Clinical Usage of Tissue Electrical Conductivity during the Electroporation: An Essential and Useful Factor
Abstract
Electric field intensity at each point is responsible for pore creation in the cell membrane during the electroporation process. These pores can increase the tissue electrical conductivity in the electroporation. Changes in electrical conductivity through the electroporation is a useful factor for imaging and tracking of electroporation inside the body. Electrical conductivity is set to become a vital factor for accurate estimation of the electric field and cell kill probability distribution in the course of electroporation for treatment planning purposes. Therefore, for more accurate treatment, tissue electrical conductivity changes due to electroporation should be considered in the treatment planning system. This paper describes the advantages of tissue electrical conductivity as a useful factor in the clinic.
1- C. Jiang, R. V Davalos, and J. C. Bischof, “A review of basic to clinical studies of irreversible electroporation therapy,” IEEE Trans. Biomed. Eng., vol. 62, no. 1, pp. 4–20, 2014.
2- E. Neumann, M. Schaefer‐Ridder, Y. Wang, and P. Hofschneider, “Gene transfer into mouse lyoma cells by electroporation in high electric fields.,” EMBO J., vol. 1, no. 7, pp. 841–845, 1982.
3- R. V Davalos, L. M. Mir, and B. Rubinsky, “Tissue ablation with irreversible electroporation,” Ann. Biomed. Eng., vol. 33, no. 2, p. 223, 2005.
4- Z. Vasilkoski, A. T. Esser, T. R. Gowrishankar, and J. C. Weaver, “Membrane electroporation: The absolute rate equation and nanosecond time scale pore creation,” Phys. Rev. E, vol. 74, no. 2, p. 21904, 2006.
5- M. Bier, W. Chen, T. R. Gowrishankar, R. D. Astumian, and R. C. Lee, “Resealing dynamics of a cell membrane after electroporation,” Phys. Rev. E, vol. 66, no. 6, p. 62905, 2002.
6- D. S. K. Lu, S. T. Kee, and E. W. Lee, “Irreversible electroporation: ready for prime time?,” Tech. Vasc. Interv. Radiol., vol. 16, no. 4, pp. 277–286, 2013.
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8- E. W. Lee et al., “Electron microscopic demonstration and evaluation of irreversible electroporation-induced nanopores on hepatocyte membranes,” J. Vasc. Interv. Radiol., vol. 23, no. 1, pp. 107–113, 2012.
9- S. Orlowski, J. Belehradek Jr, C. Paoletti, and L. M. Mir, “Transient electropermeabilization of cells in culture: increase of the cytotoxicity of anticancer drugs,” Biochem. Pharmacol., vol. 37, no. 24, pp. 4727–4733, 1988.
10- G. Sersa et al., “Electrochemotherapy of small tumors; the experience from the ESOPE (European Standard Operating Procedures for Electrochemotherapy) group,” in Clinical aspects of Electroporation, Springer, 2011, pp. 93–102.
11- D. Miklavčič, “Network for development of electroporation-based technologies and treatments: COST TD1104,” J. Membr. Biol., vol. 245, no. 10, pp. 591–598, 2012.
12- M. L. Yarmush, A. Golberg, G. Serša, T. Kotnik, and D. Miklavčič, “Electroporation-based technologies for medicine: principles, applications, and challenges,” Annu. Rev. Biomed. Eng., vol. 16, pp. 295–320, 2014.
13- S. Mahnič-Kalamiza, E. Vorobiev, and D. Miklavčič, “Electroporation in food processing and biorefinery,” J. Membr. Biol., vol. 247, no. 12, pp. 1279–1304, 2014.
14- I. Edhemovic et al., “Intraoperative electrochemotherapy of colorectal liver metastases,” J. Surg. Oncol., vol. 110, no. 3, pp. 320–327, 2014.
15- J. C. Weaver, “Electroporation of cells and tissues,” IEEE Trans. plasma Sci., vol. 28, no. 1, pp. 24–33, 2000.
16- L. Appelbaum, E. Ben-David, J. Sosna, Y. Nissenbaum, and S. N. Goldberg, “US findings after irreversible electroporation ablation: radiologic-pathologic correlation,” Radiology, vol. 262, no. 1, pp. 117–125, 2012.
