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Bacteriophages as Bio-sanitizers in Food Production and Healthcare Settings

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Abstract

Sanitization is defined as the removal of soil deposits and subsequent application of a sanitizer or disinfectant to reduce the number of residual microorganisms remaining in an environment. Sanitization may be achieved through use of physical (thermal, irradiation) or chemical approaches. Chemical sanitizing is more frequently used in food production facilities than physical techniques. Growing concerns regarding the development of antimicrobial resistance has led to questions regarding cross-resistance mechanisms against sanitizers. The potential for sanitizer resistance development makes it necessary to find alternative approaches to remove microorganisms from food contact surfaces. Bacteriophages (phages) have been proposed as a class of bio-sanitizer due to several favorable attributes including the fact that they only infect bacteria and can remain viable for long periods, which can prevent against bacterial recontamination. Additionally, phages have low toxicity, are environmentally friendly, are not corrosive, and do not have any harmful or offensive odors. There are many examples within the scientific literature in which the positive effects of phages against their target bacteria on food and health setting contact surfaces have been investigated, supplying evidence needed for adoption of phage-based bio-sanitizers. However, these studies have identified several disadvantages of phage-based bio-sanitizers in comparison to traditional chemical sanitizers including their narrow host range and the fact they only affect bacteria, which means that phage based-sanitizers do not have the broad spectrum activity needed to inactivate nonbacterial microorganisms including fungi and viruses. The development of resistance is not a concern that is limited to chemical sanitizers, and while various approaches to address this problem have been proposed, the practicality of such solutions has not yet been demonstrated. Finally, most studies have evaluated phage-based bio-sanitizers in laboratory settings, and as such, they will need to be tested in real-world scenarios to ensure robustness.

Keywords

  • Sanitizer
  • Sanitization
  • Biocides
  • Antimicrobial resistance
  • Disinfectant
  • Host range
  • Biofilms
  • Enzymes
  • Polymers
  • Contamination
  • Surfaces
  • Bacteriophage

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References

  • Abuladze T, Li M, Menetrez MY, Dean T, Senecal A, Sulakvelidze A (2008) Bacteriophages reduce experimental contamination of hard surfaces, tomato, spinach, broccoli, and ground beef by Escherichia coli O157:H7. Appl Environ Microbiol 74:6230–6238

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Agún S, Fernández L, González Menéndez E, Martínez B, Rodríguez A, García P (2018) Study of the interactions between bacteriophage phiIPLA-RODI and four chemical disinfectants for the elimination of Staphylococcus aureus contamination. Viruses 10:103

    PubMed Central  CrossRef  CAS  Google Scholar 

  • Ahiwale S, Koparde P, Deore P, Gunale V, Kapadnis BP (2012) Bacteriophage based technology for disinfection of different water systems. In: Satyanarayana T, Johri BN (eds) Microorganisms in environmental management: microbes and environment. Springer Netherlands, Dordrecht, pp 289–313

    CrossRef  Google Scholar 

  • Alavidze Z, Brown TC, Morris JG, Pasternack GR, Sulakvelidze A (2004) Method and device for sanitation using bacteriophages. Google Patents

    Google Scholar 

  • Allegranzi B, Bagheri Nejad S, Combescure C, Graafmans W, Attar H, Donaldson L, Pittet D (2011) Burden of endemic health-care-associated infection in developing countries: systematic review and meta-analysis. Lancet 377:228–241

    CrossRef  PubMed  Google Scholar 

  • Alves DR, Gaudion A, Bean JE, Perez Esteban P, Arnot TC, Harper DR, Kot W, Hansen LH, Enright MC, Jenkins AT (2014) Combined use of bacteriophage K and a novel bacteriophage to reduce Staphylococcus aureus biofilm formation. Appl Environ Microbiol 80:6694–6703

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Banach LJ, Sampers I, van Haute S, van der Fels-Klerx HJ (2015) Effect of disinfectants on preventing the cross-contamination of pathogens in fresh produce washing water. Int J Environ Res Public Health 12:8658–8677

