Emergence of Salmonella epidemics: the problems related to Salmonella enterica serotype Enteritidis and multiple antibiotic resistance in other major serotypes.

Two major changes in the epidemiology of salmonellosis occurred in the second half of the 20th century: the emergence of food-borne human infections caused by S. Enteritidis and by multiple-antibiotic resistant strains of Salmonella. This review updates information on the S. Enteritidis pandemic and focuses on the emergence of Salmonella, carrying the SGI1 antibiotic resistance gene cluster, resistant to extended-spectrum cephalosporins, or resistant to fluoroquinolones. The factors responsible for the emergence of these Salmonella strains could be either of human origin or related to bacterial genome evolution. However, our increasing understanding of the molecular fluidity of the genome shows that any attempt to counteract bacteria results in further bacterial evolution or adaptation of other bacteria to take place in the new free ecological niche. In these conditions, we can ask who is faster: humans who want to eliminate bacterial pathogens or bacteria that continuously evolve to gain new niches.

[1]  A. Cloeckaert,et al.  Role of TolC and parC mutation in high-level fluoroquinolone resistance in Salmonella enterica serotype Typhimurium DT204. , 2004, The Journal of antimicrobial chemotherapy.

[2]  H. Ochman,et al.  Evolutionary dynamics of full genome content in Escherichia coli , 2000, The EMBO journal.

[3]  C. Beaumont,et al.  Genetic resistance to mortality of day-old chicks and carrier-state of hens after inoculation with Salmonella enteritidis. , 1999, Avian pathology : journal of the W.V.P.A.

[4]  J. Kourea-Kremastinou,et al.  Multiple Clones within Multidrug-ResistantSalmonella enterica Serotype Typhimurium Phage Type DT104 , 2000, Journal of Clinical Microbiology.

[5]  C. Chiu,et al.  Materials and Methods Bacterial Isolates and Patients Emergence of Ceftriaxone-resistant Salmonella Isolates and Rapid Spread of Plasmid-encoded Cmy-2–like Cephalosporinase, Taiwan , 2022 .

[6]  J. Prescott,et al.  Salmonella typhimurium DT104: a virulent and drug-resistant pathogen. , 1998, The Canadian veterinary journal = La revue veterinaire canadienne.

[7]  P. Fratamico,et al.  Molecular Characterization of an Antibiotic Resistance Gene Cluster of Salmonella typhimuriumDT104 , 1999, Antimicrobial Agents and Chemotherapy.

[8]  J. Kourea-Kremastinou,et al.  Multiple clones within multidrug-resistant Salmonella enterica serotype Typhimurium phage type DT104. The Greek Nontyphoidal Salmonella Study Group. , 2000, Journal of clinical microbiology.

[9]  P. Holt,et al.  Persistence of Salmonella enteritidis from one day of age until maturity in experimentally infected layer chickens. , 1998, Poultry science.

[10]  P. Holt,et al.  Molting and Salmonella enterica serovar enteritidis infection: the problem and some solutions. , 2003, Poultry science.

[11]  M. Glynn,et al.  Emergence of multidrug-resistant Salmonella enterica serotype typhimurium DT104 infections in the United States. , 1998, The New England journal of medicine.

[12]  T. Aoki,et al.  The Transposon‐Like Structure of IS26‐Tetracycllne, and Kanamycin Resistance Determinant Derived from Transferable R Plasmid of Fish Pathogen, Pasteurella piscicida , 1994, Microbiology and immunology.

[13]  F. Mostashari,et al.  Emergence of domestically acquired ceftriaxone-resistant Salmonella infections associated with AmpC beta-lactamase. , 2000, JAMA.

[14]  G. Chaconas,et al.  The circle is broken: telomere resolution in linear replicons. , 2001, Current opinion in microbiology.

[15]  D. Sirot,et al.  Plasmid-mediated TEM-3 extended-spectrum beta-lactamase production in Salmonella typhimurium in Casablanca. , 2002, The Journal of antimicrobial chemotherapy.