17- E. Ben-David, L. Appelbaum, J. Sosna, I. Nissenbaum, and S. N. Goldberg, “Characterization of irreversible electroporation ablation in in vivo porcine liver,” Am. J. Roentgenol., vol. 198, no. 1, pp. W62–W68, 2012.
18- G. Onik, P. Mikus, and B. Rubinsky, “Irreversible electroporation: implications for prostate ablation,” Technol. Cancer Res. Treat., vol. 6, no. 4, pp. 295–300, 2007.
19- K. F. Chu and D. E. Dupuy, “Thermal ablation of tumours: biological mechanisms and advances in therapy,” Nat. Rev. Cancer, vol. 14, no. 3, pp. 199–208, 2014.
20- M. Ahmed, C. L. Brace, F. T. Lee Jr, and S. N. Goldberg, “Principles of and advances in percutaneous ablation,” Radiology, vol. 258, no. 2, pp. 351–369, 2011.
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22- S. Corovic, A. Zupanic, and D. Miklavcic, “Numerical modeling and optimization of electric field distribution in subcutaneous tumor treated with electrochemotherapy using needle electrodes,” IEEE Trans. Plasma Sci., vol. 36, no. 4, pp. 1665–1672, 2008.
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24- M. Kranjc et al., “In situ monitoring of electric field distribution in mouse tumor during electroporation,” Radiology, vol. 274, no. 1, pp. 115–123, 2015.
25- O. Adeyanju, H. Al-Angari, and A. Sahakian, “The optimization of needle electrode number and placement for irreversible electroporation of hepatocellular carcinoma,” Radiol. Oncol., vol. 46, no. 2, pp. 126–135, 2012.
26- M. B. Sano, M. R. DeWitt, S. D. Teeter, and L. Xing, “Optimization of a single insertion electrode array for the creation of clinically relevant ablations using high-frequency irreversible electroporation,” Comput. Biol. Med., vol. 95, pp. 107–117, 2018.
27- G. Merola, “Design and characterization of a minimally invasive bipolar electrode for electroporation,” Politecnico di Torino, 2020.
28- F. Pedersoli et al., “Single-needle electroporation and interstitial electrochemotherapy: in vivo safety and efficacy evaluation of a new system,” Eur. Radiol., vol. 29, no. 11, pp. 6300–6308, 2019.
29- C. B. Arena et al., “High-frequency irreversible electroporation (H-FIRE) for non-thermal ablation without muscle contraction,” Biomed. Eng. Online, vol. 10, no. 1, pp. 1–21, 2011.
30- S. Čorović, M. Pavlin, and D. Miklavčič, “Analytical and numerical quantification and comparison of the local electric field in the tissue for different electrode configurations,” Biomed. Eng. Online, vol. 6, no. 1, p. 37, 2007.
31- A. Ivorra and B. Rubinsky, “In vivo electrical impedance measurements during and after electroporation of rat liver,” Bioelectrochemistry, vol. 70, no. 2, pp. 287–295, 2007.
32- U. F. Pliquett and K. H. Schoenbach, “Changes in electrical impedance of biological matter due to the application of ultrashort high voltage pulses,” IEEE Trans. Dielectr. Electr. Insul., vol. 16, no. 5, pp. 1273–1279, 2009.
33- S. M. Firoozabadi, “Finite Element Analysis of Tissue Conductivity during High-frequency and Low-voltage Irreversible Electroporation,” Iran. J. Med. Phys., vol. 14, no. 3, pp. 135–140, 2017.
34- A. Khorasani, S. M. Firoozabadi, and Z. Shankayi, “Conductivity change with needle electrode during high frequency irreversible electroporation: a finite element study,” Polish J. Med. Phys. Eng., vol. 25, no. 4, pp. 237–242, 2019.
35- M. G. Moisescu, M. Radu, E. Kovacs, L. M. Mir, and T. Savopol, “Changes of cell electrical parameters induced by electroporation. A dielectrophoresis study,” Biochim. Biophys. Acta (BBA)-Biomembranes, vol. 1828, no. 2, pp. 365–372, 2013.
