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Towards the creation of decellularized organ constructs using irreversible electroporation and active mechanical perfusion

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Sano, Michael B, Neal, Robert E, Garcia, Paulo A, Gerber, David, Robertson, John, Davalos, Rafael V·2010·BioMedical Engineering OnLine
DOI 10.1186/1475-925x-9-83PMC PMC3018380
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Abstract

Background: Despite advances in transplant surgery and general medicine, the number of patients awaiting transplant organs continues to grow, while the supply of organs does not. This work outlines a method of organ decellularization using non-thermal irreversible electroporation (N-TIRE) which, in combination with reseeding, may help supplement the supply of organs for transplant. Methods: In our study, brief but intense electric pulses were applied to porcine livers while under active low temperature cardio-emulation perfusion. Histological analysis and lesion measurements were used to determine the effects of the pulses in decellularizing the livers as a first step towards the development of extracellular scaffolds that may be used with stem cell reseeding. A dynamic conductivity numerical model was developed to simulate the treatment parameters used and determine an irreversible electroporation threshold. Results: Ninety-nine individual 1000 V/cm 100-μs square pulses with repetition rates between 0.25 and 4 Hz were found to produce a lesion within 24 hours post-treatment. The livers maintained intact bile ducts and vascular structures while demonstrating hepatocytic cord disruption and cell delamination from cord basal laminae after 24 hours of perfusion. A numerical model found an electric field threshold of 423 V/cm under specific experimental conditions, which may be used in the future to plan treatments for the decellularization of entire organs. Analysis of the pulse repetition rate shows that the largest treated area and the lowest interstitial density score was achieved for a pulse frequency of 1 Hz. After 24 hours of perfusion, a maximum density score reduction of 58.5 percent had been achieved. Conclusions: This method is the first effort towards creating decellularized tissue scaffolds that could be used for organ transplantation using N-TIRE. In addition, it provides a versatile platform to study the effects of pulse parameters such as pulse length, repetition rate, and field strength on whole organ structures.

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Crossref · 10.1186/1475-925x-9-83

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Figures

Figure 1 Experimental setup and IRE lesion. (a) Placement of the electrodes on actively perfused liver tissue and (b) the resultant lesion after treatment with 99, 100 μs, 1500 V/cm pulses and 4 hours of perfusion. The approximate area of the electrode is outlined in black.
Figure 1 Experimental setup and IRE lesion. (a) Placement of the electrodes on actively perfused liver tissue and (b) the resultant lesion after treatment with 99, 100 μs, 1500 V/cm pulses and 4 hours of perfusion. The approximate area of the electrode is outlined in black.CC BY · PubMed Central
Figure 2 Numerical model of the liver tissue with conductivity map, electric field distribution, and thermal map. (a) The conductivity of the tissue changes from 0.067 to 0.256 during treatment based on changes in the (b) electric field distribution and (c) temperature changes.
Figure 2 Numerical model of the liver tissue with conductivity map, electric field distribution, and thermal map. (a) The conductivity of the tissue changes from 0.067 to 0.256 during treatment based on changes in the (b) electric field distribution and (c) temperature changes.CC BY · PubMed Central
Figure 3 Lesion diameter and density score vs. pulse frequency. Plots comparing the (a) measured lesion diameters for the plate electrodes and (b) density score for each experimental frequency. Box plots (red) which share a common symbol (+, *, or #) were not statistically different from each other for (a) α = 0.1 and (b) α = 0.05. The average value and standard deviations are represented by green and blue lines respectively. The box plots represent the interquartile range between the 25th and 75th data percentiles. The largest lesions developed and the lowest density score was observed when pulses were applied at a frequency of 1 Hz
Figure 3 Lesion diameter and density score vs. pulse frequency. Plots comparing the (a) measured lesion diameters for the plate electrodes and (b) density score for each experimental frequency. Box plots (red) which share a common symbol (+, *, or #) were not statistically different from each other for (a) α = 0.1 and (b) α = 0.05. The average value and standard deviations are represented by green and blue lines respectively. The box plots represent the interquartile range between the 25th and 75th data percentiles. The largest lesions developed and the lowest density score was observed when pulses were applied at a frequency of 1 HzCC BY · PubMed Central
Figure 4 Histological comparison of untreated liver tissue to areas which have undergone mild IRE treatments showing preservation of connective tissue and blood vessels. Histological comparison of untreated liver tissue to areas which have undergone mild IRE treatments showing preservation of connective tissue and blood vessels. Samples stained with H&E from (a) untreated and (b) ninety nine, 100 μs, 1000 V/cm pulses using plate electrodes 24 hours of cardio emulation perfusion at 10×.
Figure 4 Histological comparison of untreated liver tissue to areas which have undergone mild IRE treatments showing preservation of connective tissue and blood vessels. Histological comparison of untreated liver tissue to areas which have undergone mild IRE treatments showing preservation of connective tissue and blood vessels. Samples stained with H&E from (a) untreated and (b) ninety nine, 100 μs, 1000 V/cm pulses using plate electrodes 24 hours of cardio emulation perfusion at 10×.CC BY · PubMed Central
Figure 5 IRE treatments result in hepatocytic cord disruption and cell delamination. (a) A section of untreated liver after 24 hours of perfusion. Sections of the same liver treated with 90, 1500 V/cm, 100 μs pulses at 4 Hz using needle electrodes after 24 hours of perfusion at (b) 10× and (c) 20× magnification.
Figure 5 IRE treatments result in hepatocytic cord disruption and cell delamination. (a) A section of untreated liver after 24 hours of perfusion. Sections of the same liver treated with 90, 1500 V/cm, 100 μs pulses at 4 Hz using needle electrodes after 24 hours of perfusion at (b) 10× and (c) 20× magnification.CC BY · PubMed Central
Figure 6 Moderately severe lesions maintain bile ducts and vascular structures. (a) A section of untreated liver after 24 hours of perfusion. (b) The same liver treated with 100, 1500 V/cm, 100 μs pulses at 1 Hz using needle electrodes after 24 hours of perfusion at 20× magnification.
Figure 6 Moderately severe lesions maintain bile ducts and vascular structures. (a) A section of untreated liver after 24 hours of perfusion. (b) The same liver treated with 100, 1500 V/cm, 100 μs pulses at 1 Hz using needle electrodes after 24 hours of perfusion at 20× magnification.CC BY · PubMed Central

