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The potential roles of bacteria to improve radiation treatment outcome

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Abstract

Many combined therapies have been proposed to enhance radiotherapy outcome, but they have several limitations. As a new feasible strategy, combination of radiotherapy with bacteria showed a significant positive impact on the tumor treatment and metastasis inhibition. Although probiotic bacteria and radiotherapy alone can be effective in the treatment of different cancers, the combination of these two therapies seems to enhance therapeutic outcome and is cost-effective. Bacterial cells can act as therapeutic/gene/drug delivery vehicles as well as theranostic agents. In this communication, we reviewed current evidences, studies, suggestions, and future-based directions on combination of radiotherapy and bacteria. In another sections, an overview on tumor hypoxia, bacteria in cancer therapy, and combination of radiotherapy and bacteria is presented. A brief overview on trials and animal studies which used bacteria to protect normal tissues against radiotherapy-induced complications is also included.

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References

  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.

    Article  PubMed  Google Scholar 

  2. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86.

    Article  CAS  PubMed  Google Scholar 

  3. Bentzen SM, Heeren G, Cottier B, Slotman B, Glimelius B, Lievens Y, et al. Towards evidence-based guidelines for radiotherapy infrastructure and staffing needs in Europe: the ESTRO QUARTS project. Radiother Oncol. 2005;75(3):355–65.

    Article  PubMed  Google Scholar 

  4. Liauw SL, Connell PP, Weichselbaum RR. New paradigms and future challenges in radiation oncology: an update of biological targets and technology. Sci Tansl Med. 2013;5(173):1732sr2-sr2.

    Google Scholar 

  5. Datta N, Ordóñez SG, Gaipl U, Paulides M, Crezee H, Gellermann J, et al. Local hyperthermia combined with radiotherapy and-/or chemotherapy: recent advances and promises for the future. Cancer Treat Rev. 2015;41(9):742–53.

    Article  CAS  PubMed  Google Scholar 

  6. Hainfeld JF, Slatkin DN, Smilowitz HM. The use of gold nanoparticles to enhance radiotherapy in mice. Phys Med Biol. 2004;49(18):N309.

    Article  CAS  PubMed  Google Scholar 

  7. Hood JD, Bednarski M, Frausto R, Guccione S, Reisfeld RA, Xiang R, et al. Tumor regression by targeted gene delivery to the neovasculature. Science. 2002;296(5577):2404–7.

    Article  CAS  PubMed  Google Scholar 

  8. Higgins GS, O’Cathail SM, Muschel RJ, McKenna WG. Drug radiotherapy combinations: review of previous failures and reasons for future optimism. Cancer Treat Rev. 2015;41(2):105–13.

    Article  PubMed  Google Scholar 

  9. Winczura P, Jassem J. Combined treatment with cytoprotective agents and radiotherapy. Cancer Treat Rev. 2010;36(3):268–75.

    Article  CAS  PubMed  Google Scholar 

  10. Formenti SC, Demaria S. Combining radiotherapy and cancer immunotherapy: a paradigm shift. J Natl Cancer Inst. 2013;105(4):256–65.

  11. Begg AC, Stewart FA, Vens C. Strategies to improve radiotherapy with targeted drugs. Nat Rev Cancer. 2011;11(4):239–53.

    Article  CAS  PubMed  Google Scholar 

  12. Richardson RB, Harper M-E. Mitochondrial stress controls the radiosensitivity of the oxygen effect: implications for radiotherapy. Oncotarget. 2016;7(16):21469.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Hill RP, Bristow RG, Fyles A, Koritzinsky M, Milosevic M, Wouters BG. Hypoxia and predicting radiation response. Semin Radiat Oncol. 2015;25(4):260–72.

    Article  PubMed  Google Scholar 

  14. Chouaib S, Messai Y, Couve S, Escudier B, Hasmim M, Noman MZ. Hypoxia promotes tumor growth in linking angiogenesis to immune escape. Front Immunol. 2012;3:21.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Wang W-M, Zhao Z-L, Ma S-R, Yu G-T, Liu B, Zhang L, et al. Epidermal growth factor receptor inhibition reduces angiogenesis via hypoxia-inducible factor-1α and notch1 in head neck squamous cell carcinoma. PLoS One. 2015;10(2):e0119723.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Harris AL. Hypoxia—a key regulatory factor in tumour growth. Nat Rev Cancer. 2002;2(1):38–47.

