Previous Article | Next Article 
Antimicrobial Agents and Chemotherapy, August 2000, p. 2166-2169, Vol. 44, No. 8
Área de Microbiología,
Departamento de Biología Funcional,1 and
Departamento de Bioquímica y Biología
Molecular,2 Universidad de Oviedo, Principado de
Asturias, Spain
Received 18 February 2000/Returned for modification 28 March
2000/Accepted 24 May 2000
The resistance profiles, for 15 antimicrobial agents, of 333 Salmonella strains representing the most frequent
nontyphoidal serotypes, isolated between 1989 and 1998 in a Spanish
region, and 9 reference strains were analyzed. All strains were
susceptible to amikacin, ceftazidime, ciprofloxacin, and imipenem, and
31% were susceptible to all antimicrobials tested. The most frequent types of resistance were to sulfadiazine, tetracycline, streptomycin, spectinomycin, ampicillin, and chloramphenicol (ranging from 46 to
22%); 13% were resistant to these six drugs. This multidrug resistance pattern was found alone or together with other resistance types within serotypes Typhimurium (45%), Panama (23%), and Virchow (4%). Each isolate was also screened for the presence of class 1 integrons and selected resistance genes therein; seven variable regions
which carried one (aadA1a, aadA2, or
pse-1) or two (dfrA14-aadA1a, dfrA1-aadA1a, oxa1-aadA1a, or
sat1-aadA1a) resistance genes were found in integrons.
The worldwide use of antimicrobials
in different fields, such as human and veterinary medicine and
agriculture, and as food animal growth-promoting agents during the past
decades has created enormous pressure for the selection of
antimicrobial resistance among bacterial pathogens. Nowadays, there is
increasing concern about the development of multiresistance in bacteria
causing zoonosis and having an important animal reservoir, such as
Salmonella strains (5, 6, 9); this
multiresistance is of considerable importance in both human and
veterinary medicine and is the subject of several surveillance programs
(6, 9).
An efficient route of acquisition and vertical and horizontal
dissemination of resistance determinants is through mobile elements including plasmids, transposons, and gene cassettes in integrons (5, 14, 15, 18, 22). Four distinct classes of integrons encoding different integrases have been reported (13, 18), and class 1 integrons are the most frequent in clinical strains, being
found in many different organisms. Class 1 integrons often contain
sul1, which encodes resistance to sulfonamides (14, 16,
20). At the present time, about 60 different cassettes associated
with resistance genes have been identified, and the same cassettes can
be found in different classes of integrons (7, 16).
The aims of the present work were to (i) trace the frequencies and
major changes throughout the last decade in susceptibility patterns of
Salmonella enterica organisms representing the most frequent
nontyphoidal serotypes causing human salmonellosis in the Principality
of Asturias, Spain; (ii) ascertain the presence and spread of class 1 integrons among nontyphoidal serotypes; and (iii) characterize the
different variable regions of the class 1 integrons found in order to
identify the resistance genes located therein.
Bacterial strains.
The study included 333 apparently
epidemiologically unrelated nontyphoidal Salmonella strains
collected in the Principality of Asturias, Spain, from 1989 to 1998 (Table 1), and 9 reference strains
belonging to different serotypes: Enteritidis PHLS 2187-PT4, PHLS
2408-PT6a, PHLS 2468-PT8, and PHLS-PT13a (Public Health Laboratory Service, London, England) and ATCC 13076-PT1 (American Type Culture Collection); Typhimurium ATCC 14028-DT133 and LT2-DT104 and
BC-25268-DT195 (Bayer AG Pharma-Research Center Collection, Wuppertal,
Germany); and Virchow CECT 4154 (Colección Española de
Cultivos Tipo, Valencia, Spain). Of the Asturian strains, 296 (representing about 10% of clinical isolates registered in the
Laboratorio de Salud Pública [LSP] of the Principality of
Asturias over the period under study) were associated with sporadic
human salmonellosis episodes registered at different times and/or
hospitals, implicated in both intra- and extraintestinal processes, and
isolated from feces (246 strains), blood (33 strains), urine (9 strains), and other samples (8 strains); a further 19 strains
(collected from feces and/or food) were associated with 19 different
outbreaks; 7 strains were collected from food not associated with
outbreaks; and 11 strains were from environmental sewage samples. These
342 strains belonged to 4 serogroups (B, C, D, and G) and 18 serotypes (Table 1). Serotyping of strains and phage typing of Typhimurium strains (1) have been carried out in the LSP and the Centro Nacional de Microbiología (CNM), Madrid, Spain.