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Barnes LM, Lo MF, Adams MR, Chamberlain AH (1999) Effect of milk proteins on adhesion of bacteria to stainless steel surfaces. Appl Environ Microbiol 65:4543–4548

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Bower CK, Daeschel MA (1999) Resistance responses of microorganisms in food environments. Int J Food Microbiol 50:33–44

    CAS  PubMed  CrossRef  Google Scholar 

  • Brenner FW, Villar RG, Angulo FJ, Tauxe R, Swaminathan B (2000) Salmonella nomenclature. J Clin Microbiol 38:2465–2467

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Brown HL, Reuter M, Salt LJ, Cross KL, Betts RP, van Vliet AH (2014) Chicken juice enhances surface attachment and biofilm formation of campylobacter jejuni. Appl Environ Microbiol 80:7053–7060

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Brudzinski L, Harrison MA (1998) Influence of incubation conditions on survival and acid tolerance response of Escherichia coli O157:H7 and non-O157:H7 isolates exposed to acetic acid. J Food Prot 61:542–546

    CAS  PubMed  CrossRef  Google Scholar 

  • Bruttin A, Brüssow H (2005) Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother 49:2874–2878

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Buchanan RL, Edelson SG (1999) Effect of pH-dependent, stationary phase acid resistance on the thermal tolerance of Escherichia coli O157:H7. Food Microbiol 16:447–458

    CrossRef  Google Scholar 

  • Canadian Patient Safety Institute (2020) Healthcare associated infections (Available here). Accessed on 27 Oct 2017

    Google Scholar 

  • Centers for Disease Control and Prevention (2020) Reports of selected E. coli outbreak investigations (Available here). Accessed on 27 Oct 2017

    Google Scholar 

  • Chaitiemwong N, Hazeleger WC, Beumer RR (2014) Inactivation of Listeria monocytogenes by disinfectants and bacteriophages in suspension and stainless steel carrier tests. J Food Prot 77:2012–2020

    CAS  PubMed  CrossRef  Google Scholar 

  • Chan BK, Abedon ST (2015) Bacteriophages and their enzymes in biofilm control. Curr Pharm Des 21:85–99

    CAS  PubMed  CrossRef  Google Scholar 

  • Chanishvili N, Chanishvili T, Tediashvili M, Barrow PA (2001) Phages and their application against drug-resistant bacteria. J Chem Technol Biotechnol 76:689–699

    CAS  CrossRef  Google Scholar 

  • Chen LK, Liu YL, Hu A, Chang KC, Lin NT, Lai MJ, Tseng CC (2013) Potential of bacteriophage PhiAB2 as an environmental biocontrol agent for the control of multidrug-resistant Acinetobacter baumannii. BMC Microbiol 13:154

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Curtin JJ, Donlan RM (2006) Using bacteriophages to reduce formation of catheter- associated biofilms by Staphylococcus epidermidis. Antimicrob Agents Chemother 50:1268–1275

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Dancer SJ (2014) Controlling hospital-acquired infection: focus on the role of the environment and new technologies for decontamination. Clin Microbiol Rev 27:665–690

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Davidson PM, Harrison MA (2002) Resistance and adaptation to food antimicrobials, sanitizers, and other process controls. Food Technol Mag 56:69–78

    Google Scholar 

  • De Oliveira DC, Fernandes Junior A, Kaneno R, Silva MG, Araujo Junior JP, Silva NC, Rall VL (2014) Ability of Salmonella spp. to produce biofilm is dependent on temperature and surface material. Foodborne Pathog Dis 11:478–483

    PubMed  CrossRef  CAS  Google Scholar 

  • Debarbieux L, Pirnay JP, Verbeken G, De Vos D, Merabishvili M, Huys I, Patey O, Schoonjans D, Vaneechoutte M, Zizi M, Rohde C (2016) A bacteriophage journey at the European medicines agency. FEMS Microbiol Lett 363:fnv225

    PubMed  CrossRef  CAS  Google Scholar 

  • d’Herelle F (1917) Sur un microbe invible antagoniste des bacilles dysenteriques. C R Acad Sci 165:373–375