[16]  É. Chaslus-Dancla,et al.  A new chloramphenicol and florfenicol resistance gene flanked by two integron structures in Salmonella typhimurium DT104. , 1999, FEMS microbiology letters.

[17]  R. Hall,et al.  The integrons In0, In2, and In5 are defective transposon derivatives , 1996, Journal of bacteriology.

[18]  H. Ochman,et al.  Lateral gene transfer and the nature of bacterial innovation , 2000, Nature.

[19]  W. Demczuk,et al.  Characterization of the First Extended-Spectrum Beta-Lactamase-Producing Salmonella Isolate Identified in Canada , 2003, Journal of Clinical Microbiology.

[20]  S. Rubino,et al.  Host adapted serotypes of Salmonella enterica , 2000, Epidemiology and Infection.

[21]  B. Hargis,et al.  Tracing the Origins of Salmonella Outbreaks , 2000, Science.

[22]  R. Carlson,et al.  On-farm monitoring of mouse-invasive Salmonella enterica serovar enteritidis and a model for its association with the production of contaminated eggs , 1997, Applied and environmental microbiology.

[23]  H. Imberechts,et al.  The AcrB multidrug transporter plays a major role in high-level fluoroquinolone resistance in Salmonella enterica serovar typhimurium phage type DT204. , 2002, Microbial drug resistance.

[24]  R. Davies,et al.  Persistence of Salmonella enteritidis phage type 4 in the environment and arthropod vectors on an empty free-range chicken farm. , 2003, Environmental microbiology.

[25]  H. de Valk,et al.  Salmonella - "old" organism, continued challenges ! , 2003, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[26]  L. Majtánová Occurrence of Salmonella enterica serotype Enteritidis phage types in the Slovak Republic. , 1997, European journal of epidemiology.

[27]  R. Davies,et al.  Effects of vaccination and other preventive methods for Salmonella Enteritidis on commercial laying chicken farms , 2003, Veterinary Record.

[28]  S. Schwarz,et al.  Molecular characterization, spread and evolution of multidrug resistance in Salmonella enterica typhimurium DT104. , 2001, Veterinary research.

[29]  P. Fedorka-Cray,et al.  Detection of Multidrug-Resistant Salmonella entericaSerotype typhimurium DT104 Based on a Gene Which Confers Cross-Resistance to Florfenicol and Chloramphenicol , 1999, Journal of Clinical Microbiology.

[30]  S. Schwarz,et al.  Plasmid-Mediated Florfenicol Resistance Encoded by the floR Gene in Escherichia coli Isolated from Cattle , 2000, Antimicrobial Agents and Chemotherapy.

[31]  K. Allen,et al.  Occurrence and characterization of resistance to extended-spectrum cephalosporins mediated by beta-lactamase CMY-2 in Salmonella isolated from food-producing animals in Canada. , 2002, Canadian journal of veterinary research = Revue canadienne de recherche veterinaire.

[32]  E. Giraud,et al.  Evidence for Active Efflux as the Primary Mechanism of Resistance to Ciprofloxacin in Salmonella enterica Serovar Typhimurium , 2000, Antimicrobial Agents and Chemotherapy.

[33]  White Pl,et al.  Strategies to control Salmonella and Campylobacter in raw poultry products , 1997 .

[34]  P. Holt,et al.  Experimental horizontal transmission of Salmonella enteritidis strains (phage types 4, 8, and 13a) in chicks. , 1999, Avian diseases.

[35]  P. Holt,et al.  Effect of Prior Serial In Vivo Passage on the Frequency of Salmonella enteritidis Contamination in Eggs from Experimentally Infected Laying Hens , 2003, Avian diseases.

[36]  A. Cloeckaert,et al.  Mechanisms of quinolone resistance in Salmonella. , 2001, Veterinary research.

[37]  S. O'Brien,et al.  Molecular characterisation of an outbreak strain of multiresistant Salmonella enterica serovar Typhimurium DT104 in the UK. , 2004, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[38]  M. Barza Potential mechanisms of increased disease in humans from antimicrobial resistance in food animals. , 2002, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[39]  D. Henzler,et al.  The role of mice in the epizootiology of Salmonella enteritidis infection on chicken layer farms. , 1992, Avian diseases.

