Advertisement

Annals of Biomedical Engineering

, Volume 47, Issue 12, pp 2402–2415 | Cite as

Magnetic Resonance Navigation for Targeted Embolization in a Two-Level Bifurcation Phantom

  • Ning Li
  • Yuting Jiang
  • Rosalie Plantefève
  • Francois Michaud
  • Zeynab Nosrati
  • Charles Tremblay
  • Katayoun Saatchi
  • Urs O. Häfeli
  • Samuel Kadoury
  • Gerald Moran
  • Florian Joly
  • Sylvain Martel
  • Gilles SoulezEmail author
Article
First Online:

Abstract

This work combines a particle injection system with our proposed magnetic resonance navigation (MRN) sequence with the intention of validating MRN in a two-bifurcation phantom for endovascular treatment of hepatocellular carcinoma (HCC). A theoretical physical model used to calculate the most appropriate size of the magnetic drug-eluting bead (MDEB, 200 μm) aggregates was proposed. The aggregates were injected into the phantom by a dedicated particle injector while a trigger signal was automatically sent to the MRI to start MRN which consists of interleaved tracking and steering sequences. When the main branch of the phantom was parallel to B0, the aggregate distribution ratio in the (left–left, left–right, right–left and right–right divisions was obtained with results of 8, 68, 24 and 0% respectively at baseline (no MRN) and increased to 84%, 100, 84 and 92% (p < 0.001, p = 0.004, p < 0.001, p < 0.001) after implementing our MRN protocol. When the main branch was perpendicular to B0, the right-left branch, having the smallest baseline distribution rate of 0%, reached 80% (p < 0.001) after applying MRN. Moreover, the success rate of MRN was always more than 92% at the 1st bifurcation in the experiments above.

Keywords

Magnetic resonance navigation Two-bifurcations navigation Hepatocellular carcinoma Embolization 

Abbreviations

DEB

Drug-eluting bead

HCC

Hepatocellular carcinoma

MRI

Magnetic resonance imaging

MRN

Magnetic resonance navigation

MDEB

Magnetic drug-eluting bead

TACE

Trans-catheter arterial chemoembolization

This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

This work was supported by a grant from the Natural Sciences and Engineering Research Council of Canada (NSERC), Operating Grant—CHRP (CIHR Partnered) (CHRP 478474-15) and Canadian Institutes of Health Research (CIHR), Operating Grant—CHRP (NSERC Partnered) (CPG-140179).

