1,391
Views
13
CrossRef citations to date
0
Altmetric
Original Articles

Field investigations of multidrug-resistant Salmonella Infantis epidemic strain incursions into broiler flocks in England and Wales

, , &
Pages 631-641 | Received 30 Mar 2020, Accepted 10 Aug 2020, Published online: 08 Sep 2020

References

  • Alba, P., Leekitcharoenphon, P., Carfora, V., Amoruso, R., Cordaro, G., Di Matteo, P., Ianzano, A., Iurescia, M., Diaconu, E.L., Study Group, E.N., Pedersen, S.K., Guerra, B., Hendriksen, R.S., Franco, A. & Battisti, A. (2020). Molecular epidemiology of Salmonella Infantis in Europe: insights into the success of the bacterial host and its parasitic pESI-like megaplasmid. Microbial Genomics, 6. doi: 10.1099/mgen.0.000365
  • APHA, Animal and Plant Health Agency. (2019). Salmonella in Livestock Production in GB, 2018.
  • Baloda, S.B., Christensen, L. & Trajcevska, S. (2001). Persistence of a Salmonella enterica serovar typhimurium DT12 clone in a piggery and in agricultural soil amended with Salmonella-contaminated slurry. Applied Environmental Microbiology, 67, 2859–2862. doi: 10.1128/AEM.67.6.2859-2862.2001
  • Bennett, D.D., Higgins, S.E., Moore, R.W., Beltran, R., Caldwell, D.J., Byrd, J.A. & Hargis, B.M. (2003). Effects of lime on Salmonella enteritidis survival in vitro. Journal of Applied Poultry Research, 12, 65–68. doi: 10.1093/japr/12.1.65
  • Bogomazova, A.N., Gordeeva, V.D., Krylova, E.V., Soltynskaya, I.V., Davydova, E.E., Ivanova, O.E. & Komarov, A.A. (2019). Mega-plasmid found worldwide confers multiple antimicrobial resistance in Salmonella Infantis of broiler origin in Russia. International Journal of Food Microbiology, 319, 108497. doi: 10.1016/j.ijfoodmicro.2019.108497
  • Carattoli, A., Zankari, E., Garcia-Fernandez, A., Voldby Larsen, M., Lund, O., Villa, L., Moller Aarestrup, F. & Hasman, H. (2014). In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrobial Agents and Chemotherapy, 58, 3895–3903. doi: 10.1128/AAC.02412-14
  • Carfora, V., Alba, P., Leekitcharoenphon, P., Ballaro, D., Cordaro, G., Di Matteo, P., Donati, V., Ianzano, A., Iurescia, M., Stravino, F., Tagliaferri, T., Battisti, A. & Franco, A. (2018). Colistin resistance mediated by mcr-1 in ESBL-producing, multidrug resistant Salmonella Infantis in broiler chicken industry, Italy (2016–2017). Frontiers in Microbiology, 9, 1880. doi: 10.3389/fmicb.2018.01880
  • Carrique-Mas, J.J., Marin, C., Breslin, M., McLaren, I. & Davies, R. (2009). A comparison of the efficacy of cleaning and disinfection methods in eliminating Salmonella spp. from commercial egg laying houses. Avian Pathology, 38, 419–424. doi: 10.1080/03079450903193768
  • Chattaway, M.A., Dallman, T.J., Larkin, L., Nair, S., McCormick, J., Mikhail, A., Hartman, H., Godbole, G., Powell, D., Day, M., Smith, R. & Grant, K. (2019). The transformation of reference microbiology methods and surveillance for Salmonella with the use of whole genome sequencing in England and Wales. Frontiers in Public Health, 7, 317. doi: 10.3389/fpubh.2019.00317
  • Collignon, P., Powers, J.H., Chiller, T.M., Aidara-Kane, A. & Aarestrup, F.M. (2009). World Health Organization ranking of antimicrobials according to their importance in human medicine: a critical step for developing risk management strategies for the use of antimicrobials in food production animals. Clinical Infectious Diseases, 49, 132–141. doi: 10.1086/599374
  • Crabb, H.K., Allen, J.L., Devlin, J.M., Firestone, S.M., Wilks, C.R. & Gilkerson, J.R. (2018). Salmonella spp. transmission in a vertically integrated poultry operation: clustering and diversity analysis using phenotyping (serotyping, phage typing) and genotyping (MLVA). PloS One, 13, e0201031. doi: 10.1371/journal.pone.0201031
