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Gastric Cancer

, Volume 22, Issue 3, pp 463–472 | Cite as

Near infrared photoimmunotherapy using a fiber optic diffuser for treating peritoneal gastric cancer dissemination

  • Tadanobu Nagaya
  • Shuhei Okuyama
  • Fusa Ogata
  • Yasuhiro Maruoka
  • Peter L. Choyke
  • Hisataka KobayashiEmail author
Original Article

Abstract

Background

Peritoneal dissemination (PD) of abdominal malignancies is a common form of metastasis and its presence signals a poor prognosis. New treatment is required for patients with PD. Near infrared photoimmunotherapy (NIR-PIT) is a highly selective tumor treatment that employs an antibody–photo-absorber conjugate (APC). In this study, we investigate in vitro and in vivo efficacy of trastuzumab (tra)-IR700DX NIR-PIT on a human epidermal growth factor receptor type 2 (HER2)-positive gastric cancer cell line.

Methods

NIR-PIT effects were investigated in vitro and in vivo. Disseminated peritoneal implants mice were separated into 5 groups: (1) no treatment; (2) tra-IR700 i.v. only; (3) NIR light only; (4) NIR-PIT; (5) repeated NIR-PIT. The peritoneal cavity was irradiated with NIR light using a fiber optic diffuser delivered through the catheter.

Results

Specific binding and cell-specific killing was observed after NIR-PIT in vitro. In the in vivo study, fluorescence endoscopy showed high tumor accumulation of tra-IR700 within tumors. Significantly prolonged survival was achieved in the three treatment groups (tra-IR700 i.v. only, NIR-PIT, and repeated NIR-PIT groups) compared with control and NIR light only group (p < 0.05 for tra-IR700 i.v. only, p < 0.01 for NIR-PIT, and p < 0.0001 for repeated NIR-PIT). Moreover, most prolonged survival was shown for the repeated NIR-PIT group (p < 0.0001 vs tra-IR700 i.v. only, p < 0.01 vs NIR-PIT).

Conclusion

NIR-PIT using a fiber optic diffuser to deliver light is a promising candidate for the treatment of disseminated peritoneal metastases and could be readily translated to humans.

Keywords

Near infrared photoimmunotherapy Gastric cancer Fiber optic light probes Monoclonal antibodies Molecular imaging 

Notes

Funding

All authors were supported by the Intramural Research Program of the NIH, NCI, Center for Cancer Research.

Compliance with ethical standards

Conflict of interest

No potential conflicts of interest were disclosed.

Ethical standards

All institutional and national guidelines for the care and use of laboratory animals were followed.

Supplementary material

Supplementary material 1 (AVI 1744 KB)

10120_2018_871_MOESM2_ESM.avi (5.4 mb)
Supplementary material 2 (AVI 5579 KB)

