Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 2002 Jan;82(1 Pt 1):109–119. doi: 10.1016/S0006-3495(02)75378-2

Temperature-dependent electrical and ultrastructural characterizations of porcine skin upon electroporation.

Stephen A Gallo 1, Arindam Sen 1, Mary L Hensen 1, Sek Wen Hui 1
PMCID: PMC1302453  PMID: 11751300

Abstract

The mechanism of high-voltage pulse-induced permeabilization of the stratum corneum, the outer layer of the skin, is still not completely understood. It has been suggested that joule heating resulting from the applied pulse may play a major role in disrupting the stratum corneum. In this study, electrical and ultrastructural measurements were conducted to examine the temperature dependence of the pulse-induced permeabilization of the stratum corneum. The stratum corneum resistance was measured using a vertical diffusion holder, with the stratum corneum placed between two electrode-containing chambers. The stratum corneum resistance was reduced manyfold during the applied pulse. The extent of resistance reduction increased with pulse voltage until reaching a threshold value, above which the resistance reduction was less dependent on the pulse voltage. The stratum corneum was more susceptible to permeabilization at high temperature, the threshold voltage being lower. The stratum corneum resistance recovered within milliseconds after a single 0.3-ms pulse. High-temperature samples had a more prolonged recovery time. Using time-resolved freeze fracture electron microscopy, aggregates of lipid vesicles were observed in all samples pulsed above the threshold voltage. The sizes and fractional areas occupied by aggregates of lipid vesicles at 4 degrees C and at 25 degrees C were measured at different time points after the applied pulse. Aggregates of vesicles persisted long after the electric resistance was recovered. After pulsing at the same voltage of 80 V, samples at 4 degrees C were found to have slightly more extensive aggregate formation initially, but recovered more rapidly than those at 25 degrees C. The more rapid recovery of the 4 degrees C samples was likely due to a lower supra-threshold voltage. Viscoelastic instability propagation created by the pulse may also play a role in the recovery of the aggregates.