    Google Scholar 

  • Di Bonaventura G, Piccolomini R, Paludi D, D’Orio V, Vergara A, Conter M, Ianieri A (2008) Influence of temperature on biofilm formation by Listeria monocytogenes on various food-contact surfaces: relationship with motility and cell surface hydrophobicity. J Appl Microbiol 104:1552–1561

    PubMed  CrossRef  Google Scholar 

  • Dourou D, Beauchamp CS, Yoon Y, Geornaras I, Belk KE, Smith GC, Nychas GJ, Sofos JN (2011) Attachment and biofilm formation by Escherichia coli O157:H7 at different temperatures, on various food-contact surfaces encountered in beef processing. Int J Food Microbiol 149:262–268

    PubMed  CrossRef  Google Scholar 

  • El-Gohary FA, Huff WE, Huff GR, Rath NC, Zhou ZY, Donoghue AM (2014) Environmental augmentation with bacteriophage prevents colibacillosis in broiler chickens. Poult Sci 93:2788–2792

    CAS  PubMed  CrossRef  Google Scholar 

  • European Centre for Disease Prevention and Control (2013) Point prevalence survey of healthcare-associated infections and antimicrobial use in European acute care hospitals. In: Surveillance report, Stockholm, pp 1–141

    Google Scholar 

  • Fenton M, Keary R, McAuliffe O, Ross RP, O’Mahony J, Coffey A (2013) Bacteriophage- derived peptidase CHAP(K) eliminates and prevents staphylococcal biofilms. Int J Microbiol 2013:625341

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Ferreira V, Wiedmann M, Teixeira P, Stasiewicz MJ (2014) Listeria monocytogenes persistence in food-associated environments: epidemiology, strain characteristics, and implications for public health. J Food Prot 77:150–170

    CAS  PubMed  CrossRef  Google Scholar 

  • Fischetti VA (2005) Bacteriophage lytic enzymes: novel anti-infectives. Trends Microbiol 13:491–496

    CAS  PubMed  CrossRef  Google Scholar 

  • Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633

    CAS  PubMed  CrossRef  Google Scholar 

  • Food and Drug Administration (2006) Food additives permitted for direct addition to food for human consumption, bacteriophage preparation. 21 CFR Part 172 Fed Regis 71:47729–47732

    Google Scholar 

  • Fu W, Forster T, Mayer O, Curtin JJ, Lehman SM, Donlan RM (2010) Bacteriophage cocktail for the prevention of biofilm formation by Pseudomonas aeruginosa on catheters in an in vitro model system. Antimicrob Agents Chemother 54:397–404

    CAS  PubMed  CrossRef  Google Scholar 

  • Ganegama Arachchi GJ, Cridge AG, Dias-Wanigasekera BM, Cruz CD, McIntyre L, Liu R, Flint SH, Mutukumira AN (2013) Effectiveness of phages in the decontamination of Listeria monocytogenes adhered to clean stainless steel, stainless steel coated with fish protein, and as a biofilm. J Ind Microbiol Biotechnol 40:1105–1116

    CAS  PubMed  CrossRef  Google Scholar 

  • Gaulin C, Lê ML, Shum M, Fong D (2011) Disinfectants and sanitizers for use on food contact surfaces. National Collaborating Centre for Environmental Health, Vancouver (Available here). Accessed on 27 Oct 2017

    Google Scholar 

  • Germano F, Testi D, Melone P, Arcuri C (2014) Cell wall deficient bacteria in oral biofilm: prevalence and association with periodontitis systemic condition. In: conference abstract, meeting of ESCMID study group for biofilms (ESGB), biofilm – based Healthcare – associated infections: from microbiology to clinics

    Google Scholar 

  • Giaouris E, Heir E, Hébraud M, Chorianopoulos N, Langsrud S, Møretrø T, Habimana O, Desvaux M, Renier S, Nychas G-J (2014) Attachment and biofilm formation by foodborne bacteria in meat processing environments: causes, implications, role of bacterial interactions and control by alternative novel methods. Meat Sci 97:298–309

