Nano Research

, Volume 8, Issue 12, pp 3842–3852 | Cite as

Photothermal therapy of tumors in lymph nodes using gold nanorods and near-infrared laser light with controlled surface cooling

  • Tessai Sugiura
  • Daisuke Matsuki
  • Junnosuke Okajima
  • Atsuki Komiya
  • Shiro Mori
  • Shigenao Maruyama
  • Tetsuya Kodama
Research Article

Abstract

Photothermal therapy (PTT) using near-infrared (NIR) laser light and gold nanorods (GNRs) shows promise as a novel cancer treatment modality. However, the laser intensity required to destroy tumor cells located beneath the skin is greater than the threshold intensity that causes skin damage; thus, irradiation with laser light damages the skin as well as the tumor. Here, we show that a temperature control system allows metastatic lymph nodes (LNs) to be treated by PTT using NIR laser light and GNRs, without skin damage. A mouse model of LN metastasis was developed by injection of tumor cells, and the tumor-bearing proper axillary LN was treated with NIR laser light after injection of GNRs. The skin temperature was maintained at 45 °C during irradiation by using a temperature control system. Bioluminescence imaging revealed that tumor progression was less in LNs exposed to NIR laser light and GNRs than in LNs exposed to NIR laser light alone or controls (no irradiation or GNRs). Furthermore, the skin and LN capsule were macroscopically intact on day 9 after irradiation with NIR laser light, whereas tumor cells within the LN showed apoptosis. A numerical analysis demonstrated that the high-temperature zone and the LN region showing damage were localized to an area up to 3 mm in depth. The proposed novel PTT technique, using NIR laser light and GNRs with controlled surface cooling, could be applied clinically to treat metastatic LNs located within or outside the area accessible for surgical dissection.

