Skip to main content
SpringerLink
Log in

Bacteriophage application for biocontrolling Shigella flexneri in contaminated foods

  • Original Article
  • Published:
Journal of Food Science and Technology Aims and scope Submit manuscript

Abstract

Shigellosis (bacillary dysentery) is an acute enteric infection caused by members of Shigella genus. It causes annual deaths of approximately five million children in developing countries. Among Shigella spp., S. flexneri causes more serious forms of dysentery than other Shigella species. Due to the appearance of multidrug-resistant strains of Shigella spp., it is necessary to find alternative antimicrobial agents. The aims of this study were the isolation of a novel species-specific phage against S. flexneri and to evaluate its potential and efficacy for biocontrolling of S. flexneri in foods. Shigella flexneri PTCC 1234 was used as the host strain for bacteriophage isolation from waste water. A lytic phage of the Siphoviridae family was isolated and designated as vB_SflS-ISF001. The phage activity remained at high levels after 1 h of incubation at − 20 to 50 °C and was fairly stable for 1 h at pH values ranging from 7 to 9. The latent period and burst size were approximately 20 min and 53 ± 4 phages per host cell, respectively. Raw and cooked chicken breast were inoculated with a predetermined amount of S. flexneri and subjected to biocontrol test. The results showed that using vB_SflS-ISF001 phage led to more than two logs reduction in the count of viable S. flexneri. It was demonstrated that using vB_SflS-ISF001 phage is of high potential for developing an alternative strategy against S. flexneri contamination in foodstuffs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ackermann HW (2007) 5500 Phages examined in the electron microscope. Arch Virol 152(2):227–243

    Article  CAS  Google Scholar 

  • Ahmadi H, Anany H, Walkling-Ribeiro M, Griffiths M (2015) Biocontrol of Shigella flexneri in ground beef and Vibrio cholerae in seafood with bacteriophage-assisted high hydrostatic pressure (HHP) treatment. Food Bioprocess Technol 8(5):1160–1167

    Article  Google Scholar 

  • Ahmed AM, Shimamoto T (2014) Isolation and molecular characterization of Salmonella enterica, Escherichia coli O157: H7 and Shigella spp. from meat and dairy products in Egypt. Int J Food Microbiol 168:57–62

    Article  Google Scholar 

  • Bao H, Zhang P, Zhang H, Zhou Y, Zhang L, Wang R (2015) Bio-control of Salmonella enteritidis in foods using bacteriophages. Viruses 7(8):4836–4853

    Article  CAS  Google Scholar 

  • Faruque SM, Chowdhury N, Khan R, Hasan MR, Nahar J, Islam MJ, Yamasaki S, Ghosh A, Nair GB, Sack DA (2003) Shigella dysenteriae type 1-specific bacteriophage from environmental waters in Bangladesh. Appl Environ Microbiol 69(12):7028–7031

    Article  CAS  Google Scholar 

  • Ghasemi SM, Bouzari M, Emtiazi G (2014) Preliminary characterization of Lactococcus garvieae bacteriophage isolated from wastewater as a potential agent for biological control of lactococcosis in aquaculture. Aquac Int 22(4):1469–1480

    Article  Google Scholar 

  • Gu B, Zhou M, Ke X, Pan S, Cao Y, Huang Y, Zhuang L, Liu G, Tong M (2015) Comparison of resistance to third-generation cephalosporins in Shigella between Europe-America and Asia-Africa from 1998 to 2012. Epidemiol Infect 143(13):2687–2699

    Article  CAS  Google Scholar 

  • Guenther S, Herzig O, Fieseler L, Klumpp J, Loessner MJ (2012) Biocontrol of Salmonella typhimurium in RTE foods with the virulent bacteriophage FO1-E2. Int J Food Microbiol 154(1):66–72

