2,237
Views
29
CrossRef citations to date
0
Altmetric
Reviews

Magnetic nanoparticle hyperthermia for treating locally advanced unresectable and borderline resectable pancreatic cancers: the role of tumor size and eddy-current heating

, , , , &
Pages 108-119 | Received 19 Feb 2020, Accepted 09 Jul 2020, Published online: 10 Jan 2021

References

  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA A Cancer J Clin. 2019;69(1):7–34.
  • National Cancer Institute. Pancreas Cancer 5-Year relative survival by stage at diagnosis, 2010-2016. SEER (Surveillance Epidemiology and End Results) cancer statistics review. Available at http://www.seer.cancer.gov
  • Small W, Jr., Hayes JP, Suh WW, et al. ACR appropriateness criteria® borderline and unresectable pancreas cancer. Oncology. 2016;30(7):619–624.
  • Vincent A, Herman J, Schulick R, et al. Pancreatic cancer. The Lancet. 2011;378(9791):607–620.
  • Kamisawa T, Wood LD, Itoi T, et al. Pancreatic cancer. The Lancet. 2016;388(10039):73–85.
  • Gastrointestinal Tumor Study Group. Treatment of locally unresectable carcinoma of the pancreas: comparison of combined-modality therapy (chemotheraphy plus radiotherapy) to chemotheraphy alone. J Nat Cancer Inst. 1988;80(10):751–755.
  • Chauffert B, Mornex F, Bonnetain F, et al. Phase III trial comparing intensive induction chemoradiotherapy (60 Gy, infusional 5-FU and intermittent cisplatin) followed by maintenance gemcitabine with gemcitabine alone for locally advanced unresectable pancreatic cancer. Definitive results of the 2000-01 FFCD/SFRO study. Ann Oncol. 2008;19(9):1592–1599.
  • Klaassen DJ, MacIntyre JM, Catton GE, et al. Treatment of locally unresectable cancer of the stomach and pancreas: a randomized comparison of 5-fluorouracil alone with radiation plus concurrent and maintenance 5-fluorouracil-an Eastern Cooperative Oncology Group study. J Clin Oncol. 1985;3(3):373–378.
  • Loehrer PJ, Powell ME, Cardenes HR, et al. A randomized phase III study of gemcitabine in combination with radiation therapy versus gemcitabine alone in patients with localized, unresectable pancreatic cancer: E4201. J Cin Oncol. 2008;26(15):4506.
  • Loehrer PJ, Sr., Feng Y, Cardenes H, et al. Gemcitabine alone versus gemcitabine plus radiotherapy in patients with locally advanced pancreatic cancer: an Eastern Cooperative Oncology Group trial. J Clin Oncol. 2011;29(31):4105–4112.
  • Whatcott CJ, Posner RG, Von Hoff DD, et al. Desmoplasia and chemoresistance in pancreatic cancer. In: Grippo PJ, Munshi HG, editors. Pancreatic cancer and tumor microenvironment. Trivandrum (India): Transworld Research Network; 2012.
  • Hata H, Mori H, Matsumoto S, et al. Fibrous stroma and vascularity of pancreatic carcinoma: correlation with enhancement patterns on CT. Abdom Imaging. 2010;35(2):172–180.
  • Komar G, Kauhanen S, Liukko K, et al. Decreased blood flow with increased metabolic activity: a novel sign of pancreatic tumor aggressiveness. Clinical Cancer Res. 2009;15(17):5511–5517.
  • Balaban EP, Mangu PB, Khorana AA, et al. Locally advanced, unresectable pancreatic cancer: American Society of Clinical Oncology clinical practice guideline. J Clin Oncol. 2016;34(22):2654–2668.
  • Gillen S, Schuster T, Zum Büschenfelde CM, et al. Preoperative/neoadjuvant therapy in pancreatic cancer: a systematic review and meta-analysis of response and resection percentages. PLoS Med. 2010;7(4):e1000267.
  • Ng SP, Herman JM. SBRT for unresectable pancreatic cancer can improve local control with minimal toxicity. Int J Radiat Oncol Biol Phys. 2017;99(2):298–299.
  • Huang X, Knoble JL, Zeng M, et al. Neoadjuvant gemcitabine chemotherapy followed by concurrent IMRT simultaneous boost achieves high R0 resection in borderline resectable pancreatic cancer patients. PloS One. 2016;11(12):e0166606.
  • Chuong MD, Springett GM, Freilich JM, et al. Stereotactic body radiation therapy for locally advanced and borderline resectable pancreatic cancer is effective and well tolerated. Int J Radiation Oncol Biol Phys. 2013;86(3):516–522.
