Research Article
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Effect of Temperature on Stability of Lipid Microbubbles

Year 2019, Volume: 6 Issue: 3, 439 - 450, 20.10.2019
https://doi.org/10.18596/jotcsa.594219

Abstract

The effect of temperature on
stability of lipid microbubble shell containing polyethyleneoxide-40-stearate
(PEG40St) as emulsifier was investigated. Microbubbles at 4 °C were
subjected to different temperatures up to 48
ºC
(down-to-up) and it was found that both the number and the size of microbubbles
remained unchanged in the population up to a certain time, so called “onset
time”. The onset time was about 6 hrs at 10 °C, 2 hrs at 20 °C and shorter at
elevated temperatures, exhibiting an exponential decrease with increasing
temperature. Once the onset time was reached, the number of microbubbles
started to decrease and the average size of the population started to increase.
Observation of single microbubbles on a constant temperature heating stage exhibited
that each microbubble had its own onset time, with the smaller microbubbles
vanishing earlier than the larger ones. The Langmuir monolayer studies showed
that hydration degree of the emulsifier PEG chains decreased with temperature, causing
them go through conformational changes and subsequently destabilization of the
shell. By subjecting the freshly produced microbubbles directly to the desired
temperatures in up-to-down fashion, more stable microbubbles were able to be
produced, with their onset time increased 40% at 10 °C to 500% at 38 °C.
Overall, the results suggest that the new strategies need to be developed to
control the collapse process in the microbubble shell resulting from the
conformational changes in the PEG chains of the emulsifier for the design of
more stable microbubbles.

Supporting Institution

Tubitak

Project Number

109M494

Thanks

The author would like to thank The Scientific and Technological Research Council of Turkey (TUBITAK) for the financial support through the project number of 109M494.

