The Revolution in Breast Cancer Diagnostics: From Visual Inspection of Histopathology Slides to Using Desktop Tissue Analysers for Automated Nanomechanical Profiling of Tumours
Abstract
:1. The Need for Improved Breast Cancer Diagnosis
2. Histopathological Examination of Breast Cancer
3. Using the Standardised BI-RADS Scoring System
4. High-Resolution IT-AFM Has Great Potential for Deciphering Biological Mechanisms
5. IT-AFM Will Allow High-Precision Nanomechanical Evaluation Tools to Be Developed
6. Using Genetic Analysis of Tissue Samples to Identify Breast Cancer in the Clinic
7. Breast Cancer Therapies and Open Research Questions
8. Development of Fast IT-AFM for Clinical Tissue Diagnosis
9. Developing Desktop Tissue Analysers (DTAs) to Generate Time-Resolved Databases (Movies) of Cancer Disease Progression for Automated Cancer Diagnosis
10. Single-Cell Mechanical Testing May Not be Very Effective for Cancer Diagnosis
11. The Development of High-Speed Atomic Force Microscopy (HS-AFM)
12. Which Modes of Operation Are Suitable for Fast IT-AFM?
13. Contact Mode
14. Non-Contact Mode and Intermittent Contact Modes
15. Force–Spectroscopy and Force–Volume Mode
16. Tip Length and Geometry
17. Fabrication of a Fast IT-AFM Sensor for the DTA
18. Outlook
- IT-AFM tests are available within 10 min;
- No pathology report is needed which saves the cost of labour;
- Unlike MRI, CT, and mammography, the AFM can perform nanomechanical functional profiling, which may result in more detailed information and better treatment outcomes;
- IT-AFM analysis may aid breast cancer subtyping;
- IT-AFM could enhance the understanding of cancer aggressiveness and treatment response;
- The same high-quality tests can be performed by the DTAs in all parts of the world;
- Nanostiffness data are digital and stored in databases;
- The databases can be used to optimise treatment modalities;
- Developing cancer prevention can also benefit from the databases.
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- WHO. Fact Sheet. Available online: https://www.who.int/news-room/fact-sheets/detail/cancer (accessed on 20 January 2024).
- Potter, S.; Fairhurst, K.; Cowan, K.; Vincent, S.; Lewis, I.; Cutress, R.I.; Stobart, H.; Fairbrother, P.; Turner, S.; Davies-Crowley, K.; et al. Identifying research priorities in breast cancer surgery: A UK priority setting partnership with the James Lind Alliance. Breast Cancer Res. Treat. 2023, 197, 39–49. [Google Scholar] [CrossRef] [PubMed]
- Breast Cancer Now. Breast Cancer: Facts and Figures. 2023. Available online: https://breastcancernow.org/sites/default/files/breast_cancer_facts_and_figures_-_final.pdf (accessed on 20 January 2024).
- NICE. Suspected cancer: Recognition and referral. In 2021 Exceptional Surveillance of Suspected Cancer: Recognition and Referral (NICE Guideline NG12) and Suspected Neurological Conditions: Recognition and Referral (NICE Guideline NG127); NICE: London, UK, 2021. [Google Scholar]
- Cykowska, A.; Marano, L.; D’Ignazio, A.; Marrelli, D.; Swierblewski, M.; Jaskiewicz, J.; Roviello, F.; Polom, K. New technologies in breast cancer sentinel lymph node biopsy; from the current gold standard to artificial intelligence. Surg. Oncol. 2020, 34, 324–335. [Google Scholar] [CrossRef] [PubMed]
- Roque, R.; Henrique, H.; Aguiar, P. Preanalytic errors in anatomic pathology: Study of 10,574 cases from five Portuguese hospitals. Diagnosis 2015, 2, 181–188. [Google Scholar] [CrossRef] [PubMed]
- American College of Radiology. Breast Imaging Reporting & Data System (BI-RADS®). 2024. Available online: https://www.acr.org/Clinical-Resources/Reporting-and-Data-Systems/Bi-Rads (accessed on 20 January 2024).
