Abstract

We used high-resolution photoacoustic imaging (PAI) to guide sclerotherapy of vascular malformations in an in vivo animal model. A focus-adjustable PAI system was developed. It can adapt to the imaging needs of different depths by adjusting the focus. Blood samples drawn before and after sclerosis were examined with PAI, which could distinguish whether or not the blood had been exposed to a sclerosing agent. Superficial and deep vessels in the animal model were examined in vivo to prove the feasibility of guiding sclerotherapy. We found that PAI can distinguish sclerotic vessels from normal vessels within a certain depth range. Our findings suggest the potential of PAI to find accurate injection points and to localize thrombi, making it possible to reduce the dosage of sclerosing agents.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2017 (6)

D. M. O’Mara, P. A. Dicamillo, W. D. Gilson, D. A. Herzka, F. K. Wacker, J. S. Lewin, and C. R. Weiss, “MR-guided percutaneous sclerotherapy of low-flow vascular malformations: Clinical experience using a 1.5 tesla MR system,” J. Magn. Reson. Imaging 45(4), 1154–1162 (2017).
[Crossref] [PubMed]

X. Yang, B. Jiang, X. Song, J. Wei, and Q. Luo, “Fast axial-scanning photoacoustic microscopy using tunable acoustic gradient lens,” Opt. Express 25(7), 7349–7357 (2017).
[Crossref] [PubMed]

S. Iskander-Rizk, P. Kruizinga, G. Springeling, H. J. Vos, A. F. van der Steen, and G. van Soest, “Photoacoustic imaging of sub-diffraction objects with spectral contrast,” Opt. Lett. 42(2), 191–194 (2017).
[Crossref] [PubMed]

M. Mishra, G. Singh, A. Gaur, S. Tandon, and A. Singh, “Role of sclerotherapy in management of vascular malformation in the maxillofacial region: Our experience,” Natl. J. Maxillofac. Surg. 8(1), 64–69 (2017).
[Crossref] [PubMed]

D. Jin, F. Yang, Z. Chen, S. Yang, and D. Xing, “Biomechanical and morphological multi-parameter photoacoustic endoscope for identification of early esophageal disease,” Appl. Phys. Lett. 111(10), 103703 (2017).
[Crossref]

W. Zhou, Z. Chen, S. Yang, and D. Xing, “Optical biopsy approach to basal cell carcinoma and melanoma based on all-optically integrated photoacoustic and optical coherence tomography,” Opt. Lett. 42(11), 2145–2148 (2017).
[Crossref] [PubMed]

2016 (3)

2015 (3)

A. Taruttis and V. Ntziachristos, “Advances in real-time multispectral optoacoustic imaging and its applications,” Nat. Photonics 9(4), 219–227 (2015).
[Crossref]

G. He, D. Xu, H. Qin, S. Yang, and D. Xing, “In vivo cell characteristic extraction and identification by photoacoustic flow cytography,” Biomed. Opt. Express 6(10), 3748–3756 (2015).
[Crossref] [PubMed]

S. L. Chen, L. J. Guo, and X. Wang, “All-optical photoacoustic microscopy,” Photoacoustics 3(4), 143–150 (2015).
[Crossref]

2014 (8)

T. Wang, S. Nandy, H. S. Salehi, P. D. Kumavor, and Q. Zhu, “A low-cost photoacoustic microscopy system with a laser diode excitation,” Biomed. Opt. Express 5(9), 3053–3058 (2014).
[Crossref] [PubMed]

M. Jeon, W. Song, E. Huynh, J. Kim, J. Kim, B. L. Helfield, B. Y. C. Leung, D. E. Goertz, G. Zheng, J. Oh, J. F. Lovell, and C. Kim, “Methylene blue microbubbles as a model dual-modality contrast agent for ultrasound and activatable photoacoustic imaging,” J. Biomed. Opt. 19(1), 16005 (2014).
[Crossref] [PubMed]

X. Feng, F. Gao, and Y. Zheng, “Thermally modulated photoacoustic imaging with super-paramagnetic iron oxide nanoparticles,” Opt. Lett. 39(12), 3414–3417 (2014).
[Crossref] [PubMed]

W. Song, W. Zheng, R. Liu, R. Lin, H. Huang, X. Gong, S. Yang, R. Zhang, and L. Song, “Reflection-mode in vivo photoacoustic microscopy with subwavelength lateral resolution,” Biomed. Opt. Express 5(12), 4235–4241 (2014).
[Crossref] [PubMed]

K. Peng, L. He, B. Wang, and J. Xiao, “Detection of cervical cancer based on photoacoustic imaging-the in-vitro results,” Biomed. Opt. Express 6(1), 135–143 (2014).
[Crossref] [PubMed]

