Estimation of Cole-Cole model parameters with multifrequency-bioelectrical impedance analysis in newly diagnosed lung cancer adult patients
Keywords:
multi-frequency bioelectrical impedance analysis; newly diagnosed lung cancer adult patients; Cole-Cole distribution function; intracellular and extracellular electrical resistance; characteristic frequencyAbstract
Introduction: The bioelectrical impedance analysis is used for the evaluation and monitoring in cancer patients.
Objective: To estimate whole bioelectrical parameters obtained from the Cole-Cole distribution function with multifrequency-bioelectrical impedance analysis in newly diagnosed lung cancer adult patients.
Methods: A pilot, prospective and cross-sectional study was carried out to measure the bioelectrical parameters with multi-frequency Bioelectrical Impedance Analysis (at 5, 50, 100 and 200 kHz) in 23 newly diagnosed lung cancer adult patients. The Cole-Cole distribution function was used to estimate electrical resistance, capacitive reactance and impedance modulus between 100 Hz and 10 GHz.
Results: Differences between the simulated and experimental data (electrical impedance modulus > 10 Ω) were observed in seven lung cancer patients at 100 and 200 kHz. Cole-Cole distribution function underestimated experimental data in the majority of these patients at 5; 50 and 100 kHz, not so at 200 kHz. The intracellular resistance was higher than extracellular resistance in all them, in contrast with physiology. Furthermore, the overall cellular capacitance of cellular membrane in each lung cancer patient increased respect to that in apparently healthy subjects.
Conclusions: The bioelectrical impedance analysis reveals anomalous behaviors of bioelectrical parameters in each newly diagnosed lung cancer adult patients for frequencies above characteristic frequency. These behaviors may be described by distribution functions Cole-Cole (for 0 < α < 1) or others.
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1. Regüeiferos JCC, Luna TTB, Brooks SCA, Rodríguez MP, Zamora-Matamoros L, Legrá-Rodríguez B, Fernández AP, Bello JLG, Montoya-Pedrón A, González MM, Garcia JCN, Cascaret-Fonseca E, Cabrales LEB. Integrated analysis of clinical, bioelectrical and functional variables in newly diagnosed lung cancer adult patients: pilot study. Translational Medicine Communications, 2022 [citado 15 oct 2023];7:1. https://doi.org/10.1186/s41231-022-00127-3
2. Hui D, Dev R, Pimental L, Park M, Cerana MA, Liu D, Bruera E. Association between multi-frequency phase angle and survival in patients with advanced cancer. Journal Pain Symptom Manage, 2017 [citado 15 oct 2023];53(3):571-77. https://doi.org/10.1016/j.jpainsymman.2016.09.016
3. Toso S, Piccoli A, Gusella M, Menon D, Bononi A, Crepaldi G, Ferrazi E. Altered tissue electric properties in lung cancer patients as detected by bioelectric impedance vector analysis. Nutrition, 2000 [citado 15 oct 2023];16(2):120-124. https://doi.org/10.1016/S0899-9007(99)00230-0
4. Sasaki K, Porter E, Rashed EA, Farrugia L, Schmid G. Measurement and image-based estimation of dielectric properties of biological tissues-past, present, and future. Physics in Medicine & Biology, 2022 [citado 23 mar 2024];67(14). https://doi.org/10.1088/1361-6560/ac7b64
5. Di Meo S, Bonello J, Farhat I, Farrugia L, Pasian M, Camilleri-Podesta MT. The variability of dielectric permittivity of biological tissues with water content. Journal Electromagnetics Waves and Applications, 2022 [citado 23 mar 3024];36(1):48-68. https://doi.org/10.1080/09205071.2021.1956375
6. Robinson J, Jain A, Sherman H, Hague R, Rahman R, Sanjuan-Alberte P, Rawson F. Toward hijacking bioelectricity in cancer to develop new bioelectronic medicine. Advanced Therapeutics, 2021 [citado 23 mar 2024];4(3). https://doi.org/10.1002/adtp.202000248
7. Bory-Prevez H, Soutelo-Jiménez AA, Roca-Oria EJ, Heredia-Kindelán JA, Morales-González M, Villar-Goris NA, Hernández-Mesa N, Sierra-González VG, Infentaes-Frómeta Y, Montijano JI, Bergues-Cabrales LE. Simulations of surface charge density changes during the untreated solid tumor growth. Royal Society Open Science, 2022 [citado 05 oct 2024];9(11):220552. https://doi.org/10.1098/rsos.220552