  • Moningi S, Dholakia AS, Raman SP, et al. The role of stereotactic body radiation therapy for pancreatic cancer: a single-institution experience. Ann Surg Oncol. 2015;22(7):2352–2358.
  • Parekh A, Rosati LM, Chang DT, et al. Stereotactic body radiation for pancreatic cancer: results of an international survey of practice patterns. Int J Radiation Oncol Biol Phys. 2015;93(3):E132.
  • Herman JM, Chang DT, Goodman KA, et al. Phase 2 multi‐institutional trial evaluating gemcitabine and stereotactic body radiotherapy for patients with locally advanced unresectable pancreatic adenocarcinoma. Cancer. 2015;121(7):1128–1137.
  • Qiu H, Wild AT, Wang H, et al. Comparison of conventional and 3-dimensional computed tomography against histopathologic examination in determining pancreatic adenocarcinoma tumor size: implications for radiation therapy planning. Radiother Oncol. 2012;104(2):167–172.
  • Tozzi A, Comito T, Alongi F, et al. SBRT in unresectable advanced pancreatic cancer: preliminary results of a mono-institutional experience. Radiat Oncol. 2013;8(1):148.
  • Moningi S, Marciscano AE, Rosati LM, et al. Stereotactic body radiation therapy in pancreatic cancer: the new frontier. Expert Rev Anticancer Ther. 2014;14(12):1461–1475.
  • Schellenberg D, Goodman KA, Lee F, et al. Gemcitabine chemotherapy and single-fraction stereotactic body radiotherapy for locally advanced pancreatic cancer. Int J Radiation Oncol Biol Phys. 2008;72(3):678–686.
  • Hoyer M, Roed H, Sengelov L, et al. Phase-II study on stereotactic radiotherapy of locally advanced pancreatic carcinoma. Radiother Oncol. 2005;76(1):48–53.
  • De Jong MC, Li F, Cameron JL, et al. Re‐evaluating the impact of tumor size on survival following pancreaticoduodenectomy for pancreatic adenocarcinoma. J Surg Oncol. 2011;103(7):656–662.
  • Rwigema JC, Parikh SD, Heron DE, et al. Stereotactic body radiotherapy in the treatment of advanced adenocarcinoma of the pancreas. Am J Clin Oncol. 2011;34(1):63–69.
  • Schäfer C, Seeliger H, Bader DC, et al. Heat shock protein 27 as a prognostic and predictive biomarker in pancreatic ductal adenocarcinoma. J Cell Mol Med. 2012;16(8):1776–1791.
  • Takahashi C, Shridhar R, Huston J, et al. Correlation of tumor size and survival in pancreatic cancer. J Gastrointest Oncol. 2018;9(5):910–921.
  • Marchegiani G, Andrianello S, Malleo G, et al. Does size matter in pancreatic cancer. Annals Surg. 2017;266(1):142–148.
  • Zhang A, Ren S, Yuan Y, et al. Prognostic values of 18F-FDG PET/CT metabolic parameters and clinical figures in locally advanced pancreatic cancer underwent chemotherapy combined with stereotactic body radiation therapy. Medicine. 2019;98(13):e15064.
  • Zschaeck S, Blümke B, Wust P, et al. Dose-escalated radiotherapy for unresectable or locally recurrent pancreatic cancer: dose volume analysis, toxicity and outcome of 28 consecutive patients. PLoS One. 2017;12(10):e0186341.
  • Dholakia AS, Chaudhry M, Leal JP, et al. Baseline metabolic tumor volume and total lesion glycolysis are associated with survival outcomes in patients with locally advanced pancreatic cancer receiving stereotactic body radiation therapy. Int J Radiation Oncol Biol Phys. 2014;89(3):539–546.
  • Lee JW, Kang CM, Choi HJ, et al. Prognostic value of metabolic tumor volume and total lesion glycolysis on preoperative 18F-FDG PET/CT in patients with pancreatic cancer. J Nucl Med. 2014;55(6):898–904.
  • Chirindel A, Alluri KC, Chaudhry MA, et al. Prognostic value of FDG PET/CT–derived parameters in pancreatic adenocarcinoma at initial PET/CT staging. Am J Roentgenol. 2015; 204(5):1093–1099.
  • Yoo SH, Kang SY, Cheon GJ, et al. Predictive role of temporal changes in intratumoral metabolic heterogeneity during palliative chemotherapy in patients with advanced pancreatic cancer: a prospective cohort study. J Nucl Med. 2020;61(1):33–39.