0066-4804/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Antimicrobial Resistance and Spread of Class 1 Integrons among Salmonella Serotypes
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
TABLE 1.
Frequency of antimicrobial resistance in different
Salmonella serotypes
Antimicrobial susceptibility testing. Salmonella strains were tested for their susceptibility to 15 antimicrobial agents (Table 1) by the disk diffusion assay according to a standard procedure (17). Trimethoprim-sulfamethoxazole-resistant strains carrying an integron which generated a 1,600-bp amplicon were also tested for their resistance to trimethoprim. Each strain was assigned to a resistance pattern. Strains presenting intermediate resistance values were considered resistant strains.
Detection of class 1 integrons by PCR. All strains were tested more than once for the presence of class 1 integrons (first PCR step) using the primers 5'CS-3'CS (14). The assays were performed as described in reference 21 using a hot start cycle of 94°C for 5 min, followed by 30 cycles of 94°C for 30 s, 55°C for 30 s, and 72°C for 2.5 min and a final extension step of 72°C for 5 min (conditions which allowed the detection of fragments of at least 2,500 bp). Amplicons were analyzed by electrophoresis on 1.5% agarose gels, and a 100-bp ladder (Gibco BRL, Life Science Technologies, Barcelona, Spain) was used as the molecular size marker. Those strains generating one or more amplicons were also tested for the presence of sul1 associated with the integrons by amplification of the sul1 gene using the primers sul1-F-sul1-B (20) and by amplification of the fragment including the variable region and the sul1 gene using the 5'CS-sul1-B primers (14, 20). The PCR conditions used were the same as cited above, but with annealing temperature and extension steps of 70°C and 1 min (for sul1) or 65°C and 3 min (for the 5'CS-sul1 fragment), respectively.
The integron profiles (IPs) were defined by the number and the size of the amplicons generated by a strain. One strain of each serotype representing each IP was considered the "type strain" (IP-I: Typhimurium LSP14/92; IP-II: Virchow LSP87/92, Typhimurium LSP122/92, Worthington LSP7/93, Agona LSP51/93, Enteritidis LSP497/98, Hadar LSP186/98, Panama LSP580/95, and Poona LSP238/96; IP-III: Panama LSP304/92, Ohio LSP131/96, Brandenburg LSP331/96, Typhimurium LSP15/89, and Virchow LSP410/92; IP-IV: Typhimurium LSP31/93; IP-V: Virchow LSP159/94).DNA purification and PCR-restriction fragment length polymorphism (RFLP) analysis. PCR products generated in the first PCR step (direct amplification samples as well as agarose gel fragments) were purified with the GFX PCR DNA and gel band kit (Amersham Pharmacia Biotech, Barcelona, Spain).
The RFLP analysis of the different amplicons was carried out using several endonucleases: TaqI (T
CGA)
(Roche Diagnostics, Barcelona, Spain) and BglII
(AGATCT), PvuI (CGATCG), and HincII (GT[T/C][A/G]AC) (Amersham Pharmacia Biotech). For this,
aliquots of the amplicons obtained in the first PCR step were directly purified and digested separately with 5 U of each endonuclease, according to the manufacturer's recommendations. The restriction products were analyzed by electrophoresis on 1.5% agarose gels.
Detection of resistance genes in variable regions of integrons by PCR. The amplicons ascribed to each IP were tested in a second PCR step for the presence of aadA [ant-(3")], pse-1, oxa1, and dfr (dhfr) genes. The primers used for the amplification of the two former genes were reported in reference 20; the oxa1 (5'AGCAGCGCCAGTGCATCA3'-5'ATTCGACCCCAAGTTTCC3') and dfr (5'GTGAAACTATCACTAATGG3'-5'CCCTTTTGCCAGATTTGG3') primers were designed for the present work from the gene sequences introduced in GenBank (accession no. AJ009819 and Z8331, respectively). As template DNA, 15 µl of a 10-fold water dilution of amplicons in the first PCR step was used. For the analysis of IP-I, each of the two amplicons (1,000 and 1,200 bp) was collected from the gel, purified, and tested separately. The PCR conditions used were the same as those cited above with 1 min for the extension steps and annealing temperatures of 55°C for dfr, 65°C for pse-1 and oxa1, and 70°C for aadA.