References

  1. 1.
    Altekruse, S. F., K. A. McGlynn, and M. E. Reichman. Hepatocellular carcinoma incidence, mortality, and survival trends in the united states from 1975 to 2005. J. Clin. Oncol. 27:1485–1491, 2009.PubMedPubMedCentralGoogle Scholar
  2. 2.
    Belghiti, J., and R. Kianmanesh. Surgical treatment of hepatocellular carcinoma. Hpb 7:42–49, 2005.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Bigot, A., G. Soulez, and S. Martel. A prototype of injector to control and to detect the release of magnetic beads within the constraints of multibifurcation magnetic resonance navigation procedures. Magn. Reson. Med. 77:444–452, 2017.PubMedGoogle Scholar
  4. 4.
    Bigot, A., C. Tremblay, G. Soulez, and S. Martel. Magnetic resonance navigation of a bead inside a three-bifurcation PMMA phantom using an imaging gradient coil insert. IEEE Trans. Robot 30:719–727, 2014.Google Scholar
  5. 5.
    Buisman, F., M. Homs, D. Grünhagen, W. Filipe, R. Bennink, M. Besselink, I. B. Rinkes, R. Bruijnen, A. Cercek, and M. D’Angelica. Adjuvant hepatic arterial infusion pump chemotherapy and resection versus resection alone in patients with low-risk resectable colorectal liver metastases—the multicenter randomized controlled PUMP trial. BMC Cancer 19:327, 2019.PubMedPubMedCentralGoogle Scholar
  6. 6.
    Chaubey, G. S., C. Barcena, N. Poudyal, C. B. Rong, J. M. Gao, S. H. Sun, and J. P. Liu. Synthesis and stabilization of FeCo nanoparticles. J. Am. Chem. Soc. 129:7214–7215, 2007.PubMedGoogle Scholar
  7. 7.
    da Silveira, L. A., F. B. C. Silveira, and V. P. S. Fazan. Arterial diameter of the celiac trunk and its branches. Anatomical study. Acta Cir. Bras. 24:43–47, 2009.PubMedGoogle Scholar
  8. 8.
    Datta, J., R. R. Narayan, N. E. Kemeny, and M. I. D’Angelica. Role of hepatic artery infusion chemotherapy in treatment of initially unresectable colorectal liver metastases: a reviewhepatic artery infusion chemotherapy for initially unresectable colorectal liver metastaseshepatic artery infusion chemotherapy for initially unresectable colorectal liver metastases. JAMA Surg. 2019.  https://doi.org/10.1001/jamasurg.2019.1694.CrossRefPubMedGoogle Scholar
  9. 9.
    De Baere, T., and P. Mariani. Surgical or percutaneous hepatic artery cannulation for chemotherapy. J. Visc. Surg. 151(Suppl 1):S17–20, 2014.PubMedGoogle Scholar
  10. 10.
    Deipolyi, A. R., R. Oklu, S. Al-Ansari, A. X. Zhu, L. Goyal, and S. Ganguli. Safety and efficacy of 70–150 mum and 100–300 mum drug-eluting bead transarterial chemoembolization for hepatocellular carcinoma. J. Vasc. Interv. Radiol. 26:516–522, 2015.PubMedGoogle Scholar
  11. 11.
    Dhanasekaran, R., D. A. Kooby, C. A. Staley, J. S. Kauh, V. Khanna, and H. S. Kim. Comparison of conventional transarterial chemoembolization (TACE) and chemoembolization with doxorubicin drug eluting beads (DEB) for unresectable hepatocelluar carcinoma (HCC). J. Surg. Oncol. 101:476–480, 2010.PubMedGoogle Scholar
  12. 12.
    Felfoul, O., A. T. Becker, G. Fagogenis, and P. E. Dupont. Simultaneous steering and imaging of magnetic particles using MRI toward delivery of therapeutics. Sci. Rep. UK 6:33567, 2016.Google Scholar
  13. 13.
    Folio, D., and A. Ferreira. Two-dimensional robust magnetic resonance navigation of a ferromagnetic microrobot using Pareto optimality. IEEE Trans. Robot 33:583–593, 2017.Google Scholar
  14. 14.
