Abstract
This paper presents the development of a model framework for plasma-biofilm and plasma-tissue interactions that can link molecular simulation of plasma chemistry to functions at a cell population level or a tissue level. This is aided with a reactive penetration model for mass transfer of highly transient plasma species across the gas–liquid boundary and a panel of electrical and thermal thresholds considering pain sensation, protein denaturation and lethal electric currents. Application of this model reveals a number of previously little known findings, for example the penetration of plasma chemistry into highly hydrated biofilms is about 10–20 μm deep for low-power He–O2 plasma and this is closely correlated to the penetration of liquid-phase plasma chemistry dominated by O2 −, H2O2, and HO2 or O2 −, H2O2, and O3. Optimization by manipulating liquid-phase chemistry is expected to improve the penetration depth to 40–50 μm. For direct plasma treatment of skin tissues at radio frequencies, the key tolerance issue is thermal injuries even with a tissue temperature <50 °C and these can lead to induction of pain and protein denaturation at a small discharge density of 8–15 mA/cm2 over few tens of seconds. These and other results presented offer opportunities to improve plasma-biofilm and plasma-tissue interactions. The model framework reported may be further extended and can be used to non-biomedical applications of low-temperature plasmas.
Similar content being viewed by others
References
Kong MG, Kroesen G, Morfill G, Nosenko T, Shimizu T, van Dijk J, Zimmermann JL (2009) New J Phys 11:115012
Fridman G, Friedman G, Gutsol A, Shekhter AB, Vasilets VN, Fridman A (2008) Plasma Process Polym 5(6):503
Ginsberg GG, Barkun AN, Bosco JJ, Burdick JS, Isenberg GA, Nakao NL, Petersen BT, Silverman WB, Slivka A, Kelsey PB (2002) Gastrointest Endosc 55(7):807
Isbary G, Morfill G, Schimidt HU, Georgi M, Ramrath K, Heinlin J, Karrer S, Landthaler M, Schimizu T, Steffes B, Bunk W, Monetti R, Zimmermann JL, Pompl R, Stolz W (2010) Br J Dermatol 163(1):78
Kim HH (2004) Plasma Process Polym 1(2):91
Locke BR, Sato M, Sunka P, Hoffmann MR, Chang JS (2006) Ind Eng Chem Res 45(3):882
Liston EM, Wertheimer MR, Martinu L (1993) J Adhes Sci Technol 7:1091
Siow KS, Britcher L, Kumar S, Griesser HJ (2006) Plasma Process Polym 3(6–7):392
Vleugels M, Shama G, Deng XT, Greenacre E, Brocklehurst T, Kong MG (2004) IEEE Trans Plasma Sci 33(2):824
Perni S, Liu DW, Shama G, Kong MG (2008) J Food Protect 71(2):302
Niemira BA (2012) J Food Sci 77(3):M171
Neumann E, Schaeferridder M, Wang Y, Hofschneider PH (1982) EMBO J 1(7):841
Aihara H, Miyazaki J (1998) Nat Biotech 16(9):867
