Abstract

Temperature mapping is essential in many biomedical studies and interventions to precisely control the tissue’s thermal conditions for optimal treatment efficiency and minimal side effects. Based on the Grüneisen parameter’s temperature dependence, photoacoustic (PA) imaging can provide relative temperature measurement, but it has been traditionally challenging to measure absolute temperatures without knowing the baseline temperature, particularly in deep tissues with unknown optical and acoustic properties. Here, we report a new thermal-energy-memory-based photoacoustic thermometry (TEMPT). By illuminating the tissue with a burst of nanosecond laser pulses, TEMPT exploits the temperature dependence of the thermal energy lingering, which is probed by the corresponding PA signals acquired within the thermal confinement. A self-normalized ratiometric measurement cancels out temperature-irrelevant quantities and estimates the Grüneisen parameter. The temperature can then be evaluated, given the tissue’s temperature-dependent Grüneisen parameter, mass density, and specific heat capacity. Unlike conventional PA thermometry, TEMPT does not require knowledge of the tissue’s baseline temperature, nor the optical properties. We have developed a mathematical model to describe the temperature dependence in TEMPT. We have demonstrated the feasibility of the temperature evaluation on tissue phantoms at 1.5 cm depth within a clinically relevant temperature range. Finally, as proof-of-concept, we applied TEMPT for temperature mapping during focused ultrasound treatment in mice in vivo at 2 mm depth. As a generic temperature mapping method, TEMPT is expected to find applications in thermotherapy of cancers on small animal models.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2018 (2)

Y. Zhou, E. Tang, J. Luo, and J. Yao, “Deep-tissue temperature mapping by multi-illumination photoacoustic tomography aided by a diffusion optical model: a numerical study,” J. Biomed. Opt. 23, 1–10 (2018).
[Crossref]

M. Li, B. Lan, W. Liu, J. Xia, and J. Yao, “Internal-illumination photoacoustic computed tomography,” J. Biomed. Opt. 23, 030506 (2018).
[Crossref]

2017 (3)

X. L. Liang, L. Fang, X. D. Li, X. Zhang, and F. Wang, “Activatable near infrared dye conjugated hyaluronic acid based nanoparticles as a targeted theranostic agent for enhanced fluorescence/CT/photoacoustic imaging guided photothermal therapy,” Biomaterials 132, 72–84(2017).
[Crossref]

F. Gao, X. Feng, R. Zhang, S. Liu, R. Ding, R. Kishor, and Y. Zheng, “Single laser pulse generates dual photoacoustic signals for differential contrast photoacoustic imaging,” Sci. Rep. 7, 626 (2017).
[Crossref]

M. Alaeian and H. R. B. Orlande, “Inverse photoacoustic technique for parameter and temperature estimation in tissues,” Heat Transf. Eng. 38, 1573–1594 (2017).
[Crossref]

2016 (6)

E. V. Petrova, M. Motamedi, A. A. Oraevsky, and S. A. Ermilov, “In vivo cryoablation of prostate tissue with temperature monitoring by optoacoustic imaging,” Proc. SPIE 9708, 97080G (2016).
[Crossref]

L. L. Zou, H. Wang, B. He, L. J. Zeng, T. Tan, H. Q. Cao, X. Y. He, Z. W. Zhang, S. R. Guo, and Y. P. Li, “Current approaches of photothermal therapy in treating cancer metastasis with nanotherapeutics,” Theranostics 6, 762–772 (2016).
[Crossref]

Y. Lyu, Y. Fang, Q. Q. Miao, X. Zhen, D. Ding, and K. Y. Pu, “Intraparticle molecular orbital engineering of semiconducting polymer nanoparticles as amplified theranostics for in vivo photoacoustic imaging and photothermal therapy,” ACS Nano 10, 4472–4481 (2016).
[Crossref]

H. Odeen, S. Almquist, J. de Bever, D. A. Christensen, and D. L. Parker, “MR thermometry for focused ultrasound monitoring utilizing model predictive filtering and ultrasound beam modeling,” J. Ther. Ultrasound 4, 23 (2016).
[Crossref]

M. Chen, J. Zhang, C. Cai, Y. Gao, and J. Luo, “Fast direct reconstruction strategy of dynamic fluorescence molecular tomography using graphics processing units,” J. Biomed. Opt. 21, 66010 (2016).
[Crossref]

E. Petrova, A. Liopo, V. Nadvoretskiy, and S. Ermilov, “Imaging technique for real-time temperature monitoring during cryotherapy of lesions,” J. Biomed. Opt. 21, 116007 (2016).
[Crossref]

2015 (5)

M. A. Lewis, R. M. Staruch, and R. Chopra, “Thermometry and ablation monitoring with ultrasound,” Int. J. Hyperthermia 31, 163–181 (2015).
[Crossref]

J. Yao, L. Wang, J. M. Yang, K. I. Maslov, T. T. W. Wong, L. Li, C. H. Huang, J. Zou, and L. V. Wang, “High-speed label-free functional photoacoustic microscopy of mouse brain in action,” Nat. Methods 12, 407–410 (2015).
[Crossref]

S. DiGiulio, “FDA clears focused ultrasound system for prostate cancer treatment,” Oncology Times 37, 37 (2015).
[Crossref]

J. Yu, W. Y. Yin, X. P. Zheng, G. Tian, X. Zhang, T. Bao, X. H. Dong, Z. L. Wang, Z. J. Gu, X. Y. Ma, and Y. L. Zhao, “Smart MoS2/Fe3O4 nanotheranostic for magnetically targeted photothermal therapy guided by magnetic resonance/photoacoustic imaging,” Theranostics 5, 931–945 (2015).
[Crossref]

E. V. Petrova, A. Liopo, A. A. Oraevsky, and S. A. Ermilov, “Universal temperature-dependent normalized optoacoustic response of blood,” Proc. SPIE 9323, 93231Y (2015).
[Crossref]