References

  1. 1.
    Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65(2):87–108.CrossRefGoogle Scholar
  2. 2.
    Bang YJ, Van Cutsem E, Feyereislova A, Chung HC, Shen L, Sawaki A, et al. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet. 2010;376(9742):687–97.CrossRefGoogle Scholar
  3. 3.
    Noh SH, Park SR, Yang HK, Chung HC, Chung IJ, Kim SW, et al. Adjuvant capecitabine plus oxaliplatin for gastric cancer after D2 gastrectomy (CLASSIC): 5-year follow-up of an open-label, randomised phase 3 trial. Lancet Oncol. 2014;15(12):1389–96.CrossRefGoogle Scholar
  4. 4.
    Sasako M, Sakuramoto S, Katai H, Kinoshita T, Furukawa H, Yamaguchi T, et al. Five-year outcomes of a randomized phase III trial comparing adjuvant chemotherapy with S-1 versus surgery alone in stage II or III gastric cancer. J Clin Oncol. 2011;29(33):4387–93.CrossRefGoogle Scholar
  5. 5.
    Thomassen I, van Gestel YR, van Ramshorst B, Luyer MD, Bosscha K, Nienhuijs SW, et al. Peritoneal carcinomatosis of gastric origin: a population-based study on incidence, survival and risk factors. Int J Cancer. 2014;134(3):622–8.CrossRefGoogle Scholar
  6. 6.
    Wu CW, Lo SS, Shen KH, Hsieh MC, Chen JH, Chiang JH, et al. Incidence and factors associated with recurrence patterns after intended curative surgery for gastric cancer. World J Surg. 2003;27(2):153–8.Google Scholar
  7. 7.
    Park DI, Yun JW, Park JH, Oh SJ, Kim HJ, Cho YK, et al. HER-2/neu amplification is an independent prognostic factor in gastric cancer. Dig Dis Sci. 2006;51(8):1371–9.CrossRefGoogle Scholar
  8. 8.
    Mitsunaga M, Ogawa M, Kosaka N, Rosenblum LT, Choyke PL, Kobayashi H. Cancer cell-selective in vivo near infrared photoimmunotherapy targeting specific membrane molecules. Nat Med. 2011;17(12):1685–91.CrossRefGoogle Scholar
  9. 9.
    Hanaoka H, Nagaya T, Sato K, Nakamura Y, Watanabe R, Harada T, et al. Glypican-3 targeted human heavy chain antibody as a drug carrier for hepatocellular carcinoma therapy. Mol Pharm. 2015;12(6):2151–7.CrossRefGoogle Scholar
  10. 10.
    Nagaya T, Nakamura Y, Okuyama S, Ogata F, Maruoka Y, Choyke PL, et al. Syngeneic mouse models of oral cancer are effectively targeted by anti-CD44-Based NIR-PIT. Mol Cancer Res. 2017;15(12):1667–77.CrossRefGoogle Scholar
  11. 11.
    Nagaya T, Nakamura Y, Okuyama S, Ogata F, Maruoka Y, Choyke PL, et al. Near-infrared photoimmunotherapy targeting prostate cancer with prostate-specific membrane antigen (PSMA) Antibody. Mol Cancer Res. 2017;15(9):1153–62.CrossRefGoogle Scholar
  12. 12.
    Nagaya T, Nakamura Y, Sato K, Harada T, Choyke PL, Hodge JW, et al. Near infrared photoimmunotherapy with avelumab, an anti-programmed death-ligand 1 (PD-L1) antibody. Oncotarget. 2017;8(5):8807–17.CrossRefGoogle Scholar
  13. 13.
    Nagaya T, Nakamura Y, Sato K, Harada T, Choyke PL, Kobayashi H. Near infrared photoimmunotherapy of B-cell lymphoma. Mol Oncol. 2016;10(9):1404–14.CrossRefGoogle Scholar
  14. 14.
    Nagaya T, Nakamura Y, Sato K, Zhang YF, Ni M, Choyke PL, et al. Near infrared photoimmunotherapy with an anti-mesothelin antibody. Oncotarget. 2016;7(17):23361–9.CrossRefGoogle Scholar
  15. 15.
    Sato K, Choyke PL, Kobayashi H. Photoimmunotherapy of gastric cancer peritoneal carcinomatosis in a mouse model. PLoS One. 2014;9(11):e113276.CrossRefGoogle Scholar
  16. 16.
    Henderson TA, Morries LD. Near-infrared photonic energy penetration: can infrared phototherapy effectively reach the human brain? Neuropsychiatr Dis Treat. 2015;11:2191–208.CrossRefGoogle Scholar
  17. 17.
    Shuhei O, Tadanob N, Kazuhide S, Fusa O, Yasuhiro M, Choyke PL, et al. Interstitial near-infrared photoimmunotherapy: effective treatment areas and light doses needed for use with fiber optic diffusers. Oncotarget. 2018;9(13):11159–69.Google Scholar
  18. 18.