G. Gianfranco, F. Eloisa, C. Vito, G. Raffaele, T. Gianluca, and R. Umberto, “Color-Doppler Ultrasound in the Diagnosis of Oral Vascular Anomalies,” N. Am. J. Med. Sci. 6(1), 1–5 (2014).
[Crossref] [PubMed]

S. Steinbach, A. J. Fasunla, C. M. E. Lahme, S. P. Schäfers, W. Hundt, P. Wolf, R. Mandic, J. A. Werner, and B. Eivazi, “Smell and taste in patients with vascular malformation of the extracranial head and neck region,” Am. J. Rhinol. Allergy 28(1), 45–51 (2014).
[Crossref] [PubMed]

J. Zhang, S. Yang, X. Ji, Q. Zhou, and D. Xing, “Characterization of lipid-rich aortic plaques by intravascular photoacoustic tomography: ex vivo and in vivo validation in a rabbit atherosclerosis model with histologic correlation,” J. Am. Coll. Cardiol. 64(4), 385–390 (2014).
[Crossref] [PubMed]

2013 (2)

S. O. Odeyinde, L. Kangesu, and M. Badran, “Sclerotherapy for vascular malformations: complications and a review of techniques to avoid them,” J. Plast. Reconstr. Aesthet. Surg. 66(2), 215–223 (2013).
[Crossref] [PubMed]

H. Furukawa, S. Sasaki, A. Oyama, E. Funayama, T. Hayashi, N. Saito, M. Nagao, W. Mol, and Y. Yamamoto, “Efficacy of percutaneous ethanol sclerotherapy for venous malformation in lower extremities: a retrospective review of 21 cases,” Eur. J. Plast. Surg. 36(2), 105–110 (2013).
[Crossref]

2012 (4)

L. Xi, S. R. Grobmyer, L. Wu, R. Chen, G. Zhou, L. G. Gutwein, J. Sun, W. Liao, Q. Zhou, H. Xie, and H. Jiang, “Evaluation of breast tumor margins in vivo with intraoperative photoacoustic imaging,” Opt. Express 20(8), 8726–8731 (2012).
[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]

Z. Chen, S. Yang, and D. Xing, “In vivo detection of hemoglobin oxygen saturation and carboxyhemoglobin saturation with multiwavelength photoacoustic microscopy,” Opt. Lett. 37(16), 3414–3416 (2012).
[Crossref] [PubMed]

W. Song, Q. Wei, T. Liu, D. Kuai, J. M. Burke, S. Jiao, and H. F. Zhang, “Integrating photoacoustic ophthalmoscopy with scanning laser ophthalmoscopy, optical coherence tomography, and fluorescein angiography for a multimodal retinal imaging platform,” J. Biomed. Opt. 17(6), 061206 (2012).
[Crossref] [PubMed]

2011 (4)

J. R. Costa, M. A. Torriani, E. S. Hosni, O. P. D’Avila, and P. J. de Figueiredo, “Sclerotherapy for vascular malformations in the oral and maxillofacial region: treatment and follow-up of 66 lesions,” J. Oral Maxillofac. Surg. 69(6), e88–e92 (2011).
[Crossref] [PubMed]

Z. Xie, S. L. Chen, T. Ling, L. J. Guo, P. L. Carson, and X. Wang, “Pure optical photoacoustic microscopy,” Opt. Express 19(10), 9027–9034 (2011).
[Crossref] [PubMed]

S. Blaise, M. Charavin-Cocuzza, H. Riom, M. Brix, C. Seinturier, J. M. Diamand, G. Gachet, and P. H. Carpentier, “Treatment of low-flow vascular malformations by ultrasound-guided sclerotherapy with polidocanol foam: 24 cases and literature review,” Eur. J. Vasc. Endovasc. Surg. 41(3), 412–417 (2011).
[Crossref] [PubMed]

M. P. Hartung, T. M. Grist, and C. J. François, “Magnetic resonance angiography: current status and future directions,” J. Cardiovasc. Magn. Reson. 13(1), 19 (2011).
[Crossref] [PubMed]

2010 (3)

J. Li, J. Chen, G. Zheng, G. Liao, Z. Fu, J. Li, T. Zhang, and Y. Su, “Digital subtraction angiography-guided percutaneous sclerotherapy of venous malformations with pingyangmycin and/or absolute ethanol in the maxillofacial region,” J. Oral Maxillofac. Surg. 68(9), 2258–2266 (2010).
[Crossref] [PubMed]

