Characterizing Thermal Augmentation of Convection-Enhanced Drug Delivery with the Fiberoptic Microneedle Device

R. Lyle Hood; Rudy T. Andriani; Tobias E. Ecker; John L. Robertson; Christopher G. Rylander

doi:10.15302/J-ENG-2015077

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Engineering ›› 2015, Vol. 1 ›› Issue (3) : 344-350. DOI: 10.15302/J-ENG-2015077

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Characterizing Thermal Augmentation of Convection-Enhanced Drug Delivery with the Fiberoptic Microneedle Device

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Abstract

Convection-enhanced delivery (CED) is a promising technique leveraging pressure-driven flow to increase penetration of infused drugs into interstitial spaces. We have developed a fiberoptic microneedle device for inducing local sub-lethal hyperthermia to further improve CED drug distribution volumes, and this study seeks to quantitatively characterize this approach in agarose tissue phantoms. Infusions of dye were conducted in 0.6% (w/w) agarose tissue phantoms with isothermal conditions at 15 °C, 20 °C, 25 °C, and 30 °C. Infusion metrics were quantified using a custom shadowgraphy setup and image-processing algorithm. These data were used to build an empirical predictive temporal model of distribution volume as a function of phantom temperature. A second set of proof-of-concept experiments was conducted to evaluate a novel fiberoptic device capable of generating local photothermal heating during fluid infusion. The isothermal infusions showed a positive correlation between temperature and distribution volume, with the volume at 30 °C showing a 7-fold increase at 100 min over the 15 °C isothermal case. Infusions during photothermal heating (1064 nm at 500 mW) showed a similar effect with a 3.5-fold increase at 4 h over the control (0 mW). These results and analyses serve to provide insight into and characterization of heat-mediated enhancement of volumetric dispersal.

Keywords

near-infrared laser / thermochemotherapy / agarose / photothermal heating / micro-catheter / malignant glioma

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R. Lyle Hood, Rudy T. Andriani, Tobias E. Ecker, John L. Robertson, Christopher G. Rylander. Characterizing Thermal Augmentation of Convection-Enhanced Drug Delivery with the Fiberoptic Microneedle Device. Engineering, 2015, 1(3): 344‒350 https://doi.org/10.15302/J-ENG-2015077

References

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[1]	C. V. Pardeshi, V. S. Belgamwar. Direct nose to brain drug delivery via integrated nerve pathways bypassing the blood-brain barrier: An excellent platform for brain targeting. Expert Opin. Drug Deliv., 2013, 10(7): 957–972

[2]	B. S. Bleier, R. E. Kohman, R. E. Feldman, S. Ramanlal, X. Han. Permeabilization of the blood-brain barrier via mucosal engrafting: Implications for drug delivery to the brain. PLoS One, 2013, 8(4): e61694

[3]	M. Aryal, C. D. Arvanitis, P. M. Alexander, N. McDannold. Ultrasound-mediated blood-brain barrier disruption for targeted drug delivery in the central nervous system. Adv. Drug Deliv. Rev., 2014, 72: 94–109

[4]	F. Dilnawaz, A. Singh, S. Mewar, U. Sharma, N. R. Jagannathan, S. K. Sahoo. The transport of non-surfactant based paclitaxel loaded magnetic nanoparticles across the blood brain barrier in a rat model. Biomaterials, 2012, 33(10): 2936–2951

[5]	P. A. Garcia, 7.0-T magnetic resonance imaging characterization of acute blood-brain-barrier disruption achieved with intracranial irreversible electroporation. PLoS One, 2012, 7(11): e50482

[6]	D. W. Laske, R. J. Youle, E. H. Oldfield. Tumor regression with regional distribution of the targeted toxin TF-CRM107 in patients with malignant brain tumors. Nat. Med., 1997, 3(12): 1362–1368

[7]	R. H. Bobo, D. W. Laske, A. Akbasak, P. F. Morrison, R. L. Dedrick, E. H. Oldfield. Convection-enhanced delivery of macromolecules in the brain. Proc. Natl. Acad. Sci. U.S.A., 1994, 91(6): 2076–2080

