Abstract

Microneedle technology allows micron-sized conduits to be formed within the outermost skin layers for both localized and systemic delivery of therapeutics including nanoparticles. Histological methods are often employed for characterization, and unfortunately do not allow for the in vivo visualization of the delivery process. This study presents the utilization of optical resolution-photoacoustic microscopy to characterize the transdermal delivery of nanoparticles using microneedles. Specifically, we observe the in vivo transdermal delivery of gold nanoparticles using microneedles in mice ear and study the penetration, diffusion, and spatial distribution of the nanoparticles in the tissue. The promising results reveal that photoacoustic microscopy can be used as a potential imaging modality for the in vivo characterization of microneedles based drug delivery.

© 2017 Optical Society of America

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References

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2017 (10)

M. Wang, L. Hu, and C. Xu, “Recent advances in the design of polymeric microneedles for transdermal drug delivery and biosensing,” Lab Chip 17(8), 1373–1387 (2017).
[PubMed]

R. Liu, M. Zhang, and C. Jin, “In vivo and in situ imaging of controlled-release dissolving silk microneedles into the skin by optical coherence tomography,” J. Biophotonics 10(6-7), 870–877 (2017).
[PubMed]

R. Z. Seeni, X. Yu, H. Chang, P. Chen, L. Liu, and C. Xu, “Iron Oxide Nanoparticle-Powered Micro-Optical Coherence Tomography for in Situ Imaging the Penetration and Swelling of Polymeric Microneedles in the Skin,” ACS Appl. Mater. Interfaces 9(24), 20340–20347 (2017).
[PubMed]

M. Moothanchery and M. Pramanik, “Performance Characterization of a Switchable Acoustic Resolution and Optical Resolution Photoacoustic Microscopy System,” Sensors (Basel) 17(2), 357 (2017).
[PubMed]

M. Moothanchery, A. Sharma, and M. Pramanik, “Switchable Acoustic and Optical Resolution Photoacoustic Microscopy for in vivo small-animal blood vasculature imaging,” J. Vis. Exp. 24 (124), e55810 (2017).
[PubMed]

G. Ma and C. Wu, “Microneedle, bio-microneedle and bio-inspired microneedle: A review,” J. Control. Release 251, 11–23 (2017).
[PubMed]

K. Park, J. Y. Kim, C. Lee, S. Jeon, G. Lim, and C. Kim, “Handheld Photoacoustic Microscopy Probe,” Sci. Rep. 7(1), 13359 (2017).
[PubMed]

L. Lin, P. Zhang, S. Xu, J. Shi, L. Li, J. Yao, L. Wang, J. Zou, and L. V. Wang, “Handheld optical-resolution photoacoustic microscopy,” J. Biomed. Opt. 22(4), 41002 (2017).
[PubMed]

Y. Zhang, J. Yu, A. R. Kahkoska, and Z. Gu, “Photoacoustic Drug Delivery,” Sensors (Basel) 17(6), 1400 (2017).
[PubMed]

T. Jin, H. Guo, H. Jiang, B. Ke, and L. Xi, “Portable optical resolution photoacoustic microscopy (pORPAM) for human oral imaging,” Opt. Lett. 42(21), 4434–4437 (2017).
[PubMed]

2016 (9)

M.-T. Tsai, I. C. Lee, Z.-F. Lee, H.-L. Liu, C.-C. Wang, Y.-C. Choia, H.-Y. Chou, and J.-D. Lee, “In vivo investigation of temporal effects and drug delivery induced by transdermal microneedles with optical coherence tomography,” Biomed. Opt. Express 7(5), 1865–1876 (2016).
[PubMed]

A. K. Jain, C. H. Lee, and H. S. Gill, “5-Aminolevulinic acid coated microneedles for photodynamic therapy of skin tumors,” J. Control. Release 239, 72–81 (2016).
[PubMed]

A. Taruttis, A. C. Timmermans, P. C. Wouters, M. Kacprowicz, G. M. van Dam, and V. Ntziachristos, “Optoacoustic Imaging of Human Vasculature: Feasibility by Using a Handheld Probe,” Radiology 281(1), 256–263 (2016).
[PubMed]

S. Hu, “Listening to the Brain With Photoacoustics,” IEEE J. Sel. Top. Quantum Electron. 22, 6800610 (2016).

Y. Zhou, J. Yao, and L. V. Wang, “Tutorial on photoacoustic tomography,” J. Biomed. Opt. 21(6), 61007 (2016).
[PubMed]

L. V. Wang and J. Yao, “A practical guide to photoacoustic tomography in the life sciences,” Nat. Methods 13(8), 627–638 (2016).
[PubMed]

S. Manohar and D. Razansky, “Photoacoustics: a historical review,” Adv. Opt. Photonics 8, 586–617 (2016).

J. Yao, A. A. Kaberniuk, L. Li, D. M. Shcherbakova, R. Zhang, L. Wang, G. Li, V. V. Verkhusha, and L. V. Wang, “Multiscale photoacoustic tomography using reversibly switchable bacterial phytochrome as a near-infrared photochromic probe,” Nat. Methods 13(1), 67–73 (2016).
[PubMed]

Y. Lu, A. A. Aimetti, R. Langer, and Z. Gu, “Bioresponsive materials,” Nature Reviews Materials 2, 16075 (2016).

2015 (3)

J. Y. Kim, C. Lee, K. Park, G. Lim, and C. Kim, “Fast optical-resolution photoacoustic microscopy using a 2-axis water-proofing MEMS scanner,” Sci. Rep. 5, 7932 (2015).
[PubMed]

H. J. Kwon, Y. Byeon, H. N. Jeon, S. H. Cho, H. D. Han, and B. C. Shin, “Gold cluster-labeled thermosensitive liposmes enhance triggered drug release in the tumor microenvironment by a photothermal effect,” J. Control. Release 216, 132–139 (2015).
[PubMed]

J. Xia, C. Kim, and J. F. Lovell, “Opportunities for Photoacoustic-Guided Drug Delivery,” Curr. Drug Targets 16(6), 571–581 (2015).
[PubMed]

2014 (3)

J. Xia, J. Yao, and L. V. Wang, “Photoacoustic tomography: principles and advances,” Electromagn Waves (Camb) 147, 1–22 (2014).
[PubMed]

J. Yao and L. V. Wang, “Photoacoustic Brain Imaging: from Microscopic to Macroscopic Scales,” Neurophotonics 1(1), 011003 (2014).
[PubMed]

P. Hai, J. Yao, K. I. Maslov, Y. Zhou, and L. V. Wang, “Near-infrared optical-resolution photoacoustic microscopy,” Opt. Lett. 39(17), 5192–5195 (2014).
[PubMed]

2012 (3)

L. V. Wang and S. Hu, “Photoacoustic Tomography: In Vivo Imaging from Organelles to Organs,” Science 335(6075), 1458–1462 (2012).
[PubMed]

K. van der Maaden, W. Jiskoot, and J. Bouwstra, “Microneedle technologies for (trans)dermal drug and vaccine delivery,” J. Control. Release 161(2), 645–655 (2012).
[PubMed]

C. Zhang, K. Maslov, S. Hu, R. Chen, Q. Zhou, K. K. Shung, and L. V. Wang, “Reflection-mode submicron-resolution in vivo photoacoustic microscopy,” J. Biomed. Opt. 17(2), 020501 (2012).
[PubMed]

2011 (2)

2010 (5)

D. Pan, M. Pramanik, A. Senpan, S. Ghosh, S. A. Wickline, L. V. Wang, and G. M. Lanza, “Near infrared photoacoustic detection of sentinel lymph nodes with gold nanobeacons,” Biomaterials 31(14), 4088–4093 (2010).
[PubMed]

R. F. Donnelly, M. J. Garland, D. I. J. Morrow, K. Migalska, T. R. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

R. F. Donnelly, M. J. Garland, D. I. Morrow, K. Migalska, T. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

J. Enfield, M. L. O’Connell, K. Lawlor, E. Jonathan, C. O’Mahony, and M. Leahy, “In-vivo dynamic characterization of microneedle skin penetration using optical coherence tomography,” J. Biomed. Opt. 15(4), 046001 (2010).
[PubMed]