[40]  E. Threlfall Epidemic salmonella typhimurium DT 104--a truly international multiresistant clone. , 2000, The Journal of antimicrobial chemotherapy.

[41]  T. Besser,et al.  Changes in antimicrobial resistance among Salmonella enterica Serovar typhimurium isolates from humans and cattle in the Northwestern United States, 1982-1997. , 1999, Emerging infectious diseases.

[42]  L R Ward,et al.  A case control study of infection with an epidemic strain of multiresistant Salmonella typhimurium DT104 in England and Wales. , 1994, Communicable disease report. CDR review.

[43]  M. Evans,et al.  Foodborne Pathogens: An Illustrated Text , 1991, Annals of Internal Medicine.

[44]  W Schlosser,et al.  Epidemiology and control of egg-associated Salmonella enteritidis in the United States of America. , 1997, Revue scientifique et technique.

[45]  L. McCaig,et al.  Food-related illness and death in the United States. , 1999, Emerging infectious diseases.

[46]  C. M. Collis,et al.  Class 1 Integron Containing a New Gene Cassette, aadA10, Associated with Tn1404 from R151 , 2002, Antimicrobial Agents and Chemotherapy.

[47]  L. Ng,et al.  Partial characterization of a genomic island associated with the multidrug resistance region of Salmonella enterica Typhymurium DT104. , 2000, FEMS microbiology letters.

[48]  W. Hanage,et al.  The relative contributions of recombination and point mutation to the diversification of bacterial clones. , 2001, Current opinion in microbiology.

[49]  N. W. Davis,et al.  Genome sequence of enterohaemorrhagic Escherichia coli O157:H7 , 2001, Nature.

[50]  M. Widdowson,et al.  Laboratory surveillance of bacterial gastroenteric pathogens in The Netherlands, 1991–2001 , 2003, Epidemiology and Infection.

[51]  C. Beaumont,et al.  Differences in frequency, level, and duration of cecal carriage between four outbred chicken lines infected orally with Salmonella enteritidis. , 1997, Avian diseases.

[52]  W. Hardt,et al.  Phage mediated horizontal transfer of the sopE1 gene increases enteropathogenicity of Salmonella enterica serotype Typhimurium for calves. , 2002, FEMS microbiology letters.

[53]  T. Aoki,et al.  Sequence Analysis of the Florfenicol Resistance Gene Encoded in the Transferable R‐Plasmid of a Fish Pathogen, Pasteurella piscicida , 1996, Microbiology and immunology.

[54]  S. Rankin,et al.  Antimicrobial resistance of Salmonella enterica Typhimurium DT104 isolates and investigation of strains with transferable apramycin resistance , 1997, Epidemiology and Infection.

[55]  T J Humphrey,et al.  Contamination of egg shell and contents with Salmonella enteritidis: a review. , 1994, International journal of food microbiology.

[56]  M. Gomáriz,et al.  CMY-2-producing Salmonella enterica, Klebsiella pneumoniae, Klebsiella oxytoca, Proteus mirabilis and Escherichia coli strains isolated in Spain (October 1999-December 2000). , 2001, The Journal of antimicrobial chemotherapy.

[57]  N. Moran,et al.  50 Million Years of Genomic Stasis in Endosymbiotic Bacteria , 2002, Science.

[58]  T. O'Brien Emergence, spread, and environmental effect of antimicrobial resistance: how use of an antimicrobial anywhere can increase resistance to any antimicrobial anywhere else. , 2002, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[59]  F. Weill,et al.  Variant Salmonella Genomic Island 1 Antibiotic Resistance Gene Cluster Containing a Novel 3′-N-Aminoglycoside Acetyltransferase Gene Cassette, aac(3)-Id, in Salmonella enterica Serovar Newport , 2004, Antimicrobial Agents and Chemotherapy.