Sequencing of PCR products. PCR products, representing the different amplicons generated by the 16 type strains, were collected from the gels, purified, and directly analyzed by partial sequencing. Sequencing reactions were carried out using a DRho terminator TAQ FS kit (Perkin-Elmer) in a GeneAmp PCR system as recommended by the manufacturer. Sequences were read in an ABI Prism 310A apparatus with a 47-cm- by 50-µm capillary which allowed the reading of about 450 bp per run. The primers 5'CS and 3'CS (14) were used for sequencing both ends of the different amplicons under study. In addition, for 1,600-, 2,000-, and 2,300-bp amplicons, internal primers were synthesized and used to continue the process until the resistance genes inserted in each amplicon were identified. Sequences obtained were compared to those registered in GenBank.
| |
RESULTS AND DISCUSSION |
|---|
|
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
|
|---|
Antimicrobial susceptibility.
The findings obtained in the
antimicrobial susceptibility test (Table 1) showed the following
results. (i) Thirty-one percent of the strains were susceptible
to all antimicrobials tested, 18% presented a single type of
resistance, and 51% were multiresistant (two to nine types of
resistance). (ii) All strains were susceptible to amikacin,
ceftazidime, ciprofloxacin, and imipenem; more than 90% were
susceptible to cephalothin, gentamicin, and kanamycin. (iii) When
the study period was divided into two (1989 to 1993 and 1994 to 1998),
an increase in the number of Asturian strains resistant to nalidixic
acid and trimethoprim was found. These resistances probably emerged at
different times in different serotypes, the increase being
statistically significant (P 
0.05, 
2
test) in only some serotypes (i.e., nalidixic acid resistance in
Virchow, Panama, Hadar, and Enteritidis and
trimethoprim-sulfamethoxazole resistance in Typhimurium). (iv) The
drug-resistant strains were grouped into 82 resistance patterns, of
which only 22 were represented by more than two strains. (v)
Typhimurium stood out as the serotype with the highest percentages of
resistant strains (96%), with 37 strains showing multiresistant
phenotypes which included ampicillin, chloramphenicol,
streptomycin-spectinomycin, sulfadiazine, and tetracycline resistance.
Twenty of these strains belonged to phage type DT104, and a further 15 were non-phage typeable, a fact which could be related to some phage
conversion phenomena (2, 8). All these strains could be
considered members of an emergent clone or lineage which has become a
major cause of illness in humans and animals in several European
countries and in the United States (3, 4, 9, 15, 19, 20,
23). (vi) Multiresistant phenotypes including four or more
types of resistance were also found in 10 other serotypes (33% of
Asturian strains), being more frequent among Ohio (34%), Panama
(33%), Brandenburg (20%), Virchow (16%), and Hadar
(15%) strains.
Determination of class 1 integrons.
Class 1 integrons were
present in 68 (20%) multiresistant strains (57 from clinical
samples, 5 from pork, and 6 from sewage), none of them reference
strains. Five IPs were defined, IP-I including two integrons and
IP-II to IP-V including one integron each (Fig. 1 and Table
2). Some IPs appeared in a single
serotype: IP-I (variable regions of about 1,000 and 1,200 bp) and IP-IV
(variable regions of about 2,000 bp) in Typhimurium and IP-V
(variable regions of about 2,300 bp) in Virchow. Other
profiles appeared in several serotypes: IP-II (variable regions
of about 1,000 bp) in Virchow, Typhimurium, Worthington, Agona,
Enteritidis, Hadar, Panama, and Poona and IP-III (variable
regions of about 1,600 bp) in Panama, Ohio, Brandenburg, Typhimurium,
and Virchow. To determine the association between class 1 integrons and
the sul1 gene, the strains of the different IPs were
analyzed by PCR. With the sul1 primers, amplicons of the
expected size (about 400 bp) were generated (Fig. 1). When the 16 type
strains were analyzed with 5'CS-sul1-B primers, amplicons
of about 1,900, 2,100, 2,500, 2,900, and 3,200 bp (representing the
variable regions of 1,000, 1,200, 1,600, 2,000, and 2,300 bp,
respectively) were generated (data not shown). These results indicated that the sul1 gene was located in all the integron
types described in the present work.