L. Poon, W. Zandberg, D. Hsiao, Z. Erno, D. Sen, B. D. Gates, and N. R. Branda, “Photothermal Release of Single-Stranded DNA from the Surface of Gold Nanoparticles Through Controlled Denaturating and Au-S Bond Breaking,” ACS Nano 4(11), 6395–6403 (2010).
[PubMed]

2009 (1)

E. Z. Zhang, J. G. Laufer, R. B. Pedley, and P. C. Beard, “In vivo high-resolution 3D photoacoustic imaging of superficial vascular anatomy,” Phys. Med. Biol. 54(4), 1035–1046 (2009).
[PubMed]

2006 (1)

M. E. Wieder, D. C. Hone, M. J. Cook, M. M. Handsley, J. Gavrilovic, and D. A. Russell, “Intracellular photodynamic therapy with photosensitizer-nanoparticle conjugates: cancer therapy using a ‘Trojan horse’,” Photochem. Photobiol. Sci. 5(8), 727–734 (2006).
[PubMed]

2004 (1)

M. R. Prausnitz, “Microneedles for transdermal drug delivery,” Adv. Drug Deliv. Rev. 56(5), 581–587 (2004).
[PubMed]

2002 (1)

D. C. Hone, P. I. Walker, R. Evans-Gowing, S. FitzGerald, A. Beeby, I. Chambrier, M. J. Cook, and D. A. Russell, “Generation of Cytotoxic Singlet Oxygen via Phthalocyanine-Stabilized Gold Nanoparticles: A Potential Delivery Vehicle for Photodynamic Therapy,” Langmuir 18, 2985–2987 (2002).

Aimetti, A. A.

Y. Lu, A. A. Aimetti, R. Langer, and Z. Gu, “Bioresponsive materials,” Nature Reviews Materials 2, 16075 (2016).

Beard, P.

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

Beard, P. C.

E. Z. Zhang, J. G. Laufer, R. B. Pedley, and P. C. Beard, “In vivo high-resolution 3D photoacoustic imaging of superficial vascular anatomy,” Phys. Med. Biol. 54(4), 1035–1046 (2009).
[PubMed]

Beeby, A.

D. C. Hone, P. I. Walker, R. Evans-Gowing, S. FitzGerald, A. Beeby, I. Chambrier, M. J. Cook, and D. A. Russell, “Generation of Cytotoxic Singlet Oxygen via Phthalocyanine-Stabilized Gold Nanoparticles: A Potential Delivery Vehicle for Photodynamic Therapy,” Langmuir 18, 2985–2987 (2002).

Bouwstra, J.

K. van der Maaden, W. Jiskoot, and J. Bouwstra, “Microneedle technologies for (trans)dermal drug and vaccine delivery,” J. Control. Release 161(2), 645–655 (2012).
[PubMed]

Branda, N. R.

L. Poon, W. Zandberg, D. Hsiao, Z. Erno, D. Sen, B. D. Gates, and N. R. Branda, “Photothermal Release of Single-Stranded DNA from the Surface of Gold Nanoparticles Through Controlled Denaturating and Au-S Bond Breaking,” ACS Nano 4(11), 6395–6403 (2010).
[PubMed]

Byeon, Y.

H. J. Kwon, Y. Byeon, H. N. Jeon, S. H. Cho, H. D. Han, and B. C. Shin, “Gold cluster-labeled thermosensitive liposmes enhance triggered drug release in the tumor microenvironment by a photothermal effect,” J. Control. Release 216, 132–139 (2015).
[PubMed]

Chambrier, I.

D. C. Hone, P. I. Walker, R. Evans-Gowing, S. FitzGerald, A. Beeby, I. Chambrier, M. J. Cook, and D. A. Russell, “Generation of Cytotoxic Singlet Oxygen via Phthalocyanine-Stabilized Gold Nanoparticles: A Potential Delivery Vehicle for Photodynamic Therapy,” Langmuir 18, 2985–2987 (2002).

Chang, H.

R. Z. Seeni, X. Yu, H. Chang, P. Chen, L. Liu, and C. Xu, “Iron Oxide Nanoparticle-Powered Micro-Optical Coherence Tomography for in Situ Imaging the Penetration and Swelling of Polymeric Microneedles in the Skin,” ACS Appl. Mater. Interfaces 9(24), 20340–20347 (2017).
[PubMed]

Chen, P.

R. Z. Seeni, X. Yu, H. Chang, P. Chen, L. Liu, and C. Xu, “Iron Oxide Nanoparticle-Powered Micro-Optical Coherence Tomography for in Situ Imaging the Penetration and Swelling of Polymeric Microneedles in the Skin,” ACS Appl. Mater. Interfaces 9(24), 20340–20347 (2017).
[PubMed]

Chen, R.

C. Zhang, K. Maslov, S. Hu, R. Chen, Q. Zhou, K. K. Shung, and L. V. Wang, “Reflection-mode submicron-resolution in vivo photoacoustic microscopy,” J. Biomed. Opt. 17(2), 020501 (2012).
[PubMed]

Cho, S. H.

H. J. Kwon, Y. Byeon, H. N. Jeon, S. H. Cho, H. D. Han, and B. C. Shin, “Gold cluster-labeled thermosensitive liposmes enhance triggered drug release in the tumor microenvironment by a photothermal effect,” J. Control. Release 216, 132–139 (2015).
[PubMed]

Choia, Y.-C.

Chou, H.-Y.

Cook, M. J.

M. E. Wieder, D. C. Hone, M. J. Cook, M. M. Handsley, J. Gavrilovic, and D. A. Russell, “Intracellular photodynamic therapy with photosensitizer-nanoparticle conjugates: cancer therapy using a ‘Trojan horse’,” Photochem. Photobiol. Sci. 5(8), 727–734 (2006).
[PubMed]

D. C. Hone, P. I. Walker, R. Evans-Gowing, S. FitzGerald, A. Beeby, I. Chambrier, M. J. Cook, and D. A. Russell, “Generation of Cytotoxic Singlet Oxygen via Phthalocyanine-Stabilized Gold Nanoparticles: A Potential Delivery Vehicle for Photodynamic Therapy,” Langmuir 18, 2985–2987 (2002).

Donnelly, R. F.

R. F. Donnelly, M. J. Garland, D. I. Morrow, K. Migalska, T. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

R. F. Donnelly, M. J. Garland, D. I. J. Morrow, K. Migalska, T. R. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

Enfield, J.

J. Enfield, M. L. O’Connell, K. Lawlor, E. Jonathan, C. O’Mahony, and M. Leahy, “In-vivo dynamic characterization of microneedle skin penetration using optical coherence tomography,” J. Biomed. Opt. 15(4), 046001 (2010).
[PubMed]

Erno, Z.

L. Poon, W. Zandberg, D. Hsiao, Z. Erno, D. Sen, B. D. Gates, and N. R. Branda, “Photothermal Release of Single-Stranded DNA from the Surface of Gold Nanoparticles Through Controlled Denaturating and Au-S Bond Breaking,” ACS Nano 4(11), 6395–6403 (2010).
[PubMed]

Evans-Gowing, R.

D. C. Hone, P. I. Walker, R. Evans-Gowing, S. FitzGerald, A. Beeby, I. Chambrier, M. J. Cook, and D. A. Russell, “Generation of Cytotoxic Singlet Oxygen via Phthalocyanine-Stabilized Gold Nanoparticles: A Potential Delivery Vehicle for Photodynamic Therapy,” Langmuir 18, 2985–2987 (2002).

FitzGerald, S.

D. C. Hone, P. I. Walker, R. Evans-Gowing, S. FitzGerald, A. Beeby, I. Chambrier, M. J. Cook, and D. A. Russell, “Generation of Cytotoxic Singlet Oxygen via Phthalocyanine-Stabilized Gold Nanoparticles: A Potential Delivery Vehicle for Photodynamic Therapy,” Langmuir 18, 2985–2987 (2002).