    Article  CAS  PubMed  Google Scholar 

  17. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011;473(7347):298–307.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Feng H, Wang J, Chen W, Shan B, Guo Y, Xu J, et al. Hypoxia-induced autophagy as an additional mechanism in human osteosarcoma radioresistance. J Bone Oncol. 2016;5(2):67–73.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Corry J, Rischin D. Strategies to overcome accelerated repopulation and hypoxia—What have we learned from clinical trials? Semin Oncol. 2004;31(6):802–8.

    Article  PubMed  Google Scholar 

  20. Peters LJ. Targeting hypoxia in head and neck cancer. Act Oncol. 2001;40(8):937–40.

    Article  CAS  Google Scholar 

  21. Moeller BJ, Richardson RA, Dewhirst MW. Hypoxia and radiotherapy: opportunities for improved outcomes in cancer treatment. Cancer Metastasis Rev. 2007;26(2):241–8.

    Article  CAS  PubMed  Google Scholar 

  22. Overgaard J, Horsman MR. Modification of hypoxia-induced radioresistance in tumors by the use of oxygen and sensitizers. Semin Radiat Oncol. 1996;6(1):10–21.

    Article  CAS  PubMed  Google Scholar 

  23. Rockwell S, Dobrucki IT, Kim EY, Marrison ST, Vu VT. Hypoxia and radiation therapy: past history, ongoing research, and future promise. Curr Mol Med. 2009;9(4):442–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Machtay M, Pajak TF, Suntharalingam M, Shenouda G, Hershock D, Stripp DC, et al. Radiotherapy with or without erythropoietin for anemic patients with head and neck cancer: a randomized trial of the Radiation Therapy Oncology Group (RTOG 99-03). Int J Radiat Oncol Biol Phys. 2007;69(4):1008–17.

    Article  CAS  PubMed  Google Scholar 

  25. Varlotto J, Stevenson MA. Anemia, tumor hypoxemia, and the cancer patient. Int J Radiat Oncol Biol Phys. 2005;63(1):25–36.

    Article  PubMed  Google Scholar 

  26. Wardman P. Chemical radiosensitizers for use in radiotherapy. Clin Oncol. 2007;19(6):397–417.

    Article  CAS  Google Scholar 

  27. Denny WA, Wilson WR. Tirapazamine: a bioreductive anticancer drug that exploits tumour hypoxia. Exp Opin Invest Drugs. 2000;9(12):2889–901.

    Article  CAS  Google Scholar 

  28. Barnett GC, West CM, Dunning AM, Elliott RM, Coles CE, Pharoah PD, et al. Normal tissue reactions to radiotherapy: towards tailoring treatment dose by genotype. Nat Rev Cancer. 2009;9(2):134–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Rodemann HP, Blaese MA. Responses of normal cells to ionizing radiation. Semin Radiat Oncol. 2007;17(2):81–8.

    Article  PubMed  Google Scholar 

  30. Khanna KK, Jackson SP. DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet. 2001;27(3):247–54.

    Article  CAS  PubMed  Google Scholar 

  31. Forbes NS. Engineering the perfect (bacterial) cancer therapy. Nat Rev Cancer. 2010;10(11):785–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Patyar S, Joshi R, Byrav DP, Prakash A, Medhi B, Das B. Bacteria in cancer therapy: a novel experimental strategy. J Biomed Sci. 2010;17(1):21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Felgner S, Kocijancic D, Frahm M, Weiss S. Bacteria in cancer therapy: renaissance of an old concept. Int J Microbiol. 2016;8(45):17–28.

    Google Scholar 

  34. Nallar SC, Xu D-Q, Kalvakolanu DV. Bacteria and genetically modified bacteria as cancer therapeutics: current advances and challenges. Cytokine. 2017;89:160–72.