References

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  • 2. Lentacker I, Geers B, Demeester J, De Smedt SC, Sanders NN. Design and Evaluation of Doxorubicin-containing Microbubbles for Ultrasound-triggered Doxorubicin Delivery: Cytotoxicity and Mechanisms Involved. Molecular Therapy. 2010;18(1):101-8.
  • 3. Borden MA, Longo ML. The dependence of lipid-coated microbubble dissolution behavior on acyl chain length. Biophys J. 2002;82(1):35a-a.
  • 4. Garg S, Thomas AA, Borden MA. The effect of lipid monolayer in-plane rigidity on in vivo microbubble circulation persistence. Biomaterials. 2013;34(28):6862-70.
  • 5. Kwan JJ, Borden MA. Lipid monolayer dilatational mechanics during microbubble gas exchange. Soft Matter. 2012;8(17):4756-66.
  • 6. Pu G, Borden MA, Longo ML. Collapse and shedding transitions in binary lipid monolayers coating microbubbles. Langmuir. 2006;22(7):2993-9.
  • 7. Kabalnov A, Klein D, Pelura T, Schutt E, Weers J. Dissolution of multicomponent microbubbles in the bloodstream: 1. Theory. Ultrasound Med Biol. 1998;24(5):739-49.
  • 8. Borden MA, Longo ML. Oxygen permeability of fully condensed lipid monolayers. J Phys Chem B. 2004;108(19):6009-16.
  • 9. Kwan JJ, Borden MA. Lipid monolayer collapse and microbubble stability. Advances in Colloid and Interface Science. 2012;183:82-99.
  • 10. Shen Y, Powell RL, Longo ML. Interfacial and stability study of microbubbles coated with a mono stearin/monopalmitin-rich food emulsifier and PEG40 stearate. Journal of Colloid and Interface Science. 2008;321(1):186-94.
  • 11. Shen YY, Powell RL, Longo ML. Influence of the dissolution rate on the collapse and shedding behavior of monostearin/monopalmitin-rich coated microbubbles. Langmuir. 2008;24(18):10035-40.
  • 12. Kwan JJ, Borden MA. Microbubble Dissolution in a Multigas Environment. Langmuir. 2010;26(9):6542-8.
  • 13. Borden MA, Pu G, Runner GJ, Longo ML. Surface phase behavior and microstructure of lipid/PEG-emulsifier monolayer-coated microbubbles. Colloid Surface B. 2004;35(3-4):209-23.
  • 14. Pu G, Longo ML, Borden MA. Effect of microstructure on molecular oxygen permeation through condensed phospholipid monolayers. Journal of the American Chemical Society. 2005;127(18):6524-5.
  • 15. Petrache HI, Dodd SW, Brown MF. Area per lipid and acyl length distributions in fluid phosphatidylcholines determined by H-2 NMR spectroscopy. Biophys J. 2000;79(6):3172-92.
  • 16. Kucerka N, Nieh MP, Katsaras J. Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature. Biochimica Et Biophysica Acta-Biomembranes. 2011;1808(11):2761-71.
  • 17. Mulvana H, Stride E, Hajnal JV, Eckersley RJ. Temperature Dependent Behavior of Ultrasound Contrast Agents. Ultrasound Med Biol. 2010;36(6):925-34.
  • 18. Mulvana H, Stride E, Tang MX, Hajnal JV, Eckersley R. Temperature-Dependent Differences in the Nonlinear Acoustic Behavior of Ultrasound Contrast Agents Revealed by High-Speed Imaging and Bulk Acoustics. Ultrasound Med Biol. 2011;37(9):1509-17.
  • 19. Swanson EJ, Mohan V, Kheir J, Borden MA. Phospholipid-Stabilized Microbubble Foam for Injectable Oxygen Delivery. Langmuir. 2010;26(20):15726-9.
  • 20. Farook U, Stride E, Edirisinghe MJ. Preparation of suspensions of phospholipid-coated microbubbles by coaxial electrohydrodynamic atomization. Journal of the Royal Society Interface. 2009;6(32):271-7.
  • 21. Borden MA, Longo ML. Dissolution behavior of lipid monolayer-coated, air-filled microbubbles: Effect of lipid hydrophobic chain length. Langmuir. 2002;18(24):9225-33.
  • 22. Grant CA, McKendry JE, Evans SD. Temperature dependent stiffness and visco-elastic behaviour of lipid coated microbubbles using atomic force microscopy. Soft Matter. 2012;8(5):1321-6.