|
|
Relationships of class 1 integrons, resistance genes, and resistance patterns. Analysis of the resistance profiles of the strains, the sizes of the amplicons, and the resistance genes in class 1 integrons reported for Salmonella (3, 4, 15, 19, 20, 24) suggested that aadA (encoding streptomycin-spectinomycin resistance), pse-1 and oxa1 (encoding ampicillin resistance), and dfrA (encoding trimethoprim resistance) genes could be present in some of the variable regions. The presence of these genes was tested by PCR using specific primers. The aadA primers generated a fragment of about 500 bp in the samples representing the five IPs (in the case of IP-I, only from the 1,000-bp amplicon) which included strains ascribed to 10 serotypes. The pse-1 and the oxa1 primers generated amplicons of about 400 and 700 bp in samples from IP-I (only from the 1,200-bp amplicon) and IP-IV, respectively, both represented by only serotype Typhimurium. The dfrA primers generated amplicons of about 450 bp in samples from IP-III, which included strains from five serotypes. Whereas ampicillin and trimethoprim are antimicrobials widely used in human medicine, streptomycin has been seldom used for over 2 decades in this field. Therefore, both the selection and dispersion of aadA genes in integrons could be related to the extensive use of this antibiotic in veterinary treatments and agriculture.
It is of note that the primers used for the detection of resistance genes (mainly for aadA and dfrA) could amplify different types of each gene. To confirm the presence of the suspected resistance genes, nucleotide sequencing of the PCR products from each type strain was carried out. When the 1,200- and 1,000-bp PCR product generated by the Typhimurium DT104 strain LSP14/92, which represented IP-I, were sequenced, it was found that the 1,200-bp region carried pse-1 (GenBank accession no. AF071555), whereas the 1,000-bp region carried aadA2 (accession no. AF071555). The presence of integrons with variable regions of 1,200 bp (pse-1) and 1,000 bp (aadA2) is very common among multiresistant DT104 Typhimurium strains, in which both integrons are chromosomally located (3, 4, 19, 20). Within the series analyzed in this study, 76% of the Typhimurium DT104 and 48% of the non-phage-typeable strains carried integrons with both resistance genes and were related to the multiresistance patterns described above and compiled in Table 2. In previous work carried out in our laboratory, most of these strains had been ascribed to ribotypes and pulsed-field gel electrophoresis types which showed more than 90% similarity (10, 11). The sequencing of the 1,000-bp variable regions of the integrons generated in the eight type strains representing IP-II showed the presence of aadA1a in all of them (accession no. AJ009820). It proved interesting that the two Typhimurium strains classified as IP-II belonged to phage type DT80. Variable regions of similar size and carrying aadA1a have been found in other enterobacteria (14, 16). The sequencing of the 1,600-bp PCR products generated by the five type strains classified as IP-III revealed the presence of two different resistance gene combinations (dfrA14-aadA1a and dfrA1-aadA1a), the profiles thus being considered IP-IIIa and IP-IIIb. The type strains of serotypes Ohio, Panama, Virchow, and Brandenburg carried dfrA1 (dhfrI, accession no. X17478) located near the 5' conserved region (5'CR) and aadA1a near the 3'CR, whereas the type strain Typhimurium DT204 LSP15/89 carried dfrA14 (dhfrIb, accession no. Z50805) and aadA1a, located near the 5'CR and the 3'CR, respectively. Variable regions of similar sizes and carrying aadA1a and different dfr gene cassettes, including dfrA1, have been found in Escherichia, Klebsiella, and Serratia species (12, 14, 16). When the 2,000-bp variable region of the Typhimurium DT104 strain LSP31/93 which represented IP-IV was sequenced, the presence of oxa1 (accession no. AJ009819.1) located near the 5'CR and aadA1a near the 3'CR was confirmed. This