattern Anal. Mach. Intell. 29(9), 1563–1574 (2007).
[Crossref] [PubMed]

IEEE Trans. Ultrason. Ferroelectr. Freq. Control (1)

A. Needles, A. Heinmiller, J. Sun, C. Theodoropoulos, D. Bates, D. Hirson, M. Yin, and F. S. Foster, “Development and initial application of a fully integrated photoacoustic micro-ultrasound system,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60(5), 888–897 (2013).
[Crossref] [PubMed]

Interface Focus (1)

P. Beard, “Biomedical photoacoustic imaging,” Interface Focus 1(4), 602–631 (2011).
[Crossref] [PubMed]

J. Biomed. Opt. (4)

C. Kim, T. N. Erpelding, K. Maslov, L. Jankovic, W. J. Akers, L. Song, S. Achilefu, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Handheld array-based photoacoustic probe for guiding needle biopsy of sentinel lymph nodes,” J. Biomed. Opt. 15(4), 046010 (2010).
[Crossref] [PubMed]

L. Song, K. Maslov, R. Bitton, K. K. Shung, and L. V. Wang, “Fast 3-D dark-field reflection-mode photoacoustic microscopy in vivo with a 30-MHz ultrasound linear array,” J. Biomed. Opt. 13(5), 054028 (2008).
[Crossref] [PubMed]

R. G. Kolkman, P. J. Brands, W. Steenbergen, and T. G. van Leeuwen, “Real-time in vivo photoacoustic and ultrasound imaging,” J. Biomed. Opt. 13(5), 050510 (2008).
[Crossref] [PubMed]

K. Sivasubramanian, V. Periyasamy, K. K. Wen, and M. Pramanik, “Optimizing light delivery through fiber bundle in photoacoustic imaging with clinical ultrasound system: Monte Carlo simulation and experimental validation,” J. Biomed. Opt. 22(4), 041008 (2016).
[Crossref] [PubMed]

J. Biophotonics (2)

K. Sivasubramanian, V. Periyasamy, and M. Pramanik, “Non-invasive sentinel lymph node mapping and needle guidance using clinical handheld photoacoustic imaging system in small animal,” J. Biophotonics 10, 1–10 (2017).
[PubMed]

Y. Zhou, G. Li, L. Zhu, C. Li, L. A. Cornelius, and L. V. Wang, “Handheld photoacoustic probe to detect both melanoma depth and volume at high speed in vivo,” J. Biophotonics 8(11-12), 961–967 (2015).
[Crossref] [PubMed]

J. Clin. Oncol. (1)

A. D. Purushotham, S. Upponi, M. B. Klevesath, L. Bobrow, K. Millar, J. P. Myles, and S. W. Duffy, “Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial,” J. Clin. Oncol. 23(19), 4312–4321 (2005).
[Crossref] [PubMed]

J. Nucl. Med. (1)

G. Mariani, L. Moresco, G. Viale, G. Villa, M. Bagnasco, G. Canavese, J. Buscombe, H. W. Strauss, and G. Paganelli, “Radioguided sentinel lymph node biopsy in breast cancer surgery,” J. Nucl. Med. 42(8), 1198–1215 (2001).
[PubMed]

J. Vis. Exp. (1)

K. Sivasubramanian, V. Periyasamy, and M. Pramanik, “Hand-held clinical photoacoustic imaging system for real-time non-invasive small animal imaging,” J. Vis. Exp. 128(128), e56649 (2017).
[PubMed]

Langenbecks Arch. Surg. (1)

T. Schulze, A. Bembenek, and P. M. Schlag, “Sentinel lymph node biopsy progress in surgical treatment of cancer,” Langenbecks Arch. Surg. 389(6), 532–550 (2004).
[Crossref] [PubMed]

Nat. Photonics (1)

L. V. Wang, “Multiscale photoacoustic microscopy and computed tomography,” Nat. Photonics 3(9), 503–509 (2009).
[Crossref] [PubMed]

Opt. Express (1)

Phys. Med. Biol. (3)

L. G. Montilla, R. Olafsson, D. R. Bauer, and R. S. Witte, “Real-time photoacoustic and ultrasound imaging: a simple solution for clinical ultrasound systems with linear arrays,” Phys. Med. Biol. 58(1), N1–N12 (2013).
[Crossref] [PubMed]

S. L. Jacques, “Optical properties of biological tissues: a review,” Phys. Med. Biol. 58(11), R37–R61 (2013).
[Crossref] [PubMed]

T. Wang and Y. Jing, “Transcranial ultrasound imaging with speed of sound-based phase correction: a numerical study,” Phys. Med. Biol. 58(19), 6663–6681 (2013).
[Crossref] [PubMed]

Phys. Rev. E Stat. Nonlin. Soft Matter Phys. (1)

M. Xu and L. V. Wang, “Universal back-projection algorithm for photoacoustic computed tomography,” Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 71(1), 016706 (2005).
[Crossref] [PubMed]

Radiology (2)

T. N. Erpelding, C. Kim, M. Pramanik, L. Jankovic, K. Maslov, Z. Guo, J. A. Margenthaler, M. D. Pashley, and L. V. Wang, “Sentinel lymph nodes in the rat: noninvasive photoacoustic and US imaging with a clinical US system,” Radiology 256(1), 102–110 (2010).
[Crossref] [PubMed]