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Citations

Cites

Show all 60 references

Research works printed but not linked: 4

  1. Fabre: Report of the British Transplantation Society Working Party on Organ Donation. 1995.
  2. Davalos RV: Irreversible Electroporation to Create Tissue Scaffolds. United States patent 2009.
  3. Davalos RV, Mir LM, Rubinsky B: Tissue Ablation with Irreversible Electroporation. Ann Biomed Eng 2005, 33: 223–231. 10.1007/s10439-005-8981-8 · DOI
  4. Edd JF, Horowitz L, Davalos RV, Mir LM, Rubinsky B: In Vivo Results of a New Focal Tissue Ablation Technique: Irreversible Electroporation. Ieee Transactions on Biomedical Engineering 2006, 53: 1409–1415. 10.1109/TBME.2006.873745 · DOI

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Metadata

Authors
Sano, M. B., Neal, R. E., Garcia, P. A., Gerber, D., Robertson, J., & Davalos, R. V.
Affiliations
  • Virginia Tech - Wake Forest University School of Biomedical Engineering & Sciences (US)
  • University of North Carolina at Chapel Hill (US)
  • Virginia–Maryland College of Veterinary Medicine (US)
Corresponding author
Davalos, Rafael V
ORCID
Venue
BioMedical Engineering OnLine
Publisher
Springer Science and Business Media LLC
Published
2010-12
Volume
9
Issue
1
Pages
83-83
ISSN
1475-925X (ISSN-L)
DOI
10.1186/1475-925x-9-83
PMC
PMC3018380
OpenAlex
W2024731442
Cited by
117
References
60
Citations by year
2026: 1 · 2025: 4 · 2024: 11 · 2023: 8 · 2022: 9 · 2021: 10 · 2020: 9 · 2019: 6 · 2018: 5 · 2017: 11 · 2016: 15 · 2015: 6 · 2014: 9 · 2013: 5 · 2012: 4
FWCI
4.39
Type
journal article
Language
en
Open access
Licence
Locations
  • BioMedical Engineering OnLine (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • VTechWorks (Virginia Tech) (submittedVersion, cc-by)
Topics
  • Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Microbial Inactivation Methods
  • Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
Keywords
irreversible electroporation, porcine liver, extracellular matrix scaffolds, threshold electric field, pulse repetition rate, organ transplantation
MeSH terms
Animals, Humans, Liver, Perfusion, Swine, Electroporation, Tissue Engineering, Tissue Scaffolds, Mechanical Phenomena

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