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In-Package Inactivation of Pathogenic and Spoilage Bacteria Associated with Poultry Using Dielectric Barrier Discharge-Cold Plasma Treatments

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Abstract

The goal of this study was to test the efficacy of in-package dielectric barrier discharge-cold plasma (DBD-CP) treatment to inactivate poultry-associated spoilage (Pseudomonas fluorescens) and pathogenic (Salmonella enterica Typhimurium, Campylobacter jejuni) bacteria. Liquid cultures of the bacterial isolates were sealed within packages containing ambient air (Trial 1) or modified air (65% O2:30% CO2:5% N2; Trial 2). The packages were subjected to treatment times ranging from 30 to 180 s, and after 24 h incubation at 4 °C, bacterial titers were determined. The DBD-CP system completely inactivated the four isolates tested, although the in-package gas composition and treatment times were isolate-specific. Both C. jejuni isolates were completely inactivated between 30 s (modified air) and 120 s (ambient air), while modified air was required for the complete inactivation of S. typhimurium (90 s) and P. fluorescens (180 s). This DBD-CP system is effective for inactivating major poultry-associated spoilage and pathogenic bacteria in liquid culture, and through this study, system parameters to optimize inactivation were determined. This study demonstrates the potential for DBD-CP treatment to inactivate major bacteria of economic interest to the poultry industry, thus potentially allowing for reduced spoilage (e.g., longer shelf life) and increased safety of poultry products.

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Abbreviations

DBD-CP:

Dielectric barrier discharge-cold plasma

MA:

Modified air

CFU:

Colony forming units

References

  1. Anonymous (2014) Campylobacter general information. http://www.cdc.gov/nczved/divisions/dfbmd/diseases/campylobacter/. Accessed Sept 2015

  2. Anonymous (2014) Reports of selected Salmonella outbreak investigations. http://www.cdc.gov/salmonella/outbreaks.html. Accessed Sept 2015

  3. Atack JM, Kelly DJ (2009) Oxidative stress in Campylobacter jejuni: responses, resistance and regulation. Future Microbiol 4(6):677–690. doi:10.2217/fmb.09.44

    Article  CAS  PubMed  Google Scholar 

  4. Attri P, Arora B, Choi EH (2013) Utility of plasma: a new road from physics to chemistry. Rsc Adv 3(31):12540–12567. doi:10.1039/c3ra41277f

    Article  CAS  Google Scholar 

  5. Bardos L, Barankova H (2010) Cold atmospheric plasma: sources, processes, and applications. Thin Solid Films 518(23):6705–6713. doi:10.1016/j.tsf.2010.07.044

    Article  CAS  Google Scholar 

  6. Batz MB, Hoffmann S, Morris JG Jr (2012) Ranking the disease burden of 14 pathogens in food sources in the United States using attribution data from outbreak investigations and expert elicitation. J Food Prot 75(7):1278–1291. doi:10.4315/0362-028x.jfp-11-418

    Article  PubMed  Google Scholar 

  7. Bolton DJ (2015) Campylobacter virulence and survival factors. Food Microbiol 48:99–108. doi:10.1016/j.fm.2014.11.017

    Article  PubMed  Google Scholar 

  8. Fernández A, Noriega E, Thompson A (2013) Inactivation of Salmonella enterica serovar Typhimurium on fresh produce by cold atmospheric gas plasma technology. Food Microbiol 33(1):24–29. doi:10.1016/j.fm.2012.08.007

    Article  PubMed  Google Scholar 

  9. Fernández A, Shearer N, Wilson DR, Thompson A (2012) Effect of microbial loading on the efficiency of cold atmospheric gas plasma inactivation of Salmonella enterica serovar Typhimurium. Int J Food Microbiol 152(3):175–180. doi:10.1016/j.ijfoodmicro.2011.02.038

    Article  PubMed  Google Scholar 

  10. Garrity G, Bell J, Lilburn T (2005) Pseudomonadales Orla-Jensen 1921, 270AL. In: Brenner D, Krieg N, Staley J et al. (eds) Bergey’s Manual® of Systematic Bacteriology. Springer US, pp 323-442. doi:10.1007/0-387-28022-7_9

  11. Gaunt LF, Beggs CB, Georghiou GE (2006) Bactericidal action of the reactive species produced by gas-discharge nonthermal plasma at atmospheric pressure: a review. IEEE Trans Plasma Sci 34(4):1257–1269. doi:10.1109/tps.2006.878381

    Article  CAS  Google Scholar 

  12. Graves DB (2014) Low temperature plasma biomedicine: a tutorial review. Phys Plasmas 21(8):080901. doi:10.1063/1.4892534

    Article  Google Scholar 

  13. Han L, Patil S, Keener KM, Cullen PJ, Bourke P (2014) Bacterial inactivation by high-voltage atmospheric cold plasma: influence of process parameters and effects on cell leakage and DNA. J Appl Microbiol 116:784–794