variable region is similar to the one from In-t2 (2,100 bp) located in a 140-kb IncFI plasmid carried by other DT104 Typhimurium strains (24). The 2,300-bp variable region of the Virchow strain LSP159/94, which represented IP-V, carried two resistance genes: sat-1 (accession no. X56815), which encoded streptothricin resistance, near the 5'CR and aadA1a near the 3'CR. In light of the results obtained for the frequency and spread of class 1 integrons among nontyphoidal Salmonella serotypes, the following findings can be noted. (i) Salmonella strains carrying class 1 integrons were collected throughout the entire study period, being more frequent in serotypes Typhimurium, Ohio, Panama, and Virchow. (ii) The spread of complete integron structures, assigned to IP-II and -III, has occurred among different Salmonella serotypes. (iii) Some serotype-specific integrons were found, such as those forming IP-I and -IV in Typhimurium, as has been previously reported (3, 4, 19, 20, 24), and IP-V in Virchow. (iv) aadA1a alone or in combination with other resistance genes in different variable regions of integrons was found in several Salmonella serotypes. In Salmonella and other enterobacterial species, single and fused aadA gene cassettes in integrons have been reported (12, 14, 16, 19, 24).| |
ACKNOWLEDGMENTS |
|---|
We thank M. A. González-Hevia (LSP, Principado de
Asturias, Spain), H.-P. Kroll (Bayer AG, Pharma-Research Center,
Wuppertal, Germany) and M. A. Usera (CNM, Madrid, Spain) for
Salmonella strains and A. Aladue
a (CNM) for phage
typing of Typhimurium strains. We are also indebted to M. R. Rodicio for her critical revision of this paper.
This work was supported by grants from the "Fondo de Investigación Sanitaria" (FIS 98/0296 and 00/1084), Ministerio de Sanidad y Consumo, Spain. S. Soto is the recipient of a grant of "Formación de Personal Investigador" (Ref AP98), Ministerio de Educación y Cultura, Spain.
| |
FOOTNOTES |
|---|
* Corresponding author. Mailing address: Área de Microbiología, Dpto. Biología Funcional, Facultad Medicina, Universidad de Oviedo, C/ Julián Clavería s/n, 33006 Oviedo (Asturias), Spain. Phone: 34-985-103560. Fax: 34-985-103148. E-mail: camf{at}sauron.quimica.uniovi.es.
| |
REFERENCES |
|---|
|
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
|
|---|
| 1. | Anderson, E. S., L. R. Ward, M. J. de Saxe, and J. D. H. de Sa. 1977. Bacteriophage typing designations of Salmonella typhimurium. J. Hyg. 78:297-300. |
| 2. | Baggesen, D. L., M. N. Skov, D. J. Brown, and M. Bisgaard. 1997. Separation of Salmonella Typhimurium DT2 and DT135: molecular characterization of isolates of avian origin. Eur. J. Epidemiol. Infect. Dis. 13:347-352. |
| 3. |
Briggs, C. E., and P. Fratamico.
1999.
Molecular characterization of an antibiotic resistance gene cluster of Salmonella typhimurium DT104.
Antimicrob. Agents Chemother.
43:846-849 |
| 4. | Casin, I., J. Breuil, A. Brisabois, F. Moury, F. Grimont, and E. Collatz. 1999. 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. J. Infect. Dis. 179:1173-1182[CrossRef][Medline]. |
| 5. |
Davies, J.
1994.
Inactivation of antibiotics and the dissemination of resistance genes.
Science
264:375-382 |
| 6. | Fisher, I. S. T. 1999. The Enter-Net International surveillance network. How it works. Eurosurveillance 4:52-55. |
| 7. | Fluit, A. C., and F. J. Schmitz. 1999. Class 1 integrons, gene cassettes, mobility, and epidemiology. Eur. J. Clin. Microbiol. Infect. Dis. 18:761-770[CrossRef][Medline]. |
| 8. | Frost, J. A., B. Rowe, L. R. Ward, and E. J. Threlfall. 1982. Characterization of resistance plasmids and carried phages in an epidemic clone of multiresistant Salmonella typhimurium in India. J. Hyg. 88:193-204. |
| 9. |
Glynn, M. K.,
C. Boop,
W. Dewitt,
P. Dabney,
M. Moktar, and F. Angulo.
1998.
Emergence of multidrug-resistant Salmonella enterica serotype Typhimurium DT104 infections in the United States.
N. Engl. J. Med.
338:1333-1338 |
| 10. |
Guerra, B.,
E. Landeras,
M. A. González-Hevia, and M. C. Mendoza.
1997.
