{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T13:06:20Z","timestamp":1790082380665,"version":"4.0.1"},"reference-count":36,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2019,2,28]],"date-time":"2019-02-28T00:00:00Z","timestamp":1551312000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2019,2,28]],"date-time":"2019-02-28T00:00:00Z","timestamp":1551312000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100000065","name":"U.S. Department of Health &amp; Human Services | NIH | National Institute of Neurological Disorders and Stroke","doi-asserted-by":"publisher","award":["1R01NS091159"],"award-info":[{"award-number":["1R01NS091159"]}],"id":[{"id":"10.13039\/100000065","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>This paper provides a rigorous analysis on the measurement of the permittivity of two-dimensional anisotropic biological tissues such as skeletal muscle using the four-electrode impedance technique. The state-of-the-art technique requires individual electrodes placed at the same depth in contact with the anisotropic material, e.g. using monopolar needles. In this case, the minimum of measurements in different directions needed to estimate the complex permittivity and its anisotropy direction is 3, which translates into 12 monopolar needle insertions (i.e. 3 directions\u2009\u00d7\u20094 electrodes in each direction). Here, we extend our previous work and equip the reader with 8 new methods for multipolar needles, where 2 or more electrodes are spaced along the needle\u2019s shaft in contact with the tissue at different depths. Using multipolar needles, the new methods presented reduce the number of needle insertions by a factor of 2 with respect to the available methods. We illustrate the methods with numerical simulations and new experiments on <jats:italic>ex vivo<\/jats:italic> ovine skeletal muscle (n\u2009=\u20093). Multi-frequency longitudinal and transverse permittivity data from 30\u2009kHz to 1\u2009MHz is made publicly available in the supplementary material. The methods presented here for multipolar needles bring closer the application of needle electrical impedance to patients with neuromuscular diseases.<\/jats:p>","DOI":"10.1038\/s41598-019-39277-0","type":"journal-article","created":{"date-parts":[[2019,2,28]],"date-time":"2019-02-28T11:05:29Z","timestamp":1551351929000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":22,"title":["New electrical impedance methods for the in situ measurement of the complex permittivity of anisotropic skeletal muscle using multipolar needles"],"prefix":"10.1038","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4362-2585","authenticated-orcid":false,"given":"H.","family":"Kwon","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M.","family":"Guasch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J. A.","family":"Nagy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S. B.","family":"Rutkove","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1594-9847","authenticated-orcid":false,"given":"B.","family":"Sanchez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2019,2,28]]},"reference":[{"key":"39277_CR1","doi-asserted-by":"publisher","first-page":"394","DOI":"10.1093\/brain\/123.2.394","volume":"123","author":"U Sabatini","year":"2000","unstructured":"Sabatini, U. et al. Cortical motor reorganization in akinetic patients with Parkinson\u2019s disease. A functional MRI study. Brain 123, 394\u2013403, https:\/\/doi.org\/10.1093\/brain\/123.2.394 (2000).","journal-title":"Brain"},{"key":"39277_CR2","doi-asserted-by":"publisher","first-page":"10152","DOI":"10.1073\/pnas.0702916104","volume":"104","author":"ED Kirson","year":"2007","unstructured":"Kirson, E. D. et al. Alternating electric fields arrest cell proliferation in animal tumor models and human brain tumors. Proc. Natl. Acad. Sci. 104, 10152\u201310157, https:\/\/doi.org\/10.1073\/pnas.0702916104 (2007).","journal-title":"Proc. Natl. Acad. Sci."