2014 (5)

E. V. Petrova, S. A. Ermilov, R. Su, V. Nadvoretskiy, A. Conjusteau, and A. A. Oraevsky, “Temperature dependence of Grüneisen parameter in optically absorbing solutions measured by 2D optoacoustic imaging,” Proc. SPIE 8943, 89430S (2014).
[Crossref]

M. Pramanik, “Improving tangential resolution with a modified delay-and-sum reconstruction algorithm in photoacoustic and thermoacoustic tomography,” J. Opt. Soc. Am. A 31, 621–627 (2014).
[Crossref]

E. V. Petrova, A. A. Oraevsky, and S. A. Ermilov, “Red blood cell as a universal optoacoustic sensor for non-invasive temperature monitoring,” Appl. Phys. Lett. 105, 094103 (2014).
[Crossref]

L. W. Zhang, S. Gao, F. Zhang, K. Yang, Q. J. Ma, and L. Zhu, “Activatable hyaluronic acid nanoparticle as a theranostic agent for optical/photoacoustic image-guided photothermal therapy,” ACS Nano 8, 12250–12258 (2014).
[Crossref]

L. Cheng, J. J. Liu, X. Gu, H. Gong, X. Z. Shi, T. Liu, C. Wang, X. Y. Wang, G. Liu, H. Y. Xing, W. B. Bu, B. Q. Sun, and Z. Liu, “PEGylated WS2 nanosheets as a multifunctional theranostic agent for in vivo dual-modal CT/photoacoustic imaging guided photothermal therapy,” Adv. Mater. 26, 1886–1893 (2014).
[Crossref]

2013 (3)

2012 (3)

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

R. Brinkmann, S. Koinzer, K. Schlott, L. Ptaszynski, M. Bever, A. Baade, S. Luft, Y. Miura, J. Roider, and R. Birngruber, “Real-time temperature determination during retinal photocoagulation on patients,” J. Biomed. Opt. 17, 061219 (2012).
[Crossref]

S. M. Nikitin, T. D. Khokhlova, and I. M. Pelivanov, “Temperature dependence of the optoacoustic transformation efficiency in ex vivo tissues for application in monitoring thermal therapies,” J. Biomed. Opt. 17, 061214 (2012).
[Crossref]

2011 (1)

V. Auboiroux, E. Dumont, L. Petrusca, M. Viallon, and R. Salomir, “An MR-compliant phased-array HIFU transducer with augmented steering range, dedicated to abdominal thermotherapy,” Phys. Med. Biol. 56, 3563–3582 (2011).
[Crossref]

2010 (5)

T. Uchida, H. Ohkusa, H. Yamashita, S. Shoji, Y. Nagata, T. Hyodo, and T. Satoh, “Five years experience of transrectal high-intensity focused ultrasound using the Sonablate device in the treatment of localized prostate cancer,” Int. J. Urol. 13, 228–233 (2010).
[Crossref]

D. Liu and E. S. Ebbini, “Real-time 2-D temperature imaging using ultrasound,” IEEE Trans. Biomed. Eng. 57, 12–16 (2010).
[Crossref]

F. Orsi, P. Arnone, W. Chen, and L. Zhang, “High intensity focused ultrasound ablation: a new therapeutic option for solid tumors,” J. Cancer Res. Ther. 6, 414–420 (2010).
[Crossref]

M. Pramanik, T. N. Erpelding, L. Jankovic, and L. V. Wang, “Tissue temperature monitoring using thermoacoustic and photoacoustic techniques,” Proc. SPIE 7564, 75641Y (2010).
[Crossref]

C. Li, W. Zhang, W. Fan, J. Huang, F. Zhang, and P. Wu, “Noninvasive treatment of malignant bone tumors using high-intensity focused ultrasound,” Cancer 116, 3934–3942 (2010).
[Crossref]

2009 (2)

M. Pramanik and L. V. Wang, “Thermoacoustic and photoacoustic sensing of temperature,” J. Biomed. Opt. 14, 054024 (2009).
[Crossref]

S. H. Wang and P. C. Li, “Photoacoustic temperature measurements for monitoring of thermal therapy,” Proc. SPIE 7177, 71771S (2009).
[Crossref]

2008 (6)

J. Shah, S. Park, S. Aglyamov, T. Larson, L. Ma, K. Sokolov, K. Johnston, T. Milner, and S. Y. Emelianov, “Photoacoustic imaging and temperature measurement for photothermal cancer therapy,” J. Biomed. Opt. 13, 034024 (2008).
[Crossref]

Y. Xing, X. Lu, E. C. Pua, and P. Zhong, “The effect of high intensity focused ultrasound treatment on metastases in a murine melanoma model,” Biochem. Biophys. Res. Commun. 375, 645–650 (2008).
[Crossref]

G.-L. Sun, Z.-H. Ren, and L.-F. Li, “Clinical study of thermotherapy of HIFU in combination with 3D-CRT treating advanced primary liver cancer,” Jilin Med. J. 29, 542–543 (2008).