  • 23. Borden M. Nanostructural features on stable microbubbles. Soft Matter. 2009;5(4):716-20.
  • 24. Upadhyay A, Dalvi SV, Gupta G, Khanna N. Effect of PEGylation on performance of protein microbubbles and its comparison with lipid microbubbles. Mat Sci Eng C-Mater. 2017;71:425-30.
  • 25. Stride E, Edirisinghe M. Novel preparation techniques for controlling microbubble uniformity: a comparison. Medical & Biological Engineering & Computing. 2009;47(8):883-92.
  • 26. Epstein PS, Plesset MS. On the Stability of Gas Bubbles in Liquid-Gas Solutions. J Chem Phys 1950;18(11):1505-9.
  • 27. Wang WH, Moser CC, Wheatley MA. Langmuir trough study of surfactant mixtures used in the production of a new ultrasound contrast agent consisting of stabilized microbubbles. J Phys Chem-Us. 1996;100(32):13815-21.
  • 28. Abou-Saleh RH, Peyman SA, Johnson BRG, Marston G, Ingram N, Bushby R, et al. The influence of intercalating perfluorohexane into lipid shells on nano and microbubble stability. Soft Matter. 2016;12(34):7223-30.
  • 29. Xing ZW, Ke HT, Wang JR, Zhao B, Yue XL, Dai ZF, et al. Novel ultrasound contrast agent based on microbubbles generated from surfactant mixtures of Span 60 and polyoxyethylene 40 stearate. Acta Biomaterialia. 2010;6(9):3542-9.
  • 30. Chou TH, Chu IM. Thermodynamic characteristics of DSPC/DSPE-PEG(2000) mixed monolayers on the water subphase at different temperatures. Colloid Surface B. 2003;27(4):333-44.
  • 31. Bae YC, Lambert SM, Soane DS, Prausnitz JM. Cloud-Point Curves of Polymer-Solutions from Thermooptic Measurements. Macromolecules. 1991;24(15):4403-7.
  • 32. Gao X, Kucerka N, Nieh MP, Katsaras J, Zhu SP, Brash JL, et al. Chain Conformation of a New Class of PEG-Based Thermoresponsive Polymer Brushes Grafted on Silicon as Determined by Neutron Reflectometry. Langmuir. 2009;25(17):10271-8.
  • 33. Tyrode E, Johnson CM, Rutland MW, Claesson PM. Structure and hydration of poly(ethylene oxide) surfactants at the air/liquid interface. A vibrational sum frequency spectroscopy study. Journal of Physical Chemistry C. 2007;111(31):11642-52.
  • 34. Frey SL, Lee KYC. Temperature dependence of poloxamer insertion into and squeeze-out from lipid monolayers. Langmuir. 2007;23(5):2631-7.
  • 35. Jebrail M, Schmidt R, DeWolf CE, Tsoukanova V. Effect of aliphatic chain length on stability of poly(ethylene glycol)-grafted phospholipid monolayers at the air/water interface. Colloid Surface A. 2008;321(1-3):168-74.
  • 36. Angelova A, De Coninck J, Ionov R. Equilibrium surface properties of lipid mixtures of retinal, phosphatidylcholine and fatty acid derivatives at the air/water interface. Supramol Sci. 1997;4(3-4):207-14.
  • 37. Gopal A, Lee KYC. Morphology and collapse transitions in binary phospholipid monolayers. J Phys Chem B. 2001;105(42):10348-54.
  • 38. Lipp MM, Lee KYC, Takamoto DY, Zasadzinski JA, Waring AJ. Coexistence of buckled and flat monolayers. Physical Review Letters. 1998;81(8):1650-3.
  • 39. Hristova K, Kenworthy A, Mcintosh TJ. Effect of Bilayer Composition on the Phase-Behavior of Liposomal Suspensions Containing Poly(Ethylene Glycol)-Lipids. Macromolecules. 1995;28(23):7693-9.
  • 40. Kilic S, Bolukcu ES. Phase behavior of DSPC/PEG(40)St mixtures at higher emulsifier contents. Colloid Surface B. 2018;171:368-76.
  • 41. Kilic S. Quantification of PEG(40)St squeeze out from DSPC/PEG(40)St monolayers at higher molar ratios. Colloid Surface A. 2018;551:58-64.
Year 2019, Volume: 6 Issue: 3, 439 - 450, 20.10.2019
https://doi.org/10.18596/jotcsa.594219