36- T. Garcia-Sanchez, D. Voyer, C. Poignard, and L. M. Mir, “Physiological changes may dominate the electrical properties of liver during reversible electroporation: Measurements and modelling,” Bioelectrochemistry, vol. 136, p. 107627, 2020.
37- B. López-Alonso, H. Sarnago, O. Lucía, P. Briz, and J. M. Burdío, “Real-Time Impedance Monitoring During Electroporation Processes in Vegetal Tissue Using a High-Performance Generator,” Sensors, vol. 20, no. 11, p. 3158, 2020.
38- Y. Zhao, S. Zheng, N. Beitel-White, H. Liu, C. Yao, and R. V Davalos, “Development of a Multi-Pulse Conductivity Model for Liver Tissue Treated With Pulsed Electric Fields,” Front. Bioeng. Biotechnol., vol. 8, p. 396, 2020.
39- N. Beitel-White et al., “Multi-tissue Analysis on the Impact of Electroporation on Electrical and Thermal Properties,” IEEE Trans. Biomed. Eng., 2020.
40- D. Sel, D. Cukjati, D. Batiuskaite, T. Slivnik, L. M. Mir, and D. Miklavcic, “Sequential finite element model of tissue electropermeabilization,” IEEE Trans. Biomed. Eng., vol. 52, no. 5, pp. 816–827, 2005.
41- P. A. Garcia et al., “Intracranial nonthermal irreversible electroporation: in vivo analysis,” J. Membr. Biol., vol. 236, no. 1, pp. 127–136, 2010.
42- A. Khorasani, “A numerical study on the effect of conductivity change in cell kill distribution in irreversible electroporation,” Polish J. Med. Phys. Eng., vol. 26, no. 2, pp. 69–76, 2020.
43- A. Khorasani, S. M. Firoozabadi, and Z. Shankayi, “Conductivity Changes of Liver Tissue during Irreversible Electroporation and Calculation of the Electric Field Distribution,” mdrsjrns, vol. 9, no. 2. pp. 227–232, 2018.
44- E. Ben-David et al., “Irreversible electroporation: treatment effect is susceptible to local environment and tissue properties,” Radiology, vol. 269, no. 3, pp. 738–747, 2013.
45- U. Pliquett, R. Langer, and J. C. Weaver, “Changes in the passive electrical properties of human stratum corneum due to electroporation,” Biochim. Biophys. Acta (BBA)-Biomembranes, vol. 1239, no. 2, pp. 111–121, 1995.
46- A. Ivorra, B. Al-Sakere, B. Rubinsky, and L. M. Mir, “In vivo electrical conductivity measurements during and after tumor electroporation: conductivity changes reflect the treatment outcome,” Phys. Med. Biol., vol. 54, no. 19, p. 5949, 2009.
47- P. A. Garcia, C. B. Arena, and R. V Davalos, “Towards a predictive model of electroporation-based therapies using pre-pulse electrical measurements,” in 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society, pp. 2575–2578, 2012.
48- A. Ivorra, L. M. Mir, and B. Rubinsky, “Electric field redistribution due to conductivity changes during tissue electroporation: experiments with a simple vegetal model,” in World Congress on Medical Physics and Biomedical Engineering, September 7-12, 2009, Munich, Germany, pp. 59–62, 2009.
49- S. Corovic, I. Lackovic, P. Sustaric, T. Sustar, T. Rodic, and D. Miklavcic, “Modeling of electric field distribution in tissues during electroporation,” Biomed. Eng. Online, vol. 12, no. 1, p. 16, 2013.
50- R. V Davalos, B. Rubinsky, and D. M. Otten, “A feasibility study for electrical impedance tomography as a means to monitor tissue electroporation for molecular medicine,” IEEE Trans. Biomed. Eng., vol. 49, no. 4, pp. 400–403, 2002.
51- M. Kranjc, F. Bajd, I. Serša, and D. Miklavčič, “Magnetic resonance electrical impedance tomography for measuring electrical conductivity during electroporation,” Physiol. Meas., vol. 35, no. 6, p. 985, 2014.
2- E. Neumann, M. Schaefer‐Ridder, Y. Wang, and P. Hofschneider, “Gene transfer into mouse lyoma cells by electroporation in high electric fields.,” EMBO J., vol. 1, no. 7, pp. 841–845, 1982.