Chalise PR, Perni S, Shama G, Novac BM, Smith IR, Kong MG (2006) Appl Phys Lett 89(15):153902
Gentile AC, Kushner MJ (1995) J Appl Phys 78(3):2074
Atkinson R, Baulch DL, Cox RA, Hampson RF, Kerr JA, Rossi MJ, Troe J (1997) J Phys Chem Ref Data 26(6):1329
Wang YH, Zhang YT, Wang DZ, Kong MG (2007) Appl Phys Lett 90:071501
Liu DX, Bruggeman P, Iza F, Rong MZ, Kong MG (2010) Plasma Sour Sci Technol 19(2):025018
Sakiyama Y, Graves DB, Chang H-W, Shimizu T, Morfill G (2012) J Phys D Appl Phys 45:425201
Murakami T, Niemi K, Gans T, O’Connell D, Graham WG (2013) Plasma Sour Sci Technol 22:015003
Van Gaens W, Bogaerts A (2013) J Phys D Appl Phys 46(7):275201
Walsh JL, Shi JJ, Kong MG (2006) Appl Phys Lett 89(16):161505
Reuter S, Winter J, Schmidt-Bleker A, Trsp H, Hammer MU, Weltmann KD (2012) IEEE Trans Plasma Sci 40(11):2788
Costerton JW, Stewart PS, Greenberg EP (1999) Science 284(5418):1318
Bergan T (1981) Rev Infect Dis 3(1):45
Tannock IF, Lee CM, Tunggal JK, Cowan DSM, Egorin MJ (2002) Clin Cancer Res 8(3):878
Zhang TC, Bishop PL (1994) Water Res 28(11):2267
Stewart PS (1996) Antimicrob Agents Chemother 40(11):3517
Wang CJ, Srivastava N, Dibble TS (2009) Appl Phys Lett 95(5):051501
Langer R (1998) Nature 392(6679):5
Babaeva NY, Kushner MJ (2010) J Phys D Appl Phys 43:185206
Babaeva NY, Ning N, Graves DB, Kushner MJ (2012) J Phys D Appl Phys 45:115203
Dower WJ, Miller JF, Ragsdale CW (1988) Nucleic Acids Res 16(13):6127
Coderre TJ, Katz J, Vaccarino AL, Melzack R (1993) Pain 52(3):259
Xu F, Lu TJ, Seffen KA (2008) J Mech Phys Solids 56(5):1852
Green DR, Reed JC (1998) Science 281:1309
Treybal RE (1980) Mass-transfer operations, 3rd edn. McGraw-Hill Kohakusha Ltd, Tokyo
Wust P, Hildebrandt B, Sreenivasa G, Rau B, Gellermann J, Riess H, Felix R, Schlag PM (2002) Lancet Oncol 3(8):487
Craig AD, Reiman EM, Evans A, Bushnell MC (1996) Nature 384:258
Li Z, Scheraga HA (1987) Proc Natl Acad Sci USA 84(19):6611
Kitano H (2002) Nature 420:206
Nielsen CB, Harper HA (1954) Exp Biol Med 86:753
Kingdon KH (1960) Phys Med Biol 5(1):1
Krueger AP, Andriese PC, Kotaka S (1963) Int J Biometeorol 7(1):3
Pratt R, Barnard RW (1960) Am Pharm Ass Sci Ed 49:643
Kellogg EW III, Yost MG, Barthakur N, Krueger AP (1979) Nature 281:400
Krueger AP, Reed EJ (1976) Science 193(4259):1209
Deng XT, Shi JJ, Kong MG (2007) J Appl Phys 101(7):074701
Fridman G, Shereshevsky A, Jost MM, Brooks AD, Fridman A, Gutsol A, Vasilets V, Friedman G (2007) Plasma Chem Plasma Process 27(2):163
Lee HJ, Shon CH, Kim YS, Kim S, Kim GC, Kong MG (2009) New J Phys 11:115026
Vandamme M, Robert E, Pesnel S, Barbosa E, Dozias S, Sobilo J, Lerondel S, Le Pape A, Pouvesle JM (2012) Plasma Process Polym 7(3–4):264
Park G, Ryu YH, Hong YJ, Choi EH (2012) Appl Phys Lett 100(6):063703