8. Singh K, Awasthi R, Malviya RR. Bioelectronic medicines: Therapeutic potential and advancements in next-generation cancer therapy. Biochimica et Biophysica. Acta (BBA) Reviews on Cancer, 2022 [citado 05 oct 2024];1877(6):188808. https://doi.org/10.1016/j.bbcan.2022.188808
9. Dahlmann N, Demond V. A new anthropometric model for body composition estimation: Comparison with a bioelectrical impedance consumer device. Plos One, 2022 [citado 15 oct 2023];17(9):e0271880. https://doi.org/10.1371/journal.pone.0271880
10. Morlino D, Cioffi I, Marra M, Di Vincenzo O, Scalfi L, Pasanisi F. Bioelectrical phase angle in patients with breast cancer: a systematic review. Cancers (Basel), 2022 [citado 23 mar 2024];14(8):2002. https://doi.org/10.3390/cancers14082002
11. Praget-Bracamontes S, González-Arellanes R, Aguilar-Salinas CA, Martagón AJ. Phase angle as a potential screening tool in adults with metabolic diseases in clinical practice: A systematic review. International Journal of Environmental Research and Public Health, 2023 [citado 23 mar 2024]; 20(2):1608. https://doi.org/10.3390/ijerph20021608
12. Nieto-Villar JM, Mansilla R. Longevity, aging and cancer: Thermodynamics and complexity. Foundations, 2022 [citado 15 oct 2023];2:664. https://doi.org/10.13133/2532-5876/17613
13. Lucia U, Grisolia G. Thermal resonance in living cells to control their heat exchange: Possible applications in cancer treatment. International Communications in Heat and Mass Transfer, 2022 [citado 04 nov 2024];131:105842. https://doi.org/10.1016/j.icheatmasstransfer.2021.105842
14. WMA Declaration of Helsinki–Ethical Principles for Medical Research Involving Human Subjects. 64th WMA General Assembly, Fortaleza, Brazil, October 2013. Disponible en: https://www.wma.net/policies-post/wma-declaration-of-helsinki-ethical-principles-for-medical-research-involving-human-subjects/
15. Buenas Prácticas Clínicas en Cuba, Centro para el Control Estatal de la Calidad de los Medicamentos (CECMED), La Habana, Cuba, (2000), Disponible en: https://www.google.com/url?sa=t&rct=j&q=&esrc=s&source=web&cd=&ved=2ahUKEwiIxfLsk9vxAhXVTjABHdYjBMYQFjAAegQIBxAD&url=https%3A%2F%2Fwww.cecmed.cu%2Ffile%2F1984%2Fdownload%3Ftoken%3DOeQm92f3&usg=AOvVaw2KRGkA8C5KqWnfmDlytS25
16. Lafargue AL, Cabrales LEB, Larramendi RM. Inductance of body tissues obtained by bioelectrical impedance analysis method. Bioelectromagnetics, 2002 [citado 23 abr 2024];23:450. https://doi.org/10.1002/bem.10034
17. Nescolarde L, Núñez A, Bogónez-Franco P, Lara A, Vaillant G, Morales R, Rosell-Ferrer J. Reference values of the bioimpedance vector components in a Caribbean population. e-SPEN J, 2013 [citado 05 sep 2024];8(4):e141-e144. https://doi.org/10.1016/j.clnme.2013.04.004
18. Cole KS, Cole RH. Dispersion and absorption in dielectrics II. Direct current characteristics. Journal of Chemical Physics, 1942 [citado 03 nov 2024];10:98. https://doi.org/10.1063/1.1723677
19. Moqadam SM, Grewal PK, Haeri Z, Ingledew PA, Kohli K, Golnaraghi F. Cancer detection based on electrical impedance spectroscopy: A clinical study. Journal of Electrical Bioimpedance, 2018 [citado 12 feb 2024];9(1):17-23. https://doi.org/10.2478/joeb-2018-0004
20. Freeborn TJ, Elwakil AS, Maundy B. Compact wide frequency range fractional-order models of human body impedance against contact currents. Mathematical Problems in Engineering, 2016 [citado 17 may 2024];2016(1):4967937. https://doi.org/10.1155/2016/4967937
21. Sipers WM, Dorge J, Schols JM, Verdijk LB, Van Loon LJ. Multifrequency bioelectrical impedance analysis may represent a reproducible and practical tool to assess skeletal muscle mass in euvolemic acutely ill hospitalized geriatric patients. European Geriatric Medicine, 2020 [citado 03 ene 2024];11(1):155-162. https://doi.org/10.1007/s41999-019-00253-6
22. Osypka M, Gersing E. Tissue impedance spectra and the appropriate frequencies for EIT. Physiological Measurement, 1995 [citado 14 jun 2024];16(3A):A49. https://doi.org/10.1088/0967-3334/16/3A/005
23. Nwosu AC, Mayland CR, Mason S, Cox TF, Varro A, Ellershaw J. The association of hydration status with physical signs, symptoms and survival in advanced cancer-The use of bioelectrical impedance vector analysis (BIVA) technology to evaluate fluid volume in palliative care: an observational study. Plos One, 2016 [citado 14 jul 2024];11(9):e0163114. https://doi.org/10.1371/journal.pone.0163114