A "three-way ribotyping scheme" for Salmonella typhimurium: usefulness for phylogenetic and epidemiological purposes.
J. Med. Microbiol.
46:307-313 |
| 11. | Guerra, B., P. Schroers, and M. C. Mendoza. 2000. Application of PFGE to an epidemiological and phylogenetic study of Salmonella serotype Typhimurium. Relationships between genetic types and phage types. New Microbiol. 23:11-20[Medline]. |
| 12. | Jones, M. E., E. Peters, A. M. Weersink, A. Fluit, and J. Verhoef. 1997. Widespread occurrence of integrons causing multiple antibiotic resistance in bacteria. Lancet 14:1742-1743. |
| 13. | Kazama, H., K. Kizu, M. Iwasaki, H. Hamashima, M. Sasatsu, and T. Arai. 1995. Isolation of a new integron that includes a streptomycin resistance gene from the R plasmid of Pseudomonas aeruginosa. FEMS Microbiol. Lett. 134:137-141[CrossRef][Medline]. |
| 14. | Levèsque, C., L. Pyche, C. Larose, and P. H. Roy. 1995. PCR mapping of integrons reveals several novel combinations of resistance genes. Antimicrob. Agents Chemother. 39:185-191[Abstract]. |
| 15. |
Llanes, C.,
V. Kirchgesner, and P. Plesiat.
1999.
Propagation of TEM- and PSE-type  -lactamases among amoxicillin-resistant Salmonella spp. isolated in France.
Antimicrob. Agents Chemother.
43:2430-2436 |
| 16. |
Martínez-Freijo, P.,
A. C. Fluit,
F.-J. Schmitz,
J. Verhoev, and M. E. Jones.
1999.
Many class 1 integrons comprise stable structures occurring in different species of Enterobacteriaceae isolated from widespread geographic regions in Europe.
Antimicrob. Agents Chemother.
43:686-689 |
| 17. | National Committee for Clinical Laboratory Standards. 1997. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standard M2-A5. National Committee for Clinical Laboratory Standards, Wayne, Pa. |
| 18. |
Recchia, G. D., and R. M. Hall.
1995.
Gene cassettes: a new class of mobile element.
Microbiology
141:3015-3027 |
| 19. | Ridley, A., and J. Threlfall. 1998. Molecular epidemiology of antibiotic resistance genes in multiresistant epidemic Salmonella typhimurium DT104. Microb. Drug Resist. 4:113-118[Medline]. |
| 20. | Sandvang, D., F. M. Aarestrup, and L. B. Jensen. 1997. Characterization of integrons and antibiotic resistance genes in Danish multiresistant Salmonella typhimurium DT104. FEMS Microbiol. Lett. 160:37-41[CrossRef]. |
| 21. |
Soto, S. M.,
B. Guerra,
M. A. González-Hevia, and M. C. Mendoza.
1999.
Potential of a three-way randomly amplified polymorphic DNA analysis as a typing method for twelve Salmonella serotypes.
Appl. Environ. Microbiol.
65:4830-4836 |
| 22. | Stokes, H. W., and R. M. Hall. 1989. A novel family of potentially mobile DNA elements encoding site-specific gene integration functions: integrons. Mol. Microbiol. 3:1669-1683[Medline]. |
| 23. | Threlfall, E. J., J. A. Frost, L. R. Ward, and B. Rowe. 1994. Epidemic in cattle and humans of Salmonella typhimurium DT104 with chromosomally-integrated multiple drug resistance. Vet. Rec. 134:577[Medline]. |
| 24. |
Tosini, F.,
P. Visca,
A. M. Dionisi,
C. Pezzella,
A. Petruca, and A. Carattoli.
1998.
Class 1 integron-borne multiple antibiotic resistance carried by IncFI and IncL/M plasmids in Salmonella enterica serotype Typhimurium.
Antimicrob. Agents Chemother.
42:3053-3058 |
Antimicrobial Agents and Chemotherapy, August 2000, p. 2166-2169, Vol. 44, No. 8
0066-4804/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Marquez, C., Labbate, M., Ingold, A. J., Chowdhury, P. R., Ramirez, M. S., Centron, D., Borthagaray, G., Stokes, H. W.