3- R. V Davalos, L. M. Mir, and B. Rubinsky, “Tissue ablation with irreversible electroporation,” Ann. Biomed. Eng., vol. 33, no. 2, p. 223, 2005.
4- Z. Vasilkoski, A. T. Esser, T. R. Gowrishankar, and J. C. Weaver, “Membrane electroporation: The absolute rate equation and nanosecond time scale pore creation,” Phys. Rev. E, vol. 74, no. 2, p. 21904, 2006.
5- M. Bier, W. Chen, T. R. Gowrishankar, R. D. Astumian, and R. C. Lee, “Resealing dynamics of a cell membrane after electroporation,” Phys. Rev. E, vol. 66, no. 6, p. 62905, 2002.
6- D. S. K. Lu, S. T. Kee, and E. W. Lee, “Irreversible electroporation: ready for prime time?,” Tech. Vasc. Interv. Radiol., vol. 16, no. 4, pp. 277–286, 2013.
7- T. Kotnik, W. Frey, M. Sack, S. H. Meglič, M. Peterka, and D. Miklavčič, “Electroporation-based applications in biotechnology,” Trends Biotechnol., vol. 33, no. 8, pp. 480–488, 2015.
8- E. W. Lee et al., “Electron microscopic demonstration and evaluation of irreversible electroporation-induced nanopores on hepatocyte membranes,” J. Vasc. Interv. Radiol., vol. 23, no. 1, pp. 107–113, 2012.
9- S. Orlowski, J. Belehradek Jr, C. Paoletti, and L. M. Mir, “Transient electropermeabilization of cells in culture: increase of the cytotoxicity of anticancer drugs,” Biochem. Pharmacol., vol. 37, no. 24, pp. 4727–4733, 1988.
10- G. Sersa et al., “Electrochemotherapy of small tumors; the experience from the ESOPE (European Standard Operating Procedures for Electrochemotherapy) group,” in Clinical aspects of Electroporation, Springer, 2011, pp. 93–102.
11- D. Miklavčič, “Network for development of electroporation-based technologies and treatments: COST TD1104,” J. Membr. Biol., vol. 245, no. 10, pp. 591–598, 2012.
12- M. L. Yarmush, A. Golberg, G. Serša, T. Kotnik, and D. Miklavčič, “Electroporation-based technologies for medicine: principles, applications, and challenges,” Annu. Rev. Biomed. Eng., vol. 16, pp. 295–320, 2014.
13- S. Mahnič-Kalamiza, E. Vorobiev, and D. Miklavčič, “Electroporation in food processing and biorefinery,” J. Membr. Biol., vol. 247, no. 12, pp. 1279–1304, 2014.
14- I. Edhemovic et al., “Intraoperative electrochemotherapy of colorectal liver metastases,” J. Surg. Oncol., vol. 110, no. 3, pp. 320–327, 2014.
15- J. C. Weaver, “Electroporation of cells and tissues,” IEEE Trans. plasma Sci., vol. 28, no. 1, pp. 24–33, 2000.
16- L. Appelbaum, E. Ben-David, J. Sosna, Y. Nissenbaum, and S. N. Goldberg, “US findings after irreversible electroporation ablation: radiologic-pathologic correlation,” Radiology, vol. 262, no. 1, pp. 117–125, 2012.
17- E. Ben-David, L. Appelbaum, J. Sosna, I. Nissenbaum, and S. N. Goldberg, “Characterization of irreversible electroporation ablation in in vivo porcine liver,” Am. J. Roentgenol., vol. 198, no. 1, pp. W62–W68, 2012.
18- G. Onik, P. Mikus, and B. Rubinsky, “Irreversible electroporation: implications for prostate ablation,” Technol. Cancer Res. Treat., vol. 6, no. 4, pp. 295–300, 2007.
19- K. F. Chu and D. E. Dupuy, “Thermal ablation of tumours: biological mechanisms and advances in therapy,” Nat. Rev. Cancer, vol. 14, no. 3, pp. 199–208, 2014.
20- M. Ahmed, C. L. Brace, F. T. Lee Jr, and S. N. Goldberg, “Principles of and advances in percutaneous ablation,” Radiology, vol. 258, no. 2, pp. 351–369, 2011.