O. Seror, M. Lepetit-Coiffe, B. Le Bail, B. D. de Senneville, H. Trillaud, C. Moonen, and B. Quesson, “Real time monitoring of radiofrequency ablation based on MR thermometry and thermal dose in the pig liver in vivo,” Eur. Radiology 18, 408–416 (2008).
[Crossref]

M. Fink, “Time-reversal acoustics,” J. Phys. Conf. Ser. 118, 012001 (2008).
[Crossref]

X. Huang, P. K. Jain, I. H. El-Sayed, and M. A. El-Sayed, “Plasmonic photothermal therapy (PPTT) using gold nanoparticles,” Laser Med. Sci. 23, 217–228 (2008).
[Crossref]

2007 (1)

Z. Hu, X. Y. Yang, Y. Liu, G. N. Sankin, E. C. Pua, M. A. Morse, H. K. Lyerly, T. M. Clay, and P. Zhong, “Investigation of HIFU-induced anti-tumor immunity in a murine tumor model,” J. Transl. Med. 5, 34 (2007).
[Crossref]

2006 (3)

Y. Zhou, L. Zhai, R. Simmons, and P. Zhong, “Measurement of high intensity focused ultrasound fields by a fiber optic probe hydrophone,” J. Acoust. Soc. Am. 120, 676–685 (2006).
[Crossref]

I. H. El-Sayed, X. Huang, and M. A. El-Sayed, “Selective laser photo-thermal therapy of epithelial carcinoma using anti-EGFR antibody conjugated gold nanoparticles,” Cancer Lett. 239, 129–135 (2006).
[Crossref]

T. Uchida, H. Ohkusa, Y. Nagata, T. Hyodo, T. Satoh, and A. Irie, “Treatment of localized prostate cancer using high-intensity focused ultrasound,” BJU Int. 97, 56–61 (2006).
[Crossref]

2005 (1)

M. Xu and L. V. Wang, “Universal back-projection algorithm for photoacoustic computed tomography,” Phys. Rev. E 71, 016706 (2005).

2002 (2)

B. Hildebrandt, P. Wust, O. Ahlers, A. Dieing, G. Sreenivasa, T. Kerner, R. Felix, and H. Riess, “The cellular and molecular basis of hyperthermia,” Crit. Rev. Oncol./Hemat. 43, 33–56 (2002).
[Crossref]

E. E. Konofagou, J. Thierman, T. Karjalainen, and K. Hynynen, “The temperature dependence of ultrasound-stimulated acoustic emission,” Ultrasound Med. Biol. 28, 331–338 (2002).
[Crossref]

2001 (2)

M. Falk and R. Issels, “Hyperthermia in oncology,” Int. J. Hyperther. 17, 1–18 (2001).
[Crossref]

S. Vaezy, X. Shi, R. W. Martin, E. Chi, P. I. Nelson, M. R. Bailey, and L. A. Crum, “Real-time visualization of high-intensity focused ultrasound treatment using ultrasound imaging,” Ultrasound Med. Biol. 27, 33–42(2001).
[Crossref]

2000 (1)

B. Quesson, J. A. de Zwart, and C. T. Moonen, “Magnetic resonance temperature imaging for guidance of thermotherapy,” J. Mag. Res. Imag. 12, 525–533 (2000).
[Crossref]

1999 (2)

R. O. Esenaliev, A. A. Oraevsky, K. V. Larin, I. V. Larina, and M. Motamedi, “Real-time optoacoustic monitoring of temperature in tissues,” J. Phys. D 38, 2633–2639 (1999).
[Crossref]

C. A. Barkman, L. O. Almquist, T. Kirkhorn, and N. Holmer, “Thermotherapy: feasibility study using a single focussed ultrasound transducer,” Int. J. Hyperther. 15, 63–76 (1999).
[Crossref]

1996 (2)

R. Maassmoreno and C. A. Damianou, “Noninvasive temperature estimation in tissue via ultrasound echo-shifts. Part I. Analytical model,” J. Acoust. Soc. Am. 100, 2514–2521 (1996).
[Crossref]

K. Giering, I. Lamprecht, and O. Minet, “Specific heat capacities of human and animal tissues,” Proc. SPIE 2624, 188–197 (1996).
[Crossref]

1992 (1)

M. Fink, “Time reversal of ultrasonic fields. I. Basic principles,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 39, 555–566 (1992).
[Crossref]

1989 (1)

J. H. Barker, F. Hammersen, I. Bondar, E. Uhl, T. J. Galla, M. D. Menger, and K. Messmer, “The hairless mouse ear for in vivo studies of skin microcirculation,” Plast. Reconstr. Surg. 83, 948–959 (1989).
[Crossref]

1985 (1)

J. W. Valvano, J. R. Cochran, and K. R. Diller, “Thermal-conductivity and diffusivity of biomaterials measured with self-heated thermistors,” Int. J. Thermophys. 6, 301–311 (1985).
[Crossref]

Aglyamov, S.

J. Shah, S. Park, S. Aglyamov, T. Larson, L. Ma, K. Sokolov, K. Johnston, T. Milner, and S. Y. Emelianov, “Photoacoustic imaging and temperature measurement for photothermal cancer therapy,” J. Biomed. Opt. 13, 034024 (2008).
[Crossref]

Ahlers, O.

B. Hildebrandt, P. Wust, O. Ahlers, A. Dieing, G. Sreenivasa, T. Kerner, R. Felix, and H. Riess, “The cellular and molecular basis of hyperthermia,” Crit. Rev. Oncol./Hemat. 43, 33–56 (2002).
[Crossref]

Alaeian, M.

M. Alaeian and H. R. B. Orlande, “Inverse photoacoustic technique for parameter and temperature estimation in tissues,” Heat Transf. Eng. 38, 1573–1594 (2017).
[Crossref]

Almquist, L. O.

C. A. Barkman, L. O. Almquist, T. Kirkhorn, and N. Holmer, “Thermotherapy: feasibility study using a single focussed ultrasound transducer,” Int. J. Hyperther. 15, 63–76 (1999).
[Crossref]

Almquist, S.

H. Odeen, S. Almquist, J. de Bever, D. A. Christensen, and D. L. Parker, “MR thermometry for focused ultrasound monitoring utilizing model predictive filtering and ultrasound beam modeling,” J. Ther. Ultrasound 4, 23 (2016).
[Crossref]

Arnone, P.

F. Orsi, P. Arnone, W. Chen, and L. Zhang, “High intensity focused ultrasound ablation: a new therapeutic option for solid tumors,” J. Cancer Res. Ther. 6, 414–420 (2010).
[Crossref]

Auboiroux, V.