Keywords

lymph node metastasis photothermal therapy gold nanorods temperature control 

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References

  1. [1]
    Kodama, T.; Hatakeyama, Y.; Kato, S.; Mori, S. Visualization of fluid drainage pathways in lymphatic vessels and lymph nodes using a mouse model to test a lymphatic drug delivery system. Biomed. Opt. Express 2015, 6, 124–134.CrossRefGoogle Scholar
  2. [2]
    Ferrari, M.; Quaresima, V. A brief review on the history of human functional near-infrared spectroscopy (fNIRS) development and fields of application. Neuroimage 2012, 63, 921–935.CrossRefGoogle Scholar
  3. [3]
    Zuloaga, J.; Prodan, E.; Nordlander, P. Quantum plasmonics: Optical properties and tunability of metallic nanorods. ACS Nano 2010, 4, 5269–5276.CrossRefGoogle Scholar
  4. [4]
    Liao, J. F.; Li, W. T.; Peng, J. R.; Yang, Q.; Li, H.; Wei, Y. Q.; Zhang, X. N.; Qian, Z. Y. Combined cancer photothermalchemotherapy based on doxorubicin/gold nanorod-loaded polymersomes. Theranostics 2015, 5, 345–356.CrossRefGoogle Scholar
  5. [5]
    Niidome, T.; Akiyama, Y.; Yamagata, M.; Kawano, T.; TMori, T.; Niidome, Y.; Katayama, Y. Poly(ethylene glycol)-modified gold nanorods as a photothermal nanodevice for hyperthermia. J. Biomater. Sci. Polym. Ed. 2009, 20, 1203–1215.CrossRefGoogle Scholar
  6. [6]
    Tsai, M. F.; Chang, S. H. G.; Cheng, F. Y.; Shanmugam, V.; Cheng, Y. S.; Su, C. H.; Yeh, C. S. Au nanorod design as light-absorber in the first and second biological near-infrared windows for in vivo photothermal therapy. ACS Nano 2013, 7, 5330–5342.CrossRefGoogle Scholar
  7. [7]
    Wang, Y. H.; Chen, S. P.; Liao, A. H.; Yang, Y. C.; Lee, C. R.; Wu, C. H.; Wu, P. C.; Liu, T. M.; Wang, C. R.; Li, P. C. Synergistic delivery of gold nanorods using multifunctional microbubbles for enhanced plasmonic photothermal therapy. Sci. Rep. 2014, 4, 5685.Google Scholar
  8. [8]
    American National Standard for Safe Use of Lasers; ANSI Z136.1–2007; Laser Institute of America: Orland, FL,USA, 2007.Google Scholar
  9. [9]
    Henriques, F. C. Studies of thermal injury: V. Predictability and significance of thermally induced rate processes leading to irreversible epidermal injury. Arch. Pathol. 1947, 43, 489–502.Google Scholar
  10. [10]
    Shao, L. N.; Mori, S.; Yagishita, Y.; Okuno, T.; Hatakeyama, Y.; Sato, T.; Kodama, T. Lymphatic mapping of mice with systemic lymphoproliferative disorder: Usefulness as an inter-lymph node metastasis model of cancer. J. Immunol. Methods 2013, 389, 69–78.CrossRefGoogle Scholar
  11. [11]
    Pennes, H. H. Analysis of tissue and arterial blood temperatures in the resting human forearm. J. Appl. Physiol. 1948, 1, 93–122.Google Scholar
  12. [12]
    Sakurai, A.; Nitta, I.; Maruyama, S.; Okajima, J.; Matsubara, K. Coupled photon and heat transport simulation inside biological tissue for laser therapy. J. Therm. Sci. Tech. 2009, 4, 314–323.CrossRefGoogle Scholar
  13. [13]
    Okajima, J.; Maruyama, S.; Takeda, H.; Komiya, A. Dimensionless solutions and general characteristics of bioheat transfer during thermal therapy. J. Therm. Biol. 2009, 34, 377–384.CrossRefGoogle Scholar
  14. [14]
    Jiao, J.; Guo, Z. X. Thermal interaction of short-pulsed laser focused beams with skin tissues. Phys. Med. Biol. 2009, 54, 4225–4241.CrossRefGoogle Scholar
  15. [15]
    Heat Transfer Engineering Source Book; The Japan Society of Mechanical Engineers: Tokyo, Japan, 1986.Google Scholar
  16. [16]
    Weaver, J. A.; Stoll, A. M. Mathematical model of skin exposed to thermal radiation. Aerosp. Med. 1969, 40, 24–30.Google Scholar
  17. [17]
    Jia, W. C.; Aguilar, G.; Verkruysse, W.; Franco, W.; Nelson, J. S. Improvement of port wine stain laser therapy by skin preheating prior to cryogen spray cooling: A numerical simulation. Lasers Surg. Med. 2006, 38, 155–162.CrossRefGoogle Scholar