    Article  Google Scholar 

  • Haq IU, Chaudhry WN, Andleeb S, Qadri I (2012) Isolation and partial characterization of a virulent bacteriophage IHQ1 specific for Aeromonas punctata from stream water. Microb Ecol 63(4):954–963

    Article  Google Scholar 

  • Harley JP, Prescott LM (2002) Laboratory exercises in microbiology, 5th edn. McGraw Hill, New York, pp 105–108

    Google Scholar 

  • Jafari F, Hamidian M, Rezadehbashi M, Doyle M, Salmanzadeh-ahrabi S, Derakhshan F, Reza Zali M (2009) Prevalence and antimicrobial resistance of diarrheagenic Escherichia coli and Shigella species associated with acute diarrhea in Tehran, Iran. Can J Infect Dis Med Microbiol 20(3):e56–e62

    Google Scholar 

  • Jakhetia R, Verma NK (2015) Identification and molecular characterisation of a novel Mu-Like bacteriophage, SfMu, of Shigella flexneri. PLoS ONE 10(4):e0124053

    Article  Google Scholar 

  • Jamal M, Chaudhry WN, Hussain T, Das CR, Andleeb S (2015) Characterization of new Myoviridae bacteriophage WZ1 against multi-drug resistant (MDR) Shigella dysenteriae. J Basic Microbiol 55(4):420–431

    Article  CAS  Google Scholar 

  • Jeon J, D’Souza R, Pinto N, Ryu CM, Park J, Yong D, Lee K (2016) Characterization and complete genome sequence analysis of two Myoviral bacteriophages infecting clinical carbapenem-resistant Acinetobacter baumannii isolates. J Appl Microbiol 121(1):68–77

    Article  CAS  Google Scholar 

  • Jun JW, Kim JH, Shin SP, Han JE, Chai JY, Park SC (2013) Characterization and complete genome sequence of the Shigella bacteriophage pSf-1. Res Microbiol 164(10):979–986

    Article  CAS  Google Scholar 

  • Jun JW, Yun SK, Kim HJ, Chai JY, Park SC (2014) Characterization and complete genome sequence of a novel N4-like bacteriophage, pSb-1 infecting Shigella boydii. Res Microbiol 165(8):671–678

    Article  CAS  Google Scholar 

  • Jun JW, Giri SS, Kim HJ, Yun SK, Chi C, Chai JY, Lee BC, Park SC (2016a) Bacteriophage application to control the contaminated water with Shigella. Sci Rep 6:22636

    Article  CAS  Google Scholar 

  • Jun JW, Kim HJ, Yun SK, Chai JY, Lee BC, Park SC (2016b) Isolation and comparative genomic analysis of T1-like Shigella bacteriophage pSf-2. Curr Microbiol 72(3):235–241

    CAS  Google Scholar 

  • Kazi M, Annapure US (2015) Bacteriophage biocontrol of foodborne pathogens. J Food Sci Technol 53(3):1–8

    Google Scholar 

  • Kropinski AM, Mazzocco A, Waddell TE, Lingohr E, Johnson RP (2009a) Enumeration of bacteriophages by double agar overlay plaque assay. Bacteriophages Methods Protoc 1:69–76

    Article  Google Scholar 

  • Kropinski AM, Prangishvili D, Lavigne R (2009b) Position paper: the creation of a rational scheme for the nomenclature of viruses of bacteria and archaea. Environ Microbiol 11(11):2775–2777

    Article  Google Scholar 

  • Löfdahl M, Ivarsson S, Andersson S, Långmark J, Plym-Forshell L (2009) An outbreak of Shigella dysenteriae in Sweden, May–June 2009, with sugar snaps as the suspected source. Eurosurveillance 14(28):29–35

    Article  Google Scholar 

  • Mikoleit M (2010) Laboratory protocol: biochemical identification of Salmonella and Shigella using an abbreviated panel of tests. WHO Global Foodborne Infections Network, Geneva