V. Auboiroux, E. Dumont, L. Petrusca, M. Viallon, and R. Salomir, “An MR-compliant phased-array HIFU transducer with augmented steering range, dedicated to abdominal thermotherapy,” Phys. Med. Biol. 56, 3563–3582 (2011).
[Crossref]

Baade, A.

R. Brinkmann, S. Koinzer, K. Schlott, L. Ptaszynski, M. Bever, A. Baade, S. Luft, Y. Miura, J. Roider, and R. Birngruber, “Real-time temperature determination during retinal photocoagulation on patients,” J. Biomed. Opt. 17, 061219 (2012).
[Crossref]

Bailey, M. R.

S. Vaezy, X. Shi, R. W. Martin, E. Chi, P. I. Nelson, M. R. Bailey, and L. A. Crum, “Real-time visualization of high-intensity focused ultrasound treatment using ultrasound imaging,” Ultrasound Med. Biol. 27, 33–42(2001).
[Crossref]

Bao, T.

J. Yu, W. Y. Yin, X. P. Zheng, G. Tian, X. Zhang, T. Bao, X. H. Dong, Z. L. Wang, Z. J. Gu, X. Y. Ma, and Y. L. Zhao, “Smart MoS2/Fe3O4 nanotheranostic for magnetically targeted photothermal therapy guided by magnetic resonance/photoacoustic imaging,” Theranostics 5, 931–945 (2015).
[Crossref]

Barker, J. H.

J. H. Barker, F. Hammersen, I. Bondar, E. Uhl, T. J. Galla, M. D. Menger, and K. Messmer, “The hairless mouse ear for in vivo studies of skin microcirculation,” Plast. Reconstr. Surg. 83, 948–959 (1989).
[Crossref]

Barkman, C. A.

C. A. Barkman, L. O. Almquist, T. Kirkhorn, and N. Holmer, “Thermotherapy: feasibility study using a single focussed ultrasound transducer,” Int. J. Hyperther. 15, 63–76 (1999).
[Crossref]

Bever, M.

R. Brinkmann, S. Koinzer, K. Schlott, L. Ptaszynski, M. Bever, A. Baade, S. Luft, Y. Miura, J. Roider, and R. Birngruber, “Real-time temperature determination during retinal photocoagulation on patients,” J. Biomed. Opt. 17, 061219 (2012).
[Crossref]

Birngruber, R.

R. Brinkmann, S. Koinzer, K. Schlott, L. Ptaszynski, M. Bever, A. Baade, S. Luft, Y. Miura, J. Roider, and R. Birngruber, “Real-time temperature determination during retinal photocoagulation on patients,” J. Biomed. Opt. 17, 061219 (2012).
[Crossref]

Bondar, I.

J. H. Barker, F. Hammersen, I. Bondar, E. Uhl, T. J. Galla, M. D. Menger, and K. Messmer, “The hairless mouse ear for in vivo studies of skin microcirculation,” Plast. Reconstr. Surg. 83, 948–959 (1989).
[Crossref]

Brinkmann, R.

R. Brinkmann, S. Koinzer, K. Schlott, L. Ptaszynski, M. Bever, A. Baade, S. Luft, Y. Miura, J. Roider, and R. Birngruber, “Real-time temperature determination during retinal photocoagulation on patients,” J. Biomed. Opt. 17, 061219 (2012).
[Crossref]

Bu, W. B.

L. Cheng, J. J. Liu, X. Gu, H. Gong, X. Z. Shi, T. Liu, C. Wang, X. Y. Wang, G. Liu, H. Y. Xing, W. B. Bu, B. Q. Sun, and Z. Liu, “PEGylated WS2 nanosheets as a multifunctional theranostic agent for in vivo dual-modal CT/photoacoustic imaging guided photothermal therapy,” Adv. Mater. 26, 1886–1893 (2014).
[Crossref]

Cai, C.

M. Chen, J. Zhang, C. Cai, Y. Gao, and J. Luo, “Fast direct reconstruction strategy of dynamic fluorescence molecular tomography using graphics processing units,” J. Biomed. Opt. 21, 66010 (2016).
[Crossref]

Cao, H. Q.

L. L. Zou, H. Wang, B. He, L. J. Zeng, T. Tan, H. Q. Cao, X. Y. He, Z. W. Zhang, S. R. Guo, and Y. P. Li, “Current approaches of photothermal therapy in treating cancer metastasis with nanotherapeutics,” Theranostics 6, 762–772 (2016).
[Crossref]

Chen, M.

M. Chen, J. Zhang, C. Cai, Y. Gao, and J. Luo, “Fast direct reconstruction strategy of dynamic fluorescence molecular tomography using graphics processing units,” J. Biomed. Opt. 21, 66010 (2016).
[Crossref]

Chen, W.

F. Orsi, P. Arnone, W. Chen, and L. Zhang, “High intensity focused ultrasound ablation: a new therapeutic option for solid tumors,” J. Cancer Res. Ther. 6, 414–420 (2010).
[Crossref]

Cheng, L.

L. Cheng, J. J. Liu, X. Gu, H. Gong, X. Z. Shi, T. Liu, C. Wang, X. Y. Wang, G. Liu, H. Y. Xing, W. B. Bu, B. Q. Sun, and Z. Liu, “PEGylated WS2 nanosheets as a multifunctional theranostic agent for in vivo dual-modal CT/photoacoustic imaging guided photothermal therapy,” Adv. Mater. 26, 1886–1893 (2014).
[Crossref]

Chi, E.

S. Vaezy, X. Shi, R. W. Martin, E. Chi, P. I. Nelson, M. R. Bailey, and L. A. Crum, “Real-time visualization of high-intensity focused ultrasound treatment using ultrasound imaging,” Ultrasound Med. Biol. 27, 33–42(2001).
[Crossref]

Chopra, R.

