Changes in Tissue Fluidity Predict Tumor Aggressiveness In Vivo
Abstract Cancer progression is caused by genetic changes and associated with various alterations in cell properties, which also affect a tumor's mechanical state. While an increased stiffness has been well known for long for solid tumors, it has limited prognostic power. It is hypothesized that...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Wiley
2023-09-01
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| Series: | Advanced Science |
| Subjects: | |
| Online Access: | https://doi.org/10.1002/advs.202303523 |
| _version_ | 1797684954668204032 |
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| author | Frank Sauer Steffen Grosser Mehrgan Shahryari Alexander Hayn Jing Guo Jürgen Braun Susanne Briest Benjamin Wolf Bahriye Aktas Lars‐Christian Horn Ingolf Sack Josef A. Käs |
| author_facet | Frank Sauer Steffen Grosser Mehrgan Shahryari Alexander Hayn Jing Guo Jürgen Braun Susanne Briest Benjamin Wolf Bahriye Aktas Lars‐Christian Horn Ingolf Sack Josef A. Käs |
| author_sort | Frank Sauer |
| collection | DOAJ |
| description | Abstract Cancer progression is caused by genetic changes and associated with various alterations in cell properties, which also affect a tumor's mechanical state. While an increased stiffness has been well known for long for solid tumors, it has limited prognostic power. It is hypothesized that cancer progression is accompanied by tissue fluidization, where portions of the tissue can change position across different length scales. Supported by tabletop magnetic resonance elastography (MRE) on stroma mimicking collagen gels and microscopic analysis of live cells inside patient derived tumor explants, an overview is provided of how cancer associated mechanisms, including cellular unjamming, proliferation, microenvironment composition, and remodeling can alter a tissue's fluidity and stiffness. In vivo, state‐of‐the‐art multifrequency MRE can distinguish tumors from their surrounding host tissue by their rheological fingerprints. Most importantly, a meta‐analysis on the currently available clinical studies is conducted and universal trends are identified. The results and conclusions are condensed into a gedankenexperiment about how a tumor can grow and eventually metastasize into its environment from a physics perspective to deduce corresponding mechanical properties. Based on stiffness, fluidity, spatial heterogeneity, and texture of the tumor front a roadmap for a prognosis of a tumor's aggressiveness and metastatic potential is presented. |
| first_indexed | 2024-03-12T00:37:21Z |
| format | Article |
| id | doaj.art-9d29f8eccd8d41b8a1a12887ee8343b9 |
| institution | Directory Open Access Journal |
| issn | 2198-3844 |
| language | English |
| last_indexed | 2024-03-12T00:37:21Z |
| publishDate | 2023-09-01 |
| publisher | Wiley |
| record_format | Article |
| series | Advanced Science |
| spelling | doaj.art-9d29f8eccd8d41b8a1a12887ee8343b92023-09-15T09:29:00ZengWileyAdvanced Science2198-38442023-09-011026n/an/a10.1002/advs.202303523Changes in Tissue Fluidity Predict Tumor Aggressiveness In VivoFrank Sauer0Steffen Grosser1Mehrgan Shahryari2Alexander Hayn3Jing Guo4Jürgen Braun5Susanne Briest6Benjamin Wolf7Bahriye Aktas8Lars‐Christian Horn9Ingolf Sack10Josef A. Käs11Soft Matter Physics Division Peter‐Debye‐Institute for Soft Matter Physics 04103 Leipzig GermanySoft Matter Physics Division Peter‐Debye‐Institute for Soft Matter Physics 04103 Leipzig GermanyDepartment of Radiology Charité‐Universitätsmedizin 10117 Berlin GermanyDepartment of Hepatology Leipzig University Hospital 04103 Leipzig GermanyDepartment of Radiology Charité‐Universitätsmedizin 10117 Berlin GermanyInstitute of Medical Informatics Charité‐Universitätsmedizin 10117 Berlin GermanyDepartment of Gynecology Leipzig University Hospital 04103 Leipzig GermanyDepartment of Gynecology Leipzig University Hospital 04103 Leipzig GermanyDepartment of Gynecology Leipzig University Hospital 04103 Leipzig GermanyDivision of Breast, Urogenital and Perinatal Pathology Leipzig University Hospital 04103 Leipzig GermanyDepartment of Radiology Charité‐Universitätsmedizin 10117 Berlin GermanySoft Matter Physics Division Peter‐Debye‐Institute for Soft Matter Physics 04103 Leipzig GermanyAbstract Cancer progression is caused by genetic changes and associated with various alterations in cell properties, which also affect a tumor's mechanical state. While an increased stiffness has been well known for long for solid tumors, it has limited prognostic power. It is hypothesized that cancer progression is accompanied by tissue fluidization, where portions of the tissue can change position across different length scales. Supported by tabletop magnetic resonance elastography (MRE) on stroma mimicking collagen gels and microscopic analysis of live cells inside patient derived tumor explants, an overview is provided of how cancer associated mechanisms, including cellular unjamming, proliferation, microenvironment composition, and remodeling can alter a tissue's fluidity and stiffness. In vivo, state‐of‐the‐art multifrequency MRE can distinguish tumors from their surrounding host tissue by their rheological fingerprints. Most importantly, a meta‐analysis on the currently available clinical studies is conducted and universal trends are identified. The results and conclusions are condensed into a gedankenexperiment about how a tumor can grow and eventually metastasize into its environment from a physics perspective to deduce corresponding mechanical properties. Based on stiffness, fluidity, spatial heterogeneity, and texture of the tumor front a roadmap for a prognosis of a tumor's aggressiveness and metastatic potential is presented.https://doi.org/10.1002/advs.202303523cancerin vivo magnetic resonance elastographymedical imagingtissue fluiditytumor mechanics |
| spellingShingle | Frank Sauer Steffen Grosser Mehrgan Shahryari Alexander Hayn Jing Guo Jürgen Braun Susanne Briest Benjamin Wolf Bahriye Aktas Lars‐Christian Horn Ingolf Sack Josef A. Käs Changes in Tissue Fluidity Predict Tumor Aggressiveness In Vivo Advanced Science cancer in vivo magnetic resonance elastography medical imaging tissue fluidity tumor mechanics |
| title | Changes in Tissue Fluidity Predict Tumor Aggressiveness In Vivo |
| title_full | Changes in Tissue Fluidity Predict Tumor Aggressiveness In Vivo |
| title_fullStr | Changes in Tissue Fluidity Predict Tumor Aggressiveness In Vivo |
| title_full_unstemmed | Changes in Tissue Fluidity Predict Tumor Aggressiveness In Vivo |
| title_short | Changes in Tissue Fluidity Predict Tumor Aggressiveness In Vivo |
| title_sort | changes in tissue fluidity predict tumor aggressiveness in vivo |
| topic | cancer in vivo magnetic resonance elastography medical imaging tissue fluidity tumor mechanics |
| url | https://doi.org/10.1002/advs.202303523 |
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