[60]  W. Rabsch,et al.  Non-typhoidal salmonellosis: emerging problems. , 2001, Microbes and infection.

[61]  P. Barrow Experimental infection of chickens with Salmonella enteritidis. , 1991, Avian pathology : journal of the W.V.P.A.

[62]  A. Summers Generally overlooked fundamentals of bacterial genetics and ecology. , 2002, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[63]  S. Suzuki,et al.  Pathogenicity of Salmonella enteritidis in poultry. , 1994, International journal of food microbiology.

[64]  P. Fey,et al.  Characterization of Plasmids Carrying CMY-2 from Expanded-Spectrum Cephalosporin-Resistant Salmonella Strains Isolated in the United States between 1996 and 1998 , 2002, Antimicrobial Agents and Chemotherapy.

[65]  N. Marano,et al.  A nosocomial outbreak of fluoroquinolone-resistant salmonella infection. , 2001, The New England journal of medicine.

[66]  R. Tauxe,et al.  Public health risk from Salmonella-based rodenticides , 1996, The Lancet.

[67]  J. Terajima,et al.  Molecular typing methods for STEC. , 2003, Methods in Molecular Medicine.

[68]  H. Tillett,et al.  A national outbreak of Salmonella typhimurium DT 124 caused by contaminated salami sticks , 1989, Epidemiology and Infection.

[69]  L. Bossi,et al.  Prophage Contribution to Bacterial Population Dynamics , 2003, Journal of bacteriology.

[70]  R. Kingsley,et al.  Host adaptation and the emergence of infectious disease: the Salmonella paradigm , 2000, Molecular microbiology.

[71]  K. Poole Multidrug resistance in Gram-negative bacteria. , 2001, Current opinion in microbiology.

[72]  W. Demczuk,et al.  Virulence of Salmonella enteritidis phagetypes 4, 8 and 13 and other Salmonella spp. for day-old chicks, hens and mice. , 1993, Canadian journal of veterinary research = Revue canadienne de recherche veterinaire.

[73]  J. Bockemühl,et al.  Supplement 2001 (no. 45) to the Kauffmann-White scheme. , 2003, Research in microbiology.

[74]  A. Brisabois,et al.  Variant Salmonella Genomic Island 1 Antibiotic Resistance Gene Cluster in Salmonella enterica Serovar Albany , 2003, Emerging infectious diseases.

[75]  P. McDermott,et al.  Identification and Expression of CephamycinaseblaCMY Genes in Escherichia coliand Salmonella Isolates from Food Animals and Ground Meat , 2001, Antimicrobial Agents and Chemotherapy.

[76]  R. Hall,et al.  The partial 3'-conserved segment duplications in the integrons In6 from pSa and In7 from pDGO100 have a common origin. , 1993, Plasmid.

[77]  A. Schroeter,et al.  Molecular typing methods for S. enteritidis. , 1994, International journal of food microbiology.

[78]  D. Malo,et al.  Resistance to salmonellosis in the chicken is linked to NRAMP1 and TNC. , 1997, Genome research.

[79]  P. Heisig High-level fluoroquinolone resistance in a Salmonella typhimurium isolate due to alterations in both gyrA and gyrB genes. , 1993, The Journal of antimicrobial chemotherapy.

[80]  L. Piddock,et al.  Evidence for an Efflux Pump Mediating Multiple Antibiotic Resistance in Salmonella enterica Serovar Typhimurium , 2000, Antimicrobial Agents and Chemotherapy.

[81]  W. Rabsch,et al.  Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella typhimurium strain. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[82]  Sangwei Lu,et al.  Association of Salmonella enterica SerovarEnteritidis YafD with Resistance to Chicken EggAlbumen , 2003, Infection and Immunity.

[83]  D. Rice,et al.  Reply to drs. Angulo and collignon , 2000, Emerging Infectious Diseases.

[84]  A. Henken,et al.  Multivariate epidemiological approach to salmonellosis in broiler breeder flocks. , 1992, Poultry science.