Garland, M. J.

R. F. Donnelly, M. J. Garland, D. I. Morrow, K. Migalska, T. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

R. F. Donnelly, M. J. Garland, D. I. J. Morrow, K. Migalska, T. R. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

Gates, B. D.

L. Poon, W. Zandberg, D. Hsiao, Z. Erno, D. Sen, B. D. Gates, and N. R. Branda, “Photothermal Release of Single-Stranded DNA from the Surface of Gold Nanoparticles Through Controlled Denaturating and Au-S Bond Breaking,” ACS Nano 4(11), 6395–6403 (2010).
[PubMed]

Gavrilovic, J.

M. E. Wieder, D. C. Hone, M. J. Cook, M. M. Handsley, J. Gavrilovic, and D. A. Russell, “Intracellular photodynamic therapy with photosensitizer-nanoparticle conjugates: cancer therapy using a ‘Trojan horse’,” Photochem. Photobiol. Sci. 5(8), 727–734 (2006).
[PubMed]

Ghosh, S.

D. Pan, M. Pramanik, A. Senpan, S. Ghosh, S. A. Wickline, L. V. Wang, and G. M. Lanza, “Near infrared photoacoustic detection of sentinel lymph nodes with gold nanobeacons,” Biomaterials 31(14), 4088–4093 (2010).
[PubMed]

Gill, H. S.

A. K. Jain, C. H. Lee, and H. S. Gill, “5-Aminolevulinic acid coated microneedles for photodynamic therapy of skin tumors,” J. Control. Release 239, 72–81 (2016).
[PubMed]

Gu, Z.

Y. Zhang, J. Yu, A. R. Kahkoska, and Z. Gu, “Photoacoustic Drug Delivery,” Sensors (Basel) 17(6), 1400 (2017).
[PubMed]

Y. Lu, A. A. Aimetti, R. Langer, and Z. Gu, “Bioresponsive materials,” Nature Reviews Materials 2, 16075 (2016).

Guo, H.

Hai, P.

Han, H. D.

H. J. Kwon, Y. Byeon, H. N. Jeon, S. H. Cho, H. D. Han, and B. C. Shin, “Gold cluster-labeled thermosensitive liposmes enhance triggered drug release in the tumor microenvironment by a photothermal effect,” J. Control. Release 216, 132–139 (2015).
[PubMed]

Handsley, M. M.

M. E. Wieder, D. C. Hone, M. J. Cook, M. M. Handsley, J. Gavrilovic, and D. A. Russell, “Intracellular photodynamic therapy with photosensitizer-nanoparticle conjugates: cancer therapy using a ‘Trojan horse’,” Photochem. Photobiol. Sci. 5(8), 727–734 (2006).
[PubMed]

Hone, D. C.

M. E. Wieder, D. C. Hone, M. J. Cook, M. M. Handsley, J. Gavrilovic, and D. A. Russell, “Intracellular photodynamic therapy with photosensitizer-nanoparticle conjugates: cancer therapy using a ‘Trojan horse’,” Photochem. Photobiol. Sci. 5(8), 727–734 (2006).
[PubMed]

D. C. Hone, P. I. Walker, R. Evans-Gowing, S. FitzGerald, A. Beeby, I. Chambrier, M. J. Cook, and D. A. Russell, “Generation of Cytotoxic Singlet Oxygen via Phthalocyanine-Stabilized Gold Nanoparticles: A Potential Delivery Vehicle for Photodynamic Therapy,” Langmuir 18, 2985–2987 (2002).

Hsiao, D.

L. Poon, W. Zandberg, D. Hsiao, Z. Erno, D. Sen, B. D. Gates, and N. R. Branda, “Photothermal Release of Single-Stranded DNA from the Surface of Gold Nanoparticles Through Controlled Denaturating and Au-S Bond Breaking,” ACS Nano 4(11), 6395–6403 (2010).
[PubMed]

Hu, L.

M. Wang, L. Hu, and C. Xu, “Recent advances in the design of polymeric microneedles for transdermal drug delivery and biosensing,” Lab Chip 17(8), 1373–1387 (2017).
[PubMed]

Hu, S.

S. Hu, “Listening to the Brain With Photoacoustics,” IEEE J. Sel. Top. Quantum Electron. 22, 6800610 (2016).

C. Zhang, K. Maslov, S. Hu, R. Chen, Q. Zhou, K. K. Shung, and L. V. Wang, “Reflection-mode submicron-resolution in vivo photoacoustic microscopy,” J. Biomed. Opt. 17(2), 020501 (2012).
[PubMed]

L. V. Wang and S. Hu, “Photoacoustic Tomography: In Vivo Imaging from Organelles to Organs,” Science 335(6075), 1458–1462 (2012).
[PubMed]

S. Hu, K. Maslov, and L. V. Wang, “Second-generation optical-resolution photoacoustic microscopy with improved sensitivity and speed,” Opt. Lett. 36(7), 1134–1136 (2011).
[PubMed]

Jain, A. K.

A. K. Jain, C. H. Lee, and H. S. Gill, “5-Aminolevulinic acid coated microneedles for photodynamic therapy of skin tumors,” J. Control. Release 239, 72–81 (2016).
[PubMed]

Jeon, H. N.

H. J. Kwon, Y. Byeon, H. N. Jeon, S. H. Cho, H. D. Han, and B. C. Shin, “Gold cluster-labeled thermosensitive liposmes enhance triggered drug release in the tumor microenvironment by a photothermal effect,” J. Control. Release 216, 132–139 (2015).
[PubMed]

Jeon, S.

K. Park, J. Y. Kim, C. Lee, S. Jeon, G. Lim, and C. Kim, “Handheld Photoacoustic Microscopy Probe,” Sci. Rep. 7(1), 13359 (2017).
[PubMed]

Jiang, H.

Jin, C.

R. Liu, M. Zhang, and C. Jin, “In vivo and in situ imaging of controlled-release dissolving silk microneedles into the skin by optical coherence tomography,” J. Biophotonics 10(6-7), 870–877 (2017).
[PubMed]

Jin, T.

Jiskoot, W.

K. van der Maaden, W. Jiskoot, and J. Bouwstra, “Microneedle technologies for (trans)dermal drug and vaccine delivery,” J. Control. Release 161(2), 645–655 (2012).
[PubMed]

Jonathan, E.

J. Enfield, M. L. O’Connell, K. Lawlor, E. Jonathan, C. O’Mahony, and M. Leahy, “In-vivo dynamic characterization of microneedle skin penetration using optical coherence tomography,” J. Biomed. Opt. 15(4), 046001 (2010).
[PubMed]

Kaberniuk, A. A.

J. Yao, A. A. Kaberniuk, L. Li, D. M. Shcherbakova, R. Zhang, L. Wang, G. Li, V. V. Verkhusha, and L. V. Wang, “Multiscale photoacoustic tomography using reversibly switchable bacterial phytochrome as a near-infrared photochromic probe,” Nat. Methods 13(1), 67–73 (2016).
[PubMed]

Kacprowicz, M.

A. Taruttis, A. C. Timmermans, P. C. Wouters, M. Kacprowicz, G. M. van Dam, and V. Ntziachristos, “Optoacoustic Imaging of Human Vasculature: Feasibility by Using a Handheld Probe,” Radiology 281(1), 256–263 (2016).
[PubMed]

Kahkoska, A. R.

Y. Zhang, J. Yu, A. R. Kahkoska, and Z. Gu, “Photoacoustic Drug Delivery,” Sensors (Basel) 17(6), 1400 (2017).
[PubMed]

Ke, B.

Kim, C.