    Article  CAS  PubMed  Google Scholar 

  14. Ikawa S, Kitano K, Hamaguchi S (2010) Effects of pH on bacterial inactivation in aqueous solutions due to low-temperature atmospheric pressure plasma application. Plasma Process Polym 7(1):33–42. doi:10.1002/ppap.200900090

    Article  CAS  Google Scholar 

  15. Keener KM, Jensen JL, Valdramidis VP, Byrne E, Connolly J, Mosnier JP, Cullen PJ (2012) Decontamination of Bacillus subtilis spores in a sealed package using a non-thermal plasma system. Plasma for bio-decontamination, medicine, and food security., NATO Science for Peace and Security Series A: Chemistry and BiologySpringer, Dordrecht, pp 445–455

    Chapter  Google Scholar 

  16. Kim HS, Cho YI, Hwang IH, Lee DH, Cho DJ, Rabinovich A, Fridman A (2013) Use of plasma gliding arc discharges on the inactivation of E. coli in water. Sep Purif Technol 120:423–428. doi:10.1016/j.seppur.2013.09.041

    Article  CAS  Google Scholar 

  17. Klockow PA, Keener KM (2009) Safety and quality assessment of packaged spinach treated with a novel ozone-generation system. Lwt-Food Sci Technol 42(6):1047–1053. doi:10.1016/j.lwt.2009.02.011

    Article  CAS  Google Scholar 

  18. Kong MG (2012) Microbial decontamination of food by non-thermal plasmas. In: Demirci A, Ngadi MO (eds) Microbial decontamination in the food industry: novel methods and applications, vol 234. Woodhead Publishing in Food Science Technology and Nutrition, Cambridge, pp 472–492

    Chapter  Google Scholar 

  19. Kong MG, Kroesen G, Morfill G, Nosenko T, Shimizu T, van Dijk J, Zimmermann JL (2009) Plasma medicine: an introductory review. New J Phys 11:115012. doi:10.1088/1367-2630/11/11/115012

    Article  Google Scholar 

  20. Kronn TG, Lawrence KC, Zhuang H, Hiett KL, Rothrock MJ Jr, Huang Y, Keener KM, Abdo Z (2015) Nonthermal plasma system for extending shelf like of raw broiler breast filets. Trans ASABE 58(2):493–500

    Google Scholar 

  21. Lynch OA, Cagney C, McDowell DA, Duffy G (2010) A method for the growth and recovery of 17 species of Campylobacter and its subsequent application to inoculated beef. J Microbiol Methods 83(1):1–7. doi:10.1016/j.mimet.2010.06.003

    Article  CAS  PubMed  Google Scholar 

  22. Mastanaiah N, Banerjee P, Johnson JA, Roy S (2013) Examining the role of ozone in surface plasma sterilization using dielectric barrier discharge (DBD) plasma. Plasma Process Polym 10:1120–1133

    Article  CAS  Google Scholar 

  23. Meinersmann RJ, Helsel LO, Fields PI, Hiett KL (1997) Discrimination of Campylobacter jejuni isolates by fla gene sequencing. J Clin Microbiol 35(11):2810–2814

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Meredith H, Valdramidis V, Rotabakk BT, Sivertsvik M, McDowell D, Bolton DJ (2014) Effect of different modified atmospheric packaging (MAP) gaseous combinations on Campylobacter and the shelf-life of chilled poultry fillets. Food Microbiol 44:196–203. doi:10.1016/j.fm.2014.06.005

    Article  CAS  PubMed  Google Scholar 

  25. Mertens N, Mahmoodzada M, Helmke A, Gruenig P, Laspe P, Emmert S, Vioel W (2014) Inactivation of microorganisms using cold atmospheric pressure plasma with different temporal discharge characteristics. Plasma Process Polym 11(10):910–920. doi:10.1002/ppap.201300184

    Article  CAS  Google Scholar 

  26. Meyer C, Mueller S, Gurevich EL, Franzke J (2011) Dielectric barrier discharges in analytical chemistry. Analyst 136(12):2427–2440. doi:10.1039/c0an00994f

    Article  CAS  PubMed  Google Scholar 

  27. Misra NN, Keener KM, Bourke P, Mosnier J-P, Cullen PJ (2014) In-package atmospheric pressure cold plasma treatment of cherry tomatoes. J Biosci Bioeng 118(2):177–182. doi:10.1016/j.jbiosc.2014.02.005

    Article  CAS  PubMed  Google Scholar 

  28. Misra NN, Moiseev T, Patil S, Pankaj SK, Bourke P, Mosnier JP, Keener KM, Cullen PJ (2014) Cold Plasma in Modified Atmospheres for Post-harvest Treatment of Strawberries. Food Bioprocess Technol 7(10):3045–3054. doi:10.1007/s11947-014-1356-0

