Publication Cover
Biofouling
The Journal of Bioadhesion and Biofilm Research
Volume 32, 2016 - Issue 7
576
Views
24
CrossRef citations to date
0
Altmetric
Articles

Salmonella enterica isolates from layer farm environments are able to form biofilm on eggshell surfaces

, &
Pages 699-710 | Received 24 Feb 2016, Accepted 11 May 2016, Published online: 08 Jun 2016

References

  • Castelijn GA, van der Veen S, Zwietering MH, Moezelaar R, Abee T. 2012. Diversity in biofilm formation and production of curli fimbriae and cellulose of Salmonella Typhimurium strains of different origin in high and low nutrient medium. Biofouling. 28:51–63. doi:10.1080/08927014.2011.648927
  • Castelijn GA, Parabirsing JA, Zwietering MH, Moezelaar R, Abee T. 2013. Surface behaviour of S. Typhimurium, S. Derby, S. Brandenburg and S. Infantis. Vet Microbiol. 161:305–314. doi:10.1016/j.vetmic.2012.07.047
  • Chousalkar KK, Roberts JR. 2012. Recovery of Salmonella from eggshell wash, eggshell crush, and egg internal contents of unwashed commercial shell eggs in Australia. Poult Sci. 91:1739–1741. doi:10.3382/ps.2012-02144
  • Chousalkar KK, Sexton M, McWhorter A, Hewson K, Martin G, Shadbolt C, Goldsmith P. 2015. Salmonella Typhimurium in the Australian egg industry: multidisciplinary approach to addressing the public health challenge and future directions. Crit Rev Food Sci Nutr. doi:10.1080/10408398.2015.1113928
  • Corcoran M, Morris D, De Lappe N, O’Connor J, Lalor P, Dockery P, Cormican M. 2014. Commonly used disinfectants fail to eradicate Salmonella enterica biofilm from food contact surface materials. Appl Environ Microbiol. 80:1507–1514. doi:10.1128/AEM.03109-13
  • Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science. 284:1318–1322. doi:10.1126/science.284.5418.1318
  • 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. doi:10.1089/fpd.2013.1710
  • Fabrega A, Soto SM, Balleste-Delpierre C, Fernandez-Orth D, Jimenez de Anta MT, Vila J. 2014. Impact of quinolone-resistance acquisition on biofilm production and fitness in Salmonella enterica. J Antimicrob Chemother. 69:1815–1824. doi:10.1093/jac/dku078
  • Food Standards Australia New Zealand. 2009. Risk assessment of eggs and egg products. 1–192. Available from: https://www.foodstandards.gov.au/code/proposals/documents/P301%20Eggs%20PPPS%20DAR%20SD1%20Risk%20Assessment.pdf.
  • Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Gast R, Humphrey TJ, Van Immerseel F. 2009. Mechanisms of egg contamination by Salmonella Enteritidis. FEMS Microbiol Rev. 33:718–738. doi:10.1111/j.1574-6976.2008.00161.x
  • Gerstel U, Romling U. 2001. Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environ Microbiol. 3:638–648. doi:10.1046/j.1462-2920.2001.00235.x
  • Gerstel U, Römling U. 2003. The csgD promoter, a control unit for biofilm formation in Salmonella typhimurium. Res Microbiol. 154:659–667. doi:10.1016/j.resmic.2003.08.005
  • Gole VC, Caraguel CG, Sexton M, Fowler C, Chousalkar KK. 2014a. Shedding of Salmonella in single age caged commercial layer flock at an early stage of lay. Int J Food Microbiol. 189:61–66. doi:10.1016/j.ijfoodmicro.2014.07.030
  • Gole VC, Torok V, Sexton M, Caraguel CG, Chousalkar KK. 2014b. Association between the indoor environmental contamination of Salmonella with egg contamination on layer farms. J Clin Microbiol. 52:3250–3258. doi:10.1128/JCM.00816-14
  • Gole VC, Chousalkar KK, Roberts JR, Sexton M, May D, Tan J, Kiermeier A. 2014c. Effect of egg washing and correlation between eggshell characteristics and egg penetration by various Salmonella Typhimurium strains. PloS one. 9:e90987. doi:10.1371/journal.pone.0090987
  • Grantcharova N, Peters V, Monteiro C, Zakikhany K, Romling U. 2010. Bistable expression of CsgD in biofilm development of Salmonella enterica serovar Typhimurium. J Bacteriol. 192:456–466. doi:10.1128/JB.01826-08
  • Joseph B, Otta SK, Karunasagar I, Karunasagar I. 2001. Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers. Int J Food Microbiol. 64:367–372. doi:10.1016/S0168-1605(00)00466-9
  • Latasa C, Roux A, Toledo-Arana A, Ghigo JM, Gamazo C, Penadés JR, Lasa I. 2005. BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol Microbiol. 58:1322–1339. doi:10.1111/j.1365-2958.2005.04907.x
  • Lianou A, Koutsoumanis KP. 2012. Strain variability of the biofilm forming ability of Salmonella enterica under various environmental conditions. Int J Food Microbiol. 160:171–178. doi:10.1016/j.ijfoodmicro.2012.10.002
  • Liu Z, Niu H, Wu S, Huang R. 2014. CsgD regulatory network in a bacterial trait-altering biofilm formation. Emerg Microbes Infect. 3(1):e1. doi:10.1038/emi.2014.1
  • Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 25:402–408. 10.1006/meth.2001.1262
  • 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. doi:10.1086/649513
  • McAuley CM, Duffy LL, Subasinghe N, Hogg G, Coventry J, Fegan N. 2015. Salmonella Typhimurium and Salmonella Sofia: growth in and persistence on eggs under production and retail conditions. BioMed Res Int. Article ID 914987: 1–8. foi:10.1155/2015/914987
  • O’Leary D, Cabe EMM, McCusker MP, Martins M, Fanning S, Duffy G. 2013. Microbiological study of biofilm formation in isolates of Salmonella enterica Typhimurium DT104 and DT104b cultured from the modern pork chain. Int J Food Microbiol. 161:36–43. doi:10.1016/j.ijfoodmicro.2012.11.021
  • OzFoodNet Working Group. 2012. Monitoring the incidence and causes of diseases potentially transmitted by food in Australia: annual report of the OzFoodNet network, 2010. Commun Dis Intell Q Rep. 36:E213–241. Available from: http://www.health.gov.au/internet/main/publishing.nsf/Content/cda-cdi3603a.htm
  • OzFoodNet Working Group. 2015. OzFoodNet quarterly report, 1 January to 31 March 2014. Commun Dis Intell Q Rep. 39:E612–618. Available from: http://www.health.gov.au/internet/main/publishing.nsf/Content/cda-cdi3904i.htm
  • Romling U, Bokranz W, Rabsch W, Zogaj X, Nimtz M, Tschape H. 2003. Occurrence and regulation of the multicellular morphotype in Salmonella serovars important in human disease. Int J Med Microbiol. 293:273–285. doi:10.1078/1438-4221-00268
  • Römling U, Bian Z, Hammar M, Sierralta WD, Normark S. 1998. Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol. 180:722–731. Available from: http://jb.asm.org/content/180/3/722.full
  • Romling U, Rohde M, Olsen A, Normark S, Reinkoster J. 2000. AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol. 36:10–23. doi:10.1046/j.1365-2958.2000.01822.x
  • Romling U, Sierralta WD, Eriksson K, Normark S. 1998. Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol Microbiol. 28:249–264. doi:10.1046/j.1365-2958.1998.00791.x
  • Samberg Y, Meroz M. 1995. Application of disinfectants in poultry hatcheries. Rev Sci Tech. 14:365–380. Available from: http://europepmc.org/abstract/med/7579636
  • Schonewille E, Nesse LL, Hauck R, Windhorst D, Hafez HM, Vestby LK. 2012. Biofilm building capacity of Salmonella enterica strains from the poultry farm environment. FEMS Immunol Med Microbiol. 65:360–365. doi:10.1111/j.1574-695X.2012.00966.x
  • Seixas R, Machado J, Bernardo F, Vilela C, Oliveira M. 2014. Biofilm formation by Salmonella enterica serovar 1,4,[5],12:i:- Portuguese isolates: a phenotypic, genotypic, and socio-geographic analysis. Curr Microbiol. 68:670–677. doi:10.1007/s00284-014-0523-x
  • Shi X, Zhu X. 2009. Biofilm formation and food safety in food industries. Trends Food Sci Tech. 20:407–413. doi:10.1016/j.tifs.2009.01.054
  • Steenackers H, Hermans K, Vanderleyden J, De Keersmaecker SC. 2012. Salmonella biofilms: an overview on occurrence, structure, regulation and eradication. Food Res Int. 45:502–531. doi:10.1016/j.foodres.2011.01.038
  • Stepanović S, Ćirković I, Mijač V, Švabić-Vlahović M. 2003. Influence of the incubation temperature, atmosphere and dynamic conditions on biofilm formation by Salmonella spp. Food Microbiol. 20:339–343. doi:10.1016/S0740-0020(02)00123-5
  • Taylor JP, Barnett BJ, del Rosario L, Williams K, Barth SS. 1998. Prospective investigation of cryptic outbreaks of Salmonella agona salmonellosis. J Clin Microbiol. 36:2861–2864. Available from: http://jcm.asm.org/content/36/10/2861.full
  • Vestby LK, Møretrø T, Ballance S, Langsrud S, Nesse LL. 2009. Survival potential of wild type cellulose deficient Salmonella from the feed industry. BMC Vet Res. 5:43. doi:10.1186/1746-6148-5-43
  • Wang H, Dong Y, Wang G, Xu X, Zhou G. 2016. Effect of growth media on gene expression levels in Salmonella Typhimurium biofilm formed on stainless steel surface. Food Control. 59:546–552. doi:10.1016/j.foodcont.2015.06.026
  • White AP, Gibson DL, Grassl GA, Kay WW, Finlay BB, Vallance BA, Surette MG. 2008. Aggregation via the red, dry, and rough morphotype is not a virulence adaptation in Salmonella enterica serovar Typhimurium. Infect Immun. 76:1048–1058. doi:10.1128/IAI.01383-07
  • Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, Crawford RW, Russell JM, Bevins CL, Adams LG, Tsolis RM. 2010. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature. 467:426–429. doi:10.1038/nature09415

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.