},{"key":"39277_CR3","doi-asserted-by":"publisher","first-page":"E14","DOI":"10.3171\/2015.1.FOCUS14742","volume":"38","author":"AA Rehman","year":"2015","unstructured":"Rehman, A. A., Elmore, K. B. & Mattei, T. A. The effects of alternating electric fields in glioblastoma: current evidence on therapeutic mechanisms and clinical outcomes. Neurosurg. Focus. 38, E14, https:\/\/doi.org\/10.3171\/2015.1.FOCUS14742 (2015).","journal-title":"Neurosurg. Focus."},{"key":"39277_CR4","first-page":"25","volume":"17","author":"KR Foster","year":"1989","unstructured":"Foster, K. R. & Schwan, H. P. Dielectric properties of tissues and biological materials: a critical review. Crit. Rev. Biomed. Eng. 17, 25\u2013104 (1989).","journal-title":"Crit. Rev. Biomed. Eng."},{"key":"39277_CR5","doi-asserted-by":"publisher","first-page":"665","DOI":"10.1088\/0031-9155\/49\/5\/002","volume":"49","author":"KS Osterman","year":"2004","unstructured":"Osterman, K. S., Hoopes, P. J., DeLorenzo, C., Gladstone, D. J. & Paulsen, K. D. Non-invasive assessment of radiation injury with electrical impedance spectroscopy. Phys. Med. Biol. 49, 665\u201383 (2004).","journal-title":"Phys. Med. Biol."},{"key":"39277_CR6","doi-asserted-by":"publisher","first-page":"2223","DOI":"10.4161\/CBT.8.23.9983","volume":"8","author":"C Skourou","year":"2009","unstructured":"Skourou, C., Hoopes, P. J. & Paulsen, K. D. Tissue permittivity: a monitor for progressive tissue fibrosis as observed in bystander tissues following experimental high dose rate irradiation. Cancer Biol. Ther. 8, 2223\u20139, https:\/\/doi.org\/10.4161\/CBT.8.23.9983 (2009).","journal-title":"Cancer Biol. Ther."},{"key":"39277_CR7","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1016\/S0002-8703(43)90050-X","volume":"26","author":"W Kaufman","year":"1943","unstructured":"Kaufman, W. & Johnston, F. The electrical conductivity of the tissues near the heart and its bearing on the distribution of the cardiac action currents. Am. Hear. J. 26, 42\u201354 (1943).","journal-title":"Am. Hear. J."},{"key":"39277_CR8","doi-asserted-by":"publisher","first-page":"664","DOI":"10.1161\/01.RES.4.6.664","volume":"4","author":"H Schwan","year":"1956","unstructured":"Schwan, H. & Kay, C. Specific Resistance of Body Tissues. Circ. Res. 4, 664\u2013670, https:\/\/doi.org\/10.1161\/01.RES.4.6.664 (1956).","journal-title":"Circ. Res."},{"key":"39277_CR9","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1007\/BF02474537","volume":"5","author":"LA Geddes","year":"1967","unstructured":"Geddes, L. A. & Baker, L. E. The specific resistance of biological material\u2014A compendium of data for the biomedical engineer and physiologist. Med. Biol. Eng. 5, 271\u2013293, https:\/\/doi.org\/10.1007\/BF02474537 (1967).","journal-title":"Med. Biol. Eng."},{"key":"39277_CR10","doi-asserted-by":"publisher","first-page":"501","DOI":"10.1088\/0031-9155\/27\/4\/002","volume":"27","author":"RD Stoy","year":"1982","unstructured":"Stoy, R. D., Foster, K. R. & Schwan, H. P. Dielectric properties of mammalian tissues from 0.1 to 100 MHz; a summary of recent data. Phys. Med. Biol. 27, 501\u2013513, https:\/\/doi.org\/10.1088\/0031-9155\/27\/4\/002 (1982).","journal-title":"Phys. Med. Biol."},{"issue":"Suppl A","key":"39277_CR11","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1088\/0143-0815\/8\/4A\/002","volume":"8","author":"R Pethig","year":"1987","unstructured":"Pethig, R. Dielectric properties of body tissues. Clin. Phys. Physiol. Meas. 8(Suppl A), 5\u201312 (1987).","journal-title":"Clin. Phys. Physiol. Meas."