  • Dallman, T., Ashton, P., Schafer, U., Jironkin, A., Painset, A., Shaaban, S., Hartman, H., Myers, R., Underwood, A., Jenkins, C. & Grant, K. (2018). SnapperDB: a database solution for routine sequencing analysis of bacterial isolates. Bioinformatics (Oxford, England), 34, 3028–3029. doi: 10.1093/bioinformatics/bty212
  • Davies, R. & Breslin, M. (2003). Observations on Salmonella contamination of commercial laying farms before and after cleaning and disinfection. Veterinary Record, 152, 283–287. doi: 10.1136/vr.152.10.283
  • Davies, R., Breslin, M., Corry, J.E., Hudson, W. & Allen, V.M. (2001). Observations on the distribution and control of Salmonella species in two integrated broiler companies. Veterinary Record, 149, 227–232. doi: 10.1136/vr.149.8.227
  • Davies, R.H., Nicholas, R.A., McLaren, I.M., Corkish, J.D., Lanning, D.G. & Wray, C. (1997). Bacteriological and serological investigation of persistent Salmonella enteritidis infection in an integrated poultry organisation. Veterinary Microbiology, 58, 277–293. doi: 10.1016/S0378-1135(97)00157-0
  • Davies, R.H. & Wray, C. (1995). Observations on disinfection regimens used on Salmonella enteritidis infected poultry units. Poultry Science, 74, 638–647. doi: 10.3382/ps.0740638
  • Defra, Department for Environment, Food and Rural Affairs. (2008). UK National Control Programme for Salmonella in Chickens (Gallus gallus) Reared for Meat (Broilers ).
  • Drauch, V., Ibesich, C., Vogl, C., Hess, M. & Hess, C. (2020). In-vitro testing of bacteriostatic and bactericidal efficacy of commercial disinfectants against Salmonella Infantis reveals substantial differences between products and bacterial strains. International Journal of Food Microbiology, 328, 108660. doi: 10.1016/j.ijfoodmicro.2020.108660
  • EFSA and ECDC, European Food Safety Authority and European Centre for Disease Prevention and Control. (2018). The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2016. EFSA Journal, 270.
  • EFSA and ECDC, European Food Safety Authority and European Centre for Disease Prevention and Control. (2019). The European Union One Health 2018 Zoonoses Report. EFSA Journal, 17, 296.
  • EFSA BIOHAZ, European Food Safety Authority Panel on Biological Hazards. (2019). Salmonella control in poultry flocks and its public health impact. EFSA Journal, 17, 94.
  • Franco, A., Leekitcharoenphon, P., Feltrin, F., Alba, P., Cordaro, G., Iurescia, M., Tolli, R., D'Incau, M., Staffolani, M., Di Giannatale, E., Hendriksen, R.S. & Battisti, A. (2015). Emergence of a clonal lineage of multidrug-resistant ESBL-producing Salmonella Infantis transmitted from broilers and broiler meat to humans in Italy between 2011 and 2014. PloS One, 10, e0144802. doi: 10.1371/journal.pone.0144802
  • Gal-Mor, O., Valinsky, L., Weinberger, M., Guy, S., Jaffe, J., Schorr, Y.I., Raisfeld, A., Agmon, V. & Nissan, I. (2010). Multidrug-resistant Salmonella enterica serovar Infantis, Israel. Emerging Infectious Diseases, 16, 1754–1757. doi: 10.3201/eid1611.100100
  • Gradel, K.O., Andersen, J. & Madsen, M. (2002). Comparisons of sampling procedures and time of sampling for the detection of Salmonella in Danish infected chicken flocks raised in floor systems. Acta Veterinaria Scandinavica, 43, 21–30. doi: 10.1186/1751-0147-43-21
  • Grimont, P. & Weill, F. (2007). Antigenic Formulae of the Salmonella SErovars 9th Edn. Paris: WHO Collaborating Centre for Reference and Research on Salmonella.