24. Elkington L, Adhikari P, Pradhan P. Fractal dimension analysis to detect the progress of cancer using transmission optical microscopy. Biophysica, 2022 [citado 10 sep 2024];2(1):59-69. https://doi.org/10.3390/biophysica2010005
25. Sahu T, Tripathy MC, Sahoo SP. An intelligent fractional-order system for the biological parameters regulations. International Journal of Dynamics and Control, 2022 [citado 27 jun 2024];11(4):1880. https://doi.org/10.1007/s40435-022-01088-z
26. Ghita M, Copot D, Ionescu CM. Lung cancer dynamics using fractional order impedance modeling on a mimicked lung tumor setup. Journal of Advanced Research, 2021 [citado 14 sep 2024];32:61-71. https://doi.org/10.1016/j.jare.2020.12.016
27. Leslie TK, Brackenbury WJ. Sodium channels and the ionic microenvironment of breast tumours. Journal of Physiology, 2023 [citado 07 nov 2024];601(9):1543-1553. https://doi.org/10.1113/JP282306
28. Morales-González M, González-Joa JA, Bergues-Cabrales LE, Bergues-Pupo AE, Schneider B, Kondakci S, Camué-Ciria HM, Bory-Reyes J, Verdecia-jarque M, O´farril-Mateus MA, Rubio-González T, Acosta-Brooks SC, Hernández-Cáceres JL, Sierra-González GV. Is cancer a pure growth curve or does it follow a kinetics of dynamical structural transformation? BMC Cancer, 2017 [citado 11 dic 2024];17:1-14. https://doi.org/10.1186/s12885-017-3159-y
29. Hanahan D. Hallmarks of cancer: new dimensions. Cancer Discovery, 2022 [citado 13 dic 2024];12(1):31. https://doi.org/10.1158/2159-8290.CD-21-1059
30. Sheth M, Esfandiari L. Bioelectric dysregulation in cancer initiation, promotion, and progression. Frontiers in Oncology, 2022 [citado 04 dic 2024];12:846917. https://doi.org/10.3389/fonc.2022.846917
31. Levin M. Bioelectrical approaches to cancer as a problem of the scaling of the cellular self. Progress in Biophysics and Molecular Biology, 2021 [citado 25 jun 2024];165:102. https://doi.org/10.1016/j.pbiomolbio.2021.04.007
32. Zhang W, Wang B, Zhu Q, Li G. Triboelectric nanogenerators for cellular bioelectrical stimulation. Advanced Functional Materials, 2022 [citado 09 jul 2023];32(34):2203029. https://doi.org/10.1002/adfm.202203029
33. Di Gregorio E, Israel S, Staelens M, Tankel G, Shankar K, Tuszyński JA. The distinguishing electrical properties of cancer cells. Physics of Life Reviews, 2022 [citado 21 ene 2025];43:139-188. https://doi.org/10.1016/j.10.1016/j.plrev.2023.08.003plrev.2022.09.003
34. Kim SJ, Khadka D, Seo JH. Interplay between solid tumors and tumor microenvironment. Frontiers in Immunology, 2022 [citado 26 ago 2024];13:882718. https://doi.org/10.3389/fimmu.2022.882718
35. Elwakil AS, Al-Ali AA, Maundy BJ. Extending the double-dispersion Cole-Cole, Cole-Davidson and Havriliak-Negami electrochemical impedance spectroscopy models. European Biophysics Journal, 2021 [citado 23 ene 2025];50(6):915-926. https://doi.org/10.1007/s00249-021-01545-1
36. Lee SW, Ying CL, Ruey H, Haroon S, Kin WW, Jc Lee E, WL Lau T, Sethi S, Wee B. Evaluation of different bioimpedance methods for assessing body composition in Asian non-dialysis chronic kidney disease patients. Kidney Research and Clinical Practice, 2019 [citado 11 mar 2025];38(1):71-80. https://doi.org/10.23876/j.krcp.18.0069
37. Kibret B, Teshome AK, Lai D. Human body as antenna and its effect on human body communications. Progress in Electromagnetics Research, 2014 [citado 13 feb 2025];148:193-207. https://doi.org/10.2528/PIER14061207
38. J. M. Randall, R. T. Matthews, and M. A. Stiles, Resonant frequencies of standing humans. Ergonomics, 1997 [citado 11 mar 2025];40(9):879-886. https://doi.org/10.1080/001401397187711
39. Calabrò E, Magazù S. New perspectives in the treatment of tumor cells by electromagnetic radiation at resonance frequencies in cellular membrane channels. The Open Biotechnology Journal, 2019 [citado 17 feb 2025];13(1):105-110. https://doi.org/10.2174/187407070190130105
40. Zhou E, Cheng Y, Chen F, Luo H, Li X. Low-profile high-gain wideband multi-resonance microstrip-fed slot antenna with anisotropic metasurface. Progress in Electromagnetics Research, 2022 [citado 25 mar 2025];175:91-104. https://doi.org/10.2528/pier22062201
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Copyright (c) 2026 Arnolis Poll-Fernández, Dunia Rodríguez-Heredia, Maylet Planas-Rodríguez, Henry Bory-Prevez, Justa Carmen Columbié-Regüeiferos, Luis Enrique Bergues Cabrales

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