M. A. Lewis, R. M. Staruch, and R. Chopra, “Thermometry and ablation monitoring with ultrasound,” Int. J. Hyperthermia 31, 163–181 (2015).
[Crossref]

Christensen, D. A.

H. Odeen, S. Almquist, J. de Bever, D. A. Christensen, and D. L. Parker, “MR thermometry for focused ultrasound monitoring utilizing model predictive filtering and ultrasound beam modeling,” J. Ther. Ultrasound 4, 23 (2016).
[Crossref]

Clay, T. M.

Z. Hu, X. Y. Yang, Y. Liu, G. N. Sankin, E. C. Pua, M. A. Morse, H. K. Lyerly, T. M. Clay, and P. Zhong, “Investigation of HIFU-induced anti-tumor immunity in a murine tumor model,” J. Transl. Med. 5, 34 (2007).
[Crossref]

Cochran, J. R.

J. W. Valvano, J. R. Cochran, and K. R. Diller, “Thermal-conductivity and diffusivity of biomaterials measured with self-heated thermistors,” Int. J. Thermophys. 6, 301–311 (1985).
[Crossref]

Conjusteau, A.

E. V. Petrova, S. A. Ermilov, R. Su, V. Nadvoretskiy, A. Conjusteau, and A. A. Oraevsky, “Temperature dependence of Grüneisen parameter in optically absorbing solutions measured by 2D optoacoustic imaging,” Proc. SPIE 8943, 89430S (2014).
[Crossref]

E. Petrova, S. Ermilov, R. Su, V. Nadvoretskiy, A. Conjusteau, and A. Oraevsky, “Using optoacoustic imaging for measuring the temperature dependence of Grüneisen parameter in optically absorbing solutions,” Opt. Express 21, 25077–25090 (2013).
[Crossref]

Crum, L. A.

S. Vaezy, X. Shi, R. W. Martin, E. Chi, P. I. Nelson, M. R. Bailey, and L. A. Crum, “Real-time visualization of high-intensity focused ultrasound treatment using ultrasound imaging,” Ultrasound Med. Biol. 27, 33–42(2001).
[Crossref]

Damianou, C. A.

R. Maassmoreno and C. A. Damianou, “Noninvasive temperature estimation in tissue via ultrasound echo-shifts. Part I. Analytical model,” J. Acoust. Soc. Am. 100, 2514–2521 (1996).
[Crossref]

de Bever, J.

H. Odeen, S. Almquist, J. de Bever, D. A. Christensen, and D. L. Parker, “MR thermometry for focused ultrasound monitoring utilizing model predictive filtering and ultrasound beam modeling,” J. Ther. Ultrasound 4, 23 (2016).
[Crossref]

de Senneville, B. D.

O. Seror, M. Lepetit-Coiffe, B. Le Bail, B. D. de Senneville, H. Trillaud, C. Moonen, and B. Quesson, “Real time monitoring of radiofrequency ablation based on MR thermometry and thermal dose in the pig liver in vivo,” Eur. Radiology 18, 408–416 (2008).
[Crossref]

de Zwart, J. A.

B. Quesson, J. A. de Zwart, and C. T. Moonen, “Magnetic resonance temperature imaging for guidance of thermotherapy,” J. Mag. Res. Imag. 12, 525–533 (2000).
[Crossref]

Dieing, A.

B. Hildebrandt, P. Wust, O. Ahlers, A. Dieing, G. Sreenivasa, T. Kerner, R. Felix, and H. Riess, “The cellular and molecular basis of hyperthermia,” Crit. Rev. Oncol./Hemat. 43, 33–56 (2002).
[Crossref]

DiGiulio, S.

S. DiGiulio, “FDA clears focused ultrasound system for prostate cancer treatment,” Oncology Times 37, 37 (2015).
[Crossref]

Diller, K. R.

J. W. Valvano, J. R. Cochran, and K. R. Diller, “Thermal-conductivity and diffusivity of biomaterials measured with self-heated thermistors,” Int. J. Thermophys. 6, 301–311 (1985).
[Crossref]

Ding, D.

Y. Lyu, Y. Fang, Q. Q. Miao, X. Zhen, D. Ding, and K. Y. Pu, “Intraparticle molecular orbital engineering of semiconducting polymer nanoparticles as amplified theranostics for in vivo photoacoustic imaging and photothermal therapy,” ACS Nano 10, 4472–4481 (2016).
[Crossref]

Ding, R.

F. Gao, X. Feng, R. Zhang, S. Liu, R. Ding, R. Kishor, and Y. Zheng, “Single laser pulse generates dual photoacoustic signals for differential contrast photoacoustic imaging,” Sci. Rep. 7, 626 (2017).
[Crossref]

Dong, X. H.

J. Yu, W. Y. Yin, X. P. Zheng, G. Tian, X. Zhang, T. Bao, X. H. Dong, Z. L. Wang, Z. J. Gu, X. Y. Ma, and Y. L. Zhao, “Smart MoS2/Fe3O4 nanotheranostic for magnetically targeted photothermal therapy guided by magnetic resonance/photoacoustic imaging,” Theranostics 5, 931–945 (2015).
[Crossref]

Dumont, E.

V. Auboiroux, E. Dumont, L. Petrusca, M. Viallon, and R. Salomir, “An MR-compliant phased-array HIFU transducer with augmented steering range, dedicated to abdominal thermotherapy,” Phys. Med. Biol. 56, 3563–3582 (2011).
[Crossref]

Ebbini, E. S.

D. Liu and E. S. Ebbini, “Real-time 2-D temperature imaging using ultrasound,” IEEE Trans. Biomed. Eng. 57, 12–16 (2010).
[Crossref]

El-Sayed, I. H.