  • Gymoese, P., Kiil, K., Torpdahl, M., Osterlund, M.T., Sorensen, G., Olsen, J.E., Nielsen, E.M. & Litrup, E. (2019). WGS based study of the population structure of Salmonella enterica serovar Infantis. BMC Genomics, 20, 870. doi: 10.1186/s12864-019-6260-6
  • Hauser, E., Tietze, E., Helmuth, R., Junker, E., Prager, R., Schroeter, A., Rabsch, W., Fruth, A., Toboldt, A. & Malorny, B. (2012). Clonal dissemination of Salmonella enterica serovar Infantis in Germany. Foodborne Pathogens and Disease, 9, 352–360. doi: 10.1089/fpd.2011.1038
  • Helms, M., Vastrup, P., Gerner-Smidt, P. & Molbak, K. (2002). Excess mortality associated with antimicrobial drug-resistant Salmonella Typhimurium. Emerging Infectious Diseases, 8, 490–495. doi: 10.3201/eid0805.010267
  • Hindermann, D., Gopinath, G., Chase, H., Negrete, F., Althaus, D., Zurfluh, K., Tall, B.D., Stephan, R. & Nuesch-Inderbinen, M. (2017). Salmonella enterica serovar Infantis from food and human infections, Switzerland, 2010–2015: poultry-related multidrug resistant clones and an emerging ESBL producing clonal lineage. Frontiers in Microbiology, 8, 1322. doi: 10.3389/fmicb.2017.01322
  • Issenhuth-Jeanjean, S., Roggentin, P., Mikoleit, M., Guibourdenche, M., de Pinna, E., Nair, S., Fields, P.I. & Weill, F.X. (2014). Supplement 2008-2010 (no. 48) to the White-Kauffmann-Le Minor scheme. Research in Microbiology, 165, 526–530. doi: 10.1016/j.resmic.2014.07.004
  • Joseph, B., Otta, S.K., Karunasagar, I. & Karunasagar, I. (2001). Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers. International Journal of Food Microbiology, 64, 367–372. doi: 10.1016/S0168-1605(00)00466-9
  • Karacan Sever, N. & Akan, M. (2019). Molecular analysis of virulence genes of Salmonella Infantis isolated from chickens and turkeys. Microbial Pathogenesis, 126, 199–204. doi: 10.1016/j.micpath.2018.11.006
  • Kim, A., Lee, Y.J., Kang, M.S., Kwag, S.I. & Cho, J.K. (2007). Dissemination and tracking of Salmonella spp. in integrated broiler operation. Journal of Veterinary Science, 8, 155–161. doi: 10.4142/jvs.2007.8.2.155
  • Lindqvist, N. & Pelkonen, S. (2007). Genetic surveillance of endemic bovine Salmonella Infantis infection. Acta Veterinaria Scandinavica, 49, 15. doi: 10.1186/1751-0147-49-15
  • Maes, S., Vackier, T., Nguyen Huu, S., Heyndrickx, M., Steenackers, H., Sampers, I., Raes, K., Verplaetse, A. & De Reu, K. (2019). Occurrence and characterisation of biofilms in drinking water systems of broiler houses. BMC Microbiology, 19, 77. doi: 10.1186/s12866-019-1451-5
  • Magiorakos, A.P., Srinivasan, A., Carey, R.B., Carmeli, Y., Falagas, M.E., Giske, C.G., Harbarth, S., Hindler, J.F., Kahlmeter, G., Olsson-Liljequist, B., Paterson, D.L., Rice, L.B., Stelling, J., Struelens, M.J., Vatopoulos, A., Weber, J.T. & Monnet, D.L. (2012). Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection, 18, 268–281. doi: 10.1111/j.1469-0691.2011.03570.x
  • McDonnell, G. & Russell, A.D. (1999). Antiseptics and disinfectants: activity, action, and resistance. Clinical Microbiology Reviews, 12, 147–179. doi: 10.1128/CMR.12.1.147
  • Moraes, J.O., Cruz, E.A., Souza, E.G.F., Oliveira, T.C.M., Alvarenga, V.O., Pena, W.E.L., Sant'Ana, A.S. & Magnani, M. (2018). Predicting adhesion and biofilm formation boundaries on stainless steel surfaces by five Salmonella enterica strains belonging to different serovars as a function of pH, temperature and NaCl concentration. International Journal of Food Microbiology, 281, 90–100. doi: 10.1016/j.ijfoodmicro.2018.05.011
  • Mueller-Doblies, D., Carrique-Mas, J.J., Sayers, A.R. & Davies, R.H. (2010). A comparison of the efficacy of different disinfection methods in eliminating Salmonella contamination from turkey houses. Journal of Applied Microbiology, 109, 471–479.