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[Crossref] [PubMed]

Sci. Rep. (1)

J. Kim, S. Park, Y. Jung, S. Chang, J. Park, Y. Zhang, J. F. Lovell, and C. Kim, “Programmable real-time clinical photoacoustic and ultrasound imaging system,” Sci. Rep. 6(1), 35137 (2016).
[Crossref] [PubMed]

Science (1)

L. V. Wang and S. Hu, “Photoacoustic tomography: in vivo imaging from organelles to organs,” Science 335(6075), 1458–1462 (2012).
[Crossref] [PubMed]

Other (4)

S. A. Ermilov, M. P. Fronheiser, H.-P. Brecht, R. Su, A. Conjusteau, K. Mehta, P. Otto, and A. A. Oraevsky, “Development of laser optoacoustic and ultrasonic imaging system for breast cancer utilizing handheld array probes,” SPIE BiOS: Biomedical Optics, 717703 (2009).

P. D. Kumavor, A. Aguirre, C. Xu, J. Gamelin, Y. Ardeshirpour, B. Tavakoli, S. Zanganeh, U. S. Alqasemi, Q. Zhu, “Target detection and characterization using a hybrid handheld diffuse optical tomography and photoacoustic tomography system,” SPIE BiOS, 789614 (2011).

Laser Institute of America, American National Standard for Safe Use of Lasers ANSI Z136.1–2000 (American National Standards Institute, Inc., New York, NY, 2000).

T. Wang and Y. Jing, “A fast marching method based back projection algorithm for photoacoustic tomography in heterogeneous media,” Phys. arXiv preprint arXiv:1501.03869 (2015).

Supplementary Material (2)

NameDescription
Visualization 1       ICG accumulation dynamics in the SLN
Visualization 2       SLN needle aspiration biopsy process based on the guidance of real-time photoacoustic imaging

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Figures (8)
Fig. 1
Fig. 1 Different optical illumination schemes of photoacoustic imaging based on a handheld array ultrasound scanner. (a) Conventional dark-field illumination with angled fiber bundles. (b) Bright-field illumination proposed in this study. (c) Light illumination pattern at the tissue surface for the dark-field. (d) Light illumination pattern at the tissue surface for the bright-field. US: ultrasound.

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Fig. 2
Fig. 2 Schematic illustration and photograph of the probe design proposed in this study. (a) Side view of the probe, which includes the shell holder, optical fiber, ultrasound probe, seal rings, two cylindrical lenses and an optical/acoustic coupling module. (b) Oblique view of the probe. (c) Photograph of the probe.

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Fig. 3
Fig. 3 Schematic of the photoacoustic imaging system.

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Fig. 4
Fig. 4 Simulation results of laser fluence and absorbance at different depths in tissue mimicking scattering medium for the bright-field (a-f) and dark-field (g-l) optical illumination schemes. The white rectangles represent the detection area of the ultrasound scanner at the corresponding depth. (m) Quantitative comparison of laser fluence in the ultrasonic detection area at different depths for the two optical illumination schemes. Red line: bright-field illumination. Black line: dark-field illumination. (n) Zoomed-in view of the green rectangle in Fig. m. (o) The absorbance map of the bright-field optical illumination. (p) The absorbance map of the dark-field optical illumination.

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Fig. 5
Fig. 5 Reconstructed images of human hair using two algorithms. (a) Reconstruction image based on the conventional BP algorithm. (b) Reconstruction image based on the FMM-improved BP algorithm.

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Fig. 6
Fig. 6 Photoacoustic imaging resolution and imaging depth measurement. (a) Axial resolution at 40-mm depth. Red line: normalized plot based on experimental data. Black line: fitting curve. (b) Lateral resolution at 40-mm depth. Red line: normalized plot based on experimental data. Black line: fitting curve. (c) Photoacoustic image of striped black tape at different depths in optically scattering fat emulsion solution. (d) Photoacoustic signal-to-noise ratio calculations of the targets in c and the fitting curve.

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Fig. 7
Fig. 7 In vivo photoacoustic imaging results of rat SLN. (a) Photoacoustic imaging of SLN before ICG injection. (b) Photoacoustic imaging of SLN after ICG injection. (c) Co-registered photoacoustic and ultrasound images of the SLN region obtained 1 hour after ICG injection. (d) Photoacoustic maximum amplitude projection image of SLN. (e) Autopsy photograph of rat axillary region; the green colored staining area in the white circle indicates the SLN. (f) Co-registered photoacoustic and ultrasound images of the SLN region obtained 2 hours after ICG injection with a 15-mm-thick chicken breast layer added on top of the skin surface.

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Fig. 8
Fig. 8 In vivo photoacoustic image-guided SLN needle biopsy. (a) Photoacoustic image of the needle and SLN. (b) Ultrasound image of the needle and SLN. (c) Co-registered photoacoustic and ultrasound images of the needle and SLN.

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Equations (1)

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P ( r j → ) = ∑ i = r e c e i v e r i n d e x [ p i ( t i , j ) − t i , j ∂ p i ( t i , j ) ∂ t ]

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