X. Huang, P. K. Jain, I. H. El-Sayed, and M. A. El-Sayed, “Plasmonic photothermal therapy (PPTT) using gold nanoparticles,” Laser Med. Sci. 23, 217–228 (2008).
[Crossref]

I. H. El-Sayed, X. Huang, and M. A. El-Sayed, “Selective laser photo-thermal therapy of epithelial carcinoma using anti-EGFR antibody conjugated gold nanoparticles,” Cancer Lett. 239, 129–135 (2006).
[Crossref]

El-Sayed, M. A.

X. Huang, P. K. Jain, I. H. El-Sayed, and M. A. El-Sayed, “Plasmonic photothermal therapy (PPTT) using gold nanoparticles,” Laser Med. Sci. 23, 217–228 (2008).
[Crossref]

I. H. El-Sayed, X. Huang, and M. A. El-Sayed, “Selective laser photo-thermal therapy of epithelial carcinoma using anti-EGFR antibody conjugated gold nanoparticles,” Cancer Lett. 239, 129–135 (2006).
[Crossref]

Emelianov, S.

B. Wang, J. Su, A. Karpiouk, D. Yeager, and S. Emelianov, Intravascular Photoacoustic and Ultrasound Imaging: From Tissue Characterization to Molecular Imaging to Image-Guided Therapy (Springer, 2011).

Emelianov, S. Y.

J. Shah, S. Park, S. Aglyamov, T. Larson, L. Ma, K. Sokolov, K. Johnston, T. Milner, and S. Y. Emelianov, “Photoacoustic imaging and temperature measurement for photothermal cancer therapy,” J. Biomed. Opt. 13, 034024 (2008).
[Crossref]

Ermilov, S.

E. Petrova, A. Liopo, V. Nadvoretskiy, and S. Ermilov, “Imaging technique for real-time temperature monitoring during cryotherapy of lesions,” J. Biomed. Opt. 21, 116007 (2016).
[Crossref]

E. Petrova, S. Ermilov, R. Su, V. Nadvoretskiy, A. Conjusteau, and A. Oraevsky, “Using optoacoustic imaging for measuring the temperature dependence of Grüneisen parameter in optically absorbing solutions,” Opt. Express 21, 25077–25090 (2013).
[Crossref]

Ermilov, S. A.

E. V. Petrova, M. Motamedi, A. A. Oraevsky, and S. A. Ermilov, “In vivo cryoablation of prostate tissue with temperature monitoring by optoacoustic imaging,” Proc. SPIE 9708, 97080G (2016).
[Crossref]

E. V. Petrova, A. Liopo, A. A. Oraevsky, and S. A. Ermilov, “Universal temperature-dependent normalized optoacoustic response of blood,” Proc. SPIE 9323, 93231Y (2015).
[Crossref]

E. V. Petrova, S. A. Ermilov, R. Su, V. Nadvoretskiy, A. Conjusteau, and A. A. Oraevsky, “Temperature dependence of Grüneisen parameter in optically absorbing solutions measured by 2D optoacoustic imaging,” Proc. SPIE 8943, 89430S (2014).
[Crossref]

E. V. Petrova, A. A. Oraevsky, and S. A. Ermilov, “Red blood cell as a universal optoacoustic sensor for non-invasive temperature monitoring,” Appl. Phys. Lett. 105, 094103 (2014).
[Crossref]

Erpelding, T. N.

M. Pramanik, T. N. Erpelding, L. Jankovic, and L. V. Wang, “Tissue temperature monitoring using thermoacoustic and photoacoustic techniques,” Proc. SPIE 7564, 75641Y (2010).
[Crossref]

Esenaliev, R. O.

R. O. Esenaliev, A. A. Oraevsky, K. V. Larin, I. V. Larina, and M. Motamedi, “Real-time optoacoustic monitoring of temperature in tissues,” J. Phys. D 38, 2633–2639 (1999).
[Crossref]

Falk, M.

M. Falk and R. Issels, “Hyperthermia in oncology,” Int. J. Hyperther. 17, 1–18 (2001).
[Crossref]

Fan, W.

C. Li, W. Zhang, W. Fan, J. Huang, F. Zhang, and P. Wu, “Noninvasive treatment of malignant bone tumors using high-intensity focused ultrasound,” Cancer 116, 3934–3942 (2010).
[Crossref]

Fang, L.

X. L. Liang, L. Fang, X. D. Li, X. Zhang, and F. Wang, “Activatable near infrared dye conjugated hyaluronic acid based nanoparticles as a targeted theranostic agent for enhanced fluorescence/CT/photoacoustic imaging guided photothermal therapy,” Biomaterials 132, 72–84(2017).
[Crossref]

Fang, Y.

Y. Lyu, Y. Fang, Q. Q. Miao, X. Zhen, D. Ding, and K. Y. Pu, “Intraparticle molecular orbital engineering of semiconducting polymer nanoparticles as amplified theranostics for in vivo photoacoustic imaging and photothermal therapy,” ACS Nano 10, 4472–4481 (2016).
[Crossref]

Felix, R.

B. Hildebrandt, P. Wust, O. Ahlers, A. Dieing, G. Sreenivasa, T. Kerner, R. Felix, and H. Riess, “The cellular and molecular basis of hyperthermia,” Crit. Rev. Oncol./Hemat. 43, 33–56 (2002).
[Crossref]

Feng, X.

F. Gao, X. Feng, R. Zhang, S. Liu, R. Ding, R. Kishor, and Y. Zheng, “Single laser pulse generates dual photoacoustic signals for differential contrast photoacoustic imaging,” Sci. Rep. 7, 626 (2017).
[Crossref]

Fink, M.

M. Fink, “Time-reversal acoustics,” J. Phys. Conf. Ser. 118, 012001 (2008).
[Crossref]

M. Fink, “Time reversal of ultrasonic fields. I. Basic principles,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 39, 555–566 (1992).
[Crossref]

Galla, T. J.