21- P. A. Garcia, J. H. Rossmeisl, R. E. Neal, T. L. Ellis, and R. V Davalos, “A parametric study delineating irreversible electroporation from thermal damage based on a minimally invasive intracranial procedure,” Biomed. Eng. Online, vol. 10, no. 1, p. 34, 2011.
22- S. Corovic, A. Zupanic, and D. Miklavcic, “Numerical modeling and optimization of electric field distribution in subcutaneous tumor treated with electrochemotherapy using needle electrodes,” IEEE Trans. Plasma Sci., vol. 36, no. 4, pp. 1665–1672, 2008.
23- D. Miklavčič, K. Beravs, D. Šemrov, M. Čemažar, F. Demšar, and G. Serša, “The importance of electric field distribution for effective in vivo electroporation of tissues,” Biophys. J., vol. 74, no. 5, pp. 2152–2158, 1998.
24- M. Kranjc et al., “In situ monitoring of electric field distribution in mouse tumor during electroporation,” Radiology, vol. 274, no. 1, pp. 115–123, 2015.
25- O. Adeyanju, H. Al-Angari, and A. Sahakian, “The optimization of needle electrode number and placement for irreversible electroporation of hepatocellular carcinoma,” Radiol. Oncol., vol. 46, no. 2, pp. 126–135, 2012.
26- M. B. Sano, M. R. DeWitt, S. D. Teeter, and L. Xing, “Optimization of a single insertion electrode array for the creation of clinically relevant ablations using high-frequency irreversible electroporation,” Comput. Biol. Med., vol. 95, pp. 107–117, 2018.
27- G. Merola, “Design and characterization of a minimally invasive bipolar electrode for electroporation,” Politecnico di Torino, 2020.
28- F. Pedersoli et al., “Single-needle electroporation and interstitial electrochemotherapy: in vivo safety and efficacy evaluation of a new system,” Eur. Radiol., vol. 29, no. 11, pp. 6300–6308, 2019.
29- C. B. Arena et al., “High-frequency irreversible electroporation (H-FIRE) for non-thermal ablation without muscle contraction,” Biomed. Eng. Online, vol. 10, no. 1, pp. 1–21, 2011.
30- S. Čorović, M. Pavlin, and D. Miklavčič, “Analytical and numerical quantification and comparison of the local electric field in the tissue for different electrode configurations,” Biomed. Eng. Online, vol. 6, no. 1, p. 37, 2007.
31- A. Ivorra and B. Rubinsky, “In vivo electrical impedance measurements during and after electroporation of rat liver,” Bioelectrochemistry, vol. 70, no. 2, pp. 287–295, 2007.
32- U. F. Pliquett and K. H. Schoenbach, “Changes in electrical impedance of biological matter due to the application of ultrashort high voltage pulses,” IEEE Trans. Dielectr. Electr. Insul., vol. 16, no. 5, pp. 1273–1279, 2009.
33- S. M. Firoozabadi, “Finite Element Analysis of Tissue Conductivity during High-frequency and Low-voltage Irreversible Electroporation,” Iran. J. Med. Phys., vol. 14, no. 3, pp. 135–140, 2017.
34- A. Khorasani, S. M. Firoozabadi, and Z. Shankayi, “Conductivity change with needle electrode during high frequency irreversible electroporation: a finite element study,” Polish J. Med. Phys. Eng., vol. 25, no. 4, pp. 237–242, 2019.
35- M. G. Moisescu, M. Radu, E. Kovacs, L. M. Mir, and T. Savopol, “Changes of cell electrical parameters induced by electroporation. A dielectrophoresis study,” Biochim. Biophys. Acta (BBA)-Biomembranes, vol. 1828, no. 2, pp. 365–372, 2013.
36- T. Garcia-Sanchez, D. Voyer, C. Poignard, and L. M. Mir, “Physiological changes may dominate the electrical properties of liver during reversible electroporation: Measurements and modelling,” Bioelectrochemistry, vol. 136, p. 107627, 2020.