L. Su, X. Fan, L. Zheng, and J. Zheng, “Absolute ethanol sclerotherapy for venous malformations in the face and neck,” J. Oral Maxillofac. Surg. 68(7), 1622–1627 (2010).
[Crossref] [PubMed]

L. D. Liao, M. L. Li, H. Y. Lai, Y. Y. Shih, Y. C. Lo, S. Tsang, P. C. P. Chao, C. T. Lin, F. S. Jaw, and Y. Y. Chen, “Imaging brain hemodynamic changes during rat forepaw electrical stimulation using functional photoacoustic microscopy,” Neuroimage 52(2), 562–570 (2010).
[Crossref] [PubMed]

2009 (1)

X. Wang, X. Bai, K. Wu, and Q. Liu, “The evaluation of the management of haemangioma and vascular malformation in oral and maxillofacial region,” Int. J. Oral Maxillofac. Surg. 38(5), 529 (2009).
[Crossref]

2008 (2)

P. C. Li, C. R. C. Wang, D. B. Shieh, C. W. Wei, C. K. Liao, C. Poe, S. Jhan, A. A. Ding, and Y. N. Wu, “In vivo photoacoustic molecular imaging with simultaneous multiple selective targeting using antibody-conjugated gold nanorods,” Opt. Express 16(23), 18605–18615 (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)

P. Redondo, “Vascular malformations (I). Concept, classification, pathogenesis and clinical features,” Actas Dermosifiliogr. 98(3), 141–158 (2007).
[Crossref] [PubMed]

2006 (1)

X. Wang, X. Xie, G. Ku, L. V. Wang, and G. Stoica, “Noninvasive imaging of hemoglobin concentration and oxygenation in the rat brain using high-resolution photoacoustic tomography,” J. Biomed. Opt. 11(2), 024015 (2006).
[Crossref] [PubMed]

2005 (1)

D. T. Boll, E. M. Merkle, and J. S. Lewin, “MR-guided percutaneous sclerotherapy of low-flow vascular malformations in the head and neck,” Magn. Reson. Imaging Clin. N. Am. 13(3), 595–600 (2005).
[Crossref] [PubMed]

2004 (3)

D. T. Boll, E. M. Merkle, and J. S. Lewin, “Low-flow vascular malformations: MR-guided percutaneous sclerotherapy in qualitative and quantitative assessment of therapy and outcome,” Radiology 233(2), 376–384 (2004).
[Crossref] [PubMed]

L. Blum, S. Gallas, J. P. Cottier, C. B. Sonier Vinikoff, G. Lorette, and D. Herbreteau, “Percutaneous sclerotherapy for the treatment of soft-tissue venous malformations: a retrospective study of 68 patients,” J. Radiol. 85(2 Pt 1), 107–116 (2004).
[Crossref] [PubMed]

P. Redondo, “Classification of vascular anomalies (tumours and malformations). Clinical characteristics and natural history,” An. Sist. Sanit. Navar. 27(1Suppl 1), 9–25 (2004).
[PubMed]

2003 (2)

Y. H. Jeon, Y. S. Do, S. W. Shin, W. C. Liu, J. M. Cho, M. H. Lee, D. L. Kim, B. B. Lee, S. W. Choo, and I. W. Choo, “Ethanol embolization of arteriovenous malformations: results and complications of 33 cases,” Radiol. 235(2), 674–682 (2003).

L. Gold, L. N. Nazarian, A. S. Johar, and V. M. Rao, “Characterization of maxillofacial soft tissue vascular anomalies by ultrasound and color Doppler imaging: an adjuvant to computed tomography and magnetic resonance imaging,” J. Oral Maxillofac. Surg. 61(1), 19–31 (2003).
[Crossref] [PubMed]

1993 (1)

I. T. Jackson, R. Carreño, Z. Potparic, and K. Hussain, “Hemangiomas, vascular malformations, and lymphovenous malformations: classification and methods of treatment,” Plast. Reconstr. Surg. 91(7), 1216–1230 (1993).
[Crossref] [PubMed]

1982 (1)

J. B. Mulliken and J. Glowacki, “Hemangiomas and vascular malformations in infants and children: a classification based on endothelial characteristics,” Plast. Reconstr. Surg. 69(3), 412–422 (1982).
[Crossref] [PubMed]

Badran, M.

S. O. Odeyinde, L. Kangesu, and M. Badran, “Sclerotherapy for vascular malformations: complications and a review of techniques to avoid them,” J. Plast. Reconstr. Aesthet. Surg. 66(2), 215–223 (2013).
[Crossref] [PubMed]

Bai, X.

