{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,20]],"date-time":"2026-07-20T14:14:10Z","timestamp":1784556850928,"version":"3.55.0"},"reference-count":67,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2019,8,23]],"date-time":"2019-08-23T00:00:00Z","timestamp":1566518400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002347","name":"Bundesministerium f\u00fcr Bildung und Forschung","doi-asserted-by":"publisher","award":["03Z22DN11"],"award-info":[{"award-number":["03Z22DN11"]}],"id":[{"id":"10.13039\/501100002347","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cancers"],"abstract":"<jats:p>Cold physical plasma has limited tumor growth in many preclinical models and is, therefore, suggested as a putative therapeutic option against cancer. Yet, studies investigating the cells\u2019 metastatic behavior following plasma treatment are scarce, although being of prime importance to evaluate the safety of this technology. Therefore, we investigated four human pancreatic cancer cell lines for their metastatic behavior in vitro and in chicken embryos (in ovo). Pancreatic cancer was chosen as it is particularly metastatic to the peritoneum and systemically, which is most predictive for outcome. In vitro, treatment with the kINPen plasma jet reduced pancreatic cancer cell activity and viability, along with unchanged or decreased motility. Additionally, the expression of adhesion markers relevant for metastasis was down-regulated, except for increased CD49d. Analysis of 3D tumor spheroid outgrowth showed a lack of plasma-spurred metastatic behavior. Finally, analysis of tumor tissue grown on chicken embryos validated the absence of an increase of metabolically active cells physically or chemically detached with plasma treatment. We conclude that plasma treatment is a safe and promising therapeutic option and that it does not promote metastatic behavior in pancreatic cancer cells in vitro and in ovo.<\/jats:p>","DOI":"10.3390\/cancers11091237","type":"journal-article","created":{"date-parts":[[2019,8,26]],"date-time":"2019-08-26T04:38:23Z","timestamp":1566794303000},"page":"1237","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":48,"title":["Risk Assessment of kINPen Plasma Treatment of Four Human Pancreatic Cancer Cell Lines with Respect to Metastasis"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8773-8862","authenticated-orcid":false,"given":"Sander","family":"Bekeschus","sequence":"first","affiliation":[{"name":"ZIK plasmatis, Leibniz Institute for Plasma Science and Technology (INP Greifswald), Felix-Hausdorff-Str. 2, 17489 Greifswald, Germany"},{"name":"National Centre for Plasma Medicine (NZPM), Langenbeck-Virchow-Haus, Luisenstr. 58\/59, 10117 Berlin, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2950-0984","authenticated-orcid":false,"given":"Eric","family":"Freund","sequence":"additional","affiliation":[{"name":"ZIK plasmatis, Leibniz Institute for Plasma Science and Technology (INP Greifswald), Felix-Hausdorff-Str. 2, 17489 Greifswald, Germany"},{"name":"Department of General, Visceral, Thoracic, and Vascular Surgery, Greifswald University Medical Center, Ferdinand-Sauerbruch-Str., 17475 Greifswald, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chiara","family":"Spadola","sequence":"additional","affiliation":[{"name":"ZIK plasmatis, Leibniz Institute for Plasma Science and Technology (INP Greifswald), Felix-Hausdorff-Str. 2, 17489 Greifswald, Germany"},{"name":"Department of General, Visceral, Thoracic, and Vascular Surgery, Greifswald University Medical Center, Ferdinand-Sauerbruch-Str., 17475 Greifswald, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5616-8182","authenticated-orcid":false,"given":"Angela","family":"Privat-Maldonado","sequence":"additional","affiliation":[{"name":"PLASMANT, Chemistry Department, University of Antwerp, 2610 Antwerp, Belgium"},{"name":"Solid Tumor Immunology Group, Center for Oncological Research, University of Antwerp, 2610 Antwerp, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christine","family":"Hackbarth","sequence":"additional","affiliation":[{"name":"Department of General, Visceral, Thoracic, and Vascular Surgery, Greifswald University Medical Center, Ferdinand-Sauerbruch-Str., 17475 Greifswald, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9875-6460","authenticated-orcid":false,"given":"Annemie","family":"Bogaerts","sequence":"additional","affiliation":[{"name":"PLASMANT, Chemistry