K. Park, J. Y. Kim, C. Lee, S. Jeon, G. Lim, and C. Kim, “Handheld Photoacoustic Microscopy Probe,” Sci. Rep. 7(1), 13359 (2017).
[PubMed]

J. Y. Kim, C. Lee, K. Park, G. Lim, and C. Kim, “Fast optical-resolution photoacoustic microscopy using a 2-axis water-proofing MEMS scanner,” Sci. Rep. 5, 7932 (2015).
[PubMed]

J. Xia, C. Kim, and J. F. Lovell, “Opportunities for Photoacoustic-Guided Drug Delivery,” Curr. Drug Targets 16(6), 571–581 (2015).
[PubMed]

Kim, J. Y.

K. Park, J. Y. Kim, C. Lee, S. Jeon, G. Lim, and C. Kim, “Handheld Photoacoustic Microscopy Probe,” Sci. Rep. 7(1), 13359 (2017).
[PubMed]

J. Y. Kim, C. Lee, K. Park, G. Lim, and C. Kim, “Fast optical-resolution photoacoustic microscopy using a 2-axis water-proofing MEMS scanner,” Sci. Rep. 5, 7932 (2015).
[PubMed]

Kwon, H. J.

H. J. Kwon, Y. Byeon, H. N. Jeon, S. H. Cho, H. D. Han, and B. C. Shin, “Gold cluster-labeled thermosensitive liposmes enhance triggered drug release in the tumor microenvironment by a photothermal effect,” J. Control. Release 216, 132–139 (2015).
[PubMed]

Langer, R.

Y. Lu, A. A. Aimetti, R. Langer, and Z. Gu, “Bioresponsive materials,” Nature Reviews Materials 2, 16075 (2016).

Lanza, G. M.

D. Pan, M. Pramanik, A. Senpan, S. Ghosh, S. A. Wickline, L. V. Wang, and G. M. Lanza, “Near infrared photoacoustic detection of sentinel lymph nodes with gold nanobeacons,” Biomaterials 31(14), 4088–4093 (2010).
[PubMed]

Laufer, J. G.

E. Z. Zhang, J. G. Laufer, R. B. Pedley, and P. C. Beard, “In vivo high-resolution 3D photoacoustic imaging of superficial vascular anatomy,” Phys. Med. Biol. 54(4), 1035–1046 (2009).
[PubMed]

Lawlor, K.

J. Enfield, M. L. O’Connell, K. Lawlor, E. Jonathan, C. O’Mahony, and M. Leahy, “In-vivo dynamic characterization of microneedle skin penetration using optical coherence tomography,” J. Biomed. Opt. 15(4), 046001 (2010).
[PubMed]

Leahy, M.

J. Enfield, M. L. O’Connell, K. Lawlor, E. Jonathan, C. O’Mahony, and M. Leahy, “In-vivo dynamic characterization of microneedle skin penetration using optical coherence tomography,” J. Biomed. Opt. 15(4), 046001 (2010).
[PubMed]

Lee, C.

K. Park, J. Y. Kim, C. Lee, S. Jeon, G. Lim, and C. Kim, “Handheld Photoacoustic Microscopy Probe,” Sci. Rep. 7(1), 13359 (2017).
[PubMed]

J. Y. Kim, C. Lee, K. Park, G. Lim, and C. Kim, “Fast optical-resolution photoacoustic microscopy using a 2-axis water-proofing MEMS scanner,” Sci. Rep. 5, 7932 (2015).
[PubMed]

Lee, C. H.

A. K. Jain, C. H. Lee, and H. S. Gill, “5-Aminolevulinic acid coated microneedles for photodynamic therapy of skin tumors,” J. Control. Release 239, 72–81 (2016).
[PubMed]

Lee, I. C.

Lee, J.-D.

Lee, Z.-F.

Li, G.

J. Yao, A. A. Kaberniuk, L. Li, D. M. Shcherbakova, R. Zhang, L. Wang, G. Li, V. V. Verkhusha, and L. V. Wang, “Multiscale photoacoustic tomography using reversibly switchable bacterial phytochrome as a near-infrared photochromic probe,” Nat. Methods 13(1), 67–73 (2016).
[PubMed]

Li, L.

L. Lin, P. Zhang, S. Xu, J. Shi, L. Li, J. Yao, L. Wang, J. Zou, and L. V. Wang, “Handheld optical-resolution photoacoustic microscopy,” J. Biomed. Opt. 22(4), 41002 (2017).
[PubMed]

J. Yao, A. A. Kaberniuk, L. Li, D. M. Shcherbakova, R. Zhang, L. Wang, G. Li, V. V. Verkhusha, and L. V. Wang, “Multiscale photoacoustic tomography using reversibly switchable bacterial phytochrome as a near-infrared photochromic probe,” Nat. Methods 13(1), 67–73 (2016).
[PubMed]

Lim, G.

K. Park, J. Y. Kim, C. Lee, S. Jeon, G. Lim, and C. Kim, “Handheld Photoacoustic Microscopy Probe,” Sci. Rep. 7(1), 13359 (2017).
[PubMed]

J. Y. Kim, C. Lee, K. Park, G. Lim, and C. Kim, “Fast optical-resolution photoacoustic microscopy using a 2-axis water-proofing MEMS scanner,” Sci. Rep. 5, 7932 (2015).
[PubMed]

Lin, L.

L. Lin, P. Zhang, S. Xu, J. Shi, L. Li, J. Yao, L. Wang, J. Zou, and L. V. Wang, “Handheld optical-resolution photoacoustic microscopy,” J. Biomed. Opt. 22(4), 41002 (2017).
[PubMed]

Liu, H.-L.

Liu, L.

R. Z. Seeni, X. Yu, H. Chang, P. Chen, L. Liu, and C. Xu, “Iron Oxide Nanoparticle-Powered Micro-Optical Coherence Tomography for in Situ Imaging the Penetration and Swelling of Polymeric Microneedles in the Skin,” ACS Appl. Mater. Interfaces 9(24), 20340–20347 (2017).
[PubMed]

Liu, R.

R. Liu, M. Zhang, and C. Jin, “In vivo and in situ imaging of controlled-release dissolving silk microneedles into the skin by optical coherence tomography,” J. Biophotonics 10(6-7), 870–877 (2017).
[PubMed]

Lovell, J. F.

J. Xia, C. Kim, and J. F. Lovell, “Opportunities for Photoacoustic-Guided Drug Delivery,” Curr. Drug Targets 16(6), 571–581 (2015).
[PubMed]

Lu, Y.

Y. Lu, A. A. Aimetti, R. Langer, and Z. Gu, “Bioresponsive materials,” Nature Reviews Materials 2, 16075 (2016).

Ma, G.

G. Ma and C. Wu, “Microneedle, bio-microneedle and bio-inspired microneedle: A review,” J. Control. Release 251, 11–23 (2017).
[PubMed]

Majithiya, R.

R. F. Donnelly, M. J. Garland, D. I. Morrow, K. Migalska, T. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

R. F. Donnelly, M. J. Garland, D. I. J. Morrow, K. Migalska, T. R. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

Manohar, S.

S. Manohar and D. Razansky, “Photoacoustics: a historical review,” Adv. Opt. Photonics 8, 586–617 (2016).

Maslov, K.

C. Zhang, K. Maslov, S. Hu, R. Chen, Q. Zhou, K. K. Shung, and L. V. Wang, “Reflection-mode submicron-resolution in vivo photoacoustic microscopy,” J. Biomed. Opt. 17(2), 020501 (2012).
[PubMed]

S. Hu, K. Maslov, and L. V. Wang, “Second-generation optical-resolution photoacoustic microscopy with improved sensitivity and speed,” Opt. Lett. 36(7), 1134–1136 (2011).
[PubMed]

Maslov, K. I.

Migalska, K.

R. F. Donnelly, M. J. Garland, D. I. Morrow, K. Migalska, T. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

R. F. Donnelly, M. J. Garland, D. I. J. Morrow, K. Migalska, T. R. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

Moothanchery, M.