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S. Blaise, M. Charavin-Cocuzza, H. Riom, M. Brix, C. Seinturier, J. M. Diamand, G. Gachet, and P. H. Carpentier, “Treatment of low-flow vascular malformations by ultrasound-guided sclerotherapy with polidocanol foam: 24 cases and literature review,” Eur. J. Vasc. Endovasc. Surg. 41(3), 412–417 (2011).
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L. Blum, S. Gallas, J. P. Cottier, C. B. Sonier Vinikoff, G. Lorette, and D. Herbreteau, “Percutaneous sclerotherapy for the treatment of soft-tissue venous malformations: a retrospective study of 68 patients,” J. Radiol. 85(2 Pt 1), 107–116 (2004).
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D. T. Boll, E. M. Merkle, and J. S. Lewin, “MR-guided percutaneous sclerotherapy of low-flow vascular malformations in the head and neck,” Magn. Reson. Imaging Clin. N. Am. 13(3), 595–600 (2005).
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D. T. Boll, E. M. Merkle, and J. S. Lewin, “Low-flow vascular malformations: MR-guided percutaneous sclerotherapy in qualitative and quantitative assessment of therapy and outcome,” Radiology 233(2), 376–384 (2004).
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S. Blaise, M. Charavin-Cocuzza, H. Riom, M. Brix, C. Seinturier, J. M. Diamand, G. Gachet, and P. H. Carpentier, “Treatment of low-flow vascular malformations by ultrasound-guided sclerotherapy with polidocanol foam: 24 cases and literature review,” Eur. J. Vasc. Endovasc. Surg. 41(3), 412–417 (2011).
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W. Song, Q. Wei, T. Liu, D. Kuai, J. M. Burke, S. Jiao, and H. F. Zhang, “Integrating photoacoustic ophthalmoscopy with scanning laser ophthalmoscopy, optical coherence tomography, and fluorescein angiography for a multimodal retinal imaging platform,” J. Biomed. Opt. 17(6), 061206 (2012).
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S. Blaise, M. Charavin-Cocuzza, H. Riom, M. Brix, C. Seinturier, J. M. Diamand, G. Gachet, and P. H. Carpentier, “Treatment of low-flow vascular malformations by ultrasound-guided sclerotherapy with polidocanol foam: 24 cases and literature review,” Eur. J. Vasc. Endovasc. Surg. 41(3), 412–417 (2011).
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I. T. Jackson, R. Carreño, Z. Potparic, and K. Hussain, “Hemangiomas, vascular malformations, and lymphovenous malformations: classification and methods of treatment,” Plast. Reconstr. Surg. 91(7), 1216–1230 (1993).
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Chao, P. C. P.

L. D. Liao, M. L. Li, H. Y. Lai, Y. Y. Shih, Y. C. Lo, S. Tsang, P. C. P. Chao, C. T. Lin, F. S. Jaw, and Y. Y. Chen, “Imaging brain hemodynamic changes during rat forepaw electrical stimulation using functional photoacoustic microscopy,” Neuroimage 52(2), 562–570 (2010).
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S. Blaise, M. Charavin-Cocuzza, H. Riom, M. Brix, C. Seinturier, J. M. Diamand, G. Gachet, and P. H. Carpentier, “Treatment of low-flow vascular malformations by ultrasound-guided sclerotherapy with polidocanol foam: 24 cases and literature review,” Eur. J. Vasc. Endovasc. Surg. 41(3), 412–417 (2011).
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Chen, J.

J. Li, J. Chen, G. Zheng, G. Liao, Z. Fu, J. Li, T. Zhang, and Y. Su, “Digital subtraction angiography-guided percutaneous sclerotherapy of venous malformations with pingyangmycin and/or absolute ethanol in the maxillofacial region,” J. Oral Maxillofac. Surg. 68(9), 2258–2266 (2010).
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Chen, S. L.

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L. D. Liao, M. L. Li, H. Y. Lai, Y. Y. Shih, Y. C. Lo, S. Tsang, P. C. P. Chao, C. T. Lin, F. S. Jaw, and Y. Y. Chen, “Imaging brain hemodynamic changes during rat forepaw electrical stimulation using functional photoacoustic microscopy,” Neuroimage 52(2), 562–570 (2010).
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Chen, Z.

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Y. H. Jeon, Y. S. Do, S. W. Shin, W. C. Liu, J. M. Cho, M. H. Lee, D. L. Kim, B. B. Lee, S. W. Choo, and I. W. Choo, “Ethanol embolization of arteriovenous malformations: results and complications of 33 cases,” Radiol. 235(2), 674–682 (2003).

Choo, I. W.