J. H. Barker, F. Hammersen, I. Bondar, E. Uhl, T. J. Galla, M. D. Menger, and K. Messmer, “The hairless mouse ear for in vivo studies of skin microcirculation,” Plast. Reconstr. Surg. 83, 948–959 (1989).
[Crossref]

Gao, F.

F. Gao, X. Feng, R. Zhang, S. Liu, R. Ding, R. Kishor, and Y. Zheng, “Single laser pulse generates dual photoacoustic signals for differential contrast photoacoustic imaging,” Sci. Rep. 7, 626 (2017).
[Crossref]

Gao, L.

L. Gao, L. Wang, C. Li, Y. Liu, H. Ke, C. Zhang, and L. V. Wang, “Single-cell photoacoustic thermometry,” J. Biomed. Opt. 18, 26003 (2013).
[Crossref]

Gao, S.

L. W. Zhang, S. Gao, F. Zhang, K. Yang, Q. J. Ma, and L. Zhu, “Activatable hyaluronic acid nanoparticle as a theranostic agent for optical/photoacoustic image-guided photothermal therapy,” ACS Nano 8, 12250–12258 (2014).
[Crossref]

Gao, Y.

M. Chen, J. Zhang, C. Cai, Y. Gao, and J. Luo, “Fast direct reconstruction strategy of dynamic fluorescence molecular tomography using graphics processing units,” J. Biomed. Opt. 21, 66010 (2016).
[Crossref]

Giering, K.

K. Giering, I. Lamprecht, and O. Minet, “Specific heat capacities of human and animal tissues,” Proc. SPIE 2624, 188–197 (1996).
[Crossref]

Gong, H.

L. Cheng, J. J. Liu, X. Gu, H. Gong, X. Z. Shi, T. Liu, C. Wang, X. Y. Wang, G. Liu, H. Y. Xing, W. B. Bu, B. Q. Sun, and Z. Liu, “PEGylated WS2 nanosheets as a multifunctional theranostic agent for in vivo dual-modal CT/photoacoustic imaging guided photothermal therapy,” Adv. Mater. 26, 1886–1893 (2014).
[Crossref]

Gu, X.

L. Cheng, J. J. Liu, X. Gu, H. Gong, X. Z. Shi, T. Liu, C. Wang, X. Y. Wang, G. Liu, H. Y. Xing, W. B. Bu, B. Q. Sun, and Z. Liu, “PEGylated WS2 nanosheets as a multifunctional theranostic agent for in vivo dual-modal CT/photoacoustic imaging guided photothermal therapy,” Adv. Mater. 26, 1886–1893 (2014).
[Crossref]

Gu, Z. J.

J. Yu, W. Y. Yin, X. P. Zheng, G. Tian, X. Zhang, T. Bao, X. H. Dong, Z. L. Wang, Z. J. Gu, X. Y. Ma, and Y. L. Zhao, “Smart MoS2/Fe3O4 nanotheranostic for magnetically targeted photothermal therapy guided by magnetic resonance/photoacoustic imaging,” Theranostics 5, 931–945 (2015).
[Crossref]

Guo, S. R.

L. L. Zou, H. Wang, B. He, L. J. Zeng, T. Tan, H. Q. Cao, X. Y. He, Z. W. Zhang, S. R. Guo, and Y. P. Li, “Current approaches of photothermal therapy in treating cancer metastasis with nanotherapeutics,” Theranostics 6, 762–772 (2016).
[Crossref]

Hammersen, F.

J. H. Barker, F. Hammersen, I. Bondar, E. Uhl, T. J. Galla, M. D. Menger, and K. Messmer, “The hairless mouse ear for in vivo studies of skin microcirculation,” Plast. Reconstr. Surg. 83, 948–959 (1989).
[Crossref]

He, B.

L. L. Zou, H. Wang, B. He, L. J. Zeng, T. Tan, H. Q. Cao, X. Y. He, Z. W. Zhang, S. R. Guo, and Y. P. Li, “Current approaches of photothermal therapy in treating cancer metastasis with nanotherapeutics,” Theranostics 6, 762–772 (2016).
[Crossref]

He, X. Y.

L. L. Zou, H. Wang, B. He, L. J. Zeng, T. Tan, H. Q. Cao, X. Y. He, Z. W. Zhang, S. R. Guo, and Y. P. Li, “Current approaches of photothermal therapy in treating cancer metastasis with nanotherapeutics,” Theranostics 6, 762–772 (2016).
[Crossref]

Hildebrandt, B.

B. Hildebrandt, P. Wust, O. Ahlers, A. Dieing, G. Sreenivasa, T. Kerner, R. Felix, and H. Riess, “The cellular and molecular basis of hyperthermia,” Crit. Rev. Oncol./Hemat. 43, 33–56 (2002).
[Crossref]

Holmer, N.

C. A. Barkman, L. O. Almquist, T. Kirkhorn, and N. Holmer, “Thermotherapy: feasibility study using a single focussed ultrasound transducer,” Int. J. Hyperther. 15, 63–76 (1999).
[Crossref]

Hu, S.

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

Hu, Z.

Z. Hu, X. Y. Yang, Y. Liu, G. N. Sankin, E. C. Pua, M. A. Morse, H. K. Lyerly, T. M. Clay, and P. Zhong, “Investigation of HIFU-induced anti-tumor immunity in a murine tumor model,” J. Transl. Med. 5, 34 (2007).
[Crossref]

Huang, C. H.

J. Yao, L. Wang, J. M. Yang, K. I. Maslov, T. T. W. Wong, L. Li, C. H. Huang, J. Zou, and L. V. Wang, “High-speed label-free functional photoacoustic microscopy of mouse brain in action,” Nat. Methods 12, 407–410 (2015).
[Crossref]

Huang, J.

