[en] Introduction: Salmonella Livingstone is one of the most common serotypes responsible for nosocomial outbreaks in Tunisia. In this study, 42 isolates of Salmonella Livingstone were analyzed. Most of these were isolated from humans (31 strains from Tunisia and 9 strains from Belgium) and 2 isolates came from food products (beef and pork).
Methodology: All strains were characterized by antibiogram, multilocus sequence typing (MLST), and virulotyping. This last technique was carried out by simple PCR of five chromosomal genes (agfA, hin/H2, iroB, phoP/Q, and slyA) and two plasmid genes (spvA and spvC).
Results: All Tunisian strains were resistant to amoxicillin, amoxicillin-clavulanic acid, ticarcillin, cefalotin, gentamicin, and kanamycin. They were also resistant to third-generation cephalosporin antibiotics (cefotaxim and ceftazidim). Belgian isolates were susceptible to all antibiotics tested. Further to MLST analyses, Tunisian strains belonged to the same sequence type, ST543. For Belgian isolates, eight strains had a ST543 profile, two strains had a ST638 profile, and one strain had a ST457 profile. Analyses of the virulence gene contents showed that strains isolated in different years and from different origins had the same virulence profile. These carried all five chromosomal genes and lacked plasmid-located virulence genes spvA and spvC.
Conclusions: A combination of different typing methods showed that the majority of Belgian strains and all Tunisian strains were closely related; they belonged to the same sequence type (ST543) and had the same virulence profile, but different antibiotic resistance profiles depended on the country of origin.
Research center :
FARAH - Fundamental and Applied Research for Animals and Health - ULiège
Disciplines :
Microbiology
Author, co-author :
Guedda, Intissar
Taminiau, Bernard ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Ferjani, Asma
Boukadida, Jalel
Bertrand, Sophie; Institut Scientifique de la Santé publique = Wetenschappelijk Instituut Volksgezondheid (Belgique) - ISP = WIV
Daube, Georges ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Language :
English
Title :
Antimicrobial and molecular analysis of Salmonella serovar Livingstone strains isolated from humans in Tunisia and Belgium
Publication date :
August 2014
Journal title :
Journal of Infection in Developing Countries
ISSN :
2036-6590
eISSN :
1972-2680
Publisher :
Open Learning on Enteric Pathogens, Alghero, Italy
Litrup E, Torpdahl M, Malorny B, Huehn S, Christensen H, Nielsen EM (2010) Association between phylogeny, virulence potential and serovars of Salmonella enterica. Infect Genet Evol 10: 1132-1139.
Foley SL, Lynne AM, Nayak R (2008) Salmonella challenges: prevalence in swine and poultry and potential pathogenicity of such isolates. J Anim Sci 86: 149-162.
Popoff MY (2001) Antigenic formulas of the Salmonella serovars, 8th revision. WHO Collaborating Centre for Reference and Research on Salmonella. Paris, France: Institut Pasteur.
Picton WH, Stirrup W, Price A, Taylor J (1953) A new Salmonella type, Salm. Livingstone. J Pathol Bacteriol 66: 310-312.
Old DC, Porter-Boveri M, Munro DS (1994) Human infection in Tayside, Scotland due to Salmonella serotype Livingstone. J Med Microbiol 40: 134-140.
Bouallègue-Godet O, Ben Salem Y, Fabre L, Demartin M, Grimont P, Mzoughi R, Weill FX (2005) Nosocomial outbreak caused by Salmonella enterica serotype Livingstone producing CTX-M-27 extended-spectrum beta-lactamase in a neonatal unit in Sousse, Tunisia. J Clin Microbiol 43: 1037-1044.
Ktari S, Arlet G, Verdet C, Jaoua S, Kachrid A, Ben Redjeb S, Mahjoubi-Rhimi F, Hammami A (2009) Molecular epidemiology and genetic environment of acquired bla ACC-1 in Salmonella enterica serotype Livingstone causing a large nosocomial outbreak in Tunisia. Microb Drug Resist 15: 279-286.
Ktari S, Mahjoubi F, Jaoua S, Karray A, Marty N, Ben Redjeb S, Hammami A (2006) Application de marqueurs génotypiques dans l'investigation de deux épidémies d'infections nosocomiales à Salmonella Livingstone dans le CHU de Sfax, Tunisie. Pathol Biol 54: 331-336.
Guerin PJ, De Jong B, Heir E, Hasseltvedt V, Kapperud G, Styrmo K, Gondrosen B, Lassen J, Andersson Y (2004) Outbreak of Salmonella Livingstone infection in Norway and Sweden due to contaminated processed fish products. Epidemiol Infect 132: 889-895.
Fisher I (1997) An international outbreak of Salmonella Livingstone recognised by Enter salm-net. Euro Surveill 4.
Centre National de Référence des Salmonella et Shigella (2009) Données de surveillance du Centre National de Référence des Salmonella et Shigella, Belgique.