Y. H. Jeon, Y. S. Do, S. W. Shin, W. C. Liu, J. M. Cho, M. H. Lee, D. L. Kim, B. B. Lee, S. W. Choo, and I. W. Choo, “Ethanol embolization of arteriovenous malformations: results and complications of 33 cases,” Radiol. 235(2), 674–682 (2003).

Choo, S. W.

Y. H. Jeon, Y. S. Do, S. W. Shin, W. C. Liu, J. M. Cho, M. H. Lee, D. L. Kim, B. B. Lee, S. W. Choo, and I. W. Choo, “Ethanol embolization of arteriovenous malformations: results and complications of 33 cases,” Radiol. 235(2), 674–682 (2003).

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J. R. Costa, M. A. Torriani, E. S. Hosni, O. P. D’Avila, and P. J. de Figueiredo, “Sclerotherapy for vascular malformations in the oral and maxillofacial region: treatment and follow-up of 66 lesions,” J. Oral Maxillofac. Surg. 69(6), e88–e92 (2011).
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L. Blum, S. Gallas, J. P. Cottier, C. B. Sonier Vinikoff, G. Lorette, and D. Herbreteau, “Percutaneous sclerotherapy for the treatment of soft-tissue venous malformations: a retrospective study of 68 patients,” J. Radiol. 85(2 Pt 1), 107–116 (2004).
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J. R. Costa, M. A. Torriani, E. S. Hosni, O. P. D’Avila, and P. J. de Figueiredo, “Sclerotherapy for vascular malformations in the oral and maxillofacial region: treatment and follow-up of 66 lesions,” J. Oral Maxillofac. Surg. 69(6), e88–e92 (2011).
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J. R. Costa, M. A. Torriani, E. S. Hosni, O. P. D’Avila, and P. J. de Figueiredo, “Sclerotherapy for vascular malformations in the oral and maxillofacial region: treatment and follow-up of 66 lesions,” J. Oral Maxillofac. Surg. 69(6), e88–e92 (2011).
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Diamand, J. M.

S. Blaise, M. Charavin-Cocuzza, H. Riom, M. Brix, C. Seinturier, J. M. Diamand, G. Gachet, and P. H. Carpentier, “Treatment of low-flow vascular malformations by ultrasound-guided sclerotherapy with polidocanol foam: 24 cases and literature review,” Eur. J. Vasc. Endovasc. Surg. 41(3), 412–417 (2011).
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D. M. O’Mara, P. A. Dicamillo, W. D. Gilson, D. A. Herzka, F. K. Wacker, J. S. Lewin, and C. R. Weiss, “MR-guided percutaneous sclerotherapy of low-flow vascular malformations: Clinical experience using a 1.5 tesla MR system,” J. Magn. Reson. Imaging 45(4), 1154–1162 (2017).
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Do, Y. S.

Y. H. Jeon, Y. S. Do, S. W. Shin, W. C. Liu, J. M. Cho, M. H. Lee, D. L. Kim, B. B. Lee, S. W. Choo, and I. W. Choo, “Ethanol embolization of arteriovenous malformations: results and complications of 33 cases,” Radiol. 235(2), 674–682 (2003).

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S. Steinbach, A. J. Fasunla, C. M. E. Lahme, S. P. Schäfers, W. Hundt, P. Wolf, R. Mandic, J. A. Werner, and B. Eivazi, “Smell and taste in patients with vascular malformation of the extracranial head and neck region,” Am. J. Rhinol. Allergy 28(1), 45–51 (2014).
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François, C. J.

M. P. Hartung, T. M. Grist, and C. J. François, “Magnetic resonance angiography: current status and future directions,” J. Cardiovasc. Magn. Reson. 13(1), 19 (2011).
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J. Li, J. Chen, G. Zheng, G. Liao, Z. Fu, J. Li, T. Zhang, and Y. Su, “Digital subtraction angiography-guided percutaneous sclerotherapy of venous malformations with pingyangmycin and/or absolute ethanol in the maxillofacial region,” J. Oral Maxillofac. Surg. 68(9), 2258–2266 (2010).
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H. Furukawa, S. Sasaki, A. Oyama, E. Funayama, T. Hayashi, N. Saito, M. Nagao, W. Mol, and Y. Yamamoto, “Efficacy of percutaneous ethanol sclerotherapy for venous malformation in lower extremities: a retrospective review of 21 cases,” Eur. J. Plast. Surg. 36(2), 105–110 (2013).
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H. Furukawa, S. Sasaki, A. Oyama, E. Funayama, T. Hayashi, N. Saito, M. Nagao, W. Mol, and Y. Yamamoto, “Efficacy of percutaneous ethanol sclerotherapy for venous malformation in lower extremities: a retrospective review of 21 cases,” Eur. J. Plast. Surg. 36(2), 105–110 (2013).
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S. Blaise, M. Charavin-Cocuzza, H. Riom, M. Brix, C. Seinturier, J. M. Diamand, G. Gachet, and P. H. Carpentier, “Treatment of low-flow vascular malformations by ultrasound-guided sclerotherapy with polidocanol foam: 24 cases and literature review,” Eur. J. Vasc. Endovasc. Surg. 41(3), 412–417 (2011).
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L. Blum, S. Gallas, J. P. Cottier, C. B. Sonier Vinikoff, G. Lorette, and D. Herbreteau, “Percutaneous sclerotherapy for the treatment of soft-tissue venous malformations: a retrospective study of 68 patients,” J. Radiol. 85(2 Pt 1), 107–116 (2004).
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Gaur, A.