37- B. López-Alonso, H. Sarnago, O. Lucía, P. Briz, and J. M. Burdío, “Real-Time Impedance Monitoring During Electroporation Processes in Vegetal Tissue Using a High-Performance Generator,” Sensors, vol. 20, no. 11, p. 3158, 2020.
38- Y. Zhao, S. Zheng, N. Beitel-White, H. Liu, C. Yao, and R. V Davalos, “Development of a Multi-Pulse Conductivity Model for Liver Tissue Treated With Pulsed Electric Fields,” Front. Bioeng. Biotechnol., vol. 8, p. 396, 2020.
39- N. Beitel-White et al., “Multi-tissue Analysis on the Impact of Electroporation on Electrical and Thermal Properties,” IEEE Trans. Biomed. Eng., 2020.
40- D. Sel, D. Cukjati, D. Batiuskaite, T. Slivnik, L. M. Mir, and D. Miklavcic, “Sequential finite element model of tissue electropermeabilization,” IEEE Trans. Biomed. Eng., vol. 52, no. 5, pp. 816–827, 2005.
41- P. A. Garcia et al., “Intracranial nonthermal irreversible electroporation: in vivo analysis,” J. Membr. Biol., vol. 236, no. 1, pp. 127–136, 2010.
42- A. Khorasani, “A numerical study on the effect of conductivity change in cell kill distribution in irreversible electroporation,” Polish J. Med. Phys. Eng., vol. 26, no. 2, pp. 69–76, 2020.
43- A. Khorasani, S. M. Firoozabadi, and Z. Shankayi, “Conductivity Changes of Liver Tissue during Irreversible Electroporation and Calculation of the Electric Field Distribution,” mdrsjrns, vol. 9, no. 2. pp. 227–232, 2018.
44- E. Ben-David et al., “Irreversible electroporation: treatment effect is susceptible to local environment and tissue properties,” Radiology, vol. 269, no. 3, pp. 738–747, 2013.
45- U. Pliquett, R. Langer, and J. C. Weaver, “Changes in the passive electrical properties of human stratum corneum due to electroporation,” Biochim. Biophys. Acta (BBA)-Biomembranes, vol. 1239, no. 2, pp. 111–121, 1995.
46- A. Ivorra, B. Al-Sakere, B. Rubinsky, and L. M. Mir, “In vivo electrical conductivity measurements during and after tumor electroporation: conductivity changes reflect the treatment outcome,” Phys. Med. Biol., vol. 54, no. 19, p. 5949, 2009.
47- P. A. Garcia, C. B. Arena, and R. V Davalos, “Towards a predictive model of electroporation-based therapies using pre-pulse electrical measurements,” in 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society, pp. 2575–2578, 2012.
48- A. Ivorra, L. M. Mir, and B. Rubinsky, “Electric field redistribution due to conductivity changes during tissue electroporation: experiments with a simple vegetal model,” in World Congress on Medical Physics and Biomedical Engineering, September 7-12, 2009, Munich, Germany, pp. 59–62, 2009.
49- S. Corovic, I. Lackovic, P. Sustaric, T. Sustar, T. Rodic, and D. Miklavcic, “Modeling of electric field distribution in tissues during electroporation,” Biomed. Eng. Online, vol. 12, no. 1, p. 16, 2013.
50- R. V Davalos, B. Rubinsky, and D. M. Otten, “A feasibility study for electrical impedance tomography as a means to monitor tissue electroporation for molecular medicine,” IEEE Trans. Biomed. Eng., vol. 49, no. 4, pp. 400–403, 2002.
51- M. Kranjc, F. Bajd, I. Serša, and D. Miklavčič, “Magnetic resonance electrical impedance tomography for measuring electrical conductivity during electroporation,” Physiol. Meas., vol. 35, no. 6, p. 985, 2014.
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| Issue | Vol 8 No 1 (2021) | |
| Section | Literature (Narrative) Review(s) | |
| DOI | https://doi.org/10.18502/fbt.v8i1.5859 | |
| Keywords | ||
| Electroporation Electrical Conductivity Electric Field Numerical Modeling | ||
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How to Cite
1.
Khorasani A. Clinical Usage of Tissue Electrical Conductivity during the Electroporation: An Essential and Useful Factor. Frontiers Biomed Technol. 2021;8(1):61-69.