    Google Scholar 

  • Muller L, Jensen T, Petersen R, Mølbak K, Ethelberg S (2009) Imported fresh sugar peas as suspected source of an outbreak of Shigella sonnei in Denmark, April–May 2009. Eurosurveillance 14(24):218–226

    Article  Google Scholar 

  • Perera MN, Abuladze T, Li M, Woolston J, Sulakvelidze A (2015) Bacteriophage cocktail significantly reduces or eliminates Listeria monocytogenes contamination on lettuce, apples, cheese, smoked salmon and frozen foods. Food Microbiol 52:42–48

    Article  CAS  Google Scholar 

  • Pérez Pulido R, Grande Burgos MJ, Gálvez A, Lucas López R (2015) Application of bacteriophages in post-harvest control of human pathogenic and food spoiling bacteria. Crit Rev Biotechnol 36(5):851–861

    Google Scholar 

  • Prabhurajeshwar, Oli Ak, Ashajyothi C, Chandrakanth RK (2015) Prevalence and antibiotic susceptibility pattern of fluoroquinolone resistant Shigella species isolated from infants stool in Gulbarga district, Karnataka, India. Asian Pac J Trop Dis 5:S116–S120

    Article  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, vol 2, 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Shen G-H, Wang J-L, Wen F-S, Chang K-M, Kuo C-F, Lin C-H, Luo H-R, Hung C-H (2012) Isolation and characterization of φkm18p, a novel lytic phage with therapeutic potential against extensively drug resistant Acinetobacter baumannii. PLoS ONE 7(10):e46537

    Article  CAS  Google Scholar 

  • Silva YJ, Costa L, Pereira C, Mateus C, Cunha Â, Calado R, Gomes NC, Pardo MA, Hernandez I, Almeida A (2014) Phage therapy as an approach to prevent Vibrio anguillarum infections in fish larvae production. PLoS ONE 9(12):e114197

    Article  Google Scholar 

  • Sklar IB, Loerger RD (2001) Attempts to utilize bacteriophage to combat Salmonella Enterica serovar entemtidis infection in chickens. J Food Saf 21(1):15–29

    Article  Google Scholar 

  • Tajbakhsh M, Migura LG, Rahbar M, Svendsen CA, Mohammadzadeh M, Zali MR, Aarestrup FM, Hendriksen RS (2012) Antimicrobial-resistant Shigella infections from Iran: an overlooked problem? J Antimicrob Chemother 67(5):1128–1133

    Article  CAS  Google Scholar 

  • Taneja N, Mewara A, Kumar A, Verma G, Sharma M (2012) Cephalosporin-resistant Shigella flexneri over 9 years (2001–09) in India. J Antimicrob Chemother 67(6):1347–1353

    Article  CAS  Google Scholar 

  • WHO (2005) Shigellosis: disease burden, epidemiology and case management. Wkly Epidemiol Rec 80:94–99

    Google Scholar 

  • Zaidi MB, Estrada-García T (2014) Shigella: a highly virulent and elusive pathogen. Curr Trop Med Rep 1(2):81–87

    Google Scholar 

  • Zhang H, Wang R, Bao H (2013) Phage inactivation of foodborne Shigella on ready-to-eat spiced chicken. Poult Sci 92(1):211–217

    Article  Google Scholar 

Download references

Acknowledgements

This research was funded by an operating grant of the Dean of Research and Graduate Studies at the University of Isfahan.

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Sciences, University of Isfahan, Isfahan, 81746-73441, Iran

    Khashayar Shahin & Majid Bouzari

Authors
  1. Khashayar Shahin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Majid Bouzari
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Majid Bouzari.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shahin, K., Bouzari, M. Bacteriophage application for biocontrolling Shigella flexneri in contaminated foods. J Food Sci Technol 55, 550–559 (2018). https://doi.org/10.1007/s13197-017-2964-2

Download citation

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13197-017-2964-2

Keywords

Search

Navigation