M. Mishra, G. Singh, A. Gaur, S. Tandon, and A. Singh, “Role of sclerotherapy in management of vascular malformation in the maxillofacial region: Our experience,” Natl. J. Maxillofac. Surg. 8(1), 64–69 (2017).
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G. Gianfranco, F. Eloisa, C. Vito, G. Raffaele, T. Gianluca, and R. Umberto, “Color-Doppler Ultrasound in the Diagnosis of Oral Vascular Anomalies,” N. Am. J. Med. Sci. 6(1), 1–5 (2014).
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Gianluca, T.

G. Gianfranco, F. Eloisa, C. Vito, G. Raffaele, T. Gianluca, and R. Umberto, “Color-Doppler Ultrasound in the Diagnosis of Oral Vascular Anomalies,” N. Am. J. Med. Sci. 6(1), 1–5 (2014).
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D. M. O’Mara, P. A. Dicamillo, W. D. Gilson, D. A. Herzka, F. K. Wacker, J. S. Lewin, and C. R. Weiss, “MR-guided percutaneous sclerotherapy of low-flow vascular malformations: Clinical experience using a 1.5 tesla MR system,” J. Magn. Reson. Imaging 45(4), 1154–1162 (2017).
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J. B. Mulliken and J. Glowacki, “Hemangiomas and vascular malformations in infants and children: a classification based on endothelial characteristics,” Plast. Reconstr. Surg. 69(3), 412–422 (1982).
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L. Gold, L. N. Nazarian, A. S. Johar, and V. M. Rao, “Characterization of maxillofacial soft tissue vascular anomalies by ultrasound and color Doppler imaging: an adjuvant to computed tomography and magnetic resonance imaging,” J. Oral Maxillofac. Surg. 61(1), 19–31 (2003).
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Grist, T. M.

M. P. Hartung, T. M. Grist, and C. J. François, “Magnetic resonance angiography: current status and future directions,” J. Cardiovasc. Magn. Reson. 13(1), 19 (2011).
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Guo, L. J.

Gutwein, L. G.

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M. P. Hartung, T. M. Grist, and C. J. François, “Magnetic resonance angiography: current status and future directions,” J. Cardiovasc. Magn. Reson. 13(1), 19 (2011).
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H. Furukawa, S. Sasaki, A. Oyama, E. Funayama, T. Hayashi, N. Saito, M. Nagao, W. Mol, and Y. Yamamoto, “Efficacy of percutaneous ethanol sclerotherapy for venous malformation in lower extremities: a retrospective review of 21 cases,” Eur. J. Plast. Surg. 36(2), 105–110 (2013).
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He, L.

Helfield, B. L.

M. Jeon, W. Song, E. Huynh, J. Kim, J. Kim, B. L. Helfield, B. Y. C. Leung, D. E. Goertz, G. Zheng, J. Oh, J. F. Lovell, and C. Kim, “Methylene blue microbubbles as a model dual-modality contrast agent for ultrasound and activatable photoacoustic imaging,” J. Biomed. Opt. 19(1), 16005 (2014).
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L. Blum, S. Gallas, J. P. Cottier, C. B. Sonier Vinikoff, G. Lorette, and D. Herbreteau, “Percutaneous sclerotherapy for the treatment of soft-tissue venous malformations: a retrospective study of 68 patients,” J. Radiol. 85(2 Pt 1), 107–116 (2004).
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D. M. O’Mara, P. A. Dicamillo, W. D. Gilson, D. A. Herzka, F. K. Wacker, J. S. Lewin, and C. R. Weiss, “MR-guided percutaneous sclerotherapy of low-flow vascular malformations: Clinical experience using a 1.5 tesla MR system,” J. Magn. Reson. Imaging 45(4), 1154–1162 (2017).
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J. R. Costa, M. A. Torriani, E. S. Hosni, O. P. D’Avila, and P. J. de Figueiredo, “Sclerotherapy for vascular malformations in the oral and maxillofacial region: treatment and follow-up of 66 lesions,” J. Oral Maxillofac. Surg. 69(6), e88–e92 (2011).
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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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S. Steinbach, A. J. Fasunla, C. M. E. Lahme, S. P. Schäfers, W. Hundt, P. Wolf, R. Mandic, J. A. Werner, and B. Eivazi, “Smell and taste in patients with vascular malformation of the extracranial head and neck region,” Am. J. Rhinol. Allergy 28(1), 45–51 (2014).
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Hussain, K.