    PubMed  CrossRef  Google Scholar 

  • Gil MI, Selma MV, López-Gálvez F, Allende A (2009) Fresh-cut product sanitation and wash water disinfection: problems and solutions. Int J Food Microbiol 134:37–45

    CAS  PubMed  CrossRef  Google Scholar 

  • Gong C, Jiang X (2015) Application of bacteriophages to reduce biofilms formed by hydrogen sulfide producing bacteria on surfaces in a rendering plant. Can J Microbiol 61:539–544

    CAS  PubMed  CrossRef  Google Scholar 

  • Goodridge L, Abedon ST (2003) Bacteriophage biocontrol and bioprocessing: application of phage therapy to industry. Soc Indus Microbio News 53:254–262

    Google Scholar 

  • Government of Canada (2019) Background information: reducing the risk of illness associated with frozen raw breaded chicken products (Available here). Accessed on 27 Oct 2017

    Google Scholar 

  • Gutiérrez D, Vandenheuvel D, Martínez B, Rodríguez A, Lavigne R, García P (2015) Two phages, phiIPLA-RODI and phiIPLA-C1C, lyse mono- and dual-species staphylococcal biofilms. Appl Environ Microbiol 81:3336–3348

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Gutiérrez D, Rodríguez-Rubio L, Martínez B, Rodríguez A, García P (2016) Bacteriophages as weapons against bacterial biofilms in the food industry. Front Microbiol 7:825

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Gutiérrez D, Rodríguez-Rubio L, Fernández L, Martínez B, Rodríguez A, García P (2017) Applicability of commercial phage-based products against Listeria monocytogenes for improvement of food safety in Spanish dry-cured ham and food contact surfaces. Food Control 73:1474–1482

    CrossRef  CAS  Google Scholar 

  • Guttman B, Raya R, Kutter E (2003) Basic phage biology. In: Kutter E, Sulakvelidze A (eds) Bacteriophage: biology and applications. CRC Press, pp 29–66

    Google Scholar 

  • Hazards EPoB (2012) Scientific Opinion on the evaluation of the safety and efficacy of Listex™ P100 for the removal of Listeria monocytogenes surface contamination of raw fish. EFSA J 10:2615–2n/a

    Google Scholar 

  • Heselpoth RD, Nelson DC (2012) A new screening method for the directed evolution of thermostable bacteriolytic enzymes. J Vis Exp 69

    Google Scholar 

  • Hibma AM, Jassim SA, Griffiths MW (1997) Infection and removal of L-forms of Listeria monocytogenes with bred bacteriophage. Int J Food Microbiol 34:197–207

    CAS  PubMed  CrossRef  Google Scholar 

  • Hingston PA, Stea EC, Knochel S, Hansen T (2013) Role of initial contamination levels, biofilm maturity and presence of salt and fat on desiccation survival of Listeria monocytogenes on stainless steel surfaces. Food Microbiol 36:46–56

    CAS  PubMed  CrossRef  Google Scholar 

  • Ho YH, Tseng CC, Wang LS, Chen YT, Ho GJ, Lin TY, Wang LY, Chen LK (2016) Application of bacteriophage-containing aerosol against nosocomial transmission of carbapenem-resistant acinetobacter Baumannii in an intensive care unit. PLoS One 11:e0168380

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Holah JT, Lavaud A, Peters W, Dye KA (1998) Future techniques for disinfectant efficacy testing. Int Biodeterior Biodegradation 41:273–279

    CrossRef  Google Scholar 

  • Horn H, Morgenroth E (2006) Transport of oxygen, sodium chloride, and sodium nitrate in biofilms. Chem Eng Sci 61:1347–1356

    CAS  CrossRef  Google Scholar 

  • Hosseinidoust Z, Tufenkji N, van de Ven TG (2013) Formation of biofilms under phage predation: considerations concerning a biofilm increase. Biofouling 29:457–468

    CAS  PubMed  CrossRef  Google Scholar 

  • Iacumin L, Manzano M, Comi G (2016) Phage inactivation of Listeria monocytogenes on San Daniele dry-cured ham and elimination of biofilms from equipment and working environments. Microorganisms 4