},{"key":"39277_CR12","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1002\/bem.2250070105","volume":"7","author":"A Surowiec","year":"1986","unstructured":"Surowiec, A., Stuchly, S. S. & Swarup, A. Postmortem changes of the dielectric properties of bovine brain tissues at low radiofrequencies. Bioelectromagn. 7, 31\u201343, https:\/\/doi.org\/10.1002\/bem.2250070105 (1986).","journal-title":"Bioelectromagn."},{"key":"39277_CR13","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1088\/0143-0815\/8\/4A\/018","volume":"8","author":"J Conway","year":"1987","unstructured":"Conway, J. Electrical impedance tomography for thermal monitoring of hyperthermia treatment: an assessment using in vitro and in vivo measurements. Clin. Phys. Physiol. Meas. 8, 141\u2013146, https:\/\/doi.org\/10.1088\/0143-0815\/8\/4A\/018 (1987).","journal-title":"Clin. Phys. Physiol. Meas."},{"key":"39277_CR14","doi-asserted-by":"publisher","first-page":"217","DOI":"10.6028\/jres.066C.018","volume":"66C","author":"S Rush","year":"1962","unstructured":"Rush, S. Methods of measuring the resistivities of anisotropic conducting media in situ. J. Res. Natl. Bur. Stand. Sect. C Eng. Instrum. 66C, 217, https:\/\/doi.org\/10.6028\/jres.066C.018 (1962).","journal-title":"J. Res. Natl. Bur. Stand. Sect. C Eng. Instrum."},{"key":"39277_CR15","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1113\/jphysiol.1976.sp011283","volume":"255","author":"L Clerc","year":"1976","unstructured":"Clerc, L. Directional Differences of Impulse Spread in Trabecular Muscle from Mammalian Heart. J. Physiol. 255, 335\u2013346, https:\/\/doi.org\/10.1113\/jphysiol.1976.sp011283 (1976).","journal-title":"J. Physiol."},{"key":"39277_CR16","doi-asserted-by":"publisher","first-page":"1138","DOI":"10.1109\/10.245632","volume":"40","author":"P Steendijk","year":"1993","unstructured":"Steendijk, P., Mur, G., Van Der Velde, E. T. & Baan, J. The four-electrode resistivity technique in anisotropic media: theoretical analysis and application on myocardial tissue in vivo. IEEE Trans. Biomed. Eng. 40, 1138\u201348, https:\/\/doi.org\/10.1109\/10.245632 (1993).","journal-title":"IEEE Trans. Biomed. Eng."},{"key":"39277_CR17","doi-asserted-by":"publisher","first-page":"8616","DOI":"10.1088\/1361-6560\/aa8c95","volume":"62","author":"H Kwon","year":"2017","unstructured":"Kwon, H., Nagy, J. A., Taylor, R., Rutkove, S. B. & Sanchez, B. New electrical impedance methods for the in situ measurement of the complex permittivity of anisotropic biological tissues. Phys. Med. Biol. 62, 8616\u20138633, https:\/\/doi.org\/10.1088\/1361-6560\/aa8c95 (2017).","journal-title":"Phys. Med. Biol."},{"key":"39277_CR18","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1007\/BF01191612","volume":"3","author":"HP Schwan","year":"1966","unstructured":"Schwan, H. P. Alternating current electrode polarization. Biophys. 3, 181\u2013201, https:\/\/doi.org\/10.1007\/BF01191612 (1966).","journal-title":"Biophys."},{"key":"39277_CR19","unstructured":"Andreuccetti, D., Fossi, R. & Petrucci, C. An Internet resource for the calculation of the dielectric properties of body tissues in the frequency range 10\u2009Hz\u2013100\u2009GHz (1997)."},{"key":"39277_CR20","doi-asserted-by":"publisher","first-page":"2231","DOI":"10.1088\/0031-9155\/41\/11\/001","volume":"41","author":"C Gabriel","year":"1996","unstructured":"Gabriel, C., Gabriel, S. & Corthout, E. The dielectric properties of biological tissues: I. Literature survey. Phys. Med. Biol. 41, 2231\u201349 (1996).","journal-title":"Phys. Med. Biol."},{"key":"39277_CR21","doi-asserted-by":"publisher","first-page":"2251","DOI":"10.1088\/0031-9155\/41\/11\/002","volume":"41","author":"S Gabriel","year":"1996","unstructured":"Gabriel, S., Lau, R. W. & Gabriel, C. The dielectric properties of biological tissues : II. Measurements in the frequency range 10 Hz to 20 GHz. Phys. Med. Biol. 41, 2251\u20132269 (1996).","journal-title":"Phys. Med. Biol."