  • Tschoep-Lechner KE, Milani V, Berger F, et al. Gemcitabine and cisplatin combined with regional hyperthermia as second-line treatment in patients with gemcitabine-refractory advanced pancreatic cancer. Int J Hyperthermia. 2013;29(1):8–16.
  • Roesch M, Mueller-Huebenthal B. Review: the role of hyperthermia in treating pancreatic tumors. Indian J Surg Oncol. 2015;6(1):75–81.
  • Dewhirst MW, Stauffer PR, Das S. Hyperthermia. In: Gunderson L, Tepper J, editors. Clinical radiation oncology, 4th ed. Philadelphia (PA): Elsevier; 2015.
  • Song CW, Park HJ, Lee CK, et al. Implications of increased tumor blood flow and oxygenation caused by mild temperature hyperthermia in tumor treatment. Int J Hyperthermia. 2005;21(8):761–767.
  • Crezee J, Zweije R, Kok HP. Design and use of phased array RF systems for loco-regional hyperthermia of deep seated tumors. Paper presented at: 2018 EMF-Med 1st World Conference on Biomedical Applications of Electromagnetic Fields (EMF-Med); 2018 Sep 10–13, Splitsko-Dalmatinska Županija, Croatia.
  • Kok HP, Navarro F, Strigari L, et al. Locoregional hyperthermia of deep-seated tumours applied with capacitive and radiative systems: a simulation study. Int J Hyperthermia. 2018;34(6):714–730.
  • Kok HP, Cressman ENK, Ceelen W, et al. Heating technology for malignant tumors: a review. Int J Hyperthermia. 2020;37(1):711–741.
  • Dennis CL, Ivkov R. Physics of heat generation using magnetic nanoparticles for hyperthermia. Int J Hyperthermia. 2013;29(8):715–729.
  • Maier-Hauff K, Ulrich F, Nestler D, et al. Efficacy and safety of intratumoral thermotherapy using magnetic iron-oxide nanoparticles combined with external beam radiotherapy on patients with recurrent glioblastoma multiforme. J Neurooncol. 2011;103(2):317–324.
  • MagForce AG. The nanomedicine company. U.S. FDA IDE approval to start prostate cancer study. Shareholder Letter. [cited 2019 Jun]. Available at https://www.magforce.com/fileadmin/user_upload/MagForce_AG_Shareholder_Letter_June_20_2019.pdf
  • Herman JM, Wild AT, Wang H, et al. Randomized phase III multi-institutional study of TNFerade biologic with fluorouracil and radiotherapy for locally advanced pancreatic cancer: final results. J Cin Oncol. 2013;31(7):886–894.
  • Ungureanu BS, Pirici D, Margaritescu C, et al. Endoscopic ultrasound guided injection of iron oxide magnetic nanoparticles for liver and pancreas: a feasibility study in pigs. Med Ultrason. 2016;18(2):157–162.
  • Kossatz S, Ludwig R, Dähring H, et al. High therapeutic efficiency of magnetic hyperthermia in xenograft models achieved with moderate temperature dosages in the tumor area. Pharm Res. 2014;31(12):3274–3288.
  • Maier-Hauff K, Rothe R, Scholz R, et al. Intracranial thermotherapy using magnetic nanoparticles combined with external beam radiotherapy: results of a feasibility study on patients with glioblastoma multiforme. J Neurooncol. 2007;81(1):53–60.
  • van Landeghem FK, Maier-Hauff K, Jordan A, et al. Post-mortem studies in glioblastoma patients treated with thermotherapy using magnetic nanoparticles. Biomaterials. 2009;30(1):52–57.
  • Johannsen M, Thiesen B, Wust P, et al. Magnetic nanoparticle hyperthermia for prostate cancer. Int J Hyperthermia. 2010;26(8):790–795.
  • Johannsen M, Gneveckow U, Taymoorian K, et al. Morbidity and quality of life during thermotherapy using magnetic nanoparticles in locally recurrent prostate cancer: results of a prospective phase I trial. Int J Hyperthermia. 2007;23(3):315–323.
  • Johannsen M, Gneveckow U, Thiesen B, et al. Thermotherapy of prostate cancer using magnetic nanoparticles: feasibility, imaging, and three-dimensional temperature distribution. Eur Urol. 2007;52(6):1653–1662.
  • Kandala SK, Liapi E, Whitcomb LL, et al. Temperature-controlled power modulation compensates for heterogeneous nanoparticle distributions: a computational optimization analysis for magnetic hyperthermia. Int J Hyperthermia. 2019;36(1):115–129.