I. T. Jackson, R. Carreño, Z. Potparic, and K. Hussain, “Hemangiomas, vascular malformations, and lymphovenous malformations: classification and methods of treatment,” Plast. Reconstr. Surg. 91(7), 1216–1230 (1993).
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M. Jeon, W. Song, E. Huynh, J. Kim, J. Kim, B. L. Helfield, B. Y. C. Leung, D. E. Goertz, G. Zheng, J. Oh, J. F. Lovell, and C. Kim, “Methylene blue microbubbles as a model dual-modality contrast agent for ultrasound and activatable photoacoustic imaging,” J. Biomed. Opt. 19(1), 16005 (2014).
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Iskander-Rizk, S.

Jackson, I. T.

I. T. Jackson, R. Carreño, Z. Potparic, and K. Hussain, “Hemangiomas, vascular malformations, and lymphovenous malformations: classification and methods of treatment,” Plast. Reconstr. Surg. 91(7), 1216–1230 (1993).
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L. D. Liao, M. L. Li, H. Y. Lai, Y. Y. Shih, Y. C. Lo, S. Tsang, P. C. P. Chao, C. T. Lin, F. S. Jaw, and Y. Y. Chen, “Imaging brain hemodynamic changes during rat forepaw electrical stimulation using functional photoacoustic microscopy,” Neuroimage 52(2), 562–570 (2010).
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M. Jeon, W. Song, E. Huynh, J. Kim, J. Kim, B. L. Helfield, B. Y. C. Leung, D. E. Goertz, G. Zheng, J. Oh, J. F. Lovell, and C. Kim, “Methylene blue microbubbles as a model dual-modality contrast agent for ultrasound and activatable photoacoustic imaging,” J. Biomed. Opt. 19(1), 16005 (2014).
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Y. H. Jeon, Y. S. Do, S. W. Shin, W. C. Liu, J. M. Cho, M. H. Lee, D. L. Kim, B. B. Lee, S. W. Choo, and I. W. Choo, “Ethanol embolization of arteriovenous malformations: results and complications of 33 cases,” Radiol. 235(2), 674–682 (2003).

Jhan, S.

Ji, X.

J. Zhang, S. Yang, X. Ji, Q. Zhou, and D. Xing, “Characterization of lipid-rich aortic plaques by intravascular photoacoustic tomography: ex vivo and in vivo validation in a rabbit atherosclerosis model with histologic correlation,” J. Am. Coll. Cardiol. 64(4), 385–390 (2014).
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Jiang, H.

Jiao, S.

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Y. H. Jeon, Y. S. Do, S. W. Shin, W. C. Liu, J. M. Cho, M. H. Lee, D. L. Kim, B. B. Lee, S. W. Choo, and I. W. Choo, “Ethanol embolization of arteriovenous malformations: results and complications of 33 cases,” Radiol. 235(2), 674–682 (2003).

Kim, J.

M. Jeon, W. Song, E. Huynh, J. Kim, J. Kim, B. L. Helfield, B. Y. C. Leung, D. E. Goertz, G. Zheng, J. Oh, J. F. Lovell, and C. Kim, “Methylene blue microbubbles as a model dual-modality contrast agent for ultrasound and activatable photoacoustic imaging,” J. Biomed. Opt. 19(1), 16005 (2014).
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Kruizinga, P.

Ku, G.

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Kumavor, P. D.

Lahme, C. M. E.

S. Steinbach, A. J. Fasunla, C. M. E. Lahme, S. P. Schäfers, W. Hundt, P. Wolf, R. Mandic, J. A. Werner, and B. Eivazi, “Smell and taste in patients with vascular malformation of the extracranial head and neck region,” Am. J. Rhinol. Allergy 28(1), 45–51 (2014).
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Lai, H. Y.