Ktari S, Arlet G, Mnif B, Gautier V, Mahjoubi F, Ben Jmeaa M, Bouaziz M, Hammami A (2006) Emergence of multidrug-resistant Klebsiella pneumoniae isolates producing VIM-4 metallo-beta-lactamase, CTX-M-15 extended-spectrum beta-lactamase, and CMY-4 AmpC beta-lactamase in a Tunisian university hospital. Antimicrob Agents Chemother 50: 4198-4201.
Bell RL, González-Escalona N, Stones R, Brown EW (2011) Phylogenetic evaluation of the "Typhimurium" complex of Salmonella strains using a seven-gene multi-locus sequence analysis. Infect Genet Evol 11: 83-91.
Huehn S, La Ragione R, Anjum M, Saunders M, Woodward MJ, Bunge C, Helmuth R, Hauser E, Guerra B, Beutlich J, Brisabois A, Peters T, Svensson L, Madajczak G, Litrup E, Imre A, Herrera-Leon S, Mevius D, Newell DG, Malorny B (2010) Virulotyping and antimicrobial resistance typing of Salmonella enterica serovars relevant to human health in Europe. Foodborne Pathog Dis 7: 523-535.
Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, Zhang Q, Zhou J, Zurth K, Caugant DA, Feavers IM, Achtman M, Spratt BG (1998) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci 95: 3140-3145.
Revazishvili T, Mamuka Kotetishvili M, Stine OC, Kreger AS, Morris JG, Sulakvelidze A (2004) Comparative analysis of multilocus sequence typing and pulsed-field gel electrophoresis for characterizing Listeria monocytogenes strains isolated from environmental and clinical sources. J Clin Microbiol 42: 276-285.
Lévesque S, Frost E, Arbeit RD, Michaud S (2008) Multilocus sequence typing of Campylobacter jejuni isolates from humans, chickens, raw milk, and environmental water in Quebec, Canada. J Clin Microbiol 46: 3404-3411.
Liu B, Zhang L, Zhu X, Shi C, Chen J, Liu W, He X, Shi X (2011) PCR identification of Salmonella serogroups based on specific targets obtained by comparative genomics. Int J Food Microbiol 144: 511-518.
Ross IL, Heuzenroeder MW (2005) Discrimination within phenotypically closely related definitive types of Salmonella enterica serovar Typhimurium by the multiple amplification of phage locus typing technique. J Clin Microbiol 43: 1604-1611.
Tankouo-Sandjong B, Sessitsch A, Liebana E, Kornschober C, Allerberger F, Hächler H, Bodrossy L (2007) MLST-v, multilocus sequence typing based on virulence genes, for molecular typing of Salmonella enterica subsp. enterica serovars. J Microbiol Methods 69: 23-36.
Nicolas P, Raphenon G, Guibourdenche M, Decousset L, Stor R, Gaye AB (2000) The 1998 Senegal epidemic of meningitis was due to the clonal expansion of A:4:P1.9, clone III-1, sequence type 5 Neisseria meningitidis strains. J Clin Microbiol 38: 198-200.
Urwin R, Maiden MCJ (2003) Multi-locus sequence typing: a tool for global epidemiology. Trends Microbiol 11: 479-487.
Sánchez-Jiménez MM, Cardona-Castro NM, Canu N, Uzzau S, Rubino S (2010) Distribution of pathogenicity islands among Colombian isolates of Salmonella. J Infect Dev Ctries 4: 555-559. doi:10.3855/jidc.670.
Skyberg JA, Logue CM, Nolan LK (2006) Virulence genotyping of Salmonella spp. with multiplex PCR. Avian Dis 50: 77-81.
Heithoff DM, Shimp WR, Lau PW, Badie G, Enioutina EY, Daynes RA, Byrne BA, House JK, Mahan MJ (2008) Human Salmonella clinical isolates distinct from those of animal origin. Appl Environ Microbiol 74: 1757-1766.
Soto SM, Guerra B, Del Cerro A, González-Hevia MA, Mendoza MC (2001) Outbreaks and sporadic cases of Salmonella serovar Panama studied by DNA fingerprinting and antimicrobial resistance. Int J Food Microbiol 71: 35-43.
Smith KP, George J, Cadle KM, Kumar S, Aragon SJ, Hernandez RL, Jones SE, Floyd JL, Varela MF (2010) Elucidation of antimicrobial susceptibility profiles and genotyping of Salmonella enterica isolates from clinical cases of Salmonellosis in New Mexico in 2008. World J Microbiol Biotechnol 26: 1025-1031.
Grimont PAD, Weill FX (2007) Antigenic formulae of the Salmonella serovars. WHO Collaborating Centre for Reference. Paris, France: Institut Pasteur.
Honoré S, Lascols C, Malin D, Targaouchi, Cattoir V, Legrand P, Soussy CJ, Cambau E (2006) Émergence et diffusion chez les entérobactéries du nouveau mécanisme de résistance plasmidique aux quinolones Qnr (résultats hôpital Henri-Mondor 2002-2005). Pathol Biol 54: 270-279.