- Sinclair, D.A.; Smith, I.R.; Wickramasinghe, H.K.; McAvoy, B.R. Elastic constants measurement in the acoustic microscope. In Ultrasonics Symposium Proceedings; IEEE: New York, NY, USA, 1982; Volume 2, p. 1090. [Google Scholar]
- Mansfield, P.; Glover, P.M. Limits to magnetic resonance microscopy. Rep. Prog. Phys. 2002, 65, 1489–1511. [Google Scholar]
- Pang, B.; Ta, D.; Liu, X. A super-resolution ultrasound imaging method based on active-modulated super-resolution optical fluctuation imaging. Annu. Int. Conf. IEEE Eng. Med. Biol. Soc. 2023, 2023, 1–4. [Google Scholar] [PubMed]
- Loparic, M.; Wirz, D.; Daniels, A.U.; Raiteri, R.; Vanlandingham, M.R.; Guex, G.; Martin, I.; Aebi, U.; Stolz, M. Micro- and nanomechanical analysis of articular cartilage by indentation-type atomic force microscopy: Validation with a gel-microfiber composite. Biophys. J. 2010, 98, 2731–2740. [Google Scholar] [CrossRef] [PubMed]
- Stolz, M.; Gottardi, R.; Raiteri, R.; Miot, S.; Martin, I.; Imer, R.; Staufer, U.; Raducanu, A.; Duggelin, M.; Baschong, W.; et al. Early detection of aging cartilage and osteoarthritis in mice and patient samples using atomic force microscopy. Nat. Nanotechnol. 2009, 4, 186–192. [Google Scholar] [CrossRef]
- Stolz, M.; Raiteri, R.; Daniels, A.U.; VanLandingham, M.R.; Baschong, W.; Aebi, U. Dynamic elastic modulus of porcine articular cartilage determined at two different levels of tissue organization by indentation-type atomic force microscopy. Biophys. J. 2004, 86, 3269–3283. [Google Scholar] [CrossRef]
- Plodinec, M.; Loparic, M.; Monnier, C.A.; Obermann, E.C.; Zanetti-Dallenbach, R.; Oertle, P.; Hyotyla, J.T.; Aebi, U.; Bentires-Alj, M.; Lim, R.Y.; et al. The nanomechanical signature of breast cancer. Nat. Nanotechnol. 2012, 7, 757–765. [Google Scholar] [CrossRef]
- Tian, M.; Li, Y.; Liu, W.; Jin, L.; Jiang, X.; Wang, X.; Ding, Z.; Peng, Y.; Zhou, J.; Fan, J.; et al. The nanomechanical signature of liver cancer tissues and its molecular origin. Nanoscale 2015, 7, 12998–13010. [Google Scholar] [CrossRef]
- Horkay, F.; Basser, P.J.; Hecht, A.M.; Geissler, E. Gel-like behavior in aggrecan assemblies. J. Chem. Phys. 2008, 128, 135103. [Google Scholar] [CrossRef] [PubMed]
- Yang, L.; van der Werf, K.O.; Koopman, B.F.; Subramaniam, V.; Bennink, M.L.; Dijkstra, P.J.; Feijen, J. Micromechanical bending of single collagen fibrils using atomic force microscopy. J. Biomed. Mater. Res. A 2007, 82, 160–168. [Google Scholar] [CrossRef] [PubMed]
- FDA. Available online: http://www.fda.gov/biologicsbloodvaccines/guidancecomplianceregulatoryinformation/guidances/cellularandgenetherapy/ucm072952.htm (accessed on 20 January 2024).
- Imer, R.; Akiyama, T.; De Rooji, N.F.; Stolz, M.; Aebi, U.; Friederich, N.F.; Koenig, U.; Wirz, D.; Daniels, A.U.; Staufer, U. Development of atomic force microscope for arthroscopic knee cartilage inspection. Jpn. J. Appl. Phys. 2006, 45, 2319–2323. [Google Scholar] [CrossRef]
- Stolz, M.; Aebi, U.; Stoffler, D. Developing scanning probe-based nanodevices—Stepping out of the laboratory into the clinic. Nanomedicine 2007, 3, 53–62. [Google Scholar] [CrossRef] [PubMed]
- Evans, D.G.; Burghel, G.J.; Schlecht, H.; Harkness, E.F.; Gandhi, A.; Howell, S.J.; Howell, A.; Forde, C.; Lalloo, F.; Newman, W.G.; et al. Detection of pathogenic variants in breast cancer susceptibility genes in bilateral breast cancer. J. Med. Genet. 2023, 60, 974–979. [Google Scholar] [CrossRef] [PubMed]
- Dayan, D.; Lukac, S.; Rack, B.; Ebner, F.; Fink, V.; Leinert, E.; Veselinovic, K.; Schutze, S.; El Taie, Z.; Janni, W.; et al. Effect of histological breast cancer subtypes invasive lobular versus non-special type on survival in early intermediate-to-high-risk breast carcinoma: Results from the SUCCESS trials. Breast Cancer Res. 2023, 25, 153. [Google Scholar] [CrossRef] [PubMed]
- Kwon, M.J. Predictive biomarkers for molecularly targeted therapies and immunotherapies in breast cancer. Arch. Pharm. Res. 2022, 45, 597–617. [Google Scholar] [CrossRef] [PubMed]
- Segovia-Mendoza, M.; Romero-Garcia, S.; Lemini, C.; Prado-Garcia, H. Determining Factors in the Therapeutic Success of Checkpoint Immunotherapies against PD-L1 in Breast Cancer: A Focus on Epithelial-Mesenchymal Transition Activation. J. Immunol. Res. 2021, 2021, 6668573. [Google Scholar] [CrossRef]
- Garrido, C.; Manoogian, M.; Ghambire, D.; Lucas, S.; Karnoub, M.; Olson, M.T.; Hicks, D.G.; Tozbikian, G.; Prat, A.; Ueno, N.T.; et al. Analytical and clinical validation of PATHWAY Anti-HER-2/neu (4B5) antibody to assess HER2-low status for trastuzumab deruxtecan treatment in breast cancer. Virchows Arch. 2023, 1. [Google Scholar] [CrossRef]
- Francescatti, D.S.; Silverstein, M.J. Breast Cancer: A New Era in Management; Part IV: Surgical Management of the Breast; Springer Science & Business Media: Berlin/Heidelberg, Germany, 2014; Volume 1. [Google Scholar]
- Jhaveri, K.; Marme, F. Current and emerging treatment approaches for hormone receptor-positive/human epidermal growth factor receptor 2-negative metastatic breast cancer. Cancer Treat. Rev. 2024, 123, 102670. [Google Scholar] [CrossRef]
- Afifi, N.; Barrero, C.A. Understanding Breast Cancer Aggressiveness and Its Implications in Diagnosis and Treatment. J. Clin. Med. 2023, 12, 1375. [Google Scholar] [CrossRef] [PubMed]
- Bhattarai, S.; Saini, G.; Li, H.; Duanmu, H.; Seth, G.; Fisher, T.B.; Janssen, E.A.M.; Kiraz, U.; Kong, J.; Aneja, R. Predicting neoadjuvant treatment response in triple-negative breast cancer using machine learning. bioRxiv 2023, 14, 74. [Google Scholar] [CrossRef]
- Lan, H.R.; Chen, M.; Yao, S.Y.; Chen, J.X.; Jin, K.T. Novel immunotherapies for breast cancer: Focus on 2023 findings. Int. Immunopharmacol. 2024, 128, 111549. [Google Scholar] [CrossRef]
- Rodrigues-Ferreira, S.; Nahmias, C. Predictive biomarkers for personalized medicine in breast cancer. Cancer Lett. 2022, 545, 215828. [Google Scholar] [CrossRef] [PubMed]
- Fuksa, L.; Micuda, S.; Grim, J.; Ryska, A.; Hornychova, H. Predictive biomarkers in breast cancer: Their value in neoadjuvant chemotherapy. Cancer Investig. 2012, 30, 663–678. [Google Scholar] [CrossRef] [PubMed]
- Appleyard, R.C.; Swain, M.V.; Khanna, S.; Murrell, G.A. The accuracy and reliability of a novel handheld dynamic indentation probe for analysing articular cartilage. Phys. Med. Biol. 2001, 46, 541–550. [Google Scholar] [CrossRef] [PubMed]
- Shepherd, D.E.; Seedhom, B.B. A technique for measuring the compressive modulus of articular cartilage under physiological loading rates with preliminary results. Proc. Inst. Mech. Eng. 1997, 211, 155–165. [Google Scholar] [CrossRef] [PubMed]
- Lyyra, T.; Jurvelin, J.; Pitkanen, P.; Vaatainen, U.; Kiviranta, I. Indentation instrument for the measurement of cartilage stiffness under arthroscopic control. Med. Eng. Phys. 1995, 17, 395–399. [Google Scholar] [CrossRef]
- Aspden, R.M.; Larsson, T.; Svensson, R.; Heinegard, D. Computer-controlled mechanical testing machine for small samples of biological viscoelastic materials. J. Biomed. Eng. 1991, 13, 521–525. [Google Scholar] [CrossRef]
- Tkaczuk, H.; Norrbom, H.; Werelind, H. A cartilage elastometer for use in the living subject. J. Med. Eng. Technol. 1982, 6, 104–107. [Google Scholar] [CrossRef]
- Stolz, M. Early osteoarthritis were only detected at the nanometer scale but not at the micrometer or millimeter scale. J. Biomech. 2011, 44, 1824–1825. [Google Scholar] [CrossRef]
- Hartmann, B.; Marchi, G.; Alberton, P.; Farkas, Z.; Aszodi, A.; Roths, J.; Clausen-Schaumann, H. Early Detection of Cartilage Degeneration: A Comparison of Histology, Fiber Bragg Grating-Based Micro-Indentation, and Atomic Force Microscopy-Based Nano-Indentation. Int. J. Mol. Sci. 2020, 21, 7384. [Google Scholar] [CrossRef] [PubMed]
- Cykowska, A.; Danalache, M.; Bonnaire, F.C.; Feierabend, M.; Hofmann, U.K. Detecting early osteoarthritis through changes in biomechanical properties—A review of recent advances in indentation technologies in a clinical arthroscopic setup. J. Biomech. 2022, 132, 110955. [Google Scholar] [CrossRef] [PubMed]
- Reichlin, T.; Wild, A.; Durrenberger, M.; Daniels, A.U.; Aebi, U.; Hunziker, P.R.; Stolz, M. Investigating native coronary artery endothelium in situ and in cell culture by scanning force microscopy. J. Struct. Biol. 2005, 152, 52–63. [Google Scholar] [CrossRef] [PubMed]
- Lekka, M.; Gil, D.; Pogoda, K.; Dulinska-Litewka, J.; Jach, R.; Gostek, J.; Klymenko, O.; Prauzner-Bechcicki, S.; Stachura, Z.; Wiltowska-Zuber, J.; et al. Cancer cell detection in tissue sections using AFM. Arch. Biochem. Biophys. 2012, 518, 151–156. [Google Scholar] [CrossRef] [PubMed]
- Lekka, M.; Laidler, P.; Gil, D.; Lekki, J.; Stachura, Z.; Hrynkiewicz, A.Z. Elasticity of normal and cancerous human bladder cells studied by scanning force microscopy. Eur. Biophys. J. 1999, 28, 312–316. [Google Scholar] [CrossRef] [PubMed]
- Zemla, J.; Danilkiewicz, J.; Orzechowska, B.; Pabijan, J.; Seweryn, S.; Lekka, M. Atomic force microscopy as a tool for assessing the cellular elasticity and adhesiveness to identify cancer cells and tissues. Semin. Cell Dev. Biol. 2018, 73, 115–124. [Google Scholar] [CrossRef]
- Kaul-Ghanekar, R.; Singh, S.; Mamgain, H.; Jalota-Badhwar, A.; Paknikar, K.M.; Chattopadhyay, S. Tumor suppressor protein SMAR1 modulates the roughness of cell surface: Combined AFM and SEM study. BMC Cancer 2009, 9, 350. [Google Scholar] [CrossRef]
- Chen, W.; Brandes, Z.; Roy, R.; Chekmareva, M.; Pandya, H.J.; Desai, J.P.; Foran, D.J. Robot-Guided Atomic Force Microscopy for Mechano-Visual Phenotyping of Cancer Specimens. Microsc. Microanal. 2015, 21, 1224–1235. [Google Scholar] [CrossRef]
- Maller, O.; Hansen, K.C.; Lyons, T.R.; Acerbi, I.; Weaver, V.M.; Prekeris, R.; Tan, A.C.; Schedin, P. Collagen architecture in pregnancy-induced protection from breast cancer. J. Cell Sci. 2013, 126, 4108–4120. [Google Scholar] [CrossRef]
- Cross, S.E.; Jin, Y.S.; Rao, J.; Gimzewski, J.K. Nanomechanical analysis of cells from cancer patients. Nat. Nanotechnol. 2007, 2, 780–783. [Google Scholar] [CrossRef]
- Kwon, T.; Gunasekaran, S.; Eom, K. Atomic force microscopy-based cancer diagnosis by detecting cancer-specific biomolecules and cells. Biochim. Biophys. Acta Rev. Cancer 2019, 1871, 367–378. [Google Scholar] [CrossRef] [PubMed]
- Gaikwad, R.M.; Dokukin, M.E.; Iyer, K.S.; Woodworth, C.D.; Volkov, D.O.; Sokolov, I. Detection of cancerous cervical cells using physical adhesion of fluorescent silica particles and centripetal force. Analyst 2011, 136, 1502–1506. [Google Scholar] [CrossRef] [PubMed]
- Guz, N.V.; Dokukin, M.E.; Woodworth, C.D.; Cardin, A.; Sokolov, I. Towards early detection of cervical cancer: Fractal dimension of AFM images of human cervical epithelial cells at different stages of progression to cancer. Nanomedicine 2015, 11, 1667–1675. [Google Scholar] [CrossRef] [PubMed]
- Guz, N.V.; Patel, S.J.; Dokukin, M.E.; Clarkson, B.; Sokolov, I. Biophysical differences between chronic myelogenous leukemic quiescent and proliferating stem/progenitor cells. Nanomedicine 2016, 12, 2429–2437. [Google Scholar] [CrossRef] [PubMed]
- Petrov, M.; Sokolov, I. Machine Learning Allows for Distinguishing Precancerous and Cancerous Human Epithelial Cervical Cells Using High-Resolution AFM Imaging of Adhesion Maps. Cells 2023, 12, 2536. [Google Scholar] [CrossRef] [PubMed]
- Petrov, M.; Sokolov, I. Identification of Geometrical Features of Cell Surface Responsible for Cancer Aggressiveness: Machine Learning Analysis of Atomic Force Microscopy Images of Human Colorectal Epithelial Cells. Biomedicines 2023, 11, 191. [Google Scholar] [CrossRef] [PubMed]
- Sokolov, I.; Dokukin, M.E.; Kalaparthi, V.; Miljkovic, M.; Wang, A.; Seigne, J.D.; Grivas, P.; Demidenko, E. Noninvasive diagnostic imaging using machine-learning analysis of nanoresolution images of cell surfaces: Detection of bladder cancer. Proc. Natl. Acad. Sci. USA 2018, 115, 12920–12925. [Google Scholar] [CrossRef]
- Zambito, M.; Viti, F.; Bosio, A.G.; Ceccherini, I.; Florio, T.; Vassalli, M. The Impact of Experimental Conditions on Cell Mechanics as Measured with Nanoindentation. Nanomaterials 2023, 13, 1190. [Google Scholar] [CrossRef]
- Berardi, M.; Gnanachandran, K.; Jiang, J.; Bielawski, K.; Visser, C.W.; Lekka, M.; Akca, B.I. Dynamic mechanical analysis of suspended soft bodies via hydraulic force spectroscopy. Soft Matter 2023, 19, 615–624. [Google Scholar] [CrossRef]
- Stolz, M.; Seidel, J.; Martin, I.; Raiteri, R.; Aebi, U.; Baschong, W. Ex vivo measurement of the elasticity of extracellular matrix constituents by atomic force microscopy (AFM). Mol. Biol. Cell 1999, 10, 145a. [Google Scholar]
- Grad, S.; Loparic, M.; Peter, R.; Stolz, M.; Aebi, U.; Alini, M. Sliding motion modulates stiffness and friction coefficient at the surface of tissue engineered cartilage. Osteoarthr. Cartil. 2012, 20, 288–295. [Google Scholar] [CrossRef] [PubMed]
- Pang, X.C.; Sun, P.; Tan, Z.J.; Lin, L.J.; Tang, B. Effect of calcium ions on the nanostiffness of articular cartilage. Mater Lett. 2016, 180, 332–335. [Google Scholar] [CrossRef]
- Bouchonville, N.; Nicolas, A. Quantification of the Elastic Properties of Soft and Sticky Materials Using AFM. At. Force Microsc. Methods Protoc. 2019, 1886, 281–290. [Google Scholar]
- Muschter, D.; Fleischhauer, L.; Taheri, S.; Schilling, A.F.; Clausen-Schaumann, H.; Grässel, S. Sensory neuropeptides are required for bone and cartilage homeostasis in a murine destabilization-induced osteoarthritis model. Bone 2020, 133, 115181. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.M.; Guo, Y.; Zhou, Y.; Zhu, H.R.; Wu, P.Y.; Wang, K.; Ruan, L.T.; Wan, M.X.; Insana, M.F. Fluidity and elasticity form a concise set of viscoelastic biomarkers for breast cancer diagnosis based on Kelvin-Voigt fractional derivative modeling. Biomech. Model. Mechanobiol. 2020, 19, 2163–2177. [Google Scholar] [CrossRef] [PubMed]
- Fleischhauer, L.; Muschter, D.; Farkas, Z.; Graessel, S.; Aszodi, A.; Clausen-Schaumann, H.; Alberton, P. Nano-Scale Mechanical Properties of the Articular Cartilage Zones in a Mouse Model of Post-Traumatic Osteoarthritis. Appl. Sci. 2022, 12, 2596. [Google Scholar] [CrossRef]
- Rellmann, Y.; Eidhof, E.; Hansen, U.; Fleischhauer, L.; Vogel, J.; Clausen-Schaumann, H.; Aszodi, A.; Dreier, R. ER Stress in ERp57 Knockout Knee Joint Chondrocytes Induces Osteoarthritic Cartilage Degradation and Osteophyte Formation. Int. J. Mol. Sci. 2022, 23, 182. [Google Scholar] [CrossRef]
- Lekka, M.; Laidler, P. Applicability of AFM in cancer detection. Nat. Nanotechnol. 2009, 4, 72. [Google Scholar] [CrossRef]
- Lee, G.Y.; Lim, C.T. Biomechanics approaches to studying human diseases. Trends Biotechnol. 2007, 25, 111–118. [Google Scholar] [CrossRef]
- Ochalek, T.; Nordt, F.J.; Tullberg, K.; Burger, M.M. Correlation between cell deformability and metastatic potential in B16-F1 melanoma cell variants. Cancer Res. 1988, 48, 5124–5128. [Google Scholar] [PubMed]
- Cross, S.E.; Jin, Y.S.; Tondre, J.; Wong, R.; Rao, J.; Gimzewski, J.K. AFM-based analysis of human metastatic cancer cells. Nanotechnology 2008, 19, 384003. [Google Scholar] [CrossRef] [PubMed]
- Guck, J.; Ananthakrishnan, R.; Mahmood, H.; Moon, T.J.; Cunningham, C.C.; Kas, J. The optical stretcher: A novel laser tool to micromanipulate cells. Biophys. J. 2001, 81, 767–784. [Google Scholar] [CrossRef]
- Lincoln, B.; Wottawah, F.; Schinkinger, S.; Ebert, S.; Guck, J. High-throughput rheological measurements with an optical stretcher. Methods Cell Biol. 2007, 83, 397–423. [Google Scholar] [PubMed]
- Ando, T. High-speed AFM imaging. Curr. Opin. Struct. Biol. 2014, 28, 63–68. [Google Scholar] [CrossRef] [PubMed]
- Ando, T.; Kodera, N.; Naito, Y.; Kinoshita, T.; Furuta, K.; Toyoshima, Y.Y. A high-speed atomic force microscope for studying biological macromolecules in action. ChemPhysChem 2003, 4, 1196–1202. [Google Scholar] [CrossRef] [PubMed]
- Ando, T.; Uchihashi, T.; Scheuring, S. Filming biomolecular processes by high-speed atomic force microscopy. Chem. Rev. 2014, 114, 3120–3188. [Google Scholar] [CrossRef]
- Disseldorp, E.C.M.; Tabak, F.C.; Katan, A.J.; Hesselberth, M.B.S.; Oosterkamp, T.H.; Frenken, J.W.M.; van Spengen, W.M. MEMS-based high speed scanning probe microscopy. Rev. Sci. Instrum. 2010, 81, 043702. [Google Scholar] [CrossRef]
- Tabak, F.C.; Disseldorp, E.C.M.; Wortel, G.H.; Katan, A.J.; Hesselberth, M.B.S.; Oosterkamp, T.H.; Frenken, J.W.M.; van Spengen, W.M. MEMS-based fast scanning probe microscopes. Ultramicroscopy 2010, 110, 599–604. [Google Scholar] [CrossRef]
- Rogers, B.; Sulchek, T.; Murray, K.; York, D.; Jones, M.; Manning, L.; Malekos, S.; Beneschott, B.; Adams, J.D.; Cavazos, H.; et al. High speed tapping mode atomic force microscopy in liquid using an insulated piezoelectric cantilever. Rev. Sci. Instrum. 2003, 74, 4683–4686. [Google Scholar] [CrossRef]
- Fukuda, S.; Ando, T. Faster high-speed atomic force microscopy for imaging of biomolecular processes. Rev. Sci. Instrum. 2021, 92, 033705. [Google Scholar] [CrossRef] [PubMed]
- Fukuda, S.; Yamamoto, R.; Yanagisawa, N.; Takaya, N.; Sato, Y.; Riquelme, M.; Takeshita, N. Trade-off between Plasticity and Velocity in Mycelial Growth. mBio 2021, 12, 10–128. [Google Scholar] [CrossRef] [PubMed]
- Meyer, E.; Guggisberg, M.; Loppacher, C.; Battiston, F.; Gyalog, T.; Bammerlin, M.; Bennewitz, R.; Lü, J.; Lehmann, T.; Baratoff, A.; et al. New developments in scanning probe microscopy. NATO Sci. Ser. E App. 1999, 364, 339–357. [Google Scholar]
- Martin, Y.; Williams, C.C.; Wickramasinghe, H.K. Atomic Force Microscope Force Mapping and Profiling on a Sub 100-a Scale. J. Appl. Phys. 1987, 61, 4723–4729. [Google Scholar] [CrossRef]
- Radmacher, M.; Cleveland, J.P.; Fritz, M.; Hansma, H.G.; Hansma, P.K. Mapping interaction forces with the atomic force microscope. Biophys. J. 1994, 66, 2159–2165. [Google Scholar] [CrossRef] [PubMed]
- Hu, S.Q.; Mininni, L.; Hu, Y.; Erina, N.; Kindt, J.; Su, C.M. High-Speed Atomic Force Microscopy and Peak Force Tapping Control. In Metrology, Inspection, and Process Control for Microlithography XXVI, Pts 1 and 2; SPIE Press: St. Bellingham, WA, USA, 2012; Volume 8324. [Google Scholar]
- Yamanaka, K.; Maruyama, Y.; Tsuji, T.; Nakamoto, K. Resonance frequency and Q factor mapping by ultrasonic atomic force microscopy. Appl. Phys. Lett. 2001, 78, 1939–1941. [Google Scholar] [CrossRef]
- Marti, O.; Hild, S.; Staud, J.; Rosa, A.; Zink, B. Nanomechanical interactions of scanning force microscope tips with polymer surfaces. Micro/Nanotribol. Its Appl. 1997, 330, 455–465. [Google Scholar]
- Marti, O.; Holzwarth, M.; Beil, M. Measuring the nanomechanical properties of cancer cells by digital pulsed force mode imaging. Nanotechnology 2008, 19, 384015. [Google Scholar] [CrossRef]
- Adamcik, J.; Berquand, A.; Mezzenga, R. Single-step direct measurement of amyloid fibrils stiffness by peak force quantitative nanomechanical atomic force microscopy. Appl. Phys. Lett. 2011, 98, 193701. [Google Scholar] [CrossRef]
- Dokukin, M.E.; Sokolov, I. Quantitative Mapping of the Elastic Modulus of Soft Materials with HarmoniX and Peak Force QNM AFM Modes. Langmuir 2012, 28, 16060–16071. [Google Scholar] [CrossRef]
- Aeschimann, L.; Akiyama, T.; Staufer, U.; De Rooij, N.F.; Thiery, L.; Eckert, R.; Heinzelmann, H. Characterization and fabrication of fully metal-coated scanning near-field optical microscopy SiO tips. J. Microsc. 2003, 209, 182–187. [Google Scholar] [CrossRef] [PubMed]
- Zenhausern, F.; Adrian, M.; Tenheggelerbordier, B.; Ardizzoni, F.; Descouts, P. Enhanced Imaging of Biomolecules with Electron-Beam Deposited Tips for Scanning Force Microscopy. J. Appl. Phys. 1993, 73, 7232–7237. [Google Scholar] [CrossRef]
- Tang, B.; Sato, K.; Tanaka, H.; Gosalvez, M.A. Fabrication of Sharp Tips with High Aspect Ratio by Surfactant-Modified Wet Etching for the Afm Probe. In Proceedings of the 2011 IEEE 24th International Conference on Micro Electro Mechanical Systems, Cancun, Mexico, 23–27 January 2011; pp. 328–331. [Google Scholar]
- Paneru, G.; Thapa, P.S.; McBride, S.P.; Ramm, A.; Law, B.M.; Flanders, B.N. Long reach cantilevers for sub-cellular force measurements. Nanotechnology 2012, 23, 455105. [Google Scholar] [CrossRef] [PubMed]
- Beard, J.D.; Gordeev, S.N. Fabrication and buckling dynamics of nanoneedle AFM probes. Nanotechnology 2011, 22, 175303. [Google Scholar] [CrossRef] [PubMed]
- Dremov, V.; Fedoseev, V.; Fedorov, P.; Grebenko, A. Fast and reliable method of conductive carbon nanotube-probe fabrication for scanning probe microscopy. Rev. Sci. Instrum. 2015, 86, 053703. [Google Scholar] [CrossRef] [PubMed]
- Grech, D.; Kiang, K.S.; Zekonyte, J.; Stolz, M.; Wood, R.J.K.; Chong, H.M.H. Highly linear and large spring deflection characteristics of a Quasi-Concertina MEMS device. Microelectron. Eng. 2014, 119, 75–78. [Google Scholar] [CrossRef]
- Su, Y.; Evans, A.G.R.; Brunnschweiler, A.; Ensell, G.; Koch, M. Fabrication of improved piezoresistive silicon cantilever probes for the atomic force microscope. Sens. Actuators A Phys. 1997, 60, 163–167. [Google Scholar] [CrossRef]
- Linnemann, R.; Gotszalk, T.; Hadjiiski, L.; Rangelow, I.W. Characterization of a Cantilever with an Integrated Deflection Sensor. Thin Solid Film 1995, 264, 159–164. [Google Scholar] [CrossRef]
- Linnemann, R.; Gotszalk, T.; Rangelow, I.W.; Dumania, P.; Oesterschulze, E. Atomic force microscopy and lateral force microscopy using piezoresistive cantilevers. J. Vac. Sci. Technol. B 1996, 14, 856–860. [Google Scholar] [CrossRef]
- Thaysen, J.; Boisen, A.; Hansen, O.; Bouwstra, S. Atomic force microscopy probe with piezoresistive read-out and a highly symmetrical Wheatstone bridge arrangement. Sens. Actuators A Phys. 2000, 83, 47–53. [Google Scholar] [CrossRef]
- IBM. IBM’s ‘Millipede’ Project Demonstrates Trillion-Bit Data Storage Density. 2013. Available online: https://www.azonano.com/article.aspx?ArticleID=872 (accessed on 20 January 2024).
- Vettiger, P.; Despont, M.; Drechsler, U.; Duering, U.; Haeberle, W.; Lutwyche, M.; Rothuizen, H.; Stutz, R.; Widmer, R.; Binnig, G. The “Millipede”—More than one thousand tips for the future AFM data storage. IBM J. Res. Dev. 2000, 44, 323–340. [Google Scholar] [CrossRef]
Authors | Tissue | Comment |
---|---|---|
Stolz et al. [58] (1999) | Porcine articular cartilage | First time showing the scale dependency of IT-AFM measurements |
Stolz et al. [13] (2004) | Porcine articular cartilage | Demonstrates the scale dependency when assessing tissues |
Stolz et al. [12] (2009) | Mouse articular cartilage Human articular cartilage | Osteoarthritis and ageing in mice deficient in type IX collagen, cartilage stiffness of osteoarthritic patients |
Loparic et al. [11] (2010) | Porcine articular cartilage | Alterations of the nanostiffness profile of articular cartilage by varying the ionic strength of the PBS bathing solution |
Grad et al. [59] (2012) | Engineered cartilage | Quality of engineered cartilage |
Plodinec et al. [14] (2012) | Breast tumours | Nanomechanical signatures of breast cancer |
Tian et al. [15] (2015) | Human liver | Nanomechanical signatures of liver cancer |
Pang et al. [60] (2016) | Human articular cartilage | Effect of calcium ions on the nanostiffness of articular cartilage |
Bouchonville et al. [61] (2019) | Soft and sticky materials | Technical paper on force curve analysis |
Hartman et al. [39] (2020) | Human articular cartilage | Early detection of osteoarthritis |
Muschter et al. [62] (2020) | Mouse articular cartilage | Mechanically induced osteoarthritis model |
Zhang et al. [63] (2020) | Breast cancer | Modeling force curves |
Fleischhauer et al. [64] (2022) | Mouse articular cartilage | Mechanically induced osteoarthritis |
Rellmann [65] (2022) | ERp57 KO mice | Osteoarthritis |
Conventional AFM DNP-S (D) | HS-AFM BL-AC10DS | |
---|---|---|
Cantilever type | Long cantilevers | Short cantilevers |
Shape | V-shaped | Beam shaped |
Length | 205 μm | 9–10 μm |
Width | 25 μm | 2 μm |
Thickness | 5 μm | 130 nm |
Spring constant | k = 0.06 N/m | K = 0.1 N/m |
Resonance frequency | f = 18 kHz | f = 1.2 MHz |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Stolz, M. The Revolution in Breast Cancer Diagnostics: From Visual Inspection of Histopathology Slides to Using Desktop Tissue Analysers for Automated Nanomechanical Profiling of Tumours. Bioengineering 2024, 11, 237. https://doi.org/10.3390/bioengineering11030237
Stolz M. The Revolution in Breast Cancer Diagnostics: From Visual Inspection of Histopathology Slides to Using Desktop Tissue Analysers for Automated Nanomechanical Profiling of Tumours. Bioengineering. 2024; 11(3):237. https://doi.org/10.3390/bioengineering11030237
Chicago/Turabian StyleStolz, Martin. 2024. "The Revolution in Breast Cancer Diagnostics: From Visual Inspection of Histopathology Slides to Using Desktop Tissue Analysers for Automated Nanomechanical Profiling of Tumours" Bioengineering 11, no. 3: 237. https://doi.org/10.3390/bioengineering11030237
APA StyleStolz, M. (2024). The Revolution in Breast Cancer Diagnostics: From Visual Inspection of Histopathology Slides to Using Desktop Tissue Analysers for Automated Nanomechanical Profiling of Tumours. Bioengineering, 11(3), 237. https://doi.org/10.3390/bioengineering11030237