},{"key":"39277_CR22","doi-asserted-by":"publisher","first-page":"2271","DOI":"10.1088\/0031-9155\/41\/11\/003","volume":"41","author":"S Gabriel","year":"1996","unstructured":"Gabriel, S., Lau, R. W. & Gabriel, C. The dielectric properties of biological tissues: III. Parametric models for the dielectric spectrum of tissues. Phys. Med. Biol. 41, 2271\u201393 (1996).","journal-title":"Phys. Med. Biol."},{"key":"39277_CR23","doi-asserted-by":"publisher","first-page":"4461","DOI":"10.1088\/0031-9155\/59\/16\/4461","volume":"59","author":"DJ Eaton","year":"2014","unstructured":"Eaton, D. J. Highly cited articles in Physics in Medicine and Biology. Phys. Med. Biol. 59, 4461\u20134463, https:\/\/doi.org\/10.1088\/0031-9155\/59\/16\/4461 (2014).","journal-title":"Phys. Med. Biol."},{"key":"39277_CR24","doi-asserted-by":"publisher","DOI":"10.1109\/IRE-I.1955.5006973","author":"HP Schwan","year":"1955","unstructured":"Schwan, H. P. Application of UHF Impedance Measuring Techniques in Biophysics. Tech. Rep., DTIC Document. https:\/\/doi.org\/10.1109\/IRE-I.1955.5006973 (1955).","journal-title":"Tech. Rep., DTIC Document"},{"key":"39277_CR25","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1118\/1.597312","volume":"21","author":"WT Joines","year":"1994","unstructured":"Joines, W. T., Zhang, Y., Li, C. & Jirtle, R. L. The measured electrical properties of normal and malignant human tissues from 50 to 900 MHz. Med. Phys. 21, 547\u2013550, https:\/\/doi.org\/10.1118\/1.597312 (1994).","journal-title":"Med. Phys."},{"key":"39277_CR26","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1007\/BF02446406","volume":"21","author":"BR Epstein","year":"1983","unstructured":"Epstein, B. R. & Foster, K. R. Anisotropy in the dielectric properties of skeletal muscle. Med. Biol. Eng. Comput. 21, 51\u201355, https:\/\/doi.org\/10.1007\/BF02446406 (1983).","journal-title":"Med. Biol. Eng. Comput."},{"key":"39277_CR27","doi-asserted-by":"publisher","first-page":"569","DOI":"10.1007\/BF02443872","volume":"22","author":"FLH Gielen","year":"1984","unstructured":"Gielen, F. L. H., Wallinga-de Jonge, W. & Boon, K. L. Electrical conductivity of skeletal muscle tissue: Experimental results from different muscles in vivo. Med. Biol. Eng. Comput. 22, 569\u2013577, https:\/\/doi.org\/10.1007\/BF02443872 (1984).","journal-title":"Med. Biol. Eng. Comput."},{"key":"39277_CR28","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1088\/0031-9155\/59\/10\/2369","volume":"59","author":"B Sanchez","year":"2014","unstructured":"Sanchez, B., Li, J., Bragos, R. & Rutkove, S. B. Differentiation of the intracellular structure of slow- versus fast-twitch muscle fibers through evaluation of the dielectric properties of tissue. Phys. Med. Biol. 59, 1\u201312 (2014),\u00a0 doi: 10.1088\/0031-9155\/59\/10\/2369.","journal-title":"Phys. Med. Biol."},{"key":"39277_CR29","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1109\/10.821749","volume":"47","author":"S Kun","year":"2000","unstructured":"Kun, S. & Peura, R. Effects of sample geometry and electrode configuration on measured electrical resistivity of skeletal muscle. IEEE Trans. Biomed. Eng. 47, 163\u2013169, https:\/\/doi.org\/10.1109\/10.821749 (2000).","journal-title":"IEEE Trans. Biomed. Eng."},{"key":"39277_CR30","doi-asserted-by":"crossref","unstructured":"Kwon, H., Malik, W. Q., Rutkove, S. B. & Sanchez, B. Separation of subcutaneous fat from muscle in surface electrical impedance myography measurements using model component analysis. IEEE Trans. Biomed. Eng. in press (2018).","DOI":"10.1109\/TBME.2018.2839977"},{"key":"39277_CR31","doi-asserted-by":"publisher","first-page":"40","DOI":"10.1161\/01.RES.12.1.40","volume":"12","author":"S Rush","year":"1963","unstructured":"Rush, S., Abildskov, J. A. & McFee, R. Resistivity of body tissues at low frequencies. Circ. Res. 12, 40\u201350, https:\/\/doi.org\/10.1161\/01.RES.12.1.40 (1963).","journal-title":"Circ. Res."