The impact of detergents on the tissue decellularization process: A ToF-SIMS study
Open accessAbstract
Biologic scaffolds are derived from mammalian tissues, which must be decellularized to remove cellular antigens that would otherwise incite an adverse immune response. Although widely used clinically, the optimum balance between cell removal and the disruption of matrix architecture and surface ligand landscape remains a considerable challenge. Here we describe the use of time of flight secondary ion mass spectroscopy (ToF-SIMS) to provide sensitive, molecular specific, localized analysis of detergent decellularized biologic scaffolds. We detected residual detergent fragments, specifically from Triton X-100, sodium deoxycholate and sodium dodecyl sulphate (SDS) in decellularized scaffolds; increased SDS concentrations from 0.1% to 1.0% increased both the intensity of SDS fragments and adverse cell outcomes. We also identified cellular remnants, by detecting phosphate and phosphocholine ions in PAA and CHAPS decellularized scaffolds. The present study demonstrates ToF-SIMS is not only a powerful tool for characterization of biologic scaffold surface molecular functionality, but also enables sensitive assessment of decellularization efficacy.Statement of significance We report here on the use of a highly sensitive analytical technique, time of flight secondary ion mass spectroscopy (ToF-SIMS) to characterize detergent decellularized scaffolds. ToF-SIMS detected cellular remnants and residual detergent fragments; increased intensity of the detergent fragments correlated with adverse cell matrix interactions. This study demonstrates the importance of maintaining a balance between cell removal and detergent disruption of matrix architecture and matrix surface ligand landscape. This study also demonstrates the power of ToF-SIMS for the characterization of decellularized scaffolds and capability for assessment of decellularization efficacy. Future use of biologic scaffolds in clinical tissue reconstruction will benefit from the fundamental results described in this work.
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Complete removal of cellular materials necessitates robust decellularization, which may damage ECM ultrastructure and deplete favorable entities, with detrimental effects on scaffold function and regenerative properties.
“On the flip side, the complete removal of cellular materials necessitates the application of robust decellularization, which may accompany unwanted consequences. Such protocols damage ECM ultrastructure and deplete favorable entities that consequently have detrimental effects on yielded scaffold function and regenerative properties [51, 52].”
From Immunogenicity of decellularized extracellular matrix scaffolds: a bottleneck in tissue engineering and regenerative medicine (2023) · cites this paper as [51]
The Introduction describes a trade-off between removing cellular material and preserving ECM architecture; it explicitly says complete removal of all cell remnants is not possible. The Discussion supports the remaining point: excessive damage to ECM ultrastructure, growth factors, and critical components can adversely affect cytocompatibility and functional tissue replacement. The claim is supported as a warning about thorough decellularization, but its premise of complete removal lacks that qualification. (LLM, conf=0.86)
Experimental — accuracy not yet measuredTX100 effects are mainly dependent on its concentration; higher TX100 concentrations cause unfavorable effects on ECM.
“TX100 effects are mainly dependent on its concentration. Higher TX100 concentrations will cause unfavorable effects on ECM [51, 83].”
From Immunogenicity of decellularized extracellular matrix scaffolds: a bottleneck in tissue engineering and regenerative medicine (2023) · cites this paper as [51]
The Results (§3.5; page unavailable) report that urothelial cells on Triton X-100-treated scaffolds did not form tight junctions, which supports a limited adverse effect. But the paper does not establish that Triton X-100 effects are mainly concentration-dependent or that higher concentrations worsen ECM outcomes. Its concentration-dependent findings concern SDS; Results (§3.2) report that scaffolds treated with 3% Triton X-100 retained an intricate fibre network. (LLM, conf=0.84)
Experimental — accuracy not yet measuredIncomplete removal of cell components during decellularization may provoke severe post-implantation immune responses.
“However, incomplete removal of cell components during the decellularization process may provoke severe post-implantation immune responses [51, 52].”
From Immunogenicity of decellularized extracellular matrix scaffolds: a bottleneck in tissue engineering and regenerative medicine (2023) · cites this paper as [51]
ECM alterations impede subsequent recellularization and consequently increase availability of present antigenic sites for the host immune system.
“The second mechanism is related to the ECM alterations, which impede subsequent recellularization [51] and consequently increase the availability of present antigenic sites for the host immune system [64].”
From Immunogenicity of decellularized extracellular matrix scaffolds: a bottleneck in tissue engineering and regenerative medicine (2023) · cites this paper as [51]
Ionic detergents may alter ECM architecture and disrupt structure of protein constituents, including collagens.
“However, they may alter ECM architecture and disrupt the structure of protein constituents, including collagens [51].”
From Immunogenicity of decellularized extracellular matrix scaffolds: a bottleneck in tissue engineering and regenerative medicine (2023) · cites this paper as [51]
CHAPS deplete elastin and GAGs content of ECM.
“Of note, they have been demonstrated to deplete the elastin and GAGs content of ECM [51, 75, 82].”
From Immunogenicity of decellularized extracellular matrix scaffolds: a bottleneck in tissue engineering and regenerative medicine (2023) · cites this paper as [51]
The Results (§3.2; page unavailable) show structural changes in CHAPS-treated scaffolds, but do not report depletion of elastin or GAGs. The Discussion (§4; page unavailable) describes GAG removal by ionic detergents, not specifically by CHAPS. Searches for CHAPS with elastin and GAG depletion found no passage establishing the claim. (LLM, conf=0.76)
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Fernández-Carro, E., Remacha, A. R., Orera, I., Lattanzio, G., Barrios, A. G., del Barrio, J., Alcaine, C., & Ciriza, J. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25074020 · Cited by 20 · see citing works
Decellularized organ biomatrices facilitate quantifiable in vitro 3D cancer metastasis models
VandenHeuvel, S. N., Farris, H. A., Noltensmeyer, D. A., Roy, S., Donehoo, D. A., Kopetz, S., Haricharan, S., Walsh, A. J., & Raghavan, S. A. (2022) · Soft Matter · doi:10.1039/d1sm01796a · Cited by 19 · see citing works
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Mehrabi, A., Mousazadeh, S., Mollafilabi, A., Nafissi, N., & Milan, P. B. (2023) · Life Sciences · doi:10.1016/j.lfs.2023.122236 · Cited by 19 · see citing works
Asadian, E., Abbaszadeh, S., Ghorbani-Bidkorpeh, F., Rezaei, S., Xiao, B. J., Santos, H. A., & Shahbazi, M. (2024) · Biomaterials Science · doi:10.1039/d4bm00982g · Cited by 18 · see citing works
- Authors
- White, L. J., Taylor, A. J., Faulk, D. M., Keane, T. J., Saldin, L. T., Reing, J. E., Swinehart, I. T., Turner, N. J., Ratner, B. D., & Badylak, S. F.
- Affiliations
- University of Nottingham (GB)
- University of Washington (US)
- University of Pittsburgh (US)
- Corresponding author
- Badylak, Stephen F .
- ORCID
- Venue
- Acta Biomaterialia
- Publisher
- Elsevier BV
- Published
- 2017-03
- Volume
- 50
- Pages
- 207-219
- ISSN
- 1742-7061 (ISSN-L)
- PMC
- PMC5592694
- OpenAlex
- W2561109298
- Cited by
- 268
- References
- 76
- Citations by year
- 2026: 23 · 2025: 18 · 2024: 32 · 2023: 41 · 2022: 48 · 2021: 30 · 2020: 28 · 2019: 24 · 2018: 13 · 2017: 10
- FWCI
- 17.34
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Acta Biomaterialia (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Repository@Nottingham (University of Nottingham) (acceptedVersion, other-oa)
- Repository@Nottingham (University of Nottingham) (submittedVersion, cc-by-nc-nd)
- Nottingham ePrints (University of Nottingham) (submittedVersion, cc-by-nc-nd)
- Funders
- Commonwealth of Pennsylvania
- NIH (EB-002027)
- Marie Curie International Outgoing Fellowship (624841)
- NSF Graduate Research Fellowships
- NIH T32 fellowship (T32 EB001026)
- Topics
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Physical Sciences › Engineering › Computational Mechanics › Ion-surface interactions and analysis
- Physical Sciences › Engineering › Biomedical Engineering › Bone Tissue Engineering Materials
- Keywords
- biological scaffolds, Triton X-100, sodium deoxycholate, sodium dodecyl sulfate, phosphorylcholine, tissue reconstruction
- MeSH terms
- Animals, Urinary Bladder, Detergents, Extracellular Matrix, Swine
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