(2008). Recovery of a Functional Class 2 Integron from an Escherichia coli Strain Mediating a Urinary Tract Infection. Antimicrob. Agents Chemother.
52: 4153-4154
[Abstract] [Full Text] -
Rao, S., Maddox, C. W., Hoien-Dalen, P., Lanka, S., Weigel, R. M.
(2008). Diagnostic Accuracy of Class 1 Integron PCR Method in Detection of Antibiotic Resistance in Salmonella Isolates from Swine Production Systems. J. Clin. Microbiol.
46: 916-920
[Abstract] [Full Text] -
Martinez, N., Mendoza, M. C., Rodriguez, I., Soto, S., Bances, M., Rodicio, M. R.
(2007). Detailed structure of integrons and transposons carried by large conjugative plasmids responsible for multidrug resistance in diverse genomic types of Salmonella enterica serovar Brandenburg. J Antimicrob Chemother
60: 1227-1234
[Abstract] [Full Text] -
Ma, M., Wang, H., Yu, Y., Zhang, D., Liu, S.
(2007). Detection of antimicrobial resistance genes of pathogenic Salmonella from swine with DNA microarray. jvdi
19: 161-167
[Abstract] [Full Text] -
Rodriguez, I., Martin, M. C., Mendoza, M. C., Rodicio, M. R.
(2006). Class 1 and class 2 integrons in non-prevalent serovars of Salmonella enterica: structure and association with transposons and plasmids. J Antimicrob Chemother
58: 1124-1132
[Abstract] [Full Text] -
Antunes, P., Machado, J., Peixe, L.
(2006). Characterization of antimicrobial resistance and class 1 and 2 integrons in Salmonella enterica isolates from different sources in Portugal. J Antimicrob Chemother
58: 297-304
[Abstract] [Full Text] -
CABRERA, R., RUIZ, J., RAMIREZ, M., BRAVO, L., FERNANDEZ, A., ALADUENA, A., ECHEITA, A., GASCON, J., ALONSO, P. L., VILA, J.
(2006). DISSEMINATION OF SALMONELLA ENTERICA SEROTYPE AGONA AND MULTIDRUG-RESISTANT SALMONELLA ENTERICA SEROTYPE TYPHIMURIUM IN CUBA. Am J Trop Med Hyg
74: 1049-1053
[Abstract] [Full Text] -
Cabrera, R., Marco, F., Vila, J., Ruiz, J., Gascon, J.
(2006). Class 1 Integrons in Salmonella Strains Causing Traveler's Diarrhea.. Antimicrob. Agents Chemother.
50: 1612-1613
[Full Text] -
Herrero, A., Rodicio, M. R., Gonzalez-Hevia, M. A., Mendoza, M. C.
(2006). Molecular epidemiology of emergent multidrug-resistant Salmonella enterica serotype Typhimurium strains carrying the virulence resistance plasmid pUO-StVR2. J Antimicrob Chemother
57: 39-45
[Abstract] [Full Text] -
Miko, A., Pries, K., Schroeter, A., Helmuth, R.
(2005). Molecular mechanisms of resistance in multidrug-resistant serovars of Salmonella enterica isolated from foods in Germany. J Antimicrob Chemother
56: 1025-1033
[Abstract] [Full Text] -
Antunes, P., Machado, J., Sousa, J. C., Peixe, L.
(2005). Dissemination of Sulfonamide Resistance Genes (sul1, sul2, and sul3) in Portuguese Salmonella enterica Strains and Relation with Integrons. Antimicrob. Agents Chemother.
49: 836-839
[Abstract] [Full Text] -
Antunes, P., Machado, J., Sousa, J. C., Peixe, L.
(2004). Dissemination amongst humans and food products of animal origin of a Salmonella typhimurium clone expressing an integron-borne OXA-30 {beta}-lactamase. J Antimicrob Chemother
54: 429-434
[Abstract] [Full Text] -
Guerra, B., Junker, E., Helmuth, R.
(2004). Incidence of the Recently Described Sulfonamide Resistance Gene sul3 among German Salmonella enterica Strains Isolated from Livestock and Food. Antimicrob. Agents Chemother.
48: 2712-2715
[Abstract] [Full Text] -
Miko, A., Pries, K., Schroeter, A., Helmuth, R.