    Google Scholar 

  • Jajere SM (2019) A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance. Vet World 12:504–521

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Jassim SAA, Limoges RG (2017) Bacteriophages: practical applications for nature’s biocontrol. Springer International Publishing, Cham

    CrossRef  Google Scholar 

  • Jonczyk E, Klak M, Miedzybrodzki R, Gorski A (2011) The influence of external factors on bacteriophages—review. Folia Microbiol (Praha) 56:191–200

    CAS  CrossRef  Google Scholar 

  • Kelly D, McAuliffe O, Ross RP, Coffey A (2012) Prevention of Staphylococcus aureus biofilm formation and reduction in established biofilm density using a combination of phage K and modified derivatives. Lett Appl Microbiol 54:286–291

    CAS  PubMed  CrossRef  Google Scholar 

  • Klevens RM, Edwards JR, Richards CL Jr, Horan TC, Gaynes RP, Pollock DA, Cardo DM (2007) Estimating health care-associated infections and deaths in U.S. hospitals, 2002. Public Health Rep 122:160–166

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Kramer A, Schwebke I, Kampf G (2006) How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect Dis 6:130

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Krishnan J, Fey G, Stansfield C, Landry L, Nguy H, Klassen S, Robertson C (2012) Evaluation of a dry fogging system for laboratory decontamination. Appl Biosaf 17:132–141

    CrossRef  Google Scholar 

  • Liu H, Meng R, Wang J, Niu YD, Li J, Stanford K, McAllister TA (2015) Inactivation of Escherichia coli O157 bacteriophages by using a mixture of ferrous sulfate and tea extract. J Food Prot 78:2220–2226

    CAS  PubMed  CrossRef  Google Scholar 

  • Lopes A, Pereira C, Almeida A (2018) Sequential combined effect of phages and antibiotics on the inactivation of Escherichia coli. Microorganisms 6:125

    CAS  PubMed Central  CrossRef  Google Scholar 

  • Maillard J-Y, Sattar SA, Pinto F (2012) Virucidal activity of microbicides. In: Fraise AP, Maillard J-Y, Sattar SA (eds) Russell, Hugo & Ayliffe’s: principles and practice of disinfection, preservation and sterilization. Wiley-Blackwell, Hoboken, pp 178–207

    CrossRef  Google Scholar 

  • Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O’Brien SJ, Jones TF, Fazil A, Hoekstra RM (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50:882–889

    PubMed  CrossRef  Google Scholar 

  • Manijeh M, Mohammad J, Roha KK (2008) Biofilm formation by salmonella Enteritidis on food contact surfaces. J Biol Sci 8:502–505

    CrossRef  Google Scholar 

  • Martinez-Suarez JV, Ortiz S, Lopez-Alonso V (2016) Potential impact of the resistance to quaternary ammonium disinfectants on the persistence of Listeria monocytogenes in food processing environments. Front Microbiol 7:638

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Melo LDR, Veiga P, Cerca N, Kropinski AM, Almeida C, Azeredo J, Sillankorva S (2016) Development of a phage cocktail to control Proteus mirabilis catheter-associated urinary tract infections. Front Microbiol 7:1024

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Miller RV, Day M (2008) Contribution of lysogeny, pseudolysogeny and starvation to phage ecology. In: Bacteriophage ecology. Cambridge University Press, Cambridge, pp 114–143

    CrossRef  Google Scholar 

  • Mokgatla RM, Gouws PA, Brozel VS (2002) Mechanisms contributing to hypochlorous acid resistance of a Salmonella isolate from a poultry-processing plant. J Appl Microbiol 92:566–573

    CAS  PubMed  CrossRef  Google Scholar 

  • Montanez-Izquierdo VY, Salas-Vazquez DI, Rodriguez-Jerez JJ (2012) Use of epifluorescence microscopy to assess the effectiveness of phage P100 in controlling Listeria monocytogenes biofilms on stainless steel surfaces. Food Control 23:470–477

    CrossRef  Google Scholar 

  • Morison J (1932) Bacteriphage in the treatment and prevention of cholera. H.K. Lewis and Co. Ltd., London