Krueger AP, Smith RF (1959) Nature 183:1332
Krueger AP, Smith RF, Gan Go Ing (1957) J Gen Physiol 41(2):359
Kanazawa S, Kogoma M, Moriwaki T, Okazaki S (1988) J Phys D Appl Phys 21(5):838
Lieberman MA, Lichtenberg AJ (2005) Principle of plasma discharges and materials processing, 2nd edn. Wiley, Hoboken
Lodish H, Berk A, Zipursky SL, Matsudaira P, Baltimore D, Darnell J (2000) Molecular cell biology, 4th edn. W. H. Freeman, New York
ArthroCare, http://phx.corporate-ir.net/phoenix.zhtml?c=100786&p=irol-newsArticle&ID=300673&highlight=. Accessed on September 21, 2013
PlasmaJet from Plasma Surgical, http://www.plasmasurgical.com/pdf/1.pdf. Accessed on September 21, 2013
Lewis WK, White WG (1924) Ind Eng Chem 16(12):1215
Higbie R (1935) Am Inst Chem Eng 31:365
Dankwertz PV (1951) Ind Eng Chem 43(6):1460
Yang AJ, Wang XH, Rong MZ, Liu DX, Iza F, Kong MG (2011) Phys Plasma 18(11):113503
Yuan X, Raja LL (2003) IEEE Trans Plasma Sci 31(4):495
Liu DW, Iza F, Kong MG (2008) Appl Phys Lett 93:261503
Wang Q, Economou DJ, Donnelly VM (2006) J Appl Phys 100:023301
Sakiyama Y, Graves DB (2009) Plasma Sources Sci Technol 18:025022
Shi JJ, Kong MG (2006) Phys Rev Lett 96:105009
Iza F, Lee JK, Kong MG (2007) Phys Rev Lett 99:075004
Liu DX, Rong MZ, Wang XH, Iza F, Kong MG, Bruggeman P (2010) Plasma Process Polym 7(9–10):846
Liu DX, Iza F, Wang XH, Kong MG, Rong MZ (2011) Appl Phys Lett 98(22):221501
Liu DX, Yang AJ, Wang XH, Rong MZ, Iza F, Kong MG (2012) J Phys D Appl Phys 45(30):305205
Stewart PS (2003) J Bacteriol 185(5):1485
Stewart PS (1998) Biotechnol Bioeng 59:261
Klapper I, Dockery J (2010) SIAM Rev 52(2):221
Buettner G and Mason RP, Critical Rev. Oxidative Stress and Aging: Advances in Basic Science, Diagnostics, and Intervention (2003) Ed Cutler RG and Rodriguez, World Scientific, New Jersey, London, Singapore, Hong Kong, vol. 1, Chapter 2, pp. 27–38
Newman JS (1973) Electrochemical systems. Prentice-Hall, Englewood Cliffs
Cents AHG, Brilman DWF, Versteeg GF (2005) Chem Eng Sci 60:5830
Pastina B, LaVerne JA (2001) J Phys Chem A 105:9316
Barat F, Gilles L, Hickel B, Lesigne B (1971) J Phys Chem 75(14):2177
Schweitzer C, Schmidt R (2003) Chem Rev 103:1685
Heikes BG (1984) Atmos Environ 18(7):1433
He ZG, Liu JS, Cai WM (2005) J Electrostat 63:371
Emfietzoglou D, Nikojoo HA (2007) Radiat Res 167(1):110
Wizke M, Rumbach P, Go DB, Sankaran RM (2012) J Phys D Appl Phys 45:442001
Walsh JL, Liu DX, Iza F, Rong MZ, Kong MG (2010) J Phys D Appl Phys 43(3):032001
Eyring H (1936) J Chem Phys 4:283
Newman JS (1973) Electrochemical systems. Prentice-Hall, Englewood Cliffs
Dobrynin D, Arjunan K, Fridman A, Friedman G, Clyne AM (2011) J Phys D Appl Phys 44:075201
Boxhammer V, Morfill GE, Jokipii JR, Shimizu T, Klampfl T, Li Y-F, Koritzer J, Schlegel J, Zimmermann JL (2012) New J Phys 14:113042