[85]  J. Desenclos,et al.  Risk factors for the occurrence of sporadic Salmonella enterica serotype enteritidis infections in children in France: a national case-control study , 1998, Epidemiology and Infection.

[86]  S. Lister Salmonella enteritidis infection in broilers and broiler breeders , 1988, Veterinary Record.

[87]  I. Paulsen,et al.  Proton-dependent multidrug efflux systems , 1996, Microbiological reviews.

[88]  I. Casin,et al.  Fluoroquinolone Resistance Linked to GyrA, GyrB, and ParC Mutations in Salmonella enterica Typhimurium Isolates in Humans , 2003, Emerging infectious diseases.

[89]  P. Pardon,et al.  Quantification of experimental Salmonella enteritidis carrier state in B13 leghorn chicks. , 1995, Avian diseases.

[90]  J. Giesecke,et al.  Emergence of new Salmonella Enteritidis phage types in Europe? Surveillance of infections in returning travellers , 2004, BMC medicine.

[91]  R. Tauxe Salmonella Enteritidis and Salmonella Typhimurium DT104: Successful Subtypes in the Modern World , 1999 .

[92]  J. Threlfall,et al.  Salmonella enteritidis Epidemic , 2000, Science.

[93]  C. Beaumont,et al.  Estimated heritability of the resistance to cecal carrier state of Salmonella enteritidis in chickens. , 1998, Poultry science.

[94]  B. Wallace,et al.  From the Centers for Disease Control and Prevention. Outbreak of multi-drug resistant Salmonella Newport--United States, January-April 2002. , 2002, JAMA.

[95]  M. Hinton,et al.  Is Salmonella enteritidis PT4 a super bug , 1994 .

[96]  E. Schnabel,et al.  Distribution of Tetracycline Resistance Genes and Transposons among Phylloplane Bacteria in Michigan Apple Orchards , 1999, Applied and Environmental Microbiology.

[97]  E. Liébana,et al.  Molecular fingerprinting evidence of the contribution of wildlife vectors in the maintenance of Salmonella Enteritidis infection in layer farms , 2003, Journal of applied microbiology.

[98]  A. Cheng,et al.  Mutations in Topoisomerase Genes of Fluoroquinolone-Resistant Salmonellae in Hong Kong , 2003, Antimicrobial Agents and Chemotherapy.

[99]  F. Schmitz,et al.  Class 1 Integrons, Gene Cassettes, Mobility, and Epidemiology , 1999, European Journal of Clinical Microbiology and Infectious Diseases.

[100]  E. Sadowy,et al.  Two Different Extended-Spectrum β-Lactamases (ESBLs) in One of the First ESBL-Producing Salmonella Isolates in Poland , 2002, Journal of Clinical Microbiology.

[101]  T. Pitt,et al.  Resistance mechanisms of multiresistant serotype 012 Pseudomonas aeruginosa isolated in Europe. , 1990, Journal of Antimicrobial Chemotherapy.

[102]  B. Rowe,et al.  SALMONELLA ENTERITIDIS PHAGE TYPE 4 INFECTION: ASSOCIATION WITH HENS' EGGS , 1988, The Lancet.

[103]  J. Wu,et al.  Ciprofloxacin-resistant Salmonella enterica Typhimurium and Choleraesuis from Pigs to Humans, Taiwan , 2004, Emerging infectious diseases.

[104]  P. Barrow,et al.  Further studies on the inhibition of colonization of the chicken alimentary tract with Salmonella typhimurium by pre–colonization with an avirulent mutant , 1990, Epidemiology and Infection.

[105]  C. Hedberg,et al.  Food-related illness and death in the United States. , 1999, Emerging infectious diseases.

[106]  D. Cliver,et al.  Salmonella enteritidis epidemic. , 2000, Science.

[107]  W. Rabsch,et al.  Competitive exclusion of Salmonella enteritidis by Salmonella gallinarum in poultry. , 2000, Emerging infectious diseases.

[108]  T. Besser,et al.  Multiresistant Salmonella Typhimurium DT104 infections of humans and domestic animals in the Pacific Northwest of the United States , 2000, Epidemiology and Infection.

