Study of Tumour and Surrounding Tissue Heating with Near-Infrared Radiation after the Injection of Gold Nanoparticles into the Tissue

Vadim D. Genin; Elina A. Genina; Alla B. Bucharskaya; Marina L. Chekhonatskaya; Georgy Terentyuk; Daria K. Tuchina; Nikolay G. Khlebtsov; Valery V. Tuchin; Alexey N. Bashkatov

doi:10.18287/JBPE18.04.010505

Authors

Vadim D. Genin Saratov State University, Russia
Elina A. Genina Saratov State University, Russia Tomsk State University, Russia
Alla B. Bucharskaya Saratov State Medical University named after V.I. Razumovsky, Russia
Marina L. Chekhonatskaya Saratov State Medical University named after V.I. Razumovsky, Russia
Georgy Terentyuk Saratov State Medical University named after V.I. Razumovsky, Russia
Daria K. Tuchina Saratov State University, Russia
Nikolay G. Khlebtsov Institute of Biochemistry and Physiology of Plants and Microorganisms, Russian Academy of Sciences, Saratov, Russia
Valery V. Tuchin Saratov State University, Russia Tomsk State University, Russia Institute of Precision Mechanics and Control, Russian Academy of Sciences, Saratov, Russia
Alexey N. Bashkatov Saratov State University, Russia Tomsk State University, Russia

DOI:

https://doi.org/10.18287/JBPE18.04.010505

Keywords:

tumour, NIR laser irradiation, photothermal therapy, gold nanorods

Abstract

We study the heating kinetics in transplanted model tumours after the intravenous injection of suspension of gold nanorods having the concentration from 400 to 1200 µg/mL under the laser irradiation at the wavelength 808 nm during 15 min. The object of study were 40 outbred white laboratory rats with transplanted liver cancer tumours (Cholangiocarcinoma PC1). The obtained results allow the optimisation of the gold nanorods injection technique at different degrees of vascularisation of tumour tissues aimed to provide the maximal heating of tumours by the laser radiation. It is shown that the maximal increase of the tumour temperature is related to the maximal accumulation of gold nanorods in the tumour tissues, observed in the case of its high vascularisation.

References

N. N. Aleksandrov, N. E. Savchenko, S. Z. Fradkin, and E. A. Zhavrid, Using Hyperthermia and Hyperglycaemia in the Treatment of Malignant Tumours, Meditsina, Moscow (1980) [in Russian].

G. F. Baronzio, and E. D. Hager, Hyperthermia In Cancer Treatment: A Primer Series Medical Intelligence Unit XXIII, New York (2006).

K. K. Jain, “Advances in the field of nanooncology,” BMC Medicine 8, 83, (2010).

N. S. Abadeer, and C. J. Murphy, “Recent progress in cancer thermal therapy using gold nanoparticles,” The Journal of Physical Chemistry C 120(9), 4691-4716 (2016).

X. Huang, P. K. Jain, I. H. El-Sayed, and M. A. El-Sayed, “Plasmonic photothermal therapy (PPTT) using gold nanoparticles,” Lasers in Medical Science 23(3), 217-228 (2008).

E. B. Dickerson, E. C. Dreaden, X. Huang, I. H. El-Sayed, H. Chu, S. Pushpanketh, J. F. McDonald, and M.A. El-Sayed, “Gold nanorod assisted near-infrared plasmonic photothermal therapy (PPTT) of squamous cell carcinoma in mice,” Cancer Letters 269(1), 57-66 (2008).

M. A. Sirotkina, V. V. Elagin, M. V. Shirmanova, M. L. Bugrova, L. B. Snopova, V. A. Nadtochenko, V. V. Kamenskii, and E. V. Zagaynova, “Laser hyperthermia of tumours using nanothermosensitisers,” Sovremennye tekhnologii v meditsine 1, 6-11 (2010) [in Russian].

M. A. Sirotkina, V. V. Elagin, M. L. Bugrova, M. V. Shirmanova, V. A. Nadtochenko, and E. V. Zagaynova, “Optical diagnostics and laser hyperthermia of tumours using plasmon-resonance nanoparticles,” Al’manakh klinicheskoy meditsiny 26, 63-67 (2012) [in Russian].

A. B. Bucharskaya, G. N. Maslyakova, N. I. Dikht, N. A. Navolokin, G. S. Terentyuk, A. N. Bashkatov, E. A. Genina, V. V. Tuchin, B. N. Khlebtsov, and N. G. Khlebtsov, “Cancer cell damage pathways at laser induced plasmon-resonant photothermal therapeutics of transplanted liver tumor,” BioNanoScience 6(3), 256-260 (2016).

L. A. Dykman, and N. G. Khlebtsov, “Uptake of engineered gold nanoparticles into mammalian cells,” Chemical Reviews 114(2), 1258-1288 (2014).