M. Moothanchery and M. Pramanik, “Performance Characterization of a Switchable Acoustic Resolution and Optical Resolution Photoacoustic Microscopy System,” Sensors (Basel) 17(2), 357 (2017).
[PubMed]

M. Moothanchery, A. Sharma, and M. Pramanik, “Switchable Acoustic and Optical Resolution Photoacoustic Microscopy for in vivo small-animal blood vasculature imaging,” J. Vis. Exp. 24 (124), e55810 (2017).
[PubMed]

Morrow, D. I.

R. F. Donnelly, M. J. Garland, D. I. Morrow, K. Migalska, T. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

Morrow, D. I. J.

R. F. Donnelly, M. J. Garland, D. I. J. Morrow, K. Migalska, T. R. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

Ntziachristos, V.

A. Taruttis, A. C. Timmermans, P. C. Wouters, M. Kacprowicz, G. M. van Dam, and V. Ntziachristos, “Optoacoustic Imaging of Human Vasculature: Feasibility by Using a Handheld Probe,” Radiology 281(1), 256–263 (2016).
[PubMed]

O’Connell, M. L.

J. Enfield, M. L. O’Connell, K. Lawlor, E. Jonathan, C. O’Mahony, and M. Leahy, “In-vivo dynamic characterization of microneedle skin penetration using optical coherence tomography,” J. Biomed. Opt. 15(4), 046001 (2010).
[PubMed]

O’Mahony, C.

J. Enfield, M. L. O’Connell, K. Lawlor, E. Jonathan, C. O’Mahony, and M. Leahy, “In-vivo dynamic characterization of microneedle skin penetration using optical coherence tomography,” J. Biomed. Opt. 15(4), 046001 (2010).
[PubMed]

Pan, D.

D. Pan, M. Pramanik, A. Senpan, S. Ghosh, S. A. Wickline, L. V. Wang, and G. M. Lanza, “Near infrared photoacoustic detection of sentinel lymph nodes with gold nanobeacons,” Biomaterials 31(14), 4088–4093 (2010).
[PubMed]

Park, K.

K. Park, J. Y. Kim, C. Lee, S. Jeon, G. Lim, and C. Kim, “Handheld Photoacoustic Microscopy Probe,” Sci. Rep. 7(1), 13359 (2017).
[PubMed]

J. Y. Kim, C. Lee, K. Park, G. Lim, and C. Kim, “Fast optical-resolution photoacoustic microscopy using a 2-axis water-proofing MEMS scanner,” Sci. Rep. 5, 7932 (2015).
[PubMed]

Pedley, R. B.

E. Z. Zhang, J. G. Laufer, R. B. Pedley, and P. C. Beard, “In vivo high-resolution 3D photoacoustic imaging of superficial vascular anatomy,” Phys. Med. Biol. 54(4), 1035–1046 (2009).
[PubMed]

Poon, L.

L. Poon, W. Zandberg, D. Hsiao, Z. Erno, D. Sen, B. D. Gates, and N. R. Branda, “Photothermal Release of Single-Stranded DNA from the Surface of Gold Nanoparticles Through Controlled Denaturating and Au-S Bond Breaking,” ACS Nano 4(11), 6395–6403 (2010).
[PubMed]

Pramanik, M.

M. Moothanchery and M. Pramanik, “Performance Characterization of a Switchable Acoustic Resolution and Optical Resolution Photoacoustic Microscopy System,” Sensors (Basel) 17(2), 357 (2017).
[PubMed]

M. Moothanchery, A. Sharma, and M. Pramanik, “Switchable Acoustic and Optical Resolution Photoacoustic Microscopy for in vivo small-animal blood vasculature imaging,” J. Vis. Exp. 24 (124), e55810 (2017).
[PubMed]

D. Pan, M. Pramanik, A. Senpan, S. Ghosh, S. A. Wickline, L. V. Wang, and G. M. Lanza, “Near infrared photoacoustic detection of sentinel lymph nodes with gold nanobeacons,” Biomaterials 31(14), 4088–4093 (2010).
[PubMed]

Prausnitz, M. R.

M. R. Prausnitz, “Microneedles for transdermal drug delivery,” Adv. Drug Deliv. Rev. 56(5), 581–587 (2004).
[PubMed]

Razansky, D.

S. Manohar and D. Razansky, “Photoacoustics: a historical review,” Adv. Opt. Photonics 8, 586–617 (2016).

Russell, D. A.

M. E. Wieder, D. C. Hone, M. J. Cook, M. M. Handsley, J. Gavrilovic, and D. A. Russell, “Intracellular photodynamic therapy with photosensitizer-nanoparticle conjugates: cancer therapy using a ‘Trojan horse’,” Photochem. Photobiol. Sci. 5(8), 727–734 (2006).
[PubMed]

D. C. Hone, P. I. Walker, R. Evans-Gowing, S. FitzGerald, A. Beeby, I. Chambrier, M. J. Cook, and D. A. Russell, “Generation of Cytotoxic Singlet Oxygen via Phthalocyanine-Stabilized Gold Nanoparticles: A Potential Delivery Vehicle for Photodynamic Therapy,” Langmuir 18, 2985–2987 (2002).

Seeni, R. Z.

R. Z. Seeni, X. Yu, H. Chang, P. Chen, L. Liu, and C. Xu, “Iron Oxide Nanoparticle-Powered Micro-Optical Coherence Tomography for in Situ Imaging the Penetration and Swelling of Polymeric Microneedles in the Skin,” ACS Appl. Mater. Interfaces 9(24), 20340–20347 (2017).
[PubMed]

Sen, D.

L. Poon, W. Zandberg, D. Hsiao, Z. Erno, D. Sen, B. D. Gates, and N. R. Branda, “Photothermal Release of Single-Stranded DNA from the Surface of Gold Nanoparticles Through Controlled Denaturating and Au-S Bond Breaking,” ACS Nano 4(11), 6395–6403 (2010).
[PubMed]

Senpan, A.

D. Pan, M. Pramanik, A. Senpan, S. Ghosh, S. A. Wickline, L. V. Wang, and G. M. Lanza, “Near infrared photoacoustic detection of sentinel lymph nodes with gold nanobeacons,” Biomaterials 31(14), 4088–4093 (2010).
[PubMed]

Sharma, A.

M. Moothanchery, A. Sharma, and M. Pramanik, “Switchable Acoustic and Optical Resolution Photoacoustic Microscopy for in vivo small-animal blood vasculature imaging,” J. Vis. Exp. 24 (124), e55810 (2017).
[PubMed]

Shcherbakova, D. M.

J. Yao, A. A. Kaberniuk, L. Li, D. M. Shcherbakova, R. Zhang, L. Wang, G. Li, V. V. Verkhusha, and L. V. Wang, “Multiscale photoacoustic tomography using reversibly switchable bacterial phytochrome as a near-infrared photochromic probe,” Nat. Methods 13(1), 67–73 (2016).
[PubMed]

Shi, J.

L. Lin, P. Zhang, S. Xu, J. Shi, L. Li, J. Yao, L. Wang, J. Zou, and L. V. Wang, “Handheld optical-resolution photoacoustic microscopy,” J. Biomed. Opt. 22(4), 41002 (2017).
[PubMed]

Shin, B. C.

H. J. Kwon, Y. Byeon, H. N. Jeon, S. H. Cho, H. D. Han, and B. C. Shin, “Gold cluster-labeled thermosensitive liposmes enhance triggered drug release in the tumor microenvironment by a photothermal effect,” J. Control. Release 216, 132–139 (2015).
[PubMed]

Shung, K. K.

C. Zhang, K. Maslov, S. Hu, R. Chen, Q. Zhou, K. K. Shung, and L. V. Wang, “Reflection-mode submicron-resolution in vivo photoacoustic microscopy,” J. Biomed. Opt. 17(2), 020501 (2012).
[PubMed]

Singh, T. R.

R. F. Donnelly, M. J. Garland, D. I. Morrow, K. Migalska, T. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

Singh, T. R. R.

R. F. Donnelly, M. J. Garland, D. I. J. Morrow, K. Migalska, T. R. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

Taruttis, A.