Del Cerro A, Soto SM, Mendoza MC (2003) Virulence and antimicrobial-resistance gene profiles determined by PCR-based procedures for Salmonella isolated from samples of animal origin. Food Microbiol 20: 431-438.
Climent Y, Yero D, Martinez I, Martín A, Jolley KA, Sotolongo F, Maiden MCJ, Urwin R, Pajón R (2010) Clonal Distribution of Disease-Associated and Healthy Carrier Isolates of Neisseria meningitidis between 1983 and 2005 in Cuba. J Clin Microbiol 48: 802-810.
Ozawa M, Baba K, Asai T (2010) Molecular typing of avian pathogenic Escherichia coli O78 strains in Japan by using multilocus sequence typing and pulsed-field gel electrophoresis. J Vet Med Sci 72: 1517-1520.
Kidgell C, Reichard U, Wain J, Linz B, Torpdahl M, Dougan D, Achtman M (2002) Salmonella typhi, the causative agent of typhoid fever, is approximately 50,000 years old. Infect Genet Evol 2: 39-45.
Sangal V, Harbottle H, Mazzoni CJ, Helmuth R, Guerra B, Didelot X, Paglietti B, Rabsch W, Brisse S, Weill FX, Roumagnac P, Achtman M (2010) Evolution and population structure of Salmonella enterica serovar Newport. J Bacteriol 192: 6465-6476.
Liu F, Barrangou R, Gerner-Smidt P, Ribot E, Knabel S, Dudley E (2011) Novel Virulence Gene and Clustered Regularly Interspaced Short Palindromic Repeat (CRISPR) Multilocus Sequence Typing Scheme for Subtyping of the Major Serovars of Salmonella enterica subsp. enterica. Appl Environ Microbiol 77: 1946-1956.
Foley SL, White D, McDermott PF, Walker RD, Fedorka-Cray PJ, Simjee S, Zhao S (2006) Comparison of Subtyping Methods for Differentiating Salmonella enterica Serovar Typhimurium Isolates Obtained from Food Animal Sources. J Clin Microbiol 44: 3569-3577.
Kotetishvili M, Stine OC, Kreger A, Morris JG, Sulakvelidze A (2002) Multilocus sequence typing for characterization of clinical and environmental Salmonella strains. J Clin Microbiol 40: 1626-1635.
Ikumapayi UN, Antonio M, Sonne-Hansen J, Biney E, Enwere E, Okoko B, Oluwalana C, Vaughan A, Zaman SM, Greenwood BM, Oluwalana C, Vaughan A, Zaman SM, Greenwood BM, Cutts F, Adegbola R (2007) Molecular epidemiology of community-acquired invasive non-typhoidal Salmonella among children aged 2-29 months in rural Gambia and discovery of a new serovar, Salmonella enterica Dingiri. J Med Microbiol 56: 1479-1484.
Torpdahl M, Skov MN, Dorthe Sandvang D, Baggesen DL (2005) Genotypic characterization of Salmonella by multilocus sequence typing, pulsed-field gel electrophoresis and amplified fragment length polymorphism. J Microbiol Methods 63: 173-184.
Sukhnanand S, Alcaine S, Warnick LD, Su WL, Hof J, Craver MP, MCDonough P, Boor KJ, Wiedmann (2005) DNA sequence-based subtyping and evolutionary analysis of selected Salmonella enterica serotypes. J Clin Microbiol 43: 3688-3698.
Fakhr MK, Nolan LK, Logue CM (2005) Multilocus sequence typing lacks the discriminatory ability of pulsed-field gel electrophoresis for typing Salmonella enterica serovar Typhimurium. J Clin Microbiol 43: 2215-2219.
Liu WB, Liu B, Zhu X, Yu SJ, Shi XM (2011) Diversity of Salmonella isolates using serotyping and multilocus sequence typing. Food Microbiol 28: 1182-1189.
Wannaprasat W, Padungtod P, Chaunchuen R (2011) Class 1 integrons and virulence genes in Salmonella enterica isolates from pork and humans. Int J Antimicrob Agents 37: 457-461.
Kumar R, Surendran PK, Thampuran N (2009) Detection and characterization of virulence factors in lactose positive and lactose negative Salmonella serovars isolated from sea food. Food Control 20: 376-380.
Marcus SL, Brumell JH, Pfeifer CG, Finlay BB (2000) Salmonella pathogenicity islands: big virulence in small packages. Microbes Infect Inst Pasteur 2: 145-156.
Van Asten AJ, Van Dijk JE (2005) Distribution of "classic" virulence factors among Salmonella spp. Fems Immunol Med Microbiol 44: 251-259.
Guiney DG, Fierer J (2011) The Role of the spv Genes in Salmonella Pathogenesis. Front Microbiol 2: 129.