[8]	K. S. Bankiewicz, Convection-enhanced delivery of AAV vector in parkinsonian monkeys; in vivo detection of gene expression and restoration of dopaminergic function using pro-drug approach. Exp. Neurol., 2000, 164(1): 2–14

[9]	L. C. Vazquez, Polymer-coated cannulas for the reduction of backflow during intraparenchymal infusions. J. Mater. Sci. Mater. Med., 2012, 23(8): 2037–2046

[10]	S. S. Gill, Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease. Nat. Med., 2003, 9(5): 589–595

[11]	M. A. Rogawski. Convection-enhanced delivery in the treatment of epilepsy. Neurotherapeutics, 2009, 6(2): 344–351

[12]	J. H. Sampson, Intracerebral infusate distribution by convection-enhanced delivery in humans with malignant gliomas: Descriptive effects of target anatomy and catheter positioning. Neurosurgery, 2007, 60(2 Suppl 1): ONS89-98; discussion ONS98-9

[13]	J. F. Hamilton, Heparin coinfusion during convection-enhanced delivery (CED) increases the distribution of the glial-derived neurotrophic factor (GDNF) ligand family in rat striatum and enhances the pharmacological activity of neurturin. Exp. Neurol., 2001, 168(1): 155–161

[14]	A. A. Kanner. Convection-enhanced delivery.In: G. H. Barnett, ed. High-Grade Gliomas: Diagnosis and Treatment. Totowa, NJ: Humana Press, 2007: 303–314

[15]	W. A. Vandergrift, S. J. Patel, J. S. Nicholas, A. K. Varma. Convection-enhanced delivery of immunotoxins and radioisotopes for treatment of malignant gliomas. Neurosurg. Focus, 2006, 20(4): E13

[16]	M. Bettag, Stereotactic laser therapy in cerebral gliomas. Acta Neurochir. Suppl. (Wien), 1991, 52: 81–83

[17]	A. Carpentier, MR-guided laser-induced thermal therapy (LITT) for recurrent glioblastomas. Lasers Surg. Med., 2012, 44(5): 361–368

[18]	H. J. Schwarzmaier, I. V. Yaroslavsky, A. N. Yaroslavsky, V. Fiedler, F. Ulrich, T. Kahn. Treatment planning for MRI-guided laser-induced interstitial thermotherapy of brain tumors—The role of blood perfusion. J. Magn. Reson. Imaging, 1998, 8(1): 121–127

[19]	A. Carpentier, Real-time magnetic resonance-guided laser thermal therapy for focal metastatic brain tumors. Neurosurgery, 2008, 63(1 Suppl 1): ONS21-8; discussion ONS28-9

[20]	R. J. Stafford, D. Fuentes, A. A. Elliott, J. S. Weinberg, K. Ahrar. Laser-induced thermal therapy for tumor ablation. Crit. Rev. Biomed. Eng., 2010, 38(1): 79–100

[21]	C. G. Hadjipanayis, EGFRvIII antibody-conjugated iron oxide nanoparticles for magnetic resonance imaging-guided convection-enhanced delivery and targeted therapy of glioblastoma. Cancer Res., 2010, 70(15): 6303–6312

[22]	J. H. Sampson, , and PRECISE Trial Investigators. Poor drug distribution as a possible explanation for the results of the PRECISE trial. J. Neurosurg., 2010, 113(2): 301–309

[23]	R. Hamazoe, M. Maeta, N. Kaibara. Intraperitoneal thermochemotherapy for prevention of peritoneal recurrence of gastric cancer. Final results of a randomized controlled study. Cancer, 1994, 73(8): 2048–2052

[24]	Y. Liu, Ultrasound-induced hyperthermia increases cellular uptake and cytotoxicity of P-glycoprotein substrates in multi-drug resistant cells. Pharm. Res., 2001, 18(9): 1255–1261

[25]	A. H. Saad, G. M. Hahn. Ultrasound-enhanced effects of adriamycin against murine tumors. Ultrasound Med. Biol., 1992, 18(8): 715–723

[26]	J. B. Block, P. A. Harris, A. Peale. Preliminary observations on temperature-enhanced drug uptake by leukemic leukocytes in vitro. Cancer Chemother. Rep., 1975, 59(5): 985–988