A. Taruttis, A. C. Timmermans, P. C. Wouters, M. Kacprowicz, G. M. van Dam, and V. Ntziachristos, “Optoacoustic Imaging of Human Vasculature: Feasibility by Using a Handheld Probe,” Radiology 281(1), 256–263 (2016).
[PubMed]

Timmermans, A. C.

A. Taruttis, A. C. Timmermans, P. C. Wouters, M. Kacprowicz, G. M. van Dam, and V. Ntziachristos, “Optoacoustic Imaging of Human Vasculature: Feasibility by Using a Handheld Probe,” Radiology 281(1), 256–263 (2016).
[PubMed]

Tsai, M.-T.

van Dam, G. M.

A. Taruttis, A. C. Timmermans, P. C. Wouters, M. Kacprowicz, G. M. van Dam, and V. Ntziachristos, “Optoacoustic Imaging of Human Vasculature: Feasibility by Using a Handheld Probe,” Radiology 281(1), 256–263 (2016).
[PubMed]

van der Maaden, K.

K. van der Maaden, W. Jiskoot, and J. Bouwstra, “Microneedle technologies for (trans)dermal drug and vaccine delivery,” J. Control. Release 161(2), 645–655 (2012).
[PubMed]

Verkhusha, V. V.

J. Yao, A. A. Kaberniuk, L. Li, D. M. Shcherbakova, R. Zhang, L. Wang, G. Li, V. V. Verkhusha, and L. V. Wang, “Multiscale photoacoustic tomography using reversibly switchable bacterial phytochrome as a near-infrared photochromic probe,” Nat. Methods 13(1), 67–73 (2016).
[PubMed]

Walker, P. I.

D. C. Hone, P. I. Walker, R. Evans-Gowing, S. FitzGerald, A. Beeby, I. Chambrier, M. J. Cook, and D. A. Russell, “Generation of Cytotoxic Singlet Oxygen via Phthalocyanine-Stabilized Gold Nanoparticles: A Potential Delivery Vehicle for Photodynamic Therapy,” Langmuir 18, 2985–2987 (2002).

Wang, C.-C.

Wang, L.

L. Lin, P. Zhang, S. Xu, J. Shi, L. Li, J. Yao, L. Wang, J. Zou, and L. V. Wang, “Handheld optical-resolution photoacoustic microscopy,” J. Biomed. Opt. 22(4), 41002 (2017).
[PubMed]

J. Yao, A. A. Kaberniuk, L. Li, D. M. Shcherbakova, R. Zhang, L. Wang, G. Li, V. V. Verkhusha, and L. V. Wang, “Multiscale photoacoustic tomography using reversibly switchable bacterial phytochrome as a near-infrared photochromic probe,” Nat. Methods 13(1), 67–73 (2016).
[PubMed]

Wang, L. V.

L. Lin, P. Zhang, S. Xu, J. Shi, L. Li, J. Yao, L. Wang, J. Zou, and L. V. Wang, “Handheld optical-resolution photoacoustic microscopy,” J. Biomed. Opt. 22(4), 41002 (2017).
[PubMed]

J. Yao, A. A. Kaberniuk, L. Li, D. M. Shcherbakova, R. Zhang, L. Wang, G. Li, V. V. Verkhusha, and L. V. Wang, “Multiscale photoacoustic tomography using reversibly switchable bacterial phytochrome as a near-infrared photochromic probe,” Nat. Methods 13(1), 67–73 (2016).
[PubMed]

Y. Zhou, J. Yao, and L. V. Wang, “Tutorial on photoacoustic tomography,” J. Biomed. Opt. 21(6), 61007 (2016).
[PubMed]

L. V. Wang and J. Yao, “A practical guide to photoacoustic tomography in the life sciences,” Nat. Methods 13(8), 627–638 (2016).
[PubMed]

P. Hai, J. Yao, K. I. Maslov, Y. Zhou, and L. V. Wang, “Near-infrared optical-resolution photoacoustic microscopy,” Opt. Lett. 39(17), 5192–5195 (2014).
[PubMed]

J. Yao and L. V. Wang, “Photoacoustic Brain Imaging: from Microscopic to Macroscopic Scales,” Neurophotonics 1(1), 011003 (2014).
[PubMed]

J. Xia, J. Yao, and L. V. Wang, “Photoacoustic tomography: principles and advances,” Electromagn Waves (Camb) 147, 1–22 (2014).
[PubMed]

C. Zhang, K. Maslov, S. Hu, R. Chen, Q. Zhou, K. K. Shung, and L. V. Wang, “Reflection-mode submicron-resolution in vivo photoacoustic microscopy,” J. Biomed. Opt. 17(2), 020501 (2012).
[PubMed]

L. V. Wang and S. Hu, “Photoacoustic Tomography: In Vivo Imaging from Organelles to Organs,” Science 335(6075), 1458–1462 (2012).
[PubMed]

S. Hu, K. Maslov, and L. V. Wang, “Second-generation optical-resolution photoacoustic microscopy with improved sensitivity and speed,” Opt. Lett. 36(7), 1134–1136 (2011).
[PubMed]

D. Pan, M. Pramanik, A. Senpan, S. Ghosh, S. A. Wickline, L. V. Wang, and G. M. Lanza, “Near infrared photoacoustic detection of sentinel lymph nodes with gold nanobeacons,” Biomaterials 31(14), 4088–4093 (2010).
[PubMed]

Wang, M.

M. Wang, L. Hu, and C. Xu, “Recent advances in the design of polymeric microneedles for transdermal drug delivery and biosensing,” Lab Chip 17(8), 1373–1387 (2017).
[PubMed]

Wickline, S. A.

D. Pan, M. Pramanik, A. Senpan, S. Ghosh, S. A. Wickline, L. V. Wang, and G. M. Lanza, “Near infrared photoacoustic detection of sentinel lymph nodes with gold nanobeacons,” Biomaterials 31(14), 4088–4093 (2010).
[PubMed]

Wieder, M. E.

M. E. Wieder, D. C. Hone, M. J. Cook, M. M. Handsley, J. Gavrilovic, and D. A. Russell, “Intracellular photodynamic therapy with photosensitizer-nanoparticle conjugates: cancer therapy using a ‘Trojan horse’,” Photochem. Photobiol. Sci. 5(8), 727–734 (2006).
[PubMed]

Woolfson, A. D.

R. F. Donnelly, M. J. Garland, D. I. J. Morrow, K. Migalska, T. R. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

R. F. Donnelly, M. J. Garland, D. I. Morrow, K. Migalska, T. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

Wouters, P. C.

A. Taruttis, A. C. Timmermans, P. C. Wouters, M. Kacprowicz, G. M. van Dam, and V. Ntziachristos, “Optoacoustic Imaging of Human Vasculature: Feasibility by Using a Handheld Probe,” Radiology 281(1), 256–263 (2016).
[PubMed]

Wu, C.

G. Ma and C. Wu, “Microneedle, bio-microneedle and bio-inspired microneedle: A review,” J. Control. Release 251, 11–23 (2017).
[PubMed]

Xi, L.

Xia, J.

J. Xia, C. Kim, and J. F. Lovell, “Opportunities for Photoacoustic-Guided Drug Delivery,” Curr. Drug Targets 16(6), 571–581 (2015).
[PubMed]

J. Xia, J. Yao, and L. V. Wang, “Photoacoustic tomography: principles and advances,” Electromagn Waves (Camb) 147, 1–22 (2014).
[PubMed]

Xu, C.

M. Wang, L. Hu, and C. Xu, “Recent advances in the design of polymeric microneedles for transdermal drug delivery and biosensing,” Lab Chip 17(8), 1373–1387 (2017).
[PubMed]

R. Z. Seeni, X. Yu, H. Chang, P. Chen, L. Liu, and C. Xu, “Iron Oxide Nanoparticle-Powered Micro-Optical Coherence Tomography for in Situ Imaging the Penetration and Swelling of Polymeric Microneedles in the Skin,” ACS Appl. Mater. Interfaces 9(24), 20340–20347 (2017).
[PubMed]

Xu, S.