[109]  T. Aoki,et al.  Nucleotide Sequence Analysis of the Class G Tetracycline Resistance Determinant from Vibrio anguillarum , 1992, Microbiology and immunology.

[110]  J. Ruiz,et al.  In vitro fluoroquinolone-resistant mutants of Salmonella enterica serotype Enteritidis: analysis of mechanisms involved in resistance. , 2003, International journal of antimicrobial agents.

[111]  C. Poppe Salmonella enteritidis in Canada. , 1994, International journal of food microbiology.

[112]  R. Hall,et al.  A new trimethoprim resistance gene, dhfrX, in the In7 integron of plasmid pDGO100 , 1991, Antimicrobial Agents and Chemotherapy.

[113]  F. W. Brenner,et al.  Salmonella Nomenclature , 2000, Journal of Clinical Microbiology.

[114]  S. Andersson,et al.  Microbial genome evolution: sources of variability. , 2002, Current opinion in microbiology.

[115]  E. Giraud,et al.  Fitness cost of fluoroquinolone resistance in Salmonella enterica serovar Typhimurium. , 2003, Journal of medical microbiology.

[116]  L. H. Taylor,et al.  Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[117]  J. J. Farmer,et al.  Phage typing of Salmonella enteritidis in the United States , 1991, Journal of clinical microbiology.

[118]  Amita,et al.  Occurrence of Antibiotic Resistance Gene Cassettes aac(6′)-Ib, dfrA5, dfrA12, and ereA2 in Class I Integrons in Non-O1, Non-O139 Vibrio cholerae Strains in India , 2002, Antimicrobial Agents and Chemotherapy.

[119]  M. Mulvey,et al.  Characterization of Variant Salmonella Genomic Island 1 Multidrug Resistance Regions from Serovars Typhimurium DT104 and Agona , 2002, Antimicrobial Agents and Chemotherapy.

[120]  E. Threlfall,et al.  Epidemiological application of differentiating multiresistant Salmonella typhimurium DT104 by plasmid profile. , 1996, Communicable disease report. CDR review.

[121]  A. Dalsgaard,et al.  Distribution and Content of Class 1 Integrons in Different Vibrio cholerae O-Serotype Strains Isolated in Thailand , 2000, Antimicrobial Agents and Chemotherapy.

[122]  M. Hensel Evolution of pathogenicity islands of Salmonella enterica. , 2004, International journal of medical microbiology : IJMM.

[123]  E. Kaczmarski,et al.  An outbreak of gastro-intestinal illness caused by eggs containing Salmonella enteritidis phage type 4. , 1992, The Journal of infection.

[124]  Angela Lee,et al.  Identification and Characterization of Inhibitors of Multidrug Resistance Efflux Pumps in Pseudomonas aeruginosa: Novel Agents for Combination Therapy , 2001, Antimicrobial Agents and Chemotherapy.

[125]  M Fantasia,et al.  Salmonella enteritidis in Italy. , 1994, International journal of food microbiology.

[126]  B. Love,et al.  Molecular Characterization of Cephalosporin-Resistant Salmonella enterica Serotype Newport Isolates from Animals in Pennsylvania , 2002, Journal of Clinical Microbiology.

[127]  G. Gettinby,et al.  The efficacy of Salenvac, a Salmonella enterica subsp. Enterica serotype Enteritidis iron-restricted bacterin vaccine, in laying chickens , 2002, Avian pathology : journal of the W.V.P.A.

[128]  R. Hall,et al.  Transposons Tn1696 and Tn21and Their Integrons In4 and In2 Have Independent Origins , 2001, Antimicrobial Agents and Chemotherapy.

[129]  T. Humphrey,et al.  The rise and fall of Salmonella Enteritidis in the UK , 2003, Journal of applied microbiology.

[130]  H. Izumiya,et al.  Life-Threatening Infantile Diarrhea from Fluoroquinolone-Resistant Salmonella enteric Typhimurium with Mutations in Both gyrA and parC , 2003, Emerging infectious diseases.