    Google Scholar 

  • Motlagh AM, Bhattacharjee AS, Goel R (2016) Biofilm control with natural and genetically- modified phages. World J Microbiol Biotechnol 32:67

    PubMed  CrossRef  CAS  Google Scholar 

  • Oliveira H, Thiagarajan V, Walmagh M, Sillankorva S, Lavigne R, Neves-Petersen MT, Kluskens LD, Azeredo J (2014) A thermostable Salmonella phage endolysin, Lys68, with broad bactericidal properties against gram-negative pathogens in presence of weak acids. PLoS One 9:e108376

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • OMAFRA (2017) Foods of plant origin cleaning and sanitation guidebook (Available here). Accessed on 27 Oct 2017

    Google Scholar 

  • Pan Y, Breidt F Jr, Kathariou S (2006) Resistance of Listeria monocytogenes biofilms to sanitizing agents in a simulated food processing environment. Appl Environ Microbiol 72:7711–7717

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Patel J, Sharma M, Millner P, Calaway T, Singh M (2011) Inactivation of Escherichia coli O157:H7 attached to spinach harvester blade using bacteriophage. Foodborne Pathog Dis 8:541–546

    PubMed  CrossRef  Google Scholar 

  • Pennone V, Sanz-Gaitero M, O’Connor P, Coffey A, Jordan K, van Raaij MJ, McAuliffe O (2019) Inhibition of L. monocytogenes biofilm formation by the amidase domain of the phage vB_LmoS_293 Endolysin. Viruses 11:722

    CAS  PubMed Central  CrossRef  Google Scholar 

  • Pires DP, Oliveira H, Melo LD, Sillankorva S, Azeredo J (2016) Bacteriophage-encoded depolymerases: their diversity and biotechnological applications. Appl Microbiol Biotechnol 100:2141–2151

    CAS  PubMed  CrossRef  Google Scholar 

  • Rahman M, Kim S, Kim SM, Seol SY, Kim J (2011) Characterization of induced Staphylococcus aureus bacteriophage SAP-26 and its anti-biofilm activity with rifampicin. Biofouling 27:1087–1093

    CAS  PubMed  CrossRef  Google Scholar 

  • Rashid MH, Revazishvili T, Dean T, Butani A, Verratti K, Bishop-Lilly KA, Sozhamannan S, Sulakvelidze A, Rajanna C (2012) A Yersinia pestis-specific, lytic phage preparation significantly reduces viable Y. pestis on various hard surfaces experimentally contaminated with the bacterium. Bacteriophage 2:168–177

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Reinhard RG, Kalinowski RM, Bodnaruk PW, Eifert JD, Boyer RR, Duncan SE, Bailey RH (2020) Fate of Listeria on various food contact and noncontact surfaces when treated with bacteriophage. J Food Saf 40:e12775

    CAS  CrossRef  Google Scholar 

  • Ripp S, Miller RV (1997) The role of pseudolysogeny in bacteriophage-host interactions in a natural freshwater environment. Microbiology-UK 143:2065–2070

    CAS  CrossRef  Google Scholar 

  • Rodríguez-Rubio L, Martínez B, Donovan DM, Rodríguez A, García P (2013) Bacteriophage virion-associated peptidoglycan hydrolases: potential new enzybiotics. Crit Rev Microbiol 39:427–434

    PubMed  CrossRef  CAS  Google Scholar 

  • Roy B, Ackermann HW, Pandian S, Picard G, Goulet J (1993) Biological inactivation of adhering Listeria monocytogenes by listeriaphages and a quaternary ammonium compound. Appl Environ Microbiol 59:2914–2917

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Russell AD (1997) Plasmids and bacterial resistance to biocides. J Appl Microbiol 83:155–165

    CAS  PubMed  CrossRef  Google Scholar 

  • Russell AD, Day MJ (1996) Antibiotic and biocide resistance in bacteria. Microbios 85:45–65