L. Lin, P. Zhang, S. Xu, J. Shi, L. Li, J. Yao, L. Wang, J. Zou, and L. V. Wang, “Handheld optical-resolution photoacoustic microscopy,” J. Biomed. Opt. 22(4), 41002 (2017).
[PubMed]

Yao, J.

L. Lin, P. Zhang, S. Xu, J. Shi, L. Li, J. Yao, L. Wang, J. Zou, and L. V. Wang, “Handheld optical-resolution photoacoustic microscopy,” J. Biomed. Opt. 22(4), 41002 (2017).
[PubMed]

J. Yao, A. A. Kaberniuk, L. Li, D. M. Shcherbakova, R. Zhang, L. Wang, G. Li, V. V. Verkhusha, and L. V. Wang, “Multiscale photoacoustic tomography using reversibly switchable bacterial phytochrome as a near-infrared photochromic probe,” Nat. Methods 13(1), 67–73 (2016).
[PubMed]

Y. Zhou, J. Yao, and L. V. Wang, “Tutorial on photoacoustic tomography,” J. Biomed. Opt. 21(6), 61007 (2016).
[PubMed]

L. V. Wang and J. Yao, “A practical guide to photoacoustic tomography in the life sciences,” Nat. Methods 13(8), 627–638 (2016).
[PubMed]

P. Hai, J. Yao, K. I. Maslov, Y. Zhou, and L. V. Wang, “Near-infrared optical-resolution photoacoustic microscopy,” Opt. Lett. 39(17), 5192–5195 (2014).
[PubMed]

J. Xia, J. Yao, and L. V. Wang, “Photoacoustic tomography: principles and advances,” Electromagn Waves (Camb) 147, 1–22 (2014).
[PubMed]

J. Yao and L. V. Wang, “Photoacoustic Brain Imaging: from Microscopic to Macroscopic Scales,” Neurophotonics 1(1), 011003 (2014).
[PubMed]

Yu, J.

Y. Zhang, J. Yu, A. R. Kahkoska, and Z. Gu, “Photoacoustic Drug Delivery,” Sensors (Basel) 17(6), 1400 (2017).
[PubMed]

Yu, X.

R. Z. Seeni, X. Yu, H. Chang, P. Chen, L. Liu, and C. Xu, “Iron Oxide Nanoparticle-Powered Micro-Optical Coherence Tomography for in Situ Imaging the Penetration and Swelling of Polymeric Microneedles in the Skin,” ACS Appl. Mater. Interfaces 9(24), 20340–20347 (2017).
[PubMed]

Zandberg, W.

L. Poon, W. Zandberg, D. Hsiao, Z. Erno, D. Sen, B. D. Gates, and N. R. Branda, “Photothermal Release of Single-Stranded DNA from the Surface of Gold Nanoparticles Through Controlled Denaturating and Au-S Bond Breaking,” ACS Nano 4(11), 6395–6403 (2010).
[PubMed]

Zhang, C.

C. Zhang, K. Maslov, S. Hu, R. Chen, Q. Zhou, K. K. Shung, and L. V. Wang, “Reflection-mode submicron-resolution in vivo photoacoustic microscopy,” J. Biomed. Opt. 17(2), 020501 (2012).
[PubMed]

Zhang, E. Z.

E. Z. Zhang, J. G. Laufer, R. B. Pedley, and P. C. Beard, “In vivo high-resolution 3D photoacoustic imaging of superficial vascular anatomy,” Phys. Med. Biol. 54(4), 1035–1046 (2009).
[PubMed]

Zhang, M.

R. Liu, M. Zhang, and C. Jin, “In vivo and in situ imaging of controlled-release dissolving silk microneedles into the skin by optical coherence tomography,” J. Biophotonics 10(6-7), 870–877 (2017).
[PubMed]

Zhang, P.

L. Lin, P. Zhang, S. Xu, J. Shi, L. Li, J. Yao, L. Wang, J. Zou, and L. V. Wang, “Handheld optical-resolution photoacoustic microscopy,” J. Biomed. Opt. 22(4), 41002 (2017).
[PubMed]

Zhang, R.

J. Yao, A. A. Kaberniuk, L. Li, D. M. Shcherbakova, R. Zhang, L. Wang, G. Li, V. V. Verkhusha, and L. V. Wang, “Multiscale photoacoustic tomography using reversibly switchable bacterial phytochrome as a near-infrared photochromic probe,” Nat. Methods 13(1), 67–73 (2016).
[PubMed]

Zhang, Y.

Y. Zhang, J. Yu, A. R. Kahkoska, and Z. Gu, “Photoacoustic Drug Delivery,” Sensors (Basel) 17(6), 1400 (2017).
[PubMed]

Zhou, Q.

C. Zhang, K. Maslov, S. Hu, R. Chen, Q. Zhou, K. K. Shung, and L. V. Wang, “Reflection-mode submicron-resolution in vivo photoacoustic microscopy,” J. Biomed. Opt. 17(2), 020501 (2012).
[PubMed]

Zhou, Y.

Zou, J.

L. Lin, P. Zhang, S. Xu, J. Shi, L. Li, J. Yao, L. Wang, J. Zou, and L. V. Wang, “Handheld optical-resolution photoacoustic microscopy,” J. Biomed. Opt. 22(4), 41002 (2017).
[PubMed]

ACS Appl. Mater. Interfaces (1)

R. Z. Seeni, X. Yu, H. Chang, P. Chen, L. Liu, and C. Xu, “Iron Oxide Nanoparticle-Powered Micro-Optical Coherence Tomography for in Situ Imaging the Penetration and Swelling of Polymeric Microneedles in the Skin,” ACS Appl. Mater. Interfaces 9(24), 20340–20347 (2017).
[PubMed]

ACS Nano (1)

L. Poon, W. Zandberg, D. Hsiao, Z. Erno, D. Sen, B. D. Gates, and N. R. Branda, “Photothermal Release of Single-Stranded DNA from the Surface of Gold Nanoparticles Through Controlled Denaturating and Au-S Bond Breaking,” ACS Nano 4(11), 6395–6403 (2010).
[PubMed]

Adv. Drug Deliv. Rev. (1)

M. R. Prausnitz, “Microneedles for transdermal drug delivery,” Adv. Drug Deliv. Rev. 56(5), 581–587 (2004).
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Adv. Opt. Photonics (1)

S. Manohar and D. Razansky, “Photoacoustics: a historical review,” Adv. Opt. Photonics 8, 586–617 (2016).

Biomaterials (1)

D. Pan, M. Pramanik, A. Senpan, S. Ghosh, S. A. Wickline, L. V. Wang, and G. M. Lanza, “Near infrared photoacoustic detection of sentinel lymph nodes with gold nanobeacons,” Biomaterials 31(14), 4088–4093 (2010).
[PubMed]

Biomed. Opt. Express (1)

Curr. Drug Targets (1)

J. Xia, C. Kim, and J. F. Lovell, “Opportunities for Photoacoustic-Guided Drug Delivery,” Curr. Drug Targets 16(6), 571–581 (2015).
[PubMed]

Electromagn Waves (Camb) (1)

J. Xia, J. Yao, and L. V. Wang, “Photoacoustic tomography: principles and advances,” Electromagn Waves (Camb) 147, 1–22 (2014).
[PubMed]

IEEE J. Sel. Top. Quantum Electron. (1)

S. Hu, “Listening to the Brain With Photoacoustics,” IEEE J. Sel. Top. Quantum Electron. 22, 6800610 (2016).

Interface Focus (1)

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

J. Biomed. Opt. (4)

Y. Zhou, J. Yao, and L. V. Wang, “Tutorial on photoacoustic tomography,” J. Biomed. Opt. 21(6), 61007 (2016).
[PubMed]

J. Enfield, M. L. O’Connell, K. Lawlor, E. Jonathan, C. O’Mahony, and M. Leahy, “In-vivo dynamic characterization of microneedle skin penetration using optical coherence tomography,” J. Biomed. Opt. 15(4), 046001 (2010).
[PubMed]