Abstract

Project Number

109M494

References

  • 1. Paefgen V, Doleschel D, Kiessling F. Evolution of contrast agents for ultrasound imaging and ultrasound-mediated drug delivery. Front Pharmacol. 2015;6.
  • 2. Lentacker I, Geers B, Demeester J, De Smedt SC, Sanders NN. Design and Evaluation of Doxorubicin-containing Microbubbles for Ultrasound-triggered Doxorubicin Delivery: Cytotoxicity and Mechanisms Involved. Molecular Therapy. 2010;18(1):101-8.
  • 3. Borden MA, Longo ML. The dependence of lipid-coated microbubble dissolution behavior on acyl chain length. Biophys J. 2002;82(1):35a-a.
  • 4. Garg S, Thomas AA, Borden MA. The effect of lipid monolayer in-plane rigidity on in vivo microbubble circulation persistence. Biomaterials. 2013;34(28):6862-70.
  • 5. Kwan JJ, Borden MA. Lipid monolayer dilatational mechanics during microbubble gas exchange. Soft Matter. 2012;8(17):4756-66.
  • 6. Pu G, Borden MA, Longo ML. Collapse and shedding transitions in binary lipid monolayers coating microbubbles. Langmuir. 2006;22(7):2993-9.
  • 7. Kabalnov A, Klein D, Pelura T, Schutt E, Weers J. Dissolution of multicomponent microbubbles in the bloodstream: 1. Theory. Ultrasound Med Biol. 1998;24(5):739-49.
  • 8. Borden MA, Longo ML. Oxygen permeability of fully condensed lipid monolayers. J Phys Chem B. 2004;108(19):6009-16.
  • 9. Kwan JJ, Borden MA. Lipid monolayer collapse and microbubble stability. Advances in Colloid and Interface Science. 2012;183:82-99.
  • 10. Shen Y, Powell RL, Longo ML. Interfacial and stability study of microbubbles coated with a mono stearin/monopalmitin-rich food emulsifier and PEG40 stearate. Journal of Colloid and Interface Science. 2008;321(1):186-94.
  • 11. Shen YY, Powell RL, Longo ML. Influence of the dissolution rate on the collapse and shedding behavior of monostearin/monopalmitin-rich coated microbubbles. Langmuir. 2008;24(18):10035-40.
  • 12. Kwan JJ, Borden MA. Microbubble Dissolution in a Multigas Environment. Langmuir. 2010;26(9):6542-8.
  • 13. Borden MA, Pu G, Runner GJ, Longo ML. Surface phase behavior and microstructure of lipid/PEG-emulsifier monolayer-coated microbubbles. Colloid Surface B. 2004;35(3-4):209-23.
  • 14. Pu G, Longo ML, Borden MA. Effect of microstructure on molecular oxygen permeation through condensed phospholipid monolayers. Journal of the American Chemical Society. 2005;127(18):6524-5.
  • 15. Petrache HI, Dodd SW, Brown MF. Area per lipid and acyl length distributions in fluid phosphatidylcholines determined by H-2 NMR spectroscopy. Biophys J. 2000;79(6):3172-92.
  • 16. Kucerka N, Nieh MP, Katsaras J. Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature. Biochimica Et Biophysica Acta-Biomembranes. 2011;1808(11):2761-71.
  • 17. Mulvana H, Stride E, Hajnal JV, Eckersley RJ. Temperature Dependent Behavior of Ultrasound Contrast Agents. Ultrasound Med Biol. 2010;36(6):925-34.
  • 18. Mulvana H, Stride E, Tang MX, Hajnal JV, Eckersley R. Temperature-Dependent Differences in the Nonlinear Acoustic Behavior of Ultrasound Contrast Agents Revealed by High-Speed Imaging and Bulk Acoustics. Ultrasound Med Biol. 2011;37(9):1509-17.
  • 19. Swanson EJ, Mohan V, Kheir J, Borden MA. Phospholipid-Stabilized Microbubble Foam for Injectable Oxygen Delivery. Langmuir. 2010;26(20):15726-9.
  • 20. Farook U, Stride E, Edirisinghe MJ. Preparation of suspensions of phospholipid-coated microbubbles by coaxial electrohydrodynamic atomization. Journal of the Royal Society Interface. 2009;6(32):271-7.
  • 21. Borden MA, Longo ML. Dissolution behavior of lipid monolayer-coated, air-filled microbubbles: Effect of lipid hydrophobic chain length. Langmuir. 2002;18(24):9225-33.
  • 22. Grant CA, McKendry JE, Evans SD. Temperature dependent stiffness and visco-elastic behaviour of lipid coated microbubbles using atomic force microscopy. Soft Matter. 2012;8(5):1321-6.