    CAS  PubMed  Google Scholar 

  • Ryan EM, Alkawareek MY, Donnelly RF, Gilmore BF (2012) Synergistic phage-antibiotic combinations for the control of Escherichia coli biofilms in vitro. FEMS Immunol Med Microbiol 65:395–398

    CAS  PubMed  CrossRef  Google Scholar 

  • Sadekuzzaman M, Yang S, Mizan MFR, Kim H-S, Ha S-D (2017) Effectiveness of a phage cocktail as a biocontrol agent against L. monocytogenes biofilms. Food Control 78:256–263

    CrossRef  Google Scholar 

  • Sass P, Bierbaum G (2007) Lytic activity of recombinant bacteriophage phi11 and phi12 endolysins on whole cells and biofilms of Staphylococcus aureus. Appl Environ Microbiol 73:347–352

    CAS  PubMed  CrossRef  Google Scholar 

  • Sharma M, Ryu JH, Beuchat LR (2005) Inactivation of Escherichia coli O157:H7 in biofilm on stainless steel by treatment with an alkaline cleaner and a bacteriophage. J Appl Microbiol 99:449–459

    CAS  PubMed  CrossRef  Google Scholar 

  • Sillankorva S, Oliveira R, Vieira MJ, Sutherland IW, Azeredo J (2004) Bacteriophage Phi S1 infection of Pseudomonas fluorescens planktonic cells versus biofilms. Biofouling 20:133–138

    PubMed  CrossRef  Google Scholar 

  • Sillankorva S, Neubauer P, Azeredo J (2008) Pseudomonas fluorescens biofilms subjected to phage phiIBB-PF7A. BMC Biotechnol 8:79

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Singh R, Paul D, Jain RK (2006) Biofilms: implications in bioremediation. Trends Microbiol 14:389–397

    CAS  PubMed  CrossRef  Google Scholar 

  • Skurnik M, Pajunen M, Kiljunen S (2007) Biotechnological challenges of phage therapy. Biotechnol Lett 29:995–1003

    CAS  PubMed  CrossRef  Google Scholar 

  • Smith HW, Huggins MB, Shaw KM (1987) The control of experimental Escherichia coli diarrhoea in calves by means of bacteriophages. J Gen Microbiol 133:1111–1126

    CAS  PubMed  Google Scholar 

  • Soni KA, Nannapaneni R (2010) Removal of Listeria monocytogenes biofilms with bacteriophage P100. J Food Prot 73:1519–1524

    PubMed  CrossRef  Google Scholar 

  • Srey S, Jahid IK, Ha S-D (2013) Biofilm formation in food industries: a food safety concern. Food Control 31:572–585

    CrossRef  Google Scholar 

  • Sulakvelidze A (2013) Using lytic bacteriophages to eliminate or significantly reduce contamination of food by foodborne bacterial pathogens. J Sci Food Agric 93:3137–3146

    CAS  PubMed  CrossRef  Google Scholar 

  • Sutherland IW (2001) The biofilm matrix—an immobilized but dynamic microbial environment. Trends Microbiol 9:222–227

    CAS  PubMed  CrossRef  Google Scholar 

  • Tebbutt GM (1984) A microbiological study of various food premises with an assessment of cleaning and disinfection practices. J Hyg (Lond) 93:365–375

    CAS  CrossRef  Google Scholar 

  • Thaden JT, Park LP, Maskarinec SA, Ruffin F, Fowler VG Jr, van Duin D (2017) Results from a 13-year prospective cohort study show increased mortality associated with bloodstream infections caused by pseudomonas aeruginosa compared to other bacteria. Antimicrob Agents Chemother 61:e02671–e02616

    PubMed  PubMed Central  Google Scholar 

  • Tomat D, Quiberoni A, Mercanti D, Balagué C (2014) Hard surfaces decontamination of enteropathogenic and Shiga toxin-producing Escherichia coli using bacteriophages. FRIN Food Res Int 57:123–129

    CAS  CrossRef  Google Scholar 

  • Troller JA (1993) Chapter 5 – Sanitizing. In: Sanitation in food processing, 2nd edn. Academic Press, London, pp 52–70