Lee HWK, Lee HW, Kang SK, Kim HY, Won IH, Jeon SM, Lee JK (2013) Plasma Sources Sci Technol 22:055008
Kong MG, MRS Spring 2012; Kong GEC 2012; Kushner MJ, ICOPS 2013; Kong MG, ISPC 2013
Whitman WG (1923) Chem Met Eng 29:147
Krishna R, Standart GL (2010) A I Ch E J 22(2):383
Higbie R (1935) Trans Am Inst Chem Eng 31(2):365
Mackay D, Shiu WY (1981) J Phys Chem Ref Data 10(4):1175
Sotelo JL, Beltran FJ, Benitez FJ, Beltran-Heredia J (1989) Water Res 23(10):1239
Blauwhoff PMM, Versteeg GF, van Swaaij WPM (1984) Chem Eng Sci 39(2):207
Stewart PS (2003) J. Bacteriol 185(5):1485
Richard T Cornell composting files, science and engineering, calculating the oxygen diffusion coefficient in water, http://compost.css.cornell.edu/oxygen/oxygen.diff.water.html, accessed on September 22, 2013
Gong XB, Takagi S, Huang HX, Matsumoto Y (2007) Chem Eng Sci 62(4):1081
Svishchev IM, Plugatyr AY (2005) J Phys Chem B 109:4123
Zhang JJ, Oloman CW (2005) J Appl Electrochem 35:945
Kahlert H, Retter U (1998) J Phys Chem 102:8757
Nedeltchev S, Jordan U, Schumpe A (2007) Chem Eng Sci 62:6263
Limtrakul S, Kongto A, Vatanatham T, Ramachandran PA (2010) Chem Eng Sci 65(15):4420
Marchello JM, Toor HL (1963) Ind Eng Chem 2(1):8
Toor HL, Marchello JM (1958) A I Ch E J 4(1):97
Sieck LW, Herron JT, Green DS (2000) Plasma Chem Plasma Process 20:235
Molina-Cuberos GJ, Lopez-Moreno JJ, Rodrigo R, Lichtenegger H, Schwingenschuh K (2001) Adv Space Res 27(1):1801
Lindinger W, Albritton DL (1975) J Chem Phys 62:3517
Shi JJ, Liu DW, Kong MG (2006) Appl Phys Lett 89:081502
Liu JJ, Kong MG (2011) J Phys D Appl Phys 44(34):345203
Vroom JM, De Grauw KJ, Gerritsen HC, Bradshaw DJ, Marsh PD, Watson GK, Birmingham JJ, Allison C (1999) Appl Environ Microbiol 65(8):3502
Sander R (1999) Compilation of Henry’s law constants for inorganic and organic species of potential importance in environmental chemistry (Version 3). http://www.henrys-law.org. Accessed in Nov 2008
Perry’s Chemical Engineers’ Handbook, P173
Orazov M, Sakiyama Y, Graves DB (2012) J Phys D Appl Phys 45:445201
Deng S, Ruan R, Mok CK, Huang G, Lin X, Chen P (2007) J Food Sci 72(2):M62
Perni S, Shama G, Kong MG (2008) J. Food Protect 71(8):1619
Ragni L, Berardinelli A, Vannini L, Montanari C, Sim F, Guerzoni ME, Guarnieri A (2010) J Food Eng 100(1):125
Noriega W, Shama G, Laca A, Diaz M, Kong MG (2011) Food Microbiol 28(7):1293
Dobrynin D, Fridman G, Friedman G, Fridman A (2009) New J Phys 11:115020
Lademann J, Kramer A, Weltmann KD, Hartmann B, Fluhr JW, Hinz P, Hubner G, Lademann O, Ottomann C, Richter H, Alborova A, Humme D, Patzelt A (2009) J. Biomed Optics 14(5):054025