A. V. Alekseeva, V. A. Bogatyrev, B. N. Khlebtsov, A. G. Mel’nikov, L. A. Dykman, and N. G. Khlebtsov, “Gold nanorods: Synthesis and optical properties,” Colloid Journal 68(6), 661-678 (2006).

M. A. Sirotkina, V. V Elagin., M. V. Shirmanova, E. V. Zagainova, P. V. Subochev, and N. N. Denisov, “Laser hyperthermia of tumors using gold nanoparticles monitored by optical coherence tomography and acoustic thermometry,” Biophysics 56(6), 1102-1105 (2011).

M. Bonesi, S. G. Proskurin, and I. V. Meglinski, “Imaging of subcutaneous blood vessels and flow velocity profiles by optical coherence tomography,” Laser Physics 20(4), 891-899 (2010).

E. A. Genina, Yu. I. Svenskaya, I. Yu. Yanina, L. E. Dolotov, A. N. Bashkatov, N. A. Navolokin, G. S. Terentyuk, A. B. Bucharskaya, G. N. Maslyakova, D. A. Gorin, V. V. Tuchin, and G. B. Sukhorukov, “In vivo optical monitoring of transcutaneous delivery of calcium carbonate microcontainers,” Biomedical Optics Express 7(6), 2082-2087 (2016).

S. Schuh, J. Holmes, M. Ulrich, L. Themstrup, G. B. E. Jemec, N. De Carvalho, G. Pellacani, and J. Welzel, “Imaging Blood Vessel Morphology in Skin: Dynamic Optical Coherence Tomography as a Novel Potential Diagnostic Tool in Dermatology,” Dermatology and Therapy (Heidelb) 7(2), 187-202 (2017).

L. Li, R. Wang, D. Wilcox, X. Zhao, J. Song, X. Lin, W. M. Kohlbrenner, S. W. Fesik, and Y. Shen, “Tumor vasculature is a key determinant for the efficiency of nanoparticle-mediated siRNA delivery,” Gene Therapy 19, 775-780 (2012).

H. B. Frieboes, M. Wu, J. Lowengrub, P. Decuzzi, and V. Cristini, “A computational model for predicting nanoparticle accumulation in tumor vasculature,” PLoS ONE 8(2), e56876 (2013).

K.-C. Mei, J. Bai, S. Lorrio, J. T.-W. Wang, and K. T. Al-Jamal, “Investigating the effect of tumor vascularization on magnetic targeting in vivo using retrospective design of experiment,” Biomaterials 106, 276-285 (2016).

International Guiding Principles for Biomedical Research Involving Animals, CIOMS-ICLAS (2012).

W. T. Yang, G. M. K. Tse, P. K. W. Lam, C. Metreweli, and J. Chang, “Correlation between color power Doppler sonographic measurement of breast tumor vasculature and immunohistochemical analysis of microvessel density for the quantitation of angiogenesis,” Journal of Ultrasound in Medicine 21(11), 1227-1235, (2002).

D. Kidron, J. Bernheim, R. Aviram, I. Cohen, A. Fishman, Y. Beyth, and R. Tepper, “Resistance to blood flow in ovarian tumors: correlation between resistance index and histological pattern of vascularization,” Ultrasound Obstet Gynecol 13(6), 425-430 (1999).

M. Emoto, H. Iwasaki, K. Mimura, T. Kawarabayashi, and M. Kikuchi, “Differences in the angiogenesis of benign and malignant ovarian tumors, demonstrated by analyses of color doppler ultrasound, immunohistochemistry, and microvessel density,” Cancer 80(5), 899-907 (1997).

B. N. Khlebtsov, E. S. Tuchina, V. A. Khanadeev, E. V. Panfilova, P. O. Petrov, V. V. Tuchin, and N. G. Khlebtsov, “Enhanced photoinactivation of Staphylococcus aureus with nanocomposites containing plasmonic particles and hematoporphyrin,” Journal of Biophotonics 6(4), 338-351 (2013).

P. Puvanakrishnan, J. Park, D. Chatterjee, S. Krishnan, and J. W Tunnell, “In vivo tumor targeting of gold nanoparticles: effect of particle type and dosing strategy,” International Journal of Nanomedicine 7, 1251-1258 (2012).

A. B. Bucharskaya, G. N. Maslyakova, N. I. Dikht, N. A. Navolokin, G. S. Terentyuk, A. N. Bashkatov, E. A. Genina, B. N. Khlebtsov, N. G. Khlebtsov, and V. V. Tuchin, “Plasmonic photothermal therapy of transplanted tumors in rats at multiple intravenous injection of gold nanorods,” BioNanoScience 7(1), 216-221 (2017).

L. R. Hirsch, R. J. Stafford, J. A. Bankson, S. R. Sershen, B. Rivera, R. E. Price, J. D. Hazle, N. J. Halas, and J. L. West, “Nanoshell-mediated near-infrared thermal therapy of tumors under magnetic resonance guidance,” Proceedings of the National Academy of Sciences 100(23), 13549-13554 (2003).