[27]	M. R. DeWitt, A. M. Pekkanen, J. Robertson, C. G. Rylander, M. Nichole Rylander. Influence of hyperthermia on efficacy and uptake of carbon nanohorn-cisplatin conjugates. J. Biomech. Eng., 2014, 136(2): 021003

[28]	R. L. Hood, R. T. Andriani Jr., S. Emch, J. L. Robertson, C. G. Rylander, J. H. Rossmeisl Jr. Fiberoptic microneedle device facilitates volumetric infusate dispersion during convection-enhanced delivery in the brain. Lasers Surg. Med., 2013, 45(7): 418–426

[29]	M. A. Kosoglu, R. L. Hood, Y. Chen, Y. Xu, M. N. Rylander, C. G. Rylander. Fiber optic microneedles for transdermal light delivery: Ex vivo porcine skin penetration experiments. J. Biomech. Eng., 2010, 132(9): 091014

[30]	M. A. Kosoglu, Fiberoptic microneedles for microscale interstitial delivery of therapeutic light. Laser. Surg. Med., 2011, 43(9): 914–920

[31]	R. L. Hood, M. A. Kosoglu, M. Parker, C. G. Rylander. Effects of microneedle design parameters on hydraulic resistance. J. Med. Device., 2011, 5(3): 31012–31016

[32]	Z. J. Chen, A realistic brain tissue phantom for intraparenchymal infusion studies. J. Neurosurg., 2004, 101(2): 314–322

[33]	T. Gill, In vitro and in vivo testing of a novel recessed-step catheter for reflux-free convection-enhanced drug delivery to the brain. J. Neurosci. Methods, 2013, 219(1): 1–9

[34]

R. L. Hood, T. Ecker, R. Andriani, J. Robertson, J. Rossmeisl, C. G. Rylander. Augmenting convection-enhanced delivery through simultaneous co-delivery of fluids and laser energy with a fiberoptic microneedle device. In: I. Gannot, ed. Proceedings of SPIE 8576: Optical Fibers and Sensors for Medical Diagnostics and Treatment Applications XIII. San Francisco, CA, USA, 2013

[35]	F. Casanova, P. R. Carney, M. Sarntinoranont. Influence of needle insertion speed on backflow for convection-enhanced delivery. J. Biomech. Eng., 2012, 134(4): 041006

[36]	W. Martanto, J. S. Moore, T. Couse, M. R. Prousnitz. Mechanism of fluid infusion during microneedle insertion and retraction. J. Contrd. Release, 2006, 112(37): 357–361

[37]	Z. J. Chen, W. C. Broaddus, R. R. Viswanathan, R. Raghavan, G. T. Gillies. Intraparenchymal drug delivery via positive-pressure infusion: Experimental and modeling studies of poroelasticity in brain phantom gels. IEEE Trans. Biomed. Eng., 2002, 49(2): 85–96

[38]	Z. J. Chen, W. C. Broaddus, R. R. Viswanathan, R. Raghavan, G. T. Gillies. Intraparenchymal drug delivery via positive-pressure infusion: Experimental and modeling studies of poroelasticity in brain phantom gels. IEEE Trans. Biomed. Eng., 2002, 49(2): 85–96

[39]	G. T. Gillies, J. H. Smith, J. A. Humphrey, W. C. Broaddus. Positive pressure infusion of therapeutic agents into brain tissues: Mathematical and experimental simulations. Technol. Health Care, 2005, 13(4): 235–243

[40]	S. J. Panse, H. L. Fillmore, Z. J. Chen, G. T. Gillies, W. C. Broaddus. A novel coaxial tube catheter for central nervous system infusions: Performance characteristics in brain phantom gel. J. Med. Eng. Technol., 2010, 34(7−8): 408–414

Acknowledgements

The authors would like to acknowledge the Coulter Foundation and NIH (NIH/NCI 1R21CA156078) for their funding of this project. Fiberoptic microneedle device fabrication methods and applications are described in US patent application 13/203800 and PCT/US2012/026968, which are managed by the Virginia Tech Intellectual Properties Group.

Compliance with ethics guidelines

R. Lyle Hood, Rudy T. Andriani, Tobias E. Ecker, John L. Robertson, and Christopher G. Rylander declare that they have no conflict of interest or financial conflicts to disclose.

Funding