},{"key":"39277_CR32","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-017-18360-4","volume":"8","author":"J Park","year":"2018","unstructured":"Park, J. et al. Biopsy Needle Integrated with Electrical Impedance Sensing Microelectrode Array towards Real-time Needle Guidance and Tissue Discrimination. Sci. Rep. 8, 264, https:\/\/doi.org\/10.1038\/s41598-017-18360-4 (2018).","journal-title":"Sci. Rep."},{"key":"39277_CR33","doi-asserted-by":"publisher","unstructured":"Cheng, Z., Davies, B. L., Caldwell, D. G. & Mattos, L. S. A New Venous Entry Detection Method Based on Electrical Bio-impedance Sensing. Ann. Biomed. Eng. 1\u201310, https:\/\/doi.org\/10.1007\/s10439-018-2025-7 (2018).","DOI":"10.1007\/s10439-018-2025-7"},{"key":"39277_CR34","doi-asserted-by":"publisher","DOI":"10.1007\/s11910-017-0793-3","volume":"17","author":"B Sanchez","year":"2017","unstructured":"Sanchez, B. & Rutkove, S. B. Present Uses, Future Applications, and Technical Underpinnings of Electrical Impedance Myography. Curr. Neurol. Neurosci. Rep. 17, 86, https:\/\/doi.org\/10.1007\/s11910-017-0793-3 (2017).","journal-title":"Curr. Neurol. Neurosci. Rep."},{"key":"39277_CR35","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1007\/s13311-016-0491-x","volume":"14","author":"B Sanchez","year":"2017","unstructured":"Sanchez, B. & Rutkove, S. B. Electrical impedance myography and its applications in neuromuscular disorders. Neurother. 14, 107\u2013118, https:\/\/doi.org\/10.1007\/s13311-016-0491-x (2017).","journal-title":"Neurother."},{"key":"39277_CR36","doi-asserted-by":"publisher","first-page":"055005","DOI":"10.1088\/1361-6579\/aabb8c","volume":"39","author":"H Kwon","year":"2018","unstructured":"Kwon, H., Di Cristina, J. F., Rutkove, S. B. & Sanchez, B. Recording characteristics of electrical impedanceelectromyography needle electrodes. Physiol. Meas. 39, 055005, https:\/\/doi.org\/10.1088\/1361-6579\/aabb8c (2018).","journal-title":"Physiol. Meas."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-39277-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-39277-0","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-39277-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,17]],"date-time":"2022-12-17T06:43:23Z","timestamp":1671259403000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-39277-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,2,28]]},"references-count":36,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2019,12]]}},"alternative-id":["39277"],"URL":"https:\/\/doi.org\/10.1038\/s41598-019-39277-0","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,2,28]]},"assertion":[{"value":"4 October 2018","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 January 2019","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"28 February 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Dr. Rutkove serves as scientific advisor and consultant to Skulpt, Inc., a company that commercializes impedance technology. Dr. Rutkove is also a member of the company\u2019s Board of Directors. Dr. Sanchez serves as a consultant to Impedimed, Inc., a company that develop impedance technology for research and clinical use. Dr. Sanchez and Dr. Rutkove are Co-Founders of Haystack Diagnostics, Inc., a company that commercializes needle impedance technology. Haystack Diagnostics, Inc., has the option to license patented needle impedance technology of which Dr. Sanchez, Dr. Rutkove and Dr. Kwon are named inventors.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"3145"}}