Lademann J, Ulrich C, Richter H, Kluschke F, Lademann O, Kramer A, Weltmann KD, Lange-Asschenfeldt B (2013) Clin Plasma Med 1:5
Foster KR (2000) IEEE Trans Plasma Sci 28(1):15
Chichel A, Skowronek J, Kubasewska M, Kanikowski M (2007) Rep Pract Radiother 12(5):267
Pennes HH (1948) J Appl Physiol 1:93
Xu F, Lu TJ, Seffen KA (2008) Acta Mech Sinica 24:1
Edd JF, Horowitz L, Davalos RV, Mir LM, Rubinsky B (2006) IEEE Trans Biomed Eng 53(5):1409
Lee RC (1997) Curr Probl Surg Sep 34(9):677
Lee RC and Astumian RD (1996) 22(7): 509
Weaver JC, Chizmadzhev Yu A (1996) Bioelectrochem Bioenetics 41(2):135
Marrink SJ, de Vries AH, Tieleman DP (2009) Biochim Biophys Acta Biomembr 1788(1):149
Joshi RP, Schoenbach KH (2000) Phys Rev E 62(1):1025
Vernier PT, Ziegler MJ, Sun Y, Chang W, Gundersen MA, Tieleman DP (2006) J Am Chem Soc 128(9):6288
Hu Q, Zhang Z, Kong MG, Joshi RP (2013) Phys Rev E 87(3):032704
Shao Y et al (2006) Phys Chem Chem Phys 8(27):3172
Henzler-Wildman KA, Lei M, Thai V, Kerns SJ, Karplus M, Kern D (2007) Nature 450:913
Kamerlin SCL, Warshel A (2009) Proteins Struct Funct Bioinform 78(6):1339
Chang IA, Nguyen UD (2004) Biomed Eng Online 3:27
Kosturski N, Margenov S, Vutov Y (2012) AIP Conf Proc 1497:120
Henriques FC, Moritz AR (1947) Am J Pathol 23:531
Berjano EJ (2006) BioMed Eng OnLine 5:24
Park J, Henins I, Herrmann HW, Selwyn GS (2001) J Appl Phys 89(1):15
Walsh JL, Zhang YT, Iza F, Kong MG (2008) Appl Phys Lett 93(22):221505
Yang AJ, Rong MZ, Wang XH, Liu DX, Kong MG (2013) J Phys D Appl Phys 46(41):415201
Sakiyama Y, Graves DB (2006) J Phys D Appl Phys 39:3644
Gabriel S, Lau RW, Gabriel C (1996) Phys Med Biol 41:2271
Diller KR (1994) Ann N Y Acad Sci 720:38
D’Ambrosio V, Dughiero F (2007) Med Bio Eng Comput 45:459
Kurgan E, Gas P (2011) PREEGLAD ELECKTROTECHINCZNY 87(12b):103
Safety Code 6 Regulation, Limits of human exposure to radio frequency electromagnetic fields in the frequency range from 3 kHz to 300 GHz, Health Canada HC Pub: 091029, 2009
Deng XT, Shi JJ, Kong MG (2006) IEEE Trans Plasma Sci 34(4):1310
Deng XT, Shi JJ, Chen HL, Kong MG (2007) Appl Phys Lett 90(1):013903
Ellerweg D, Benedikt J, von Keudell A, Knake N, Schulz-von der Gathern V (2010) New J Phys 12(1):013021
Waskoenig J, Niemi K, Knake N, Graham LM, Reuter S, Schulz-von der Gathern V, Gans T (2010) Plasma Sour Sci Technol 19(4):045018
O’Connell D, Cox LJ, Hyland WB, McMahon SJ, Reuter S, Graham WG, Gans T, Currell FJ (2011) Appl Phys Lett 98(4):043701
Lissi EA, Encinas MV, Lemp E, Rubio MA (1993) Chem Rev 93(2):699
Schweitzer C, Schmidt R (2003) Chem Rev 103(5):1685
Ionin AA, Kochetov IV, Yuryshev NN (2007) J Phys D Appl Phys 40(2):R25
Sousa JS, Bauville G, Lacour B, Puech V, Touzeau M, Pitchford LC (2008) Appl Phys Lett 93(10):011502