  • Attaluri A, Kandala SK, Wabler M, et al. Magnetic nanoparticle hyperthermia enhances radiation therapy: a study in mouse models of human prostate cancer. Int J Hyperthermia. 2015;31(4):359–374.
  • Atkinson WJ, Brezovich IA, Chakraborty DP. Usable frequencies in hyperthermia with thermal seeds. IEEE Trans Biomed Eng. 1984;31(1):70–75.
  • Stigliano RV, Shubitidze F, Petryk JD, et al. Mitigation of eddy current heating during magnetic nanoparticle hyperthermia therapy. Int J Hyperthermia. 2016;32(7):735–748.
  • Kumar A, Attaluri A, Mallipudi R, et al. Method to reduce non-specific tissue heating of small animals in solenoid coils. Int J Hyperthermia. 2013;29(2):106–120.
  • Attaluri A, Jackowski J, Sharma A, et al. Design and construction of a Maxwell-type induction coil for magnetic nanoparticle hyperthermia. Int J Hyperthermia. 2020;37(1):1–4.
  • Ivkov R, DeNardo SJ, Daum W, et al. Application of high amplitude alternating magnetic fields for heat induction of nanoparticles localized in cancer. Clin Cancer Res. 2005;11(19):7093s–7103s.
  • Dennis CL, Krycka KL, Borchers JA, et al. Internal magnetic structure of nanoparticles dominates time‐dependent relaxation processes in a magnetic field. Adv Funct Mater. 2015;25(27):4300–4311.
  • Soetaert F, Kandala SK, Bakuzis A, et al. Experimental estimation and analysis of variance of the measured loss power of magnetic nanoparticles. Sci Rep. 2017;7(1):1–5.
  • Hedayati M, Attaluri A, Bordelon D, et al. New iron-oxide particles for magnetic nanoparticle hyperthermia: an in-vitro and in-vivo pilot study. Energy-Based Treat Tissue Assess. 2013;8584:858404.
  • Attaluri A, Nusbaum C, Wabler M, et al. Calibration of a quasi-adiabatic magneto-thermal calorimeter used to characterize magnetic nanoparticle heating. J Nanotechnol Eng Med. 2013;4(1):1–8.
  • Woodard LE, Dennis CL, Borchers JA, et al. Nanoparticle architecture preserves magnetic properties during coating to enable robust multi-modal functionality. Sci Rep. 2018;8(1):1–3.
  • Hasgall PA, Gennaro F, Baumgartner C, et al. IT’IS Database for thermal and electromagnetic parameters of biological tissues. Version 4.0 [Internet]. Zurich (Switzerland): IT’IS Foundation; 2018 [cited 2018 May 15]. Available from: https://itis.swiss/virtual-population/tissue-properties/downloads/database-v4-0/
  • Soetaert F, Dupré L, Ivkov R, et al. Computational evaluation of amplitude modulation for enhanced magnetic nanoparticle hyperthermia. Biomed Tech. 2015;60(5):491–504.
  • Ivkov R. Johns Hopkins University, assignee. Process for making iron oxide nanoparticle preparations for cancer hyperthermia. US Patent 10,406,228. 2019 July 25.
  • Pennes HH. Analysis of tissue and arterial blood temperatures in the resting human forearm. J Appl Physiol. 1948;1(2):93–122.
  • Brown JM, Giaccia AJ. The unique physiology of solid tumors: opportunities (and problems) for cancer therapy. Cancer Res. 1998;58(7):1408–1416.
  • Yamada K, Oda T, Hashimoto S, et al. Minimally required heat doses for various tumour sizes in induction heating cancer therapy determined by computer simulation using experimental data. Int J Hyperthermia. 2010;26(5):465–474.
  • Rabin Y. Is intracellular hyperthermia superior to extracellular hyperthermia in the thermal sense? Int J Hyperthermia. 2002;18(3):194–202.
  • Hedayati M, Thomas O, Abubaker-Sharif B, et al. The effect of cell cluster size on intracellular nanoparticle-mediated hyperthermia: is it possible to treat microscopic tumors? Nanomedicine. 2013;8(1):29–41.
  • Tay ZW, Chandrasekharan P, Chiu-Lam A, et al. Magnetic Particle Imaging-Guided Heating in Vivo Using Gradient Fields for Arbitrary Localization of Magnetic Hyperthermia Therapy. ACS Nano. 2018;12(4):3699–3713.