Full Text

The Full Text of this article is available as a PDF (531.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bouwstra J. A., Gooris G. S., van der Spek J. A., Bras W. Structural investigations of human stratum corneum by small-angle X-ray scattering. J Invest Dermatol. 1991 Dec;97(6):1005–1012. doi: 10.1111/1523-1747.ep12492217. [DOI] [PubMed] [Google Scholar]
  2. Chizmadzhev Y. A., Zarnitsin V. G., Weaver J. C., Potts R. O. Mechanism of electroinduced ionic species transport through a multilamellar lipid system. Biophys J. 1995 Mar;68(3):749–765. doi: 10.1016/S0006-3495(95)80250-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Gallo S. A., Oseroff A. R., Johnson P. G., Hui S. W. Characterization of electric-pulse-induced permeabilization of porcine skin using surface electrodes. Biophys J. 1997 Jun;72(6):2805–2811. doi: 10.1016/S0006-3495(97)78922-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Gallo S. A., Sen A., Hensen M. L., Hui S. W. Time-dependent ultrastructural changes to porcine stratum corneum following an electric pulse. Biophys J. 1999 May;76(5):2824–2832. doi: 10.1016/S0006-3495(99)77436-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Golden G. M., Guzek D. B., Kennedy A. H., McKie J. E., Potts R. O. Stratum corneum lipid phase transitions and water barrier properties. Biochemistry. 1987 Apr 21;26(8):2382–2388. doi: 10.1021/bi00382a045. [DOI] [PubMed] [Google Scholar]
  6. Helfrich W. Elastic properties of lipid bilayers: theory and possible experiments. Z Naturforsch C. 1973 Nov-Dec;28(11):693–703. doi: 10.1515/znc-1973-11-1209. [DOI] [PubMed] [Google Scholar]
  7. Jadoul A., Tanojo H., Préat V., Bouwstra J. A., Spies F., Boddé H. E. Electroperturbation of human stratum corneum fine structure by high voltage pulses: a freeze-fracture electron microscopy and differential thermal analysis study. J Investig Dermatol Symp Proc. 1998 Aug;3(2):153–158. doi: 10.1038/jidsymp.1998.31. [DOI] [PubMed] [Google Scholar]
  8. Johnson P. G., Gallo S. A., Hui S. W., Oseroff A. R. A pulsed electric field enhances cutaneous delivery of methylene blue in excised full-thickness porcine skin. J Invest Dermatol. 1998 Sep;111(3):457–463. doi: 10.1046/j.1523-1747.1998.00301.x. [DOI] [PubMed] [Google Scholar]
  9. Kasting G. B., Bowman L. A. Electrical analysis of fresh, excised human skin: a comparison with frozen skin. Pharm Res. 1990 Nov;7(11):1141–1146. doi: 10.1023/a:1015928225089. [DOI] [PubMed] [Google Scholar]
  10. Madison K. C., Swartzendruber D. C., Wertz P. W., Downing D. T. Presence of intact intercellular lipid lamellae in the upper layers of the stratum corneum. J Invest Dermatol. 1987 Jun;88(6):714–718. doi: 10.1111/1523-1747.ep12470386. [DOI] [PubMed] [Google Scholar]
  11. Mitragotri S., Edwards D. A., Blankschtein D., Langer R. A mechanistic study of ultrasonically-enhanced transdermal drug delivery. J Pharm Sci. 1995 Jun;84(6):697–706. doi: 10.1002/jps.2600840607. [DOI] [PubMed] [Google Scholar]
  12. Nagle J. F., Tristram-Nagle S. Structure of lipid bilayers. Biochim Biophys Acta. 2000 Nov 10;1469(3):159–195. doi: 10.1016/s0304-4157(00)00016-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Needham D., Hochmuth R. M. Electro-mechanical permeabilization of lipid vesicles. Role of membrane tension and compressibility. Biophys J. 1989 May;55(5):1001–1009. doi: 10.1016/S0006-3495(89)82898-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Panescu D., Webster J. G., Stratbucker R. A. A nonlinear electrical-thermal model of the skin. IEEE Trans Biomed Eng. 1994 Jul;41(7):672–680. doi: 10.1109/10.301734. [DOI] [PubMed] [Google Scholar]
  15. Pawlowski P., Gallo S. A., Johnson P. G., Hui S. W. Electrorheological modeling of the permeabilization of the stratum corneum: theory and experiment. Biophys J. 1998 Dec;75(6):2721–2731. doi: 10.1016/S0006-3495(98)77716-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Pliquett U. F., Gusbeth C. A. Perturbation of human skin due to application of high voltage. Bioelectrochemistry. 2000 Feb;51(1):41–51. doi: 10.1016/s0302-4598(99)00070-7. [DOI] [PubMed] [Google Scholar]
  17. Pliquett U. F., Zewert T. E., Chen T., Langer R., Weaver J. C. Imaging of fluorescent molecule and small ion transport through human stratum corneum during high voltage pulsing: localized transport regions are involved. Biophys Chem. 1996 Jan 16;58(1-2):185–204. doi: 10.1016/0301-4622(95)00098-4. [DOI] [PubMed] [Google Scholar]
  18. Pliquett U., Langer R., Weaver J. C. Changes in the passive electrical properties of human stratum corneum due to electroporation. Biochim Biophys Acta. 1995 Nov 1;1239(2):111–121. doi: 10.1016/0005-2736(95)00139-t. [DOI] [PubMed] [Google Scholar]
  19. Prausnitz M. R., Bose V. G., Langer R., Weaver J. C. Electroporation of mammalian skin: a mechanism to enhance transdermal drug delivery. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10504–10508. doi: 10.1073/pnas.90.22.10504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Schurer N. Y., Elias P. M. The biochemistry and function of stratum corneum lipids. Adv Lipid Res. 1991;24:27–56. doi: 10.1016/b978-0-12-024924-4.50006-7. [DOI] [PubMed] [Google Scholar]
  21. Wilkes G. L., Wildnauer R. H. Structure-property relationships of the stratum corneum of human and neonatal rat. II. Dynamic mechanical studies. Biochim Biophys Acta. 1973 Apr 28;304(2):276–289. doi: 10.1016/0304-4165(73)90245-6. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES