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Putative mechanobiological impact of surface texture on cell activity around soft-tissue implants undergoing micromotion

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Abstract

Recent reports of adverse health effects (e.g., capsular contracture, lymphoma) linked to the absence or presence of texture on soft-tissue implants (e.g., breast implants) suggest surface topography may have pathological impact(s). We propose that surface texture influences the transfer of displacements, experienced by an implant undergoing micromotion, to surrounding interfacial extracellular matrix, which in turn impacts the activity of the resident cells and is based on degree of tissue integration. We hypothesize that transfer of displacements due to micromotion promotes interstitial fluid movement that imposes hydrodynamic stresses (pressures, shear stresses) on cells residing in the interfacial tissues and impacts their activity. To address this, we developed a computer simulation to approximate hydrodynamic stresses in the interstitial environment of saturated poroelastic tissues (model soft-tissue implantation sites) generated from oscillatory implant micromotion as a function of the magnitude of translational displacement, direction of motion, degree of tissue integration, and surface roughness of the implant. Highly integrated implants were predicted to generate the highest fluid shear stresses within model tissues, with oscillatory fluid shear stresses up to 80 dyn/cm2 for a 20-μm displacement. Notably, application of oscillatory 80 dyn/cm2 shear stress to cultured human fibroblasts elicited cell death after 20 h compared to cells maintained under static conditions or exposed to 80 dyn/cm2 steady, unidirectional shear. These results indicate that oscillatory interstitial fluid stresses generated by micromotion of an integrated implant may influence the activity of the surrounding cells and play a role in the body’s fibrotic response to textured soft-tissue implants.

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Availability of data and material

The principal data generated during the experiments conducted in this study are available within the manuscript and its Supplementary Information. Raw datasets generated during the study are available for research purposes from the corresponding author upon request.

Code availability

The computational model used in the study is available upon request.

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Acknowledgements

This work was supported by a grant from Office of Women’s Health of the United States Food and Drug Administration (FDA; Department of Health and Human Services) and partially administered by the Oak Ridge Institute for Science and Education through an agreement between the U.S. Department of Energy and FDA. The authors would also like to thank Dr. Sung Yoon, Dr. Min Zhang, and Dr. Cynthia Chang of the Office of Product Evaluation and Quality (OPEQ) in the Center for Devices and Radiological Health (CDRH) at FDA for their feedback during the development and/or execution of this study. This article reflects the views of the author and should not be construed to represent FDA's views or policies.

Funding

This work was supported by a grant from Office of Women’s Health of the United States Food and Drug Administration (FDA; Department of Health and Human Services) and partially administered by the Oak Ridge Institute for Science and Education through an agreement between the U.S. Department of Energy and FDA.

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BPH and HYS wrote the paper. BPH, HYS, and DS formulated the computational model, designed the experimental studies, and analyzed data. BPH conducted the experiments, carried out the statistical analyses, and prepared displays communicating datasets. II and KSP provided substantive scientific contributions to hypothesis development and overall study design as well as technical advice and editorial support.

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Correspondence to Hainsworth Y. Shin.

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Any mention of commercial products, their sources, or their use in connection with material reported herein is not to be construed as either an actual or implied endorsement of such products by the Department of Health and Human Services. The findings and conclusions in this article have not been formally disseminated by the U.S. Food and Drug Administration and should not be construed to represent any Agency determination or policy.

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Hung, B.P., Simon, D.D., Phillips, K.S. et al. Putative mechanobiological impact of surface texture on cell activity around soft-tissue implants undergoing micromotion. Biomech Model Mechanobiol 21, 1117–1131 (2022). https://doi.org/10.1007/s10237-022-01578-1

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