  • 23. Borden M. Nanostructural features on stable microbubbles. Soft Matter. 2009;5(4):716-20.
  • 24. Upadhyay A, Dalvi SV, Gupta G, Khanna N. Effect of PEGylation on performance of protein microbubbles and its comparison with lipid microbubbles. Mat Sci Eng C-Mater. 2017;71:425-30.
  • 25. Stride E, Edirisinghe M. Novel preparation techniques for controlling microbubble uniformity: a comparison. Medical & Biological Engineering & Computing. 2009;47(8):883-92.
  • 26. Epstein PS, Plesset MS. On the Stability of Gas Bubbles in Liquid-Gas Solutions. J Chem Phys 1950;18(11):1505-9.
  • 27. Wang WH, Moser CC, Wheatley MA. Langmuir trough study of surfactant mixtures used in the production of a new ultrasound contrast agent consisting of stabilized microbubbles. J Phys Chem-Us. 1996;100(32):13815-21.
  • 28. Abou-Saleh RH, Peyman SA, Johnson BRG, Marston G, Ingram N, Bushby R, et al. The influence of intercalating perfluorohexane into lipid shells on nano and microbubble stability. Soft Matter. 2016;12(34):7223-30.
  • 29. Xing ZW, Ke HT, Wang JR, Zhao B, Yue XL, Dai ZF, et al. Novel ultrasound contrast agent based on microbubbles generated from surfactant mixtures of Span 60 and polyoxyethylene 40 stearate. Acta Biomaterialia. 2010;6(9):3542-9.
  • 30. Chou TH, Chu IM. Thermodynamic characteristics of DSPC/DSPE-PEG(2000) mixed monolayers on the water subphase at different temperatures. Colloid Surface B. 2003;27(4):333-44.
  • 31. Bae YC, Lambert SM, Soane DS, Prausnitz JM. Cloud-Point Curves of Polymer-Solutions from Thermooptic Measurements. Macromolecules. 1991;24(15):4403-7.
  • 32. Gao X, Kucerka N, Nieh MP, Katsaras J, Zhu SP, Brash JL, et al. Chain Conformation of a New Class of PEG-Based Thermoresponsive Polymer Brushes Grafted on Silicon as Determined by Neutron Reflectometry. Langmuir. 2009;25(17):10271-8.
  • 33. Tyrode E, Johnson CM, Rutland MW, Claesson PM. Structure and hydration of poly(ethylene oxide) surfactants at the air/liquid interface. A vibrational sum frequency spectroscopy study. Journal of Physical Chemistry C. 2007;111(31):11642-52.
  • 34. Frey SL, Lee KYC. Temperature dependence of poloxamer insertion into and squeeze-out from lipid monolayers. Langmuir. 2007;23(5):2631-7.
  • 35. Jebrail M, Schmidt R, DeWolf CE, Tsoukanova V. Effect of aliphatic chain length on stability of poly(ethylene glycol)-grafted phospholipid monolayers at the air/water interface. Colloid Surface A. 2008;321(1-3):168-74.
  • 36. Angelova A, De Coninck J, Ionov R. Equilibrium surface properties of lipid mixtures of retinal, phosphatidylcholine and fatty acid derivatives at the air/water interface. Supramol Sci. 1997;4(3-4):207-14.
  • 37. Gopal A, Lee KYC. Morphology and collapse transitions in binary phospholipid monolayers. J Phys Chem B. 2001;105(42):10348-54.
  • 38. Lipp MM, Lee KYC, Takamoto DY, Zasadzinski JA, Waring AJ. Coexistence of buckled and flat monolayers. Physical Review Letters. 1998;81(8):1650-3.
  • 39. Hristova K, Kenworthy A, Mcintosh TJ. Effect of Bilayer Composition on the Phase-Behavior of Liposomal Suspensions Containing Poly(Ethylene Glycol)-Lipids. Macromolecules. 1995;28(23):7693-9.
  • 40. Kilic S, Bolukcu ES. Phase behavior of DSPC/PEG(40)St mixtures at higher emulsifier contents. Colloid Surface B. 2018;171:368-76.
  • 41. Kilic S. Quantification of PEG(40)St squeeze out from DSPC/PEG(40)St monolayers at higher molar ratios. Colloid Surface A. 2018;551:58-64.
There are 41 citations in total.

Details

Primary Language English
Subjects Physical Chemistry
Journal Section Articles
Authors

Sevgi Kilic 0000-0002-1184-0123

Project Number 109M494
Publication Date October 20, 2019
Submission Date July 19, 2019
Acceptance Date October 1, 2019
Published in Issue Year 2019 Volume: 6 Issue: 3

Cite

Vancouver Kilic S. Effect of Temperature on Stability of Lipid Microbubbles. JOTCSA. 2019;6(3):439-50.