C. Li, W. Zhang, W. Fan, J. Huang, F. Zhang, and P. Wu, “Noninvasive treatment of malignant bone tumors using high-intensity focused ultrasound,” Cancer 116, 3934–3942 (2010).
[Crossref]

Huang, X.

X. Huang, P. K. Jain, I. H. El-Sayed, and M. A. El-Sayed, “Plasmonic photothermal therapy (PPTT) using gold nanoparticles,” Laser Med. Sci. 23, 217–228 (2008).
[Crossref]

I. H. El-Sayed, X. Huang, and M. A. El-Sayed, “Selective laser photo-thermal therapy of epithelial carcinoma using anti-EGFR antibody conjugated gold nanoparticles,” Cancer Lett. 239, 129–135 (2006).
[Crossref]

Hynynen, K.

E. E. Konofagou, J. Thierman, T. Karjalainen, and K. Hynynen, “The temperature dependence of ultrasound-stimulated acoustic emission,” Ultrasound Med. Biol. 28, 331–338 (2002).
[Crossref]

E. Konofagou, J. Thierman, and K. Hynynen, “Experimental temperature monitoring and coagulation detection using ultrasound-stimulated acoustic emission,” in Ultrasonics Symposium (IEEE, 2001), vol. 1292, pp. 1299–1302.

Hyodo, T.

T. Uchida, H. Ohkusa, H. Yamashita, S. Shoji, Y. Nagata, T. Hyodo, and T. Satoh, “Five years experience of transrectal high-intensity focused ultrasound using the Sonablate device in the treatment of localized prostate cancer,” Int. J. Urol. 13, 228–233 (2010).
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T. Uchida, H. Ohkusa, Y. Nagata, T. Hyodo, T. Satoh, and A. Irie, “Treatment of localized prostate cancer using high-intensity focused ultrasound,” BJU Int. 97, 56–61 (2006).
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Irie, A.

T. Uchida, H. Ohkusa, Y. Nagata, T. Hyodo, T. Satoh, and A. Irie, “Treatment of localized prostate cancer using high-intensity focused ultrasound,” BJU Int. 97, 56–61 (2006).
[Crossref]

Issels, R.

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Supplementary Material (3)

NameDescription
» Supplement 1       Supplemental Document
» Visualization 1       The dynamic temperature mapping by TEMPT during HIFU treatment.
» Visualization 2       The dynamic temperature mapping by traditional PA thermometry during HIFU treatment.

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Figures (5)

Fig. 1.
Fig. 1. Thermal energy memory effect in TEMPT. (a) PA signal generation by a single laser pulse. (b) TEMPT measurement performed at time t0 during the thermotherapy. The local temperature is T0. (c) The temporal pattern of a burst of laser pulses used in TEMPT. (d) The thermal energy accumulation during the laser pulse burst leads to a local temperature rise. (e) The pattern of PA signals generated by the laser pulse burst. Note that PA signal amplitude depends on the local temperature when the laser pulse strikes. The accumulated thermal energy from earlier laser pulses leads to increased PA signal amplitudes by later pulses.

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Fig. 2.
Fig. 2. Three key steps of TEMPT. Step 1: PA signal excitation, acquisition, and reconstruction with a burst of laser pulses. Step 2: Ratiometric measurement and reconstruction of the Grüneisen parameter. Step 3: Absolute temperature mapping at a single time point and during the thermotherapy treatment.

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Fig. 3.
Fig. 3. TEMPT of temperatures on tissue phantoms. (a) Schematic of the PAT system. UT, ultrasonic transducer. Two ink-filled tubes with different temperatures were sandwiched between two slices of chicken tissue (each 1.5 cm thick). (b) Reconstructed PAT image of the tissue phantom, showing the positions of the two tubes. (c) Increase in PA signal amplitudes of the two tubes as a function of the laser pulse number, reflecting the elevated local temperatures. (d) TEMPT temperature map of the two tubes (shown in color) overlaid onto the ultrasound image (shown in gray). The temperatures measured by the thermocouple in Tube 1 and Tube 2 were 32°C and 40°C, respectively. (e) TEMPT temperatures of the two tubes as a function of the reference temperatures measured by the needle thermometer.

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Fig. 4.
Fig. 4. Schematic of in vivo TEMPT during HIFU heating. Note that the HIFU focus was located at about 2 mm beneath the skin surface of the mouse left limb.

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Fig. 5.
Fig. 5. TEMPT of absolute temperatures in vivo during HIFU treatment. (a) Reconstructed PAT image of the mouse left hindlimb. (b) TEMPT temperature maps at different HIFU heating times. Note that the temperature maps are thresholded at 37°C. The dashed lines indicate the approximate the HIFU focus. (c) TEMPT temperatures (shown in color) overlaid on the corresponding ultrasound images (shown in gray). (d) TEMPT temperatures in the HIFU focus [red box in (a)] and in a representative surrounding tissue area [blue box in (a)] as a function of the heating time. (e) Conventional PA thermometry of relative temperature changes at different HIFU heating times. (f) Conventional PA thermometry of relative temperature changes in the HIFU focus [red box in (a)] and in the surrounding tissue [blue box in (a)] as a function of the heating time.

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Equations (5)

Equations on this page are rendered with MathJax. Learn more.

p1=Γ0(T0)ημaϕδt,
pN=(Γ0(T0)+ΔΓ)ημaϕδt=[Γ0(T0)+bημaϕδt(N−1)]ημaϕδt,N≥2,where  b=kTρCV,
pN−p1p12=bη2μa2ϕ2δt2Γ02η2μa2ϕ2δt2·(N−1)=bΓ02·(N−1),N≥2.
Γ0(T0)=p12b(N−1)pN−p1,N≥2.
T0=115.89Γ0−13.14.