Department, University of Antwerp, 2610 Antwerp, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6488-3904","authenticated-orcid":false,"given":"Anke","family":"Schmidt","sequence":"additional","affiliation":[{"name":"ZIK plasmatis, Leibniz Institute for Plasma Science and Technology (INP Greifswald), Felix-Hausdorff-Str. 2, 17489 Greifswald, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kristian","family":"Wende","sequence":"additional","affiliation":[{"name":"ZIK plasmatis, Leibniz Institute for Plasma Science and Technology (INP Greifswald), Felix-Hausdorff-Str. 2, 17489 Greifswald, Germany"},{"name":"National Centre for Plasma Medicine (NZPM), Langenbeck-Virchow-Haus, Luisenstr. 58\/59, 10117 Berlin, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4161-205X","authenticated-orcid":false,"given":"Klaus-Dieter","family":"Weltmann","sequence":"additional","affiliation":[{"name":"ZIK plasmatis, Leibniz Institute for Plasma Science and Technology (INP Greifswald), Felix-Hausdorff-Str. 2, 17489 Greifswald, Germany"},{"name":"National Centre for Plasma Medicine (NZPM), Langenbeck-Virchow-Haus, Luisenstr. 58\/59, 10117 Berlin, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1097-4832","authenticated-orcid":false,"given":"Thomas","family":"von Woedtke","sequence":"additional","affiliation":[{"name":"ZIK plasmatis, Leibniz Institute for Plasma Science and Technology (INP Greifswald), Felix-Hausdorff-Str. 2, 17489 Greifswald, Germany"},{"name":"National Centre for Plasma Medicine (NZPM), Langenbeck-Virchow-Haus, Luisenstr. 58\/59, 10117 Berlin, Germany"},{"name":"Institute for Hygiene and Environmental Medicine, Greifswald University Medical Center, Walther-Rathenau-Str. 48, 17489 Greifswald, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Claus-Dieter","family":"Heidecke","sequence":"additional","affiliation":[{"name":"Department of General, Visceral, Thoracic, and Vascular Surgery, Greifswald University Medical Center, Ferdinand-Sauerbruch-Str., 17475 Greifswald, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lars-Ivo","family":"Partecke","sequence":"additional","affiliation":[{"name":"Department of General, Visceral, Thoracic, and Vascular Surgery, Greifswald University Medical Center, Ferdinand-Sauerbruch-Str., 17475 Greifswald, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1989-8784","authenticated-orcid":false,"given":"Andr\u00e9","family":"K\u00e4ding","sequence":"additional","affiliation":[{"name":"Department of General, Visceral, Thoracic, and Vascular Surgery, Greifswald University Medical Center, Ferdinand-Sauerbruch-Str., 17475 Greifswald, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,8,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"87","DOI":"10.3322\/caac.21262","article-title":"Global Cancer Statistics, 2012","volume":"65","author":"Torre","year":"2015","journal-title":"CA Cancer J. Clin."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.drup.2009.12.001","article-title":"Evading Tumor Evasion: Current Concepts and Perspectives of Anti-angiogenic Cancer Therapy","volume":"13","author":"Abdollahi","year":"2010","journal-title":"Drug. Resist. Updat."},{"key":"ref_3","first-page":"29","article-title":"Beyond Checkpoint Inhibition\u2014Immunotherapeutical Strategies in Combination with Radiation","volume":"2","author":"Eckert","year":"2017","journal-title":"Clin. Transl. Radiat. Oncol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"83155","DOI":"10.18632\/oncotarget.17950","article-title":"HDAC Inhibitors Enhance the Immunotherapy Response of Melanoma Cells","volume":"8","author":"Booth","year":"2017","journal-title":"Oncotarget"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"24932","DOI":"10.18632\/oncotarget.15326","article-title":"The tlr7 Agonist Imiquimod Induces Anti-cancer Effects Via Autophagic Cell Death and Enhances Anti-tumoral and Systemic Immunity during Radiotherapy for Melanoma","volume":"8","author":"Cho","year":"2017","journal-title":"Oncotarget"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"16686","DOI":"10.1021\/jacs.6b09538","article-title":"Photodynamic Therapy Mediated by Nontoxic Core-shell Nanoparticles Synergizes with Immune Checkpoint Blockade to Elicit Antitumor Immunity and Antimetastatic Effect on Breast Cancer","volume":"138","author":"Duan","year":"2016","journal-title":"J. Am. Chem. Soc."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"e28131","DOI":"10.4161\/onci.28131","article-title":"Electrochemotherapy with Bleomycin Induces Hallmarks of Immunogenic Cell Death in Murine Colon Cancer Cells","volume":"3","author":"Calvet","year":"2014","journal-title":"Oncoimmunology"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1802062","DOI":"10.1002\/advs.201802062","article-title":"Non-thermal Plasma as a Unique Delivery System of Short-lived Reactive Oxygen and Nitrogen Species for Immunogenic Cell Death in Melanoma Cells","volume":"6","author":"Lin","year":"2019","journal-title":"Adv. Sci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"582","DOI":"10.1111\/exd.12201","article-title":"Comparison between Cold Plasma, Electrochemotherapy and Combined Therapy in a Melanoma Mouse Model","volume":"22","author":"Daeschlein","year":"2013","journal-title":"Exp. Dermatol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2185","DOI":"10.1002\/ijc.26252","article-title":"ROS Implication in a New Antitumor Strategy Based on Non-thermal Plasma","volume":"130","author":"Vandamme","year":"2012","journal-title":"Int. J. Cancer"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"014031","DOI":"10.1088\/0741-3335\/59\/1\/014031","article-title":"Plasma Medicine\u2014Current State of Research and Medical Application","volume":"59","author":"Weltmann","year":"2017","journal-title":"Plasma Phys. Controlled Fusion"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1517","DOI":"10.1002\/ijc.28323","article-title":"Effect of Atmospheric Gas Plasmas on Cancer Cell Signaling","volume":"134","author":"Ishaq","year":"2014","journal-title":"Int. J. Cancer"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Koritzer, J., Boxhammer, V., Schafer, A., Shimizu, T., Klampfl, T.G., Li, Y.F., Welz, C., Schwenk-Zieger, S., Morfill, G.E., and Zimmermann, J.L. (2013). Restoration of Sensitivity in Chemo-resistant Glioma Cells by Cold Atmospheric Plasma. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0064498"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"8587","DOI":"10.1038\/srep08587","article-title":"Responses of Solid Tumor Cells in DMEM to Reactive Oxygen Species Generated by Non-thermal Plasma and Chemically Induced ROS Systems","volume":"5","author":"Kaushik","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Binenbaum, Y., Ben-David, G., Gil, Z., Slutsker, Y.Z., Ryzhkov, M.A., Felsteiner, J., Krasik, Y.E., and Cohen, J.T. (2017). Cold Atmospheric Plasma, Created at the Tip of an Elongated Flexible Capillary Using Low Electric Current, Can Slow the Progression of Melanoma. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0169457"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Brulle, L., Vandamme, M., Ries, D., Martel, E., Robert, E., Lerondel, S., Trichet, V., Richard, S., Pouvesle, J.M., and Le Pape, A. (2012). Effects of a Non Thermal Plasma Treatment Alone or in Combination with Gemcitabine in a MIA PaCa2-luc Orthotopic Pancreatic Carcinoma Model. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0052653"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"12LT01","DOI":"10.1088\/1361-6463\/aa5dbb","article-title":"Anti-tumor Immune Response Induced by Nanosecond Pulsed Streamer Discharge in Mice","volume":"50","author":"Mizuno","year":"2017","journal-title":"J. Phys. D"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1002\/ctpp.201700085","article-title":"Treating Cancer with Cold Physical Plasma: On the Way to Evidence-based Medicine","volume":"58","author":"Metelmann","year":"2018","journal-title":"Contrib. Plasma Phys."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.cpme.2015.02.001","article-title":"Head and Neck Cancer Treatment and Physical Plasma","volume":"3","author":"Metelmann","year":"2015","journal-title":"Clin. Plas. Med."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1445","DOI":"10.1016\/j.jcms.2016.07.001","article-title":"Visible Tumor Surface Response to Physical Plasma and Apoptotic Cell Kill in Head and Neck Cancer","volume":"44","author":"Schuster","year":"2016","journal-title":"J. Craniomaxillofac. Surg."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1016\/j.cpme.2017.09.001","article-title":"Clinical Experience with Cold Plasma in the Treatment of Locally Advanced Head and Neck Cancer","volume":"9","author":"Metelmann","year":"2018","journal-title":"Clin. Plas. Med."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.cpme.2016.01.001","article-title":"The Plasma Jet kINPen\u2014A Powerful Tool for Wound Healing","volume":"4","author":"Bekeschus","year":"2016","journal-title":"Clin. Plas. Med."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1002\/em.22172","article-title":"High Throughput Image Cytometry Micronucleus Assay to Investigate the Presence or Absence of Mutagenic Effects of Cold Physical Plasma","volume":"59","author":"Bekeschus","year":"2018","journal-title":"Environ. Mol. Mutagen."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Kluge, S., Bekeschus, S., Bender, C., Benkhai, H., Sckell, A., Below, H., Stope, M.B., and Kramer, A. (2016). Investigating the Mutagenicity of a Cold Argon-plasma Jet in An HET-MN Model. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0160667"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.mrgentox.2016.02.003","article-title":"Risk Assessment of a Cold Argon Plasma jet in Respect to Its Mutagenicity","volume":"798","author":"Wende","year":"2016","journal-title":"Mutat. Res. Genet. Toxicol. Environ. Mutagen"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/j.cpme.2013.01.001","article-title":"Risk Assessment of the Application of Tissue-tolerable Plasma on Human Skin","volume":"1","author":"Lademann","year":"2013","journal-title":"Clin. Plas. Med."},{"key":"ref_27","first-page":"509","article-title":"Cold Plasma is Well-tolerated and Does Not Disturb Skin Barrier or Reduce Skin Moisture","volume":"10","author":"Daeschlein","year":"2012","journal-title":"J. Dtsch. Dermatol Ges."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.cpme.2012.12.001","article-title":"Scar Formation of Laser Skin Lesions after Cold Atmospheric Pressure Plasma (CAP) Treatment: A Clinical Long Term Observation","volume":"1","author":"Metelmann","year":"2013","journal-title":"Clin. Plas. Med."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.cpme.2018.04.001","article-title":"Side effects in Cold Plasma Treatment of Advanced Oral Cancer\u2014Clinical Data and Biological Interpretation","volume":"10","author":"Schuster","year":"2018","journal-title":"Clin. Plas. Med."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Schmidt, A., von Woedtke, T., Stenzel, J., Lindner, T., Polei, S., Vollmar, B., and Bekeschus, S. (2017). One Year Follow-up Risk Assessment in SKH-1 Mice and Wounds Treated with an Argon Plasma Jet. Int. J. Mol. Sci., 18.","DOI":"10.3390\/ijms18040868"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1038\/nrclinonc.2009.236","article-title":"Advanced pancreatic carcinoma: Current Treatment and Future Challenges","volume":"7","author":"Stathis","year":"2010","journal-title":"Nat. Rev. Clin. Oncol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"7","DOI":"10.3322\/caac.21551","article-title":"Cancer Statistics, 2019","volume":"69","author":"Siegel","year":"2019","journal-title":"CA Cancer J. Clin."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"932","DOI":"10.1002\/jso.25440","article-title":"Adjuvant Chemotherapy and Outcomes in Patients with Nodal and Resection Margin-negative Pancreatic Ductal Adenocarcinoma: A Systematic Review and Meta-Analysis","volume":"119","author":"Flaum","year":"2019","journal-title":"J. Surg. Oncol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"824","DOI":"10.2174\/1871520618666180507130243","article-title":"Cold Physical Plasma Treated Buffered Saline Solution as Effective Agent Against Pancreatic Cancer Cells","volume":"18","author":"Bekeschus","year":"2018","journal-title":"Anticancer Agents Med. Chem."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"5655","DOI":"10.21873\/anticanres.12901","article-title":"Cold Physical Plasma Selectively Elicits Apoptosis in Murine Pancreatic Cancer Cells in Vitro and in Ovo","volume":"38","author":"Liedtke","year":"2018","journal-title":"Anticancer Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1377","DOI":"10.1002\/ppap.201500123","article-title":"Synergistic Inhibition of Tumor Cell Proliferation by Cold Plasma and Gemcitabine","volume":"12","author":"Masur","year":"2015","journal-title":"Plasma Process. Polym."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"4479","DOI":"10.1038\/s41598-017-04770-x","article-title":"The Specific Vulnerabilities of Cancer Cells to the Cold Atmospheric Plasma-stimulated Solutions","volume":"7","author":"Yan","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1655","DOI":"10.3892\/ijo.2015.3149","article-title":"Effectiveness of Plasma Treatment on Pancreatic Cancer Cells","volume":"47","author":"Hattori","year":"2015","journal-title":"Int. J. Oncol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"8319","DOI":"10.1038\/s41598-017-08560-3","article-title":"Non-thermal Plasma-treated Solution Demonstrates Antitumor Activity against Pancreatic Cancer Cells in Vitro and in Vivo","volume":"7","author":"Liedtke","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1245\/s10434-017-6239-y","article-title":"Effect of Plasma-activated Lactated Ringer\u2019s Solution on Pancreatic Cancer Cells in Vitro and in Vivo","volume":"25","author":"Sato","year":"2018","journal-title":"Ann. Surg. Oncol."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Partecke, L.I., Evert, K., Haugk, J., Doering, F., Normann, L., Diedrich, S., Weiss, F.U., Evert, M., Huebner, N.O., and Guenther, C. (2012). Tissue Tolerable Plasma (TTP) Induces Apoptosis in Pancreatic Cancer Cells in Vitro and in Vivo. BMC Cancer, 12.","DOI":"10.1186\/1471-2407-12-473"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"S169","DOI":"10.1088\/0963-0252\/15\/4\/S03","article-title":"Plasma Needle for in Vivo Medical Treatment: Recent Developments and Perspectives","volume":"15","author":"Stoffels","year":"2006","journal-title":"Plasma Sources Sci. Technol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1002\/ppap.200800028","article-title":"Delayed Effects of Cold Atmospheric Plasma on Vascular Cells","volume":"5","author":"Stoffels","year":"2008","journal-title":"Plasma Process. Polym."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1441","DOI":"10.1109\/TPS.2008.2001084","article-title":"Cold Atmospheric Plasma: Charged Species and Their Interactions with Cells and Tissues","volume":"36","author":"Stoffels","year":"2008","journal-title":"IEEE Trans. Plasma Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"2871","DOI":"10.21873\/anticanres.13416","article-title":"RAW 264.7 Macrophage Polarization by Pancreatic Cancer Cells\u2014A Model for Studying Tumour-promoting Macrophages","volume":"39","author":"Khabipov","year":"2019","journal-title":"Anticancer Res."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1006\/scbi.2001.0416","article-title":"Critical Determinants of Metastasis","volume":"12","author":"Fidler","year":"2002","journal-title":"Semin. Cancer Biol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"21421","DOI":"10.1038\/srep21421","article-title":"Short and Long Time Effects of Low Temperature Plasma Activated Media on 3D Multicellular Tumor Spheroids","volume":"6","author":"Judee","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"4866","DOI":"10.1038\/s41598-019-41408-6","article-title":"Elucidation of in Vitro Cellular Steps Induced by Antitumor Treatment with Plasma-activated Medium","volume":"9","author":"Chauvin","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"634","DOI":"10.1038\/s41598-018-37169-3","article-title":"Physical Plasma-treated Saline Promotes an Immunogenic Phenotype in CT26 Colon Cancer Cells in Vitro and in Vivo","volume":"9","author":"Freund","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"12734","DOI":"10.1038\/s41598-018-31031-2","article-title":"Cytochrome c Oxidase Inhibition and Cold Plasma-derived Oxidants Synergize in Melanoma Cell Death Induction","volume":"8","author":"Gandhirajan","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1179","DOI":"10.1038\/s41419-018-1221-6","article-title":"Combination of Chemotherapy and Physical Plasma Elicits Melanoma Cell Death Via Upregulation of SLC22A16","volume":"9","author":"Sagwal","year":"2018","journal-title":"Cell Death Dis."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Privat-Maldonado, A., Gorbanev, Y., Dewilde, S., Smits, E., and Bogaerts, A. (2018). Reduction of Human Glioblastoma Spheroids Using Cold Atmospheric Plasma: The Combined Effect of Short- and Long-lived Reactive Species. Cancers, 10.","DOI":"10.3390\/cancers10110394"},{"key":"ref_53","first-page":"2162","article-title":"Persistence of Solitary Mammary Carcinoma Cells in a Secondary Site: A Possible Contributor to Dormancy","volume":"62","author":"Naumov","year":"2002","journal-title":"Cancer Res."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"4396467","DOI":"10.1155\/2017\/4396467","article-title":"Toxicity and Immunogenicity in Murine Melanoma Following Exposure to Physical Plasma-derived Oxidants","volume":"2017","author":"Bekeschus","year":"2017","journal-title":"Oxid. Med. Cell. Longev."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Freund, E., Liedtke, K.R., Gebbe, R., Heidecke, A.K., Partecke, L.-I., and Bekeschus, S. (2019). In Vitro Anticancer Efficacy of Six Different Clinically Approved Types of Liquids Exposed to Physical Plasma. IEEE Trans. Radiation Plasma Med. Sci.","DOI":"10.1109\/TRPMS.2019.2902015"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1515\/hsz-2018-0223","article-title":"Stimulation of Melanin Synthesis in Melanoma Cells by Cold Plasma","volume":"400","author":"Hasse","year":"2018","journal-title":"Biol. Chem."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"R\u00f6dder, K., Moritz, J., Miller, V., Weltmann, K.-D., Metelmann, H.-R., Gandhirajan, R., and Bekeschus, S. (2019). Activation of Murine Immune Cells Upon Co-culture with Plasma-treated B16F10 Melanoma Cells. Applied Sci., 9.","DOI":"10.3390\/app9040660"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.cpme.2015.05.003","article-title":"Cell Migration and Adhesion of a Human Melanoma Cell Line is Decreased by Cold Plasma Treatment","volume":"3","author":"Schmidt","year":"2015","journal-title":"Clin. Plas. Med."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1207","DOI":"10.1002\/ijc.29864","article-title":"CXCL12\/CXCR4 Activation by Cancer-associated Fibroblasts Promotes Integrin Beta1 Clustering and Invasiveness in Gastric Cancer","volume":"138","author":"Izumi","year":"2016","journal-title":"Int. J. Cancer"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1016\/j.apsb.2015.07.005","article-title":"Cancer metastases: Challenges and Opportunities","volume":"5","author":"Guan","year":"2015","journal-title":"Acta. Pharm. Sin. B."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1242\/jcs.100115","article-title":"E-cadherin-integrin Crosstalk in Cancer Invasion and Metastasis","volume":"126","author":"Canel","year":"2013","journal-title":"J. Cell Sci."},{"key":"ref_62","first-page":"3508","article-title":"Down-regulation of E-cadherin Gene Expression by Collagen Type I and Type III in Pancreatic Cancer Cell Lines","volume":"61","author":"Menke","year":"2001","journal-title":"Cancer Res."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1007\/s10555-012-9389-1","article-title":"Role of the EpCAM (CD326) in Prostate Cancer Metastasis and Progression","volume":"31","author":"Ni","year":"2012","journal-title":"Cancer Metastasis Rev."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1007\/BF02788372","article-title":"Expression and Potential Role of E-cadherin in Pancreatic Carcinoma","volume":"19","author":"Weinel","year":"1996","journal-title":"Int. J. Pancreatol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"S46","DOI":"10.1093\/annonc\/10.suppl_4.S46","article-title":"Invasion and Metastasis in Pancreatic Cancer","volume":"10","author":"Ellenrieder","year":"1999","journal-title":"Ann. Oncol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1097\/mpa.0b013e31811f4526","article-title":"The Integrin-extracellular Matrix Axis in Pancreatic Cancer","volume":"35","author":"Grzesiak","year":"2007","journal-title":"Pancreas"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"6965","DOI":"10.1158\/0008-5472.CAN-11-0588","article-title":"Combined Blockade of Integrin-alpha4beta1 Plus Cytokines SDF-1alpha or IL-1beta Potently Inhibits Tumor Inflammation and Growth","volume":"71","author":"Schmid","year":"2011","journal-title":"Cancer Res."}],"container-title":["Cancers"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6694\/11\/9\/1237\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:13:30Z","timestamp":1760188410000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6694\/11\/9\/1237"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,8,23]]},"references-count":67,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2019,9]]}},"alternative-id":["cancers11091237"],"URL":"https:\/\/doi.org\/10.3390\/cancers11091237","relation":{},"ISSN":["2072-6694"],"issn-type":[{"value":"2072-6694","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,8,23]]}}}