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Long-Term Preservation of Bacteriophage Antimicrobials Using Sugar Glasses

  • Vincent Leung
    Vincent Leung
    Department of Chemical Engineering, 1280 Main Street West, McMaster University, Hamilton, Ontario, Canada L8S 4L7
  • Alexandra Szewczyk
    Alexandra Szewczyk
    Department of Chemical Engineering, 1280 Main Street West, McMaster University, Hamilton, Ontario, Canada L8S 4L7
  • Jacqueline Chau
    Jacqueline Chau
    Department of Chemical Engineering, 1280 Main Street West, McMaster University, Hamilton, Ontario, Canada L8S 4L7
  • Zeinab Hosseinidoust
    Zeinab Hosseinidoust
    Department of Chemical Engineering, 1280 Main Street West, McMaster University, Hamilton, Ontario, Canada L8S 4L7
  • Logan Groves
    Logan Groves
    Department of Chemical Engineering, 1280 Main Street West, McMaster University, Hamilton, Ontario, Canada L8S 4L7
    More by Logan Groves
  • Hajar Hawsawi
    Hajar Hawsawi
    Canadian Research Institute for Food Safety, 50 Stone Road East, University of Guelph, Guelph, Ontario, Canada N1G 2W1
  • Hany Anany
    Hany Anany
    Canadian Research Institute for Food Safety, 50 Stone Road East, University of Guelph, Guelph, Ontario, Canada N1G 2W1
    Agriculture and Agri-Food Canada, Guelph Research and Development Center, 93 Stone Road West, Guelph, Ontario, Canada N1G 5C9
    More by Hany Anany
  • Mansel W. Griffiths
    Mansel W. Griffiths
    Canadian Research Institute for Food Safety, 50 Stone Road East, University of Guelph, Guelph, Ontario, Canada N1G 2W1
  • M. Monsur Ali*
    M. Monsur Ali
    Department of Chemical Engineering, 1280 Main Street West, McMaster University, Hamilton, Ontario, Canada L8S 4L7
    *E-mail: [email protected]
  • , and 
  • Carlos D. M. Filipe*
    Carlos D. M. Filipe
    Department of Chemical Engineering, 1280 Main Street West, McMaster University, Hamilton, Ontario, Canada L8S 4L7
    *E-mail: [email protected]
Cite this: ACS Biomater. Sci. Eng. 2018, 4, 11, 3802–3808
Publication Date (Web):October 16, 2017
https://doi.org/10.1021/acsbiomaterials.7b00468
Copyright © 2017 American Chemical Society
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Supporting Info (1)»

Abstract

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The antimicrobial activity of LISTEX P100, Salmonella CG4, and E. coli AG10 bacteriophages were preserved in pullulan-trehalose mixture as dried films and as coatings on food packaging. The phages encapsulated in pullulan-trehalose films were able to retain infectivity for up to 3 months at ambient storage conditions. Various buffers, disaccharides and disaccharide concentrations were investigated to optimize the long-term stability of the phages in the films. It was found that pullulan and trehalose need to be simultaneously present in the film to provide the stabilizing effect and that the presence of buffers that lead to the formation of crystals in the films must be avoided for phage activity to be maintained. Overall, this study describes a method of preserving bacteriophage activity in a dried format that has great potential for use as coatings, which can be used to create antimicrobial surfaces for food preparation and for food preservation.

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The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsbiomaterials.7b00468.

  • LISTEX P100; kinetics of phage elution from paper; microscope images of pullulan films casted using various buffers; decay constants for LISTEX P100 and Salmonella phage CG4 immobilized in films with various compositions; plaque assay at 6 weeks storage of phage-coated paper with different coating solutions; XRD profiles for pullulan films casted in water, CM buffer, and PBS (PDF)

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Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

Cited By

This article is cited by 27 publications.