[131]  A. Berndt,et al.  Combination of vaccination and competitive exclusion to prevent Salmonella colonization in chickens: experimental studies. , 1999, International journal of food microbiology.

[132]  S. Notermans,et al.  Intervention strategies for Salmonella enteritidis in poultry flocks: a basic approach. , 1994, International journal of food microbiology.

[133]  G. Olsen,et al.  Comparative genomics of closely related salmonellae. , 2002, Trends in microbiology.

[134]  Henzler Dj,et al.  The role of mice in the epizootiology of Salmonella enteritidis infection on chicken layer farms. , 1992 .

[135]  Michael R. Mulvey,et al.  Salmonella enterica Serotype Typhimurium DT 104 Antibiotic Resistance Genomic Island I in Serotype Paratyphi B , 2002, Emerging infectious diseases.

[136]  B. Rowe,et al.  A phage-typing scheme for Salmonella enteritidis , 1987, Epidemiology and Infection.

[137]  V. Miriagou,et al.  Expanded-Spectrum Cephalosporin-Resistant Salmonella Strains in Romania , 2002, Journal of Clinical Microbiology.

[138]  R M Hall,et al.  Mobile gene cassettes and integrons: capture and spread of genes by site‐specific recombination , 1995, Molecular microbiology.

[139]  M. Mulvey,et al.  Complete Nucleotide Sequence of a 43-Kilobase Genomic Island Associated with the Multidrug Resistance Region of Salmonella enterica Serovar Typhimurium DT104 and Its Identification in Phage Type DT120 and Serovar Agona , 2001, Journal of bacteriology.

[140]  S. Ladely,et al.  Salmonella enterica Serotype enteritidis in Table Egg Layer House Environments and in Mice in U.S. Layer Houses and Associated Risk Factors , 2003, Avian diseases.

[141]  G. Mead,et al.  Phage typing of Salmonella enteritidis from different sources in Brazil. , 2003, Journal of food protection.

[142]  J Hacker,et al.  Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution , 1997, Molecular microbiology.

[143]  R. Tauxe,et al.  Origins and consequences of antimicrobial-resistant nontyphoidal Salmonella: implications for the use of fluoroquinolones in food animals. , 2000, Microbial drug resistance.

[144]  D G White,et al.  The isolation of antibiotic-resistant salmonella from retail ground meats. , 2001, The New England journal of medicine.

[145]  A. Brisabois,et al.  Multidrug-resistant human and animal Salmonella typhimurium isolates in France belong predominantly to a DT104 clone with the chromosome- and integron-encoded beta-lactamase PSE-1. , 1999, The Journal of infectious diseases.

[146]  R. Hall,et al.  Family of Class 1 Integrons Related to In4 from Tn1696 , 2001, Antimicrobial Agents and Chemotherapy.

[147]  E. Threlfall,et al.  Epidemic in cattle and humans of Salmonella typhimurium DT 104 with chromosomally integrated multiple drug resistance , 1994, Veterinary Record.

[148]  R. Hall,et al.  In34, a Complex In5 Family Class 1 Integron Containing orf513 and dfrA10 , 2003, Antimicrobial Agents and Chemotherapy.

[149]  R. May,et al.  The maintenance of strain structure in populations of recombining infectious agents , 1996, Nature Medicine.

[150]  W. Rabsch,et al.  Identification of DNA gyrase A mutations in ciprofloxacin-resistant isolates of Salmonella typhimurium from men and cattle in Germany. , 1995, Microbial drug resistance.

[151]  F. Taddei,et al.  The rise and fall of mutator bacteria. , 2001, Current opinion in microbiology.

[152]  A. Cloeckaert,et al.  Salmonella typhimurium acrB-like gene: identification and role in resistance to biliary salts and detergents and in murine infection. , 1996, FEMS microbiology letters.

[153]  Howard Ochman,et al.  Pathogenicity Islands: Bacterial Evolution in Quantum Leaps , 1996, Cell.