L. D. Liao, M. L. Li, H. Y. Lai, Y. Y. Shih, Y. C. Lo, S. Tsang, P. C. P. Chao, C. T. Lin, F. S. Jaw, and Y. Y. Chen, “Imaging brain hemodynamic changes during rat forepaw electrical stimulation using functional photoacoustic microscopy,” Neuroimage 52(2), 562–570 (2010).
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Y. H. Jeon, Y. S. Do, S. W. Shin, W. C. Liu, J. M. Cho, M. H. Lee, D. L. Kim, B. B. Lee, S. W. Choo, and I. W. Choo, “Ethanol embolization of arteriovenous malformations: results and complications of 33 cases,” Radiol. 235(2), 674–682 (2003).

Lee, M. H.

Y. H. Jeon, Y. S. Do, S. W. Shin, W. C. Liu, J. M. Cho, M. H. Lee, D. L. Kim, B. B. Lee, S. W. Choo, and I. W. Choo, “Ethanol embolization of arteriovenous malformations: results and complications of 33 cases,” Radiol. 235(2), 674–682 (2003).

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M. Jeon, W. Song, E. Huynh, J. Kim, J. Kim, B. L. Helfield, B. Y. C. Leung, D. E. Goertz, G. Zheng, J. Oh, J. F. Lovell, and C. Kim, “Methylene blue microbubbles as a model dual-modality contrast agent for ultrasound and activatable photoacoustic imaging,” J. Biomed. Opt. 19(1), 16005 (2014).
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D. M. O’Mara, P. A. Dicamillo, W. D. Gilson, D. A. Herzka, F. K. Wacker, J. S. Lewin, and C. R. Weiss, “MR-guided percutaneous sclerotherapy of low-flow vascular malformations: Clinical experience using a 1.5 tesla MR system,” J. Magn. Reson. Imaging 45(4), 1154–1162 (2017).
[Crossref] [PubMed]

D. T. Boll, E. M. Merkle, and J. S. Lewin, “MR-guided percutaneous sclerotherapy of low-flow vascular malformations in the head and neck,” Magn. Reson. Imaging Clin. N. Am. 13(3), 595–600 (2005).
[Crossref] [PubMed]

D. T. Boll, E. M. Merkle, and J. S. Lewin, “Low-flow vascular malformations: MR-guided percutaneous sclerotherapy in qualitative and quantitative assessment of therapy and outcome,” Radiology 233(2), 376–384 (2004).
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Figures (7)

Fig. 1
Fig. 1 Schematic of the photoacoustic imaging system. BS, beam splitter; OL, optical lens; OFC, optical fiber coupler; OF, optical fiber; CL, conical lens; UT, ultrasound transducer; PA signal, photoacoustic signal; DAS, data-acquisition system; PD, photodiode; NDF, neutral density filter.
Fig. 2
Fig. 2 Schematic diagram of hemoglobin denaturation (other cells and proteins in blood are omitted).
Fig. 3
Fig. 3 Schematic diagram of photoacoustic imaging guided sclerotherapy for vascular malformations.
Fig. 4
Fig. 4 (a) Schematic of focal depth adjustment. (b) Lateral resolutions of system at different depths (1 mm, 3 mm, and 5 mm) when focal depth is 1 mm. (c) Lateral resolutions of system at different depths (1 mm, 3 mm, and 5 mm) when focal depth is 3 mm. (d) Lateral resolutions of system at different depths (1 mm, 3 mm, and 5 mm) when focal depth is 5 mm.
Fig. 5
Fig. 5 (a) Absorption spectrum of normal blood and sclerotic blood (both of them were freeze- dried). (b) Photographs and photoacoustic images of blood samples with different mass fractions of precipitation. (1) normal blood; (2) supernatant of sclerotic blood; (3) sclerotic blood (mixed normal blood with the same amount of ethanol); (4) precipitate of sclerotic blood (freeze-dried). 1% means the mass ratio of (4) to (2) is 1% and so on. (c) Comparison of photoacoustic signal intensities between normal blood and sclerotic blood with different mass fractions of precipitation in (b).
Fig. 6
Fig. 6 In vivo photoacoustic imaging of superficial vessels in rabbit ear before ethanol injection (a) and after injection (b). (c) Average photoacoustic signal intensities of black tape, vessels 1 and thrombi in (a) and (b). (d) Average photoacoustic signal intensities of vessels 1 in (a) and (b). The error bars represent standard deviations of photoacoustic signal values.
Fig. 7
Fig. 7 In vivo photoacoustic imaging of deep vessels in rabbit ear before ethanol injection (a) and after injection (b). (c) Average photoacoustic signals of black tape and vessel 1 before and after focus deepening in (a). (d) Average photoacoustic signals of black tape and thrombus before and after focus deepening in (b).

Tables (1)

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Table 1 Comparison of guiding methods for sclerotherapy of vascular malformations

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