    Gaba, R. C., R. J. Lewandowski, R. Hickey, M. O. Baerlocher, E. I. Cohen, S. R. Dariushnia, B. J. d’Othee, S. A. Padia, R. Salem, D. S. Wang, B. Nikolic, D. B. Brown, and Society of Interventional Radiology Technology Assessment. Transcatheter therapy for hepatic malignancy: standardization of terminology and reporting criteria. J. Vasc. Interv. Radiol. 27:457–473, 2016.PubMedGoogle Scholar
  15. 15.
    Gaba, R. C., R. P. Lokken, R. M. Hickey, A. J. Lipnik, R. J. Lewandowski, R. Salem, D. B. Brown, T. G. Walker, J. E. Silberzweig, M. O. Baerlocher, A. M. Echenique, M. Midia, J. W. Mitchell, S. A. Padia, S. Ganguli, T. J. Ward, J. L. Weinstein, B. Nikolic, and S. R. Dariushnia. quality improvement guidelines for transarterial chemoembolization and embolization of hepatic malignancy. J. Vasc. Interv. Radiol. 28:1210–1223.e1213, 2017.PubMedGoogle Scholar
  16. 16.
    Hama, N., Y. Totoki, F. Miura, K. Tatsuno, M. Saito-Adachi, H. Nakamura, Y. Arai, F. Hosoda, T. Urushidate, and S. Ohashi. Epigenetic landscape influences the liver cancer genome architecture. Nat. Commun. 9:1643, 2018.PubMedPubMedCentralGoogle Scholar
  17. 17.
    Herber, S., J. Schneider, B. Brecher, T. Höhler, M. Thelen, G. Otto, and M. Pitton. TACE: therapy of the HCC before liver transplantation—experiences. RoFo: Fortschr. auf dem Gebiete der Rontgenstrahlen und der Nuklearmed. 177:681–690, 2005.Google Scholar
  18. 18.
    Lee, K. H., E. Liapi, J. A. Vossen, M. Buijs, V. P. Ventura, C. Georgiades, K. Hong, I. Kamel, M. S. Torbenson, and J. F. Geschwind. Distribution of iron oxide-containing Embosphere particles after transcatheter arterial embolization in an animal model of liver cancer: evaluation with MR imaging and implication for therapy. J. Vasc. Interv. Radiol. 19:1490–1496, 2008.PubMedPubMedCentralGoogle Scholar
  19. 19.
    Lewandowski, R. J., J. F. Geschwind, E. Liapi, and R. Salem. Transcatheter intraarterial therapies: rationale and overview. Radiology 259:641–657, 2011.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Li, N., F. Michaud, Z. Nosrati, D. Loghin, C. Tremblay, R. Plantefève, K. Saatchi, U. O. Häfeli, S. Martel and G. Soulez. MRI-compatible injection system for magnetic microparticle embolization. IEEE Transactions on Biomedical Engineering, 2018.Google Scholar
  21. 21.
    Li, N., C. Tremblay and S. Martel. Combining oscillating flow and clinical MRI gradients for targeted therapy. In: 2017 International Conference on Manipulation, Automation and Robotics at Small Scales (MARSS). IEEE, 2017, pp. 1–4.Google Scholar
  22. 22.
    Lyu, N., Y. Kong, T. Pan, L. Mu, S. Li, Y. Liu, H. Deng, J. Li, M. Shi, and L. Xu. Hepatic arterial infusion of oxaliplatin, fluorouracil, and leucovorin in hepatocellular cancer with extrahepatic spread. J. Vasc. Interv. Radiol. 30:349–357, 2019.PubMedGoogle Scholar
  23. 23.
    Ma, S. Biology and clinical implications of CD133 + liver cancer stem cells. Exp. Cell Res. 319:126–132, 2013.PubMedGoogle Scholar
  24. 24.
    Martel, S. Microrobotics in the vascular network: present status and next challenges. J. Micro-Bio Robot. 8:41–52, 2013.Google Scholar
  25. 25.
    Mathieu, J. B., and S. Martel. Aggregation of magnetic microparticles in the context of targeted therapies actuated by a magnetic resonance imaging system. J. Appl. Phys. 106:044904, 2009.Google Scholar
  26. 26.