  1. Kunyu Qiu, Aaron C. Anselmo. Enhanced Storage of Anaerobic Bacteria through Polymeric Encapsulation. ACS Applied Materials & Interfaces 2021, 13 (39) , 46282-46290. https://doi.org/10.1021/acsami.1c11785
  2. Vincent Leung, Logan Groves, Alexandra Szewczyk, Zeinab Hosseinidoust, Carlos D. M. Filipe. Long-Term Antimicrobial Activity of Phage–Sugar Glasses is Closely Tied to the Processing Conditions. ACS Omega 2018, 3 (12) , 18295-18303. https://doi.org/10.1021/acsomega.8b02679
  3. Milica Radisic (Associate Editor). Biomaterials Going Strong in Canada for Half a Century. ACS Biomaterials Science & Engineering 2018, 4 (11) , 3625-3626. https://doi.org/10.1021/acsbiomaterials.8b01319
  4. Jalal Bacharouche, Ozge Erdemli, Romain Rivet, Balla Doucouré, Céline Caillet, Angela Mutschler, Philippe Lavalle, Jérôme F.L. Duval, Christophe Gantzer, Grégory Francius. On the Infectivity of Bacteriophages in Polyelectrolyte Multilayer Films: Inhibition or Preservation of Their Bacteriolytic Activity?. ACS Applied Materials & Interfaces 2018, 10 (39) , 33545-33555. https://doi.org/10.1021/acsami.8b10424
  5. Sara Kamali, Masoud Yavarmanesh, Mohammad B. Habibi Najafi, Arash Koocheki. Poly (lactic acid) and whey protein/pullulan composite bilayer film containing phage A511 as an anti-Listerial packaging for chicken breast at refrigerated temperatures. LWT 2022, 170 , 114085. https://doi.org/10.1016/j.lwt.2022.114085
  6. Sara Kamali, Masoud Yavarmanesh, Mohammad B. Habibi Najafi, Arash Koocheki. Development of whey protein concentrate/pullulan composite films containing bacteriophage A511: Functional properties and anti-Listerial effects during storage. Food Packaging and Shelf Life 2022, 33 , 100902. https://doi.org/10.1016/j.fpsl.2022.100902
  7. Mateusz Wdowiak, Jan Paczesny, Sada Raza. Enhancing the Stability of Bacteriophages Using Physical, Chemical, and Nano-Based Approaches: A Review. Pharmaceutics 2022, 14 (9) , 1936. https://doi.org/10.3390/pharmaceutics14091936
  8. Ruyin Liu, Ganghua Han, Zong Li, Shujuan Cun, Bin Hao, Jianping Zhang, Xinchun Liu. Bacteriophage therapy in aquaculture: current status and future challenges. Folia Microbiologica 2022, 67 (4) , 573-590. https://doi.org/10.1007/s12223-022-00965-6
  9. Honglin Jiang, Yan Li, Serge Cosnier, Mingying Yang, Weilian Sun, Chuanbin Mao. Exploring phage engineering to advance nanobiotechnology. Materials Today Nano 2022, 19 , 100229. https://doi.org/10.1016/j.mtnano.2022.100229
  10. Lei Tian, Kyle Jackson, Amy Zhang, Zeqi Wan, Ahmed Saif, Zeinab Hosseinidoust. Bacteriophage‐built gels as platforms for biomedical applications. The Canadian Journal of Chemical Engineering 2022, 6 https://doi.org/10.1002/cjce.24497
  11. Nathida Manbua, Teeraporn Suteewong, Udom Sae-Ueng. Efficacy of sugar excipients on lyophilized C22 phage infectivity evaluated by atomic force microscopy. Biological Control 2022, 170 , 104922. https://doi.org/10.1016/j.biocontrol.2022.104922
  12. Abdallah Abdelsattar, Alyaa Dawoud, Salsabil Makky, Rana Nofal, Ramy Aziz, Ayman El-Shibiny. Bacteriophages: from Isolation to Application. Current Pharmaceutical Biotechnology 2022, 23 (3) , 337-360. https://doi.org/10.2174/1389201022666210426092002
  13. Sneh Punia Bangar, Vandana Chaudhary, Neha Thakur, Priyanka Kajla, Manoj Kumar, Monica Trif. Natural Antimicrobials as Additives for Edible Food Packaging Applications: A Review. Foods 2021, 10 (10) , 2282. https://doi.org/10.3390/foods10102282
  14. Mateusz Wdowiak, Enkhlin Ochirbat, Jan Paczesny. Gold—Polyoxoborates Nanocomposite Prohibits Adsorption of Bacteriophages on Inner Surfaces of Polypropylene Labware and Protects Samples from Bacterial and Yeast Infections. Viruses 2021, 13 (7) , 1206. https://doi.org/10.3390/v13071206