C. Zhang, K. Maslov, S. Hu, R. Chen, Q. Zhou, K. K. Shung, and L. V. Wang, “Reflection-mode submicron-resolution in vivo photoacoustic microscopy,” J. Biomed. Opt. 17(2), 020501 (2012).
[PubMed]

L. Lin, P. Zhang, S. Xu, J. Shi, L. Li, J. Yao, L. Wang, J. Zou, and L. V. Wang, “Handheld optical-resolution photoacoustic microscopy,” J. Biomed. Opt. 22(4), 41002 (2017).
[PubMed]

J. Biophotonics (1)

R. Liu, M. Zhang, and C. Jin, “In vivo and in situ imaging of controlled-release dissolving silk microneedles into the skin by optical coherence tomography,” J. Biophotonics 10(6-7), 870–877 (2017).
[PubMed]

J. Control. Release (6)

R. F. Donnelly, M. J. Garland, D. I. Morrow, K. Migalska, T. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

K. van der Maaden, W. Jiskoot, and J. Bouwstra, “Microneedle technologies for (trans)dermal drug and vaccine delivery,” J. Control. Release 161(2), 645–655 (2012).
[PubMed]

R. F. Donnelly, M. J. Garland, D. I. J. Morrow, K. Migalska, T. R. R. Singh, R. Majithiya, and A. D. Woolfson, “Optical coherence tomography is a valuable tool in the study of the effects of microneedle geometry on skin penetration characteristics and in-skin dissolution,” J. Control. Release 147(3), 333–341 (2010).
[PubMed]

A. K. Jain, C. H. Lee, and H. S. Gill, “5-Aminolevulinic acid coated microneedles for photodynamic therapy of skin tumors,” J. Control. Release 239, 72–81 (2016).
[PubMed]

G. Ma and C. Wu, “Microneedle, bio-microneedle and bio-inspired microneedle: A review,” J. Control. Release 251, 11–23 (2017).
[PubMed]

H. J. Kwon, Y. Byeon, H. N. Jeon, S. H. Cho, H. D. Han, and B. C. Shin, “Gold cluster-labeled thermosensitive liposmes enhance triggered drug release in the tumor microenvironment by a photothermal effect,” J. Control. Release 216, 132–139 (2015).
[PubMed]

J. Vis. Exp. (1)

M. Moothanchery, A. Sharma, and M. Pramanik, “Switchable Acoustic and Optical Resolution Photoacoustic Microscopy for in vivo small-animal blood vasculature imaging,” J. Vis. Exp. 24 (124), e55810 (2017).
[PubMed]

Lab Chip (1)

M. Wang, L. Hu, and C. Xu, “Recent advances in the design of polymeric microneedles for transdermal drug delivery and biosensing,” Lab Chip 17(8), 1373–1387 (2017).
[PubMed]

Langmuir (1)

D. C. Hone, P. I. Walker, R. Evans-Gowing, S. FitzGerald, A. Beeby, I. Chambrier, M. J. Cook, and D. A. Russell, “Generation of Cytotoxic Singlet Oxygen via Phthalocyanine-Stabilized Gold Nanoparticles: A Potential Delivery Vehicle for Photodynamic Therapy,” Langmuir 18, 2985–2987 (2002).

Nat. Methods (2)

L. V. Wang and J. Yao, “A practical guide to photoacoustic tomography in the life sciences,” Nat. Methods 13(8), 627–638 (2016).
[PubMed]

J. Yao, A. A. Kaberniuk, L. Li, D. M. Shcherbakova, R. Zhang, L. Wang, G. Li, V. V. Verkhusha, and L. V. Wang, “Multiscale photoacoustic tomography using reversibly switchable bacterial phytochrome as a near-infrared photochromic probe,” Nat. Methods 13(1), 67–73 (2016).
[PubMed]

Nature Reviews Materials (1)

Y. Lu, A. A. Aimetti, R. Langer, and Z. Gu, “Bioresponsive materials,” Nature Reviews Materials 2, 16075 (2016).

Neurophotonics (1)

J. Yao and L. V. Wang, “Photoacoustic Brain Imaging: from Microscopic to Macroscopic Scales,” Neurophotonics 1(1), 011003 (2014).
[PubMed]

Opt. Lett. (3)

Photochem. Photobiol. Sci. (1)

M. E. Wieder, D. C. Hone, M. J. Cook, M. M. Handsley, J. Gavrilovic, and D. A. Russell, “Intracellular photodynamic therapy with photosensitizer-nanoparticle conjugates: cancer therapy using a ‘Trojan horse’,” Photochem. Photobiol. Sci. 5(8), 727–734 (2006).
[PubMed]

Phys. Med. Biol. (1)

E. Z. Zhang, J. G. Laufer, R. B. Pedley, and P. C. Beard, “In vivo high-resolution 3D photoacoustic imaging of superficial vascular anatomy,” Phys. Med. Biol. 54(4), 1035–1046 (2009).
[PubMed]

Radiology (1)

A. Taruttis, A. C. Timmermans, P. C. Wouters, M. Kacprowicz, G. M. van Dam, and V. Ntziachristos, “Optoacoustic Imaging of Human Vasculature: Feasibility by Using a Handheld Probe,” Radiology 281(1), 256–263 (2016).
[PubMed]

Sci. Rep. (2)

K. Park, J. Y. Kim, C. Lee, S. Jeon, G. Lim, and C. Kim, “Handheld Photoacoustic Microscopy Probe,” Sci. Rep. 7(1), 13359 (2017).
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J. Y. Kim, C. Lee, K. Park, G. Lim, and C. Kim, “Fast optical-resolution photoacoustic microscopy using a 2-axis water-proofing MEMS scanner,” Sci. Rep. 5, 7932 (2015).
[PubMed]

Science (1)

L. V. Wang and S. Hu, “Photoacoustic Tomography: In Vivo Imaging from Organelles to Organs,” Science 335(6075), 1458–1462 (2012).
[PubMed]

Sensors (Basel) (2)

M. Moothanchery and M. Pramanik, “Performance Characterization of a Switchable Acoustic Resolution and Optical Resolution Photoacoustic Microscopy System,” Sensors (Basel) 17(2), 357 (2017).
[PubMed]

Y. Zhang, J. Yu, A. R. Kahkoska, and Z. Gu, “Photoacoustic Drug Delivery,” Sensors (Basel) 17(6), 1400 (2017).
[PubMed]

Other (1)

“American National Standard for Safe Use of Lasers,” ANSI Standard Z136.1–2007, NY (2007).

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Figures (5)

Fig. 1
Fig. 1

Schematic of the optical resolution photoacoustic microscopy imaging system. BS - Beam Sampler, CL - Condenser lens, PH – Pinhole, NDF- Neutral density filter, PD – photodiode, FC – Fiber coupler, SMF - Single mode fiber, L1&L2 - Achromatic lens, M - Mirror, UST – Ultrasound transducer, DAQ - Data acquisition card,, RA - Right angle prism, RP - Rhomboid prism,, SO – Silicon oil, AL - Acoustic lens.

Fig. 2
Fig. 2

Characterization of PMMA MNs patch: (a) camera image of the PMMA MNs patch; (b) close view of the MNs array on the patch under optical microscope; (c) H&E staining of porcine skin treated with PMMA MNs patch.

Fig. 3
Fig. 3

SEM characterization of AuNPs coated PMMA MNs: (a) A top view; (b) Zoom-in visualization of the AuNPs on a coated PMMA MNs.

Fig. 4
Fig. 4

In vivo photoacoustic imaging of mouse ear (a) before and (b) after the AuNPs coated MNs insertion.

Fig. 5
Fig. 5

In vivo photoacoustic microscopy (Maximum amplitude projection) image of mouse ear; data acquisition started (a) 5 Min, (b) 40 Min, (c) 95 Min, and (d) 150 Min after AuNPs coated microneedle insertion. (e) Image slices of (a) at various depths. (f) Variation of photoacoustic signal amplitudes over time for various depths.