    Article  CAS  PubMed  Google Scholar 

  35. Minton NP. Clostridia in cancer therapy. Nat Rev Microbiol. 2003;1(3):237–42.

    Article  CAS  PubMed  Google Scholar 

  36. Carswell E, Old LJ, Kassel R, Green S, Fiore N, Williamson B. An endotoxin-induced serum factor that causes necrosis of tumors. Proc Nat Acad Sci. 1975;72(9):3666–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Nougayrède J-P, Taieb F, De Rycke J, Oswald E. Cyclomodulins: bacterial effectors that modulate the eukaryotic cell cycle. Trend Microbiol. 2005;13(3):103–10.

    Article  Google Scholar 

  38. Oswald E, Sugai M, Labigne A, Wu HC, Fiorentini C, Boquet P, et al. Cytotoxic necrotizing factor type 2 produced by virulent Escherichia coli modifies the small GTP-binding proteins Rho involved in assembly of actin stress fibers. Proc Nat Acad Sci. 1994;91(9):3814–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Pastan I, FitzGerald D. Recombinant toxins for cancer treatment. Science. 1991;254(5035):1173.

    Article  CAS  PubMed  Google Scholar 

  40. Antignani A, FitzGerald D. Immunotoxins: the role of the toxin. Toxins. 2013;5(8):1486–502.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Wei MQ, Ellem KA, Dunn P, West MJ, Bai CX, Vogelstein B. Facultative or obligate anaerobic bacteria have the potential for multimodality therapy of solid tumours. Eur J Cancer. 2007;43(3):490–6.

    Article  PubMed  Google Scholar 

  42. Ryan RM, Green J, Lewis CE. Use of bacteria in anti-cancer therapies. BioEssays. 2006;28(1):84–94.

    Article  CAS  PubMed  Google Scholar 

  43. Van Mellaert L, Barbé S, Anné J. Clostridium spores as anti-tumour agents. Trend Microbiol. 2006;14(4):190–6.

    Article  Google Scholar 

  44. Zhou S. Synthetic biology: bacteria synchronized for drug delivery. Nature. 2016;536(7614):33–4.

    Article  CAS  PubMed  Google Scholar 

  45. Fensterle J, Bergmann B, Yone C, Hotz C, Meyer S, Spreng S, et al. Cancer immunotherapy based on recombinant Salmonella enterica serovar Typhimurium aroA strains secreting prostate-specific antigen and cholera toxin subunit B. Cancer Gene Ther. 2008;15(2):85–93.

    Article  CAS  PubMed  Google Scholar 

  46. Zhao M, Yang M, Ma H, Li X, Tan X, Li S, et al. Targeted therapy with a Salmonella typhimurium leucine-arginine auxotroph cures orthotopic human breast tumors in nude mice. Cancer Res. 2006;66(15):7647–52.

    Article  CAS  PubMed  Google Scholar 

  47. Avogadri F, Martinoli C, Petrovska L, Chiodoni C, Transidico P, Bronte V, et al. Cancer immunotherapy based on killing of Salmonella-infected tumor cells. Cancer Res. 2005;65(9):3920–7.

    Article  CAS  PubMed  Google Scholar 

  48. Frankel AE, Rossi P, Kuzel TM, Foss F. Diphtheria fusion protein therapy of chemoresistant malignancies. Curr Cancer Drug Targets. 2002;2(1):19–36.

    Article  CAS  PubMed  Google Scholar 

  49. Hagihara N, Walbridge S, Olson AW, Oldfield EH, Youle RJ. Vascular protection by chloroquine during brain tumor therapy with Tf-CRM107. Cancer Res. 2000;60(2):230–4.

    CAS  PubMed  Google Scholar 

  50. Xu J, Liu XS, Zhou S-F, Wei MQ. Combination of immunotherapy with anaerobic bacteria for immunogene therapy of solid tumours. Gene Ther Mol Biol. 2009;13:36–52.

    CAS  Google Scholar 

  51. Sznol M, Lin SL, Bermudes D, Zheng L-M, King I. Use of preferentially replicating bacteria for the treatment of cancer. J Clin Invest. 2000;105(8):1027–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Jain RK, Forbes NS. Can engineered bacteria help control cancer? Proc Nat Acad Sci. 2001;98(26):14748–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Parvez S, Malik KA, Ah Kang S, Kim HY. Probiotics and their fermented food products are beneficial for health. J Appl Microbiol. 2006;100(6):1171–85.