  • Nogrady, N., Kardos, G., Bistyak, A., Turcsanyi, I., Meszaros, J., Galantai, Z., Juhasz, A., Samu, P., Kaszanyitzky, J.E., Paszti, J. & Kiss, I. (2008). Prevalence and characterization of Salmonella Infantis isolates originating from different points of the broiler chicken-human food chain in Hungary. International Journal of Food Microbiology, 127, 162–167. doi: 10.1016/j.ijfoodmicro.2008.07.005
  • Nogrady, N., Kiraly, M., Davies, R. & Nagy, B. (2012). Multidrug resistant clones of Salmonella Infantis of broiler origin in Europe. International Journal of Food Microbiology, 157, 108–112. doi: 10.1016/j.ijfoodmicro.2012.04.007
  • Nogrady, N., Toth, A., Kostyak, A., Paszti, J. & Nagy, B. (2007). Emergence of multidrug-resistant clones of Salmonella Infantis in broiler chickens and humans in Hungary. Journal of Antimicrobial Chemotherapy, 60, 645–648. doi: 10.1093/jac/dkm249
  • Nyberg, K.A., Vinneras, B., Lewerin, S.S., Kjellberg, E. & Albihn, A. (2011). Treatment with Ca(OH)2 for inactivation of Salmonella Typhimurium and Enterococcus faecalis in soil contaminated with infected horse manure. Journal of Applied Microbiology, 110, 1515–1523. doi: 10.1111/j.1365-2672.2011.05006.x
  • Parisi, A., Crump, J.A., Glass, K., Howden, B.P., Furuya-Kanamori, L., Vilkins, S., Gray, D.J. & Kirk, M.D. (2018). Health outcomes from multidrug-resistant Salmonella infections in high-income countries: a systematic review and meta-analysis. Foodborne Pathogens and Disease, 15, 428–436. doi: 10.1089/fpd.2017.2403
  • Pate, M., Micunovic, J., Golob, M., Vestby, L.K. & Ocepek, M. (2019). Salmonella Infantis in broiler flocks in Slovenia: the prevalence of multidrug resistant strains with high genetic homogeneity and low biofilm-forming ability. Biomed Research International, 2019, 4981463. doi: 10.1155/2019/4981463
  • Petrovska, L., Mather, A.E., AbuOun, M., Branchu, P., Harris, S.R., Connor, T., Hopkins, K.L., Underwood, A., Lettini, A.A., Page, A., Bagnall, M., Wain, J., Parkhill, J., Dougan, G., Davies, R. & Kingsley, R.A. (2016). Microevolution of monophasic Salmonella Typhimurium during epidemic, United Kingdom, 2005-2010. Emerging Infectious Diseases, 22, 617–624. doi: 10.3201/eid2204.150531
  • Sandvang, D., Jensen, L.B., Baggesen, D.L. & Baloda, S.B. (2000). Persistence of a Salmonella enterica serotype typhimurium clone in Danish pig production units and farmhouse environment studied by pulsed field gel electrophoresis (PFGE). FEMS Microbiology Letters, 187, 21–25. doi: 10.1111/j.1574-6968.2000.tb09130.x
  • Schonewille, E., Nesse, L.L., Hauck, R., Windhorst, D., Hafez, H.M. & Vestby, L.K. (2012). Biofilm building capacity of Salmonella enterica strains from the poultry farm environment. FEMS Immunology and Medical Microbiology, 65, 360–365. doi: 10.1111/j.1574-695X.2012.00966.x
  • Su, L.H., Chiu, C.H., Chu, C. & Ou, J.T. (2004). Antimicrobial resistance in nontyphoid Salmonella serotypes: a global challenge. Clinical Infectious Diseases, 39, 546–551. doi: 10.1086/422726
  • Tang, Y., Davies, R. & Petrovska, L. (2019). Identification of genetic features for attenuation of two Salmonella enteritidis vaccine strains and differentiation of these from wildtype isolates using whole genome sequencing. Frontiers in Veterinary Science, 6, 447. doi: 10.3389/fvets.2019.00447
  • Tate, H., Folster, J.P., Hsu, C.H., Chen, J., Hoffmann, M., Li, C., Morales, C., Tyson, G.H., Mukherjee, S., Brown, A.C., Green, A., Wilson, W., Dessai, U., Abbott, J., Joseph, L., Haro, J., Ayers, S., McDermott, P.F. & Zhao, S. (2017). Comparative analysis of extended-spectrum-beta-lactamase CTX-M-65-producing Salmonella enterica serovar Infantis isolates from humans, food animals, and retail chickens in the United States. Antimicrobial Agents and Chemotherapy, 61. doi: 10.1128/AAC.00488-17
  • UK-VARSS, Veterinary Medicines Directorate. (2018). UK Veterinary Antibiotic Resistance and Sales Surveillance, UK-VARSS, Supplementary Material.
  • van de Giessen, A.W., Ament, A.J. & Notermans, S.H. (1994). Intervention strategies for Salmonella enteritidis in poultry flocks: a basic approach. International Journal of Food Microbiology, 21, 145–154. doi: 10.1016/0168-1605(94)90207-0
  • Wales, A., Breslin, M. & Davies, R. (2006). Assessment of cleaning and disinfection in Salmonella-contaminated poultry layer houses using qualitative and semi-quantitative culture techniques. Veterinary Microbiology, 116, 283–293. doi: 10.1016/j.vetmic.2006.04.026

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.