    Berretta M, Fisichella R, Borsatti E, Lleshi A, Ioffredo S, Meneguzzo N, et al. Feasibility of intraperitoneal Trastuzumab treatment in a patient with peritoneal carcinomatosis from gastric cancer. Eur Rev Med Pharmacol Sci. 2014;18(5):689–92.Google Scholar
  19. 19.
    Mitsunaga M, Nakajima T, Sano K, Choyke PL, Kobayashi H. Near-infrared theranostic photoimmunotherapy (PIT): repeated exposure of light enhances the effect of immunoconjugate. Bioconjug Chem. 2012;23(3):604–9.CrossRefGoogle Scholar
  20. 20.
    Nagaya T, Sato K, Harada T, Nakamura Y, Choyke PL, Kobayashi H. Near infrared photoimmunotherapy targeting EGFR positive triple negative breast cancer: optimizing the conjugate-light regimen. PLoS One. 2015;10(8):e0136829.CrossRefGoogle Scholar
  21. 21.
    DeLaney TF, Sindelar WF, Tochner Z, Smith PD, Friauf WS, Thomas G, et al. Phase I study of debulking surgery and photodynamic therapy for disseminated intraperitoneal tumors. Int J Radiat Oncol Biol Phys. 1993;25(3):445–57.CrossRefGoogle Scholar
  22. 22.
    Hino H, Murayama Y, Nakanishi M, Inoue K, Nakajima M, Otsuji E. 5-Aminolevulinic acid-mediated photodynamic therapy using light-emitting diodes of different wavelengths in a mouse model of peritoneally disseminated gastric cancer. J Surg Res. 2013;185(1):119–26.CrossRefGoogle Scholar
  23. 23.
    Kishi K, Yano M, Inoue M, Miyashiro I, Motoori M, Tanaka K, et al. Talaporfin-mediated photodynamic therapy for peritoneal metastasis of gastric cancer in an in vivo mouse model: drug distribution and efficacy studies. Int J Oncol. 2010;36(2):313–20.Google Scholar
  24. 24.
    Fidler IJ, Kripke ML. Metastasis results from preexisting variant cells within a malignant tumor. Science. 1977;197(4306):893–5.CrossRefGoogle Scholar
  25. 25.
    Nowell PC. Mechanisms of tumor progression. Cancer Res. 1986;46(5):2203–7.Google Scholar
  26. 26.
    Shirasu N, Yamada H, Shibaguchi H, Kuroki M, Kuroki M. Potent and specific antitumor effect of CEA-targeted photoimmunotherapy. Int J Cancer. 2014;135(11):2697–710.CrossRefGoogle Scholar
  27. 27.
    Wilson BC, Patterson MS. The physics, biophysics and technology of photodynamic therapy. Phys Med Biol. 2008;53(9):R61–109.CrossRefGoogle Scholar
  28. 28.
    Ishida M, Kagawa S, Shimoyama K, Takehara K, Noma K, Tanabe S, et al. Trastuzumab-based photoimmunotherapy integrated with viral HER2 transduction inhibits peritoneally disseminated HER2-negative cancer. Mol Cancer Ther. 2016;15(3):402–11.CrossRefGoogle Scholar
  29. 29.
    Kepp O, Senovilla L, Vitale I, Vacchelli E, Adjemian S, Agostinis P, et al. Consensus guidelines for the detection of immunogenic cell death. Oncoimmunology. 2014;3(9):e955691.CrossRefGoogle Scholar
  30. 30.
    Mitsunaga M, Nakajima T, Sano K, Kramer-Marek G, Choyke PL, Kobayashi H. Immediate in vivo target-specific cancer cell death after near infrared photoimmunotherapy. BMC Cancer. 2012;12:345.CrossRefGoogle Scholar
  31. 31.
    Sato K, Nagaya T, Choyke PL, Kobayashi H. Near infrared photoimmunotherapy in the treatment of pleural disseminated NSCLC: preclinical experience. Theranostics. 2015;5(7):698–709.CrossRefGoogle Scholar
  32. 32.
    Sano K, Mitsunaga M, Nakajima T, Choyke PL, Kobayashi H. Acute cytotoxic effects of photoimmunotherapy assessed by 18F-FDG PET. J Nucl Med. 2013;54(5):770–5.CrossRefGoogle Scholar
  33. 33.
    Ogawa M, Tomita Y, Nakamura Y, Lee MJ, Lee S, Tomita S, et al. Immunogenic cancer cell death selectively induced by near infrared photoimmunotherapy initiates host tumor immunity. Oncotarget. 2017;8(6):10425–36.CrossRefGoogle Scholar

Copyright information

© This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection 2018

Authors and Affiliations

  1. 1.Molecular Imaging Program, Center for Cancer Research, National Cancer InstituteNational Institutes of HealthBethesdaUSA

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