    Article  CAS  PubMed  Google Scholar 

  54. Wollowski I, Rechkemmer G, Pool-Zobel BL. Protective role of probiotics and prebiotics in colon cancer. Am J Clin Nutr. 2001;73(2):451s–5s.

    CAS  PubMed  Google Scholar 

  55. Bettegowda C, Dang LH, Abrams R, Huso DL, Dillehay L, Cheong I, et al. Overcoming the hypoxic barrier to radiation therapy with anaerobic bacteria. Proc Nat Acad Sci. 2003;100(25):15083–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Nuyts S, Van Mellaert L, Theys J, Landuyt W, Lambin P, Anné J. The use of radiation-induced bacterial promoters in anaerobic conditions: a means to control gene expression in clostridium-mediated therapy for cancer. Radiat Res. 2001;155(5):716–23.

    Article  CAS  PubMed  Google Scholar 

  57. Nuyts S, Van Mellaert L, Theys J, Landuyt W, Bosmans E, Anné J, et al. Radio-responsive recA promoter significantly increases TNF [alpha] production in recombinant clostridia after 2 Gy irradiation. Gene Ther. 2001;8(15):1197.

    Article  CAS  PubMed  Google Scholar 

  58. Jiang S-N, Phan TX, Nam T-K, Nguyen VH, Kim H-S, Bom H-S, et al. Inhibition of tumor growth and metastasis by a combination of Escherichia coli–mediated cytolytic therapy and radiotherapy. Mol Ther. 2010;18(3):635–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Platt J, Sodi S, Kelley M, Rockwell S, Bermudes D, Low K, et al. Antitumour effects of genetically engineered Salmonella in combination with radiation. Euro J Cancer. 2000;36(18):2397–402.

    Article  CAS  Google Scholar 

  60. Liu X, Jiang S, Piao L, Yuan F. Radiotherapy combined with an engineered Salmonella typhimurium inhibits tumor growth in a mouse model of colon cancer. Exp Anim. 2016;65(4):413–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Abdollahi H. Beneficial effects of cellular autofluorescence following ionization radiation: hypothetical approaches for radiation protection and enhancing radiotherapy effectiveness. Med Hypotheses. 2015;84(3):194–8.

    Article  PubMed  Google Scholar 

  62. Brizel DM, Wasserman TH, Henke M, Strnad V, Rudat V, Monnier A, et al. Phase III randomized trial of amifostine as a radioprotector in head and neck cancer. J Clin Oncol. 2000;18(19):3339–45.

    Article  CAS  PubMed  Google Scholar 

  63. Abdollahi H. Probiotic-based protection of normal tissues during radiotherapy. Nutrition. 2014;30(4):495.

    Article  PubMed  Google Scholar 

  64. Khademi S, Abdollahi H. Application of hydrogen producing microorganisms in radiotherapy: an idea. Iran J Public Health. 2014;43:1018–9.

    PubMed  PubMed Central  Google Scholar 

  65. Abdollahi H, Shiri I, Atashzar M, Sarebani M, Moloudi K, Samadian H. Radiation protection and secondary cancer prevention using biological radioprotectors in radiotherapy. Int J Cancer Ther Oncol. 2015;3(3):1–9.

  66. Abdollahi H, Atashzar M, Amini M. The potential use of biogas producing microorganisms in radiation protection. J Med Hypotheses Ideas. 2015;9(2):67–71.

    Article  Google Scholar 

  67. Group JFWW, Group JFWW. Guidelines for the evaluation of probiotics in food. London: World Health Organization, ON, Canada: Food and Agriculture Organization. 2002.

  68. Ciorba MA, Riehl TE, Rao MS, Moon C, Ee X, Nava GM, et al. Lactobacillus probiotic protects intestinal epithelium from radiation injury in a TLR-2/cyclo-oxygenase-2-dependent manner. Gut. 2012;61(6):829–38.

    Article  CAS  PubMed  Google Scholar 

  69. Demirer S, Aydıntug S, Aslım B, Kepenekci I, Sengül N, Evirgen O, et al. Effects of probiotics on radiation-induced intestinal injury in rats. Nutrition. 2006;22(2):179–86.