    Article  CAS  Google Scholar 

  29. Misra NN, Ziuzina D, Cullen PJ, Keener KM (2013) Characterization of a novel atmospheric air cold plasma system for treatment of packaged biomaterials. Trans ASABE 56(3):1011–1016

    CAS  Google Scholar 

  30. Niemira BA (2012) Cold plasma decontamination of foods. Annu Rev Food Sci Technol 3(3):125–142. doi:10.1146/annurev-food-022811-101132

    Article  CAS  PubMed  Google Scholar 

  31. Oehmigen K, Haehnel M, Brandenburg R, Wilke C, Weltmann KD, von Woedtke T (2010) The role of acidification for antimicrobial activity of atmospheric pressure plasma in liquids. Plasma Processes Polym 7(3–4):250–257. doi:10.1002/ppap.200900077

    Article  CAS  Google Scholar 

  32. Oh E, McMullen L, Jeon B (2015) Impact of oxidative stress defense on bacterial survival and morphological change in Campylobacter jejuni under aerobic conditions. Front Microbiol. doi:10.3389/fmicb.2015.00295

    Google Scholar 

  33. Pankaj SK, Bueno-Ferrer C, Misra NN, Milosavljevic V, O’Donnell CP, Bourke P, Keener KM, Cullen PJ (2014) Applications of cold plasma technology in food packaging. Trends Food Sci Technol 35(1):5–17. doi:10.1016/j.tifs.2013.10.009

    Article  CAS  Google Scholar 

  34. Patil S, Moiseev T, Misra NN, Cullen PJ, Mosnier JP, Keener KM, Bourke P (2014) Influence of high voltage atmospheric cold plasma process parameters and role of relative humidity on inactivation of Bacillus atrophaeus spores inside a sealed package. J Hosp Infect 88(3):162–169

    Article  CAS  PubMed  Google Scholar 

  35. Russell SM (2009) Understanding poultry products spoilage. Watt AgNet.com. http://www.wattagnet.com/Poultry_USA/11993.html. Accessed Jan 2015

  36. Stintzi A (2003) Gene expression profile of Campylobacter jejuni in response to growth temperature variation. J Bacteriol 185(6):2009–2016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Tendero C, Tixier C, Tristant P, Desmaison J, Leprince P (2006) Atmospheric pressure plasmas: a review. Spectrochim Acta Part B-At Spectrosc 61(1):2–30. doi:10.1016/j.sab.2005.10.003

    Article  Google Scholar 

  38. Vaze ND, Gallagher MJ Jr, Park SH, Fridman G, Vasilets VN, Gutsol AF, Anandan S, Friedman G, Fridman AA (2010) Inactivation of bacteria in flight by direct exposire to nonthermal plasma. IEEE Transactions on Plasma Science 38(11):3234–3240

    Article  Google Scholar 

  39. Ziuzina D, Han L, Cullen PJ, Bourke P (2015) Cold plasma inactivation of internalised bacteria and biofilms for Salmonella enterica serovar Typhimurium, Listeria monocytogenes and Escherichia coli. Int J Food Microbiol 210:53–61. doi:10.1016/j.ijfoodmicro.2015.05.019

    Article  PubMed  Google Scholar 

  40. Ziuzina D, Patil S, Cullen PJ, Keener KM, Bourke P (2013) Atmospheric cold plasma inactivation of Escherichia coli in liquid media inside a sealed package. J Appl Microbiol 114(3):778–787. doi:10.1111/jam.12087

    Article  CAS  PubMed  Google Scholar 

  41. Ziuzina D, Petil S, Cullen PJ, Keener KM, Bourke P (2014) Atmospheric cold plasma inactivation of Escherichia coli, Salmonella enterica serovar Typhimurium and Listeria monocytogenes inoculated on fresh produce. Food Microbiol 42:109–116. doi:10.1016/j.fm.2014.02.007

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to acknowledge Taylor Kronn, Latoya Wiggins, and Candace McKinney for their assistance in sample preparation, technical assistance, and sample processing. These investigations were supported by the Agricultural Research Service, USDA CRIS Projects “Assessment and Improvement of Poultry Meet, Egg, and Feed Quality” #6040-41440-002-00, “Genetic Analysis of Poultry-Associated Salmonella enterica to Identify and Characterize Properties and Markers Associated with Egg-Borne Transmission of Illness” #6040-32000-007-00 and “Molecular Approaches for the Characterization of Foodborne Pathogens in Poultry” #6612-32000-059-00.

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Correspondence to Michael J. Rothrock Jr..

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Michael J. Rothrock Jr., Hong Zhuang, and Kelli L. Hiett contributed equally to conception, design, and completion of both the investigations and manuscript preparation.

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Rothrock, M.J., Zhuang, H., Lawrence, K.C. et al. In-Package Inactivation of Pathogenic and Spoilage Bacteria Associated with Poultry Using Dielectric Barrier Discharge-Cold Plasma Treatments. Curr Microbiol 74, 149–158 (2017). https://doi.org/10.1007/s00284-016-1158-x

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