    CrossRef  Google Scholar 

  • Twort FW (1915) An investigation on the nature of ultra-microscopic viruses. Lancet Infect Dis II:1241–1243

    Google Scholar 

  • Valerio N, Oliveira C, Jesus V, Branco T, Pereira C, Moreirinha C, Almeida A (2017) Effects of single and combined use of bacteriophages and antibiotics to inactivate Escherichia coli. Virus Res 240:8–17

    CAS  PubMed  CrossRef  Google Scholar 

  • Vandenheuvel D, Lavigne R, Brüssow H (2015) Bacteriophage therapy: advances in formulation strategies and human clinical trials. Ann Rev Virology 2:599–618

    CAS  CrossRef  Google Scholar 

  • Viazis S, Akhtar M, Feirtag J, Diez-Gonzalez F (2011) Reduction of Escherichia coli O157:H7 viability on hard surfaces by treatment with a bacteriophage mixture. Int J Food Microbiol 145:37–42

    PubMed  CrossRef  Google Scholar 

  • Viazis S, Labuza TP, Diez-Gonzalez F (2015) Bacteriophage mixture inactivation kinetics against Escherichia coli O157:H7 on hard surfaces. J Food Saf 35:66–74

    CAS  CrossRef  Google Scholar 

  • Wang R, Kalchayanand N, King DA, Luedtke BE, Bosilevac JM, Arthur TM (2014) Biofilm formation and sanitizer resistance of Escherichia coli O157:H7 strains isolated from “high event period” meat contamination. J Food Prot 77:1982–1987

    PubMed  CrossRef  CAS  Google Scholar 

  • Wang H, Tay M, Palmer J, Flint S (2017) Biofilm formation of Yersinia enterocolitica and its persistence following treatment with different sanitation agents. JFCO Food Control 73:433–437

    CAS  CrossRef  Google Scholar 

  • Weber DJ, Rutala WA (1997) Role of environmental contamination in the transmission of vancomycin-resistant enterococci. Infect Control Hosp Epidemiol 18:306–309

    CAS  PubMed  CrossRef  Google Scholar 

  • Weber DJ, Rutala WA, Miller MB, Huslage K, Sickbert-Bennett E (2010) Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, Clostridium difficile, and Acinetobacter species. Am J Infect Control 38:S25–S33

    PubMed  CrossRef  Google Scholar 

  • Woolston J, Parks AR, Abuladze T, Anderson B, Li M, Carter C, Hanna LF, Heyse S, Charbonneau D, Sulakvelidze A (2013) Bacteriophages lytic for Salmonella rapidly reduce Salmonella contamination on glass and stainless steel surfaces. Bacteriophage 3:e25697

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • World Health Organization (2014) Health care-associated infections. In: Fact sheet (Available here). Accessed on 27 Oct 2017

    Google Scholar 

  • Young R (1992) Bacteriophage lysis: mechanism and regulation. Microbiol Rev 56:430–481

    CAS  PubMed  PubMed Central  CrossRef  Google Scholar 

  • Zhang Y, Hu Z (2013) Combined treatment of Pseudomonas aeruginosa biofilms with bacteriophages and chlorine. Biotechnol Bioeng 110:286–295

    CAS  PubMed  CrossRef  Google Scholar 

  • Zhang Y, Hunt HK, Hu Z (2013) Application of bacteriophages to selectively remove Pseudomonas aeruginosa in water and wastewater filtration systems. Water Res 47:4507–4518

    CAS  PubMed  CrossRef  Google Scholar 

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Acknowledgments

SB’s and LG’s work was supported by the National Sciences and Engineering Council of Canada Discovery Grants Program (grant number RGPIN-2014-0574).

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Bhandare, S., Goodridge, L. (2020). Bacteriophages as Bio-sanitizers in Food Production and Healthcare Settings. In: Harper, D.R., Abedon, S.T., Burrowes, B.H., McConville, M.L. (eds) Bacteriophages. Springer, Cham. https://doi.org/10.1007/978-3-319-40598-8_26-1

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  • DOI: https://doi.org/10.1007/978-3-319-40598-8_26-1

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