    Article  CAS  PubMed  Google Scholar 

  70. Seal M, Naito Y, Barreto R, Lorenzetti A, Safran P, Marotta F. Experimental radiotherapy-induced enteritis: a probiotic interventional study. J Dig Dis. 2007;8(3):143–7.

    Article  PubMed  Google Scholar 

  71. Mego M, Holec V, Drgona L, Hainova K, Ciernikova S, Zajac V. Probiotic bacteria in cancer patients undergoing chemotherapy and radiation therapy. Complement Ther Med. 2013;21(6):712–23.

    Article  PubMed  Google Scholar 

  72. Delia P, Sansotta G, Donato V, Frosina P, Messina G, De Renzis C, et al. Use of probiotics for prevention of radiation-induced diarrhea. World J Gastroenterol. 2007;13(6):912.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Sharma A, Rath G, Chaudhary S, Thakar A, Mohanti BK, Bahadur S. Lactobacillus brevis CD2 lozenges reduce radiation-and chemotherapy-induced mucositis in patients with head and neck cancer: a randomized double-blind placebo-controlled study. Eur J Cancer. 2012;48(6):875–81.

    Article  CAS  PubMed  Google Scholar 

  74. Demers M, Dagnault A, Desjardins J. A randomized double-blind controlled trial: impact of probiotics on diarrhea in patients treated with pelvic radiation. Clin Nutr. 2014;33(5):761–7.

    Article  PubMed  Google Scholar 

  75. Österlund P, Ruotsalainen T, Korpela R, Saxelin M, Ollus A, Valta P, et al. Lactobacillus supplementation for diarrhoea related to chemotherapy of colorectal cancer: a randomised study. Br J Cancer. 2007;97(8):1028–34.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Giralt J, Regadera JP, Verges R, Romero J, de la Fuente I, Biete A, et al. Effects of probiotic Lactobacillus casei DN-114 001 in prevention of radiation-induced diarrhea: results from multicenter, randomized, placebo-controlled nutritional trial. Int J Radiat Oncol Biol Phys. 2008;71(4):1213–9.

    Article  PubMed  Google Scholar 

  77. Delia P, Sansotta G, Donato V, Messina G, Frosina P, Pergolizzi S, et al. Prevention of radiation-induced diarrhea with the use of VSL# 3, a new high-potency probiotic preparation. Am J Gastroenterol. 2002;97(8):2150.

    Article  PubMed  Google Scholar 

  78. Xie J, Lee S, Chen X. Nanoparticle-based theranostic agents. Adv Drug Deliv Rev. 2010;62(11):1064–79.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Janib SM, Moses AS, MacKay JA. Imaging and drug delivery using theranostic nanoparticles. Adv Drug Deliv Rev. 2010;62(11):1052–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Chen F, Ehlerding EB, Cai W. Theranostic nanoparticles. J Nucl Med. 2014;55(12):1919–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Miladi I, Alric C, Dufort S, Mowat P, Dutour A, Mandon C, et al. The in vivo radiosensitizing effect of gold nanoparticles based MRI contrast agents. Small. 2014;10(6):1116–24.

    Article  CAS  PubMed  Google Scholar 

  82. Detappe A, Lux F, Tillement O. Pushing radiation therapy limitations with theranostic nanoparticles. Nanomed. 2016;11(9):997–9.

    Article  CAS  Google Scholar 

  83. Sancey L, Lux F, Kotb S, Roux S, Dufort S, Bianchi A, et al. The use of theranostic gadolinium-based nanoprobes to improve radiotherapy efficacy. Br J Radiol. 1041;2014(87):20140134.

    Google Scholar 

  84. Park SJ, Park S-H, Cho S, Kim D-M, Lee Y, Ko SY, et al. New paradigm for tumor theranostic methodology using bacteria-based microrobot. Sci Rep. 2013;3:3394.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Kojima R, Aubel D, Fussenegger M. Toward a world of theranostic medication: programming biological sentinel systems for therapeutic intervention. Adv Drug Deliv Rev. 2016;105:66–76.