Yusupov M, Neyts EC, Simon P, Bergiyorov G, Snoeckx R, van Duin ACT, Bogaerts A (2014) J Phys D Appl Phys 47:025025
Yusupov M, Bogaert A, Huygh S, Snoeckx R, van Duin ACT, Neyts EC (2013) J Phys Chem C 117:5993
Fridovich I (1978) Science 201(4):875
Reaume AG, Elliott JL, Hoffman EK, Kowall NW, Ferrante RJ, Siwek DR, Wilcox HM, Flood DG, Beal MF, Brown RH Jr, Scott RW, Snider WD (1996) Nat Genet 13:43
Yang AJ, Rong MZ, Wang XH, Liu DX, Kong MG (2013) J Phys D Appl Phys 46(41):415201
Pryor WA (1986) Ann Rev Physiol 48:657
Behl C, Davis JB, Lesley R, Schubert D (1994) Cell 77(6):817
Imlay JA (2008) Ann Rev Biochem 77:755
Janero DR (1990) Free Radic Biol Med 9(6):515
Gutteridge JMC (1995) Clin Chem 41(12):1819
Stewart PS, Peyton BM, Drury WJ, Murga R (1993) Appl Environ Microbiol 59(1):327
Rittmann BE, McCarty PL (1980) Biotechnol Bioeng 22:2343
Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP (1998) Science 280:295
Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersboll BK, Molin S (2000) Microbiology 146:2395
Kong MG, Deng XT, Shi JJ, Shama G, Greenacre E and Buckhurst T, presented at ElectroMed 2005 Symposium, May 15–18, 2005, Portland, Oregon, USA
Xiong ZL, Du TF, Lu XP, Cao YG, Pan Y (2011) Appl Phys Lett 98:221503
Imlay JA, Linn S (1986) J Bacteriol 166:519
Otero MC, Nader-Macias ME (2006) Anim Reprod Sci 96:35
Broadwater WT, Hoehn RC, King PH (1973) Appl Microbiol 26:391
Pei X, Lu X, Liu J, Liu D, Yang Y, Ostrikov K, Chu PK, Pan Y (2012) J Phys D Appl Phys 45:165205
Ikawa S, Kitano K, Hamaguchi S (2009) Plasma Process Polym 7(1):33
Balcon N, Aanesland A, Boswell R (2007) Plasma Sour Sci Technol 16(2):217
Shi JJ, Zhang J, Qiu G, Walsh JL, Kong MG (2008) Appl Phys Lett 93(4):041502
Li WP, Zhu MS et al (2006) Burn 32:986
Eden JG, Park S-J, Ostrom NP, McCain ST, Wagner CJ, Vojak BA, Chen J, Liu C, von Allmen P, Zenhausern F, Sadler DJ, Jensen C, Wilcox DL, Ewing JJ (2003) J Phys D Appl Phys 36(23):2869
Cao Z, Nie Q, Bayliss DL, Walsh JL, Ren CS, Wang DZ, Kong MG (2010) Plasma Sour Sci Technol 19(2):025003
Graves DB (2012) J Phys D Appl Phys 45(26):263001
Stamler JS, Singel DJ, Loscalzo J (1992) Science 258(5090):1898
Richmonds C, Sankaran RM (2008) Appl Phys Lett 93(13):131501
Li J, Sato M, Ohshima T (2007) Thin Solid Films 515(9):4283
Acknowledgments
This work was supported by the National Natural Science Foundation of China (Grant No. 51307134 and 51221005), and Old Dominion University, USA.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Chen, C., Liu, D.X., Liu, Z.C. et al. A Model of Plasma-Biofilm and Plasma-Tissue Interactions at Ambient Pressure. Plasma Chem Plasma Process 34, 403–441 (2014). https://doi.org/10.1007/s11090-014-9545-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11090-014-9545-1