    Mellal, L., K. Belharet, D. Folio, and A. Ferreira. Optimal structure of particles-based superparamagnetic microrobots: application to MRI guided targeted drug therapy. J. Nanopart. Res. 17:64, 2015.Google Scholar
  27. 27.
    Michaud, F., N. Li, R. Plantefeve, Z. Nosrati, C. Tremblay, K. Saatchi, G. Moran, A. Bigot, U. O. Hafeli, S. Kadoury, A. Tang, P. Perreault, S. Martel, and G. Soulez. Selective embolization with magnetized microbeads using magnetic resonance navigation in a controlled-flow liver model. Med. Phys. 46:789–799, 2019.PubMedGoogle Scholar
  28. 28.
    Moran, A., L. F. Ramos, O. Picado, F. Pendola, D. Sleeman, V. Dudeja, N. Merchant, and D. Yakoub. Hepatocellular carcinoma: resection with adjuvant hepatic artery infusion therapy vs resection alone. A systematic review and meta-analysis. J. Surg. Oncol. 119:455–463, 2019.PubMedGoogle Scholar
  29. 29.
    Ni, J.-Y., S.-S. Liu, H.-L. Sun, W.-D. Wang, Z.-L. Zhong, S.-N. Hou, Y.-T. Chen, and L.-F. Xu. Transcatheter hepatic arterial infusion chemotherapy vs sorafenib in the treatment of patients with hepatocellular carcinoma of Barcelona clinic liver cancer stage c: a meta-analysis of asian population. OncoTargets Therapy 11:7883, 2018.PubMedGoogle Scholar
  30. 30.
    Nosrati, Z., N. Li, F. Michaud, S. Ranamukhaarachchi, S. Karagiozov, G. Soulez, S. Martel, K. Saatchi, and U. O. Hafeli. Development of a Coflowing device for the size-controlled preparation of magnetic-polymeric microspheres as embolization agents in magnetic resonance navigation technology. Acs Biomater. Sci. Eng. 4:1092–1102, 2018.Google Scholar
  31. 31.
    Odisio, B. C., A. Ashton, Y. Yan, W. Wei, A. Kaseb, M. J. Wallace, J. N. Vauthey, S. Gupta, and A. L. Tam. Transarterial hepatic chemoembolization with 70–150 microm drug-eluting beads: assessment of clinical safety and liver toxicity profile. J. Vasc. Interv. Radiol. 26:965–971, 2015.PubMedPubMedCentralGoogle Scholar
  32. 32.
    Olamaei, N., F. Cheriet, S. Deschenes, and S. Martel. Dynamic tracking of magnetic nanoparticles for mapping microvascular networks using a clinical 1.5 T magnetic resonance scanner. Appl. Phys. Lett. 104:213703, 2014.Google Scholar
  33. 33.
    Pernot, S., G. Velut, R. H. Kourie, G. Amouyal, M. Sapoval, A. L. Pointet, B. Landi, Y. Zaimi, C. Lepere, and O. Pellerin. 5-FU or mitomycin C hepatic arterial infusion after failure of arterial oxaliplatin in patients with colorectal cancer unresectable liver metastases. Clin. Res. Hepatol. Gastroenterol. 42:255–260, 2018.PubMedGoogle Scholar
  34. 34.
    Pouponneau, P., J. C. Leroux, and S. Martel. Magnetic nanoparticles encapsulated into biodegradable microparticles steered with an upgraded magnetic resonance imaging system for tumor chemoembolization. Biomaterials 30:6327–6332, 2009.PubMedGoogle Scholar
  35. 35.
    Pouponneau, P., J. C. Leroux, G. Soulez, L. Gaboury, and S. Martel. Co-encapsulation of magnetic nanoparticles and doxorubicin into biodegradable microcarriers for deep tissue targeting by vascular MRI navigation. Biomaterials 32:3481–3486, 2011.PubMedGoogle Scholar
  36. 36.
    Pouponneau, P., G. Soulez, G. Beaudoin, J.-C. Leroux, and S. Martel. MR imaging of therapeutic magnetic microcarriers guided by magnetic resonance navigation for targeted liver chemoembolization. Cardiovasc. Intervent. Radiol. 37:784–790, 2014.PubMedGoogle Scholar
  37. 37.
    Rahib, L., B. D. Smith, R. Aizenberg, A. B. Rosenzweig, J. M. Fleshman, and L. M. Matrisian. Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res. 74:2913–2921, 2014.PubMedGoogle Scholar