  18. [18]
    Okuno, T.; Kato, S.; Hatakeyama, Y.; Okajima, J.; Maruyama, S.; Sakamoto, M.; Mori, S.; Kodama, T. Photothermal therapy of tumors in lymph nodes using gold nanorods and nearinfrared laser light. J. Control. Release 2013, 172, 879–884.CrossRefGoogle Scholar
  19. [19]
    Li, L.; Mori, S.; Kodama, M.; Sakamoto, M.; Takahashi, S.; Kodama, T. Enhanced sonographic imaging to diagnose lymph node metastasis: Importance of blood vessel volume and density. Cancer Res. 2013, 73, 2082–2092.CrossRefGoogle Scholar
  20. [20]
    Kodama, T.; Tomita, N.; Yagishita, Y.; Horie, S.; Funamoto, K.; Hayase, T.; Sakamoto, M.; Mori, S. Volumetric and angiogenic evaluation of antitumor effects with acoustic liposome and high-frequency ultrasound. Cancer Res. 2011, 71, 6957–6964.CrossRefGoogle Scholar
  21. [21]
    Horie, S.; Chen, R.; Li, L.; Mori, S.; Kodama, T. Contrastenhanced high-frequency ultrasound imaging of early stage liver metastasis in a preclinical mouse model. Cancer Lett. 2013, 339, 208–213.CrossRefGoogle Scholar
  22. [22]
    Iizuka, M. N.; Vitkin, I. A.; Kolios, M. C.; Sherar, M. D. The effects of dynamic optical properties during interstitial laser photocoagulation. Phys. Med. Biol. 2000, 45, 1335–1357.CrossRefGoogle Scholar
  23. [23]
    Vera, J.; Bayazitoglu, Y. A note on laser penetration in nanoshell deposited tissue. Int. J. Heat Mass Transfer 2009, 52, 3402–3406.CrossRefGoogle Scholar
  24. [24]
    Jang, B.; Kim, Y. S.; Choi, Y. Effects of gold nanorod concentration on the depth-related temperature increase during hyperthermic ablation. Small 2011, 7, 265–270.CrossRefGoogle Scholar
  25. [25]
    Stern, J. M.; Cadeddu, J. A. Emerging use of nanoparticles for the therapeutic ablation of urologic malignancies. Urol. Oncol. 2008, 26, 93–96.CrossRefGoogle Scholar
  26. [26]
    Huang, X. H.; El-Sayed, I. H.; Qian, W.; El-Sayed, M. A. Cancer cell imaging and photothermal therapy in the nearinfrared region by using gold nanorods. J. Am. Chem. Soc. 2006, 128, 2115–2120.CrossRefGoogle Scholar
  27. [27]
    Zhang, Z. J.; Wang, L. M.; Wang, J.; Jiang, X. M.; Li, X. H.; Hu, Z. J.; Ji, Y. L.; Wu, X. C.; Chen, C. Y. Mesoporous silicacoated gold nanorods as a light-mediated multifunctional theranostic platform for cancer treatment. Adv. Mater. 2012, 24, 1418–1423.CrossRefGoogle Scholar
  28. [28]
    Takahashi, H.; Niidome, Y; Niidome, T.; Kaneko, K.; Kawasaki, H.; Yamada, S. Modification of gold nanorods using phosphatidylcholine to reduce cytotoxicity. Langmuir 2006, 22, 2–5.CrossRefGoogle Scholar
  29. [29]
    Peralta, D. V.; Heidari, Z.; Dash, S.; Tarr, M. A. Hybrid paclitaxel and gold nanorod-loaded human serum albumin nanoparticles for simultaneous chemotherapeutic and photothermal therapy on 4T1 breast cancer cells. ACS Appl. Mater. Interfaces 2015, 7, 7101–7111.CrossRefGoogle Scholar
  30. [30]
    Goodrich, G. P.; Bao, L. L.; Gill-Sharp, K.; Sang, K. L.; Wang, J.; Payne, J. D. Photothermal therapy in a murine colon cancer model using near-infrared absorbing gold nanorods. J. Biomed. Opt. 2010, 15, 018001.CrossRefGoogle Scholar

Copyright information

© Tsinghua University Press and Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Tessai Sugiura
    • 1
  • Daisuke Matsuki
    • 2
  • Junnosuke Okajima
    • 3
  • Atsuki Komiya
    • 3
  • Shiro Mori
    • 4
  • Shigenao Maruyama
    • 3
  • Tetsuya Kodama
    • 2
  1. 1.Department of Mechanical Systems and Design, Graduate School of EngineeringTohoku UniversitySendaiJapan
  2. 2.Laboratory of Biomedical Engineering for Cancer, Department of Biomedical Engineering, Graduate School of Biomedical EngineeringTohoku UniversitySendaiJapan
  3. 3.Institute of Fluid ScienceTohoku UniversitySendaiJapan
  4. 4.Department of Oral and Maxillofacial SurgeryTohoku University HospitalSendaiJapan

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