(2003). Multiple-Drug Resistance in D-Tartrate-Positive Salmonella enterica Serovar Paratyphi B Isolates from Poultry Is Mediated by Class 2 Integrons Inserted into the Bacterial Chromosome. Antimicrob. Agents Chemother.
47: 3640-3643
[Abstract] [Full Text] -
Lee, K., Yong, D., Yum, J. H., Kim, H. H., Chong, Y.
(2003). Diversity of TEM-52 extended-spectrum {beta}-lactamase-producing non-typhoidal Salmonella isolates in Korea. J Antimicrob Chemother
52: 493-496
[Abstract] [Full Text] -
DeLappe, N., O'Halloran, F., Fanning, S., Corbett-Feeney, G., Cheasty, T., Cormican, M.
(2003). Antimicrobial Resistance and Genetic Diversity of Shigella sonnei Isolates from Western Ireland, an Area of Low Incidence of Infection. J. Clin. Microbiol.
41: 1919-1924
[Abstract] [Full Text] -
Ploy, M.-C., Chainier, D., Tran Thi, N. H., Poilane, I., Cruaud, P., Denis, F., Collignon, A., Lambert, T.
(2003). Integron-Associated Antibiotic Resistance in Salmonella enterica Serovar Typhi from Asia. Antimicrob. Agents Chemother.
47: 1427-1429
[Abstract] [Full Text] -
Soto, S. M., Lobato, M. J., Mendoza, M. C.
(2003). Class 1 Integron-Borne Gene Cassettes in Multidrug-Resistant Yersinia enterocolitica Strains of Different Phenotypic and Genetic Types. Antimicrob. Agents Chemother.
47: 421-426
[Abstract] [Full Text] -
Orman, B. E., Pineiro, S. A., Arduino, S., Galas, M., Melano, R., Caffer, M. I., Sordelli, D. O., Centron, D.
(2002). Evolution of Multiresistance in Nontyphoid Salmonella Serovars from 1984 to 1998 in Argentina. Antimicrob. Agents Chemother.
46: 3963-3970
[Abstract] [Full Text] -
Maidhof, H., Guerra, B., Abbas, S., Elsheikha, H. M., Whittam, T. S., Beutin, L.
(2002). A Multiresistant Clone of Shiga Toxin-Producing Escherichia coli O118:[H16] Is Spread in Cattle and Humans over Different European Countries. Appl. Environ. Microbiol.
68: 5834-5842
[Abstract] [Full Text] -
Guerra, B., Soto, S., Helmuth, R., Mendoza, M. C.
(2002). Characterization of a Self-Transferable Plasmid from Salmonella enterica Serotype Typhimurium Clinical Isolates Carrying Two Integron-Borne Gene Cassettes Together with Virulence and Drug Resistance Genes. Antimicrob. Agents Chemother.
46: 2977-2981
[Abstract] [Full Text] -
Miko, A., Guerra, B., Schroeter, A., Dorn, C., Helmuth, R.
(2002). Molecular Characterization of Multiresistant d-Tartrate-Positive Salmonella enterica Serovar Paratyphi B Isolates. J. Clin. Microbiol.
40: 3184-3191
[Abstract] [Full Text] -
Boyd, D., Cloeckaert, A., Chaslus-Dancla, E., Mulvey, M. R.
(2002). Characterization of Variant Salmonella Genomic Island 1 Multidrug Resistance Regions from Serovars Typhimurium DT104 and Agona. Antimicrob. Agents Chemother.
46: 1714-1722
[Abstract] [Full Text] -
White, D. G., Zhao, S., Sudler, R., Ayers, S., Friedman, S., Chen, S., McDermott, P. F., McDermott, S., Wagner, D. D., Meng, J.
(2001). The Isolation of Antibiotic-Resistant Salmonella from Retail Ground Meats. NEJM
345: 1147-1154
[Abstract] [Full Text] -
Guerra, B., Soto, S. M., Argüelles, J. M., Mendoza, M. C.
(2001). Multidrug Resistance Is Mediated by Large Plasmids Carrying a Class 1 Integron in the Emergent Salmonella enterica Serotype [4,5,12:i:{-}]. Antimicrob. Agents Chemother.
45: 1305-1308
[Abstract] [Full Text]
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Copyright © 2009 by the American Society for Microbiology. For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»