    Article  CAS  PubMed  Google Scholar 

  86. Wu HC, Tsao CY, Quan DN, Cheng Y, Servinsky MD, Carter KK, et al. Autonomous bacterial localization and gene expression based on nearby cell receptor density. Mol Syst Biol. 2013;9(1):636.

    Article  PubMed  PubMed Central  Google Scholar 

  87. Quispe-Tintaya W, Chandra D, Jahangir A, Harris M, Casadevall A, Dadachova E, et al. Nontoxic radioactive Listeriaat is a highly effective therapy against metastatic pancreatic cancer. Proc Nat Acad Sci. 2013;110(21):8668–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Luo C-H, Huang C-T, Su C-H, Yeh C-S. Bacteria-mediated hypoxia-specific delivery of nanoparticles for tumors imaging and therapy. Nano Lett. 2016;16(6):3493–9.

    Article  CAS  PubMed  Google Scholar 

  89. Martel S, Mohammadi M, Felfoul O, Lu Z, Pouponneau P. Flagellated magnetotactic bacteria as controlled MRI-trackable propulsion and steering systems for medical nanorobots operating in the human microvasculature. Int J Robot Res. 2009;28(4):571–82.

    Article  Google Scholar 

  90. Zurkiya O, Chan AW, Hu X. MagA is sufficient for producing magnetic nanoparticles in mammalian cells, making it an MRI reporter. Mag Resonan Med. 2008;59(6):1225–31.

    Article  CAS  Google Scholar 

  91. Pfeifer F. Distribution, formation and regulation of gas vesicles. Nat Rev Microbiol. 2012;10(10):705–15.

    Article  CAS  PubMed  Google Scholar 

  92. Oren A. The function of gas vesicles in halophilic archaea and bacteria: theories and experimental evidence. Life. 2012;3(1):1–20.

    Article  PubMed  PubMed Central  Google Scholar 

  93. Shapiro MG, Goodwill PW, Neogy A, Yin M, Foster FS, Schaffer DV, et al. Biogenic gas nanostructures as ultrasonic molecular reporters. Nat Nanotechnol. 2014;9(4):311–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Ibsen S, Schutt CE, Esener S. Microbubble-mediated ultrasound therapy: a review of its potential in cancer treatment. Drug Des Dev Ther. 2013;7:375–88.

    Article  CAS  Google Scholar 

  95. Kiessling F, Fokong S, Koczera P, Lederle W, Lammers T. Ultrasound microbubbles for molecular diagnosis, therapy, and theranostics. J Nucl Med. 2012;53(3):345–8.

    Article  CAS  PubMed  Google Scholar 

  96. Wang X, Gkanatsas Y, Palasubramaniam J, Hohmann JD, Chen YC, Lim B, et al. Thrombus-targeted theranostic microbubbles: a new technology towards concurrent rapid ultrasound diagnosis and bleeding-free fibrinolytic treatment of thrombosis. Theranostics. 2016;6(5):726.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Jibu T, Ando K, Matsumoto T, Koike S, Kobori O, Morioka Y, et al. Active components of intestinal bacteria for abdominal irradiation-induced inhibition of lung metastases. Clin Exp Metastasis. 1991;9(6):529–40.

    Article  CAS  PubMed  Google Scholar 

  98. Fang J, Liao L, Yin H, Nakamura H, Shin T, Maeda H. Enhanced bacterial tumor delivery by modulating the EPR effect and therapeutic potential of Lactobacillus casei. J Pharm Sci. 2014;103(10):3235–43.

    Article  CAS  PubMed  Google Scholar 

  99. Dietzel F, Gericke D, König W. Tumor hyperthermia using high frequency for increase of oncolysis by Clostridium butyricum (M 55). Strahlentherapie. 1976;152(6):537–41.

    CAS  PubMed  Google Scholar 

  100. Dietzel F, Gericke D. Intensification of the oncolysis by clostridia by means of radio-frequency hyperthermy in experiments on animals–dependence on dosage and on intervals (author’s transl). Strahlentherapie. 1977;153(4):263–6.