  15. Naveen Chaudhary, Chandradeo Narayan, Balvinder Mohan, Neelam Taneja. Characterization and in vitro activity of a lytic phage RDN37 isolated from community sewage water active against MDR Uropathogenic E. coli. Indian Journal of Medical Microbiology 2021, 39 (3) , 343-348. https://doi.org/10.1016/j.ijmmb.2021.04.011
  16. Daniel Rosner, Jason Clark. Formulations for Bacteriophage Therapy and the Potential Uses of Immobilization. Pharmaceuticals 2021, 14 (4) , 359. https://doi.org/10.3390/ph14040359
  17. Fereshteh Bayat, Tohid F. Didar, Zeinab Hosseinidoust. Emerging investigator series: bacteriophages as nano engineering tools for quality monitoring and pathogen detection in water and wastewater. Environmental Science: Nano 2021, 8 (2) , 367-389. https://doi.org/10.1039/D0EN00962H
  18. Carol López de Dicastillo, Laura Settier-Ramírez, Rafael Gavara, Pilar Hernández-Muñoz, Gracia López Carballo. Development of Biodegradable Films Loaded with Phages with Antilisterial Properties. Polymers 2021, 13 (3) , 327. https://doi.org/10.3390/polym13030327
  19. Miroslav Veverka, Tibor Dubaj, Ján Gallovič, Eva Veverková, Peter Šimon, Ján Lokaj, Vladimír Jorík. Formulations of Staphylococcus aureus bacteriophage in biodegradable beta-glucan and arabinogalactan-based matrices. Journal of Drug Delivery Science and Technology 2020, 59 , 101909. https://doi.org/10.1016/j.jddst.2020.101909
  20. Jan Paczesny, Krzysztof Bielec. Application of Bacteriophages in Nanotechnology. Nanomaterials 2020, 10 (10) , 1944. https://doi.org/10.3390/nano10101944
  21. Nicholas B. Carrigy, Lu Liang, Hui Wang, Samuel Kariuki, Tobi E. Nagel, Ian F. Connerton, Reinhard Vehring. Trileucine and Pullulan Improve Anti-Campylobacter Bacteriophage Stability in Engineered Spray-Dried Microparticles. Annals of Biomedical Engineering 2020, 48 (4) , 1169-1180. https://doi.org/10.1007/s10439-019-02435-6
  22. Kunyu Qiu, Isabella Young, Blaide M. Woodburn, Yirui Huang, Aaron C. Anselmo. Polymeric Films for the Encapsulation, Storage, and Tunable Release of Therapeutic Microbes. Advanced Healthcare Materials 2020, 9 (6) , 1901643. https://doi.org/10.1002/adhm.201901643
  23. Vincent Leung, Jonathan Mapletoft, Ali Zhang, Amanda Lee, Fatemeh Vahedi, Marianne Chew, Alexandra Szewczyk, Sana Jahanshahi-Anbuhi, Jann Ang, Braeden Cowbrough, Matthew S. Miller, Ali Ashkar, Carlos D. M. Filipe. Thermal Stabilization of Viral Vaccines in Low-Cost Sugar Films. Scientific Reports 2019, 9 (1) https://doi.org/10.1038/s41598-019-44020-w
  24. J. García-Bernalt Diego, P. Fernández-Soto, B. Crego-Vicente, S. Alonso-Castrillejo, B. Febrer-Sendra, A. Gómez-Sánchez, B. Vicente, J. López-Abán, A. Muro. Progress in loop-mediated isothermal amplification assay for detection of Schistosoma mansoni DNA: towards a ready-to-use test. Scientific Reports 2019, 9 (1) https://doi.org/10.1038/s41598-019-51342-2
  25. Ganeshan, Hosseinidoust. Phage Therapy with a focus on the Human Microbiota. Antibiotics 2019, 8 (3) , 131. https://doi.org/10.3390/antibiotics8030131
  26. Nicholas B. Carrigy, Mani Ordoubadi, Yushan Liu, Omar Melhem, David Barona, Hui Wang, Leanne Milburn, Conor A. Ruzycki, Warren H. Finlay, Reinhard Vehring. Amorphous pullulan trehalose microparticle platform for respiratory delivery. International Journal of Pharmaceutics 2019, 563 , 156-168. https://doi.org/10.1016/j.ijpharm.2019.04.004
  27. Vincent Leung, Meredith Brooks, Sophia Emerson, Monsur Ali, Carlos D. M. Filipe. Ready‐to‐use thermally stable mastermix pills for molecular biology applications. Biotechnology Progress 2019, 35 (2) , e2764. https://doi.org/10.1002/btpr.2764

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