  38. 38.
    Roberts, L. R., C. B. Sirlin, F. Zaiem, J. Almasri, L. J. Prokop, J. K. Heimbach, M. H. Murad, and K. Mohammed. Imaging for the diagnosis of hepatocellular carcinoma: a systematic review and meta-analysis. Hepatology 67:401–421, 2018.PubMedPubMedCentralGoogle Scholar
  39. 39.
    Schenck, J. F. The role of magnetic susceptibility in magnetic resonance imaging: MRI magnetic compatibility of the first and second kinds. Med. Phys. 23:815–850, 1996.PubMedGoogle Scholar
  40. 40.
    Tajiri, K., Y. Futsukaichi, S. Kobayashi, K. Nagata, S. Yasumura, T. Takahara, M. Minemura, and I. Yasuda. Efficacy of on-demand intrahepatic arterial therapy in combination with sorafenib for advanced hepatocellular carcinoma. OncoTargets Therapy 12:2205, 2019.PubMedGoogle Scholar
  41. 41.
    Varela, M., M. I. Real, M. Burrel, A. Forner, M. Sala, M. Brunet, C. Ayuso, L. Castells, X. Montana, J. M. Llovet, and J. Bruix. Chemoembolization of hepatocellular carcinoma with drug eluting beads: efficacy and doxorubicin pharmacokinetics. J. Hepatol. 46:474–481, 2007.PubMedGoogle Scholar
  42. 42.
    Vartholomeos, P., M. Fruchard, A. Ferreira, and C. Mavroidis. MRI-guided nanorobotic systems for therapeutic and diagnostic applications. Annu. Rev. Biomed. Eng. 13:157–184, 2011.PubMedGoogle Scholar
  43. 43.
    Waller, L. P., V. Deshpande, and N. Pyrsopoulos. Hepatocellular carcinoma: a comprehensive review. World J. Hepatol. 7:2648–2663, 2015.PubMedPubMedCentralGoogle Scholar
  44. 44.
    Weinstein, J. S., C. G. Varallyay, E. Dosa, S. Gahramanov, B. Hamilton, W. D. Rooney, L. L. Muldoon, and E. A. Neuwelt. Superparamagnetic iron oxide nanoparticles: diagnostic magnetic resonance imaging and potential therapeutic applications in neurooncology and central nervous system inflammatory pathologies, a review. J. Cerebr. Blood F Met 30:15–35, 2010.Google Scholar
  45. 45.
    Yan, X., Q. Zhou, M. Vincent, Y. Deng, J. Yu, J. Xu, T. Xu, T. Tang, L. Bian, and Y.-X. J. Wang. Multifunctional biohybrid magnetite microrobots for imaging-guided therapy. Sci. Robot. 2:eaaq1155, 2017.Google Scholar
  46. 46.
    Zhuang, B.-W., W. Li, X.-H. Xie, H.-T. Hu, M.-D. Lu, and X.-Y. Xie. Sorafenib versus hepatic arterial infusion chemotherapy for advanced hepatocellular carcinoma: a systematic review and meta-analysis. Jpn. J. Clin. Oncol. 2019.  https://doi.org/10.1093/jjco/hyz06.CrossRefPubMedGoogle Scholar

Copyright information

© Biomedical Engineering Society 2019

Authors and Affiliations

  • Ning Li
    • 1
    • 2
  • Yuting Jiang
    • 2
    • 3
  • Rosalie Plantefève
    • 2
  • Francois Michaud
    • 2
    • 3
  • Zeynab Nosrati
    • 4
  • Charles Tremblay
    • 1
  • Katayoun Saatchi
    • 4
  • Urs O. Häfeli
    • 4
  • Samuel Kadoury
    • 1
    • 2
  • Gerald Moran
    • 5
  • Florian Joly
    • 6
  • Sylvain Martel
    • 1
  • Gilles Soulez
    • 2
    • 3
    Email author
  1. 1.Polytechnique Montréal, Chemin de PolytechniqueMontréalCanada
  2. 2.Laboratory of Clinical Image ProcessingLe Centre de recherche du CHUM (CRCHUM)MontréalCanada
  3. 3.Department of Radiology, Radiation-Oncology and Nuclear Medicine and Institute of Biomedical Engineering, Université de MontréalMontréalCanada
  4. 4.University of British ColumbiaVancouverCanada
  5. 5.Siemens CanadaOakvilleCanada
  6. 6.INRIA ParisParisFrance

Personalised recommendations

Cite article

Buy options