    CAS  PubMed  Google Scholar 

  101. Crawford PA, Gordon JI. Microbial regulation of intestinal radiosensitivity. Proc Nat Acad Sci USA. 2005;102(37):13254–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Kainthola A, Gupta N, Agrawala PK. Gastrointestinal microflora in radiation injury and countermeasure. Ann Res Rev Biol. 2016;10(1):1–22.

  103. Liu Q, Nobaek S, Adawi D, Mao Y, Wang M, Molin G, et al. Administration of Lactobacillus plantarum 299v reduces side‐effects of external radiation on colon anastomotic healing in an experimental model. Colorectal Dis. 2001;3(4):245–52.

  104. Chitapanarux I, Chitapanarux T, Traisathit P, Kudumpee S, Tharavichitkul E, Lorvidhaya V. Randomized controlled trial of live lactobacillus acidophilus plus bifidobacterium bifidum in prophylaxis of diarrhea during radiotherapy in cervical cancer patients. Radiat Oncol. 2010;5(1):31.

  105. Tanaka I, Tanaka M, Satoh A, Kurematsu A, Ishiwata A, Suzuki K, et al. Alteration of radioprotective effects of heat-killed Lactobacillus casei in X-irradiated C3H/He mouse related to blood level of proinflammatory cytokines by corticoids. J Radiat Res. 2010;51(1):81–6.

  106. García-Peris P, Gimeno CV, Lozano M, Moreno Y, Paron L, de la Cuerda Compés C, et al. Effect of a mixture of inulin and fructo-oligosaccharide on lactobacillus and bifidobacterium intestinal microbiota of patients receiving radiotherapy; a randomised, double-blind, placebo-controlled trial. Nutr Hosp. 2012;27(6):1908–15.

  107. Ki Y, Kim W, Cho H, Ahn K, Choi Y, Kim D. The effect of probiotics for preventing radiation-induced morphological changes in intestinal mucosa of rats. J Korean Med Sci. 2014;29(10):1372–8.

  108. Nomoto K, Yokokura T, Tsuneoka K, Shikita M. Radioprotection of mice by a single subcutaneous injection of heat-killed Lactobacillus casei after irradiation. Radiation Res. 1991;125(3):293–7.

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Authors and Affiliations

  1. Department of Medical Bacteriology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran

    E. Kouhsari, N. Amirmozafari & S. Abbasian

  2. Department of Medical Biotechnology, Faculty of Allied Medicine, Iran University of Medical Sciences, Tehran, Iran

    A. Ghadimi-Daresajini

  3. Department of Medical Physics, School of Medicine, Iran University of Medical Sciences, Shahid Hemmat and Shahid Chamran Expressways, Tehran, 14496-14535, Iran

    H. Abdollahi & S. R. Mahdavi

  4. Radiation Biology Research Center, Iran University of Medical Sciences, Tehran, Iran

    S. R. Mahdavi

  5. Department of General Surgery, Rasoul Akram Hospital, Iran University of Medical Sciences, Tehran, Iran

    S. H. Mousavi

  6. Research Center for Gastroenterology and Liver Disease, Firoozgar Hospital, Iran University of Medical Sciences, Tehran, Iran

    H. F. Yaseri

  7. Department of Traditional Medicine, School of Traditional Medicine, Kerman University of Medical Sciences, Kerman, Iran

    M. Moghaderi

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  1. E. Kouhsari
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Correspondence to H. Abdollahi.

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Ebrahim Kouhsari declares that he has no conflict of interest. Ali Ghadimi-Daresajini declares that he has no conflict of interest. Noor Amirmozafari declares that he has no conflict of interest. Seied Rabi Mahdavi declares that he has no conflict of interest. Sara Abbasian declares that she has no conflict of interest. Seyed Hamzeh Mousavi declares that he has no conflict of interest. Hashem Fakhre Yaseri declares that he has no conflict of interest. Masoud Moghaderi declares that he has no conflict of interest. Hamid Abdollahi declares that he has no conflict of interest.

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Kouhsari, E., Ghadimi-Daresajini, A., Abdollahi, H. et al. The potential roles of bacteria to improve radiation treatment outcome. Clin Transl Oncol 20, 127–139 (2018). https://doi.org/10.1007/s12094-017-1701-7

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