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Antimicrobial Agents and Chemotherapy, May 2005, p. 2142-2143, Vol. 49, No. 5
0066-4804/05/$08.00+0     doi:10.1128/AAC.49.5.2142-2143.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

LETTER TO THE EDITOR

Salmonella enterica Serovar Infantis Producing a CTX-M-9 ß-Lactamase


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LETTER
 
Since extended-spectrum ß-lactamases (ESBLs) were first described, some 20 years ago, these enzymes have been described in several species, including most enterobacteria. ESBLs have been described in some Salmonella enterica serovars (5) but remain infrequent in this genus.

CTX-M-like ß-lactamases belong to Ambler class A (1). CTX-M-9 was first described in Escherichia coli in 2000, though the isolate was obtained from a patient with a urinary tract infection in 1996 (8). Since then, CTX-M-9 has been isolated in some other gram negatives. In 2000, a CTX-M-like ß-lactamase was found in four S. enterica serovar Virchow isolates in Spain in 1997 and 1998 that, according its pI, around 8, and PCR amplification with primers specific for CTX-M-9, probably belonged to this group, though the authors did not publish the sequence (9).

This letter describes the first CTX-M-9-producing S. enterica serovar Infantis strain, isolated in our Department in December 2003. This isolate was obtained from stool samples of a male adult patient (43 years old) admitted to the hospital for gastroenteritis with dehydration and acute renal failure. The renal failure remitted after rehydration, and the patient was discharged 7 days later. No antibiotic treatment was prescribed. The patient had not received any antibiotic treatments recently.

The isolate was identified biochemically by using the Wider System (Dade-Behring, Sacramento, Calif.). The serogroup was determined at our department, and the serotype was determined by the Servicio de Bacteriología, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Madrid, Spain. The isolate was identified as S. enterica, subsp. I, serovar Infantis. MICs were determined by the broth microdilution method by using the Wider System (Dade-Behring). ß-Lactam and fluoroquinolone susceptibility was then checked by the agar dilution method, according NCCLS guidelines. The MICs were as follows: amoxicillin, >128 µg/ml; amoxicillin/clavulanic acid, 8/4 µg/ml; ticarcillin, >128 µg/ml; piperacillin/tazobactam, 32/4 µg/ml; cefuroxime, >128 µg/ml; cefoxitin, 8 µg/ml; ceftazidime, 2 µg/ml; ceftazidime/clavulanic acid, ≤1/4 µg/ml; cefotaxime, 32 µg/ml; cefepime, 0.5 µg/ml; imipenem, 0.2 µg/ml; meropenem, 0.2 µg/ml; gentamicin, ≤2 µg/ml; tobramycin, ≤2 µg/ml; amikacin, ≤4 µg/ml; norfloxacin, 0.5 µg/ml; ciprofloxacin, 0.1 µg/ml; trimethoprim/sulfamethoxazole, >4/76 µg/ml.

There was synergy between clavulanic acid and cefotaxime, ceftazidime, and aztreonam by the double-disk diffusion method (4).

The ß-lactamase extracts and isoelectric focusing were performed by using the Phast System (Amersham Pharmacia). The isolate produced a ß-lactamase with a pI of around 8 and activity against ceftriaxone, as was shown when the gel was revealed by an iodometric overlay system using ceftriaxone as the substrate (7).

Total DNA was extracted from a single colony and amplified by PCR, by using previously described primers specific for TEM, SHV, and CTX-M ß-lactamases (9). The assay was positive for CTX-M-9-specific primers, yielding an 856-bp fragment whose sequence was identical to the sequence existing in GenBank for CTX-M-9 (accession number AF174129).

E. coli BM21, nalidixic acid resistant and lactose fermentation positive, was used as the recipient for conjugation experiments, which were performed as previously described (2). MacConkey agar plates (Difco) containing 2 mg/ml of cefotaxime and 64 mg/ml of nalidixic acid were used for selection. The experiment was repeated three times, but no transconjugants were found.

CTX-M-type ß-lactamase-producing strains have been identified sporadically in very different geographical areas (Western and Eastern Europe, South America, Asia).

CTX-M-9 was first described in 22 E. coli and 1 S. enterica serovar Virchow in Barcelona (Spain), isolated between 1996 and 1998. Three more S. enterica serovar Virchow strains producing this ß-lactamase were found in the same period in Murcia, Spain (8).

Only one CTX-M-type ß-lactamase has been previously described in S. enterica serovar Infantis (3). This is a CTX-M-2 enzyme, included in a class 1 integron (inS21), described in a cefotaxime-resistant S. enterica serovar Infantis outbreak that happened in Santa Fe, Argentina, in 1997 to 1998. CTX-M-2 is the most frequently found ESBL in Argentinian isolates of enterobacteria; thus, is not surprising that CTX-M-2 was transferred to a infrequent ESBL-bearer genus such as Salmonella.

A similar evolution may happen in Spain. Recent studies show that CTX-M-9 is becoming the most frequent ESBL in E. coli in Spain (6). Sixty-four percent of community-acquired E. coli isolates producing an ESBL bear a CTX-M-9 enzyme. Thus, CTX-M-9 can become more frequent even in genera which produce ESBLs infrequently. However, this isolate is the only ESBL-producing Salmonella found in our department in the last 5 years.

These isolates represent the first description of an ESBL in S. enterica serovar Infantis in Spain and the first description of a CTX-M-9 enzyme in serovar Infantis. The spread of ESBLs among S. enterica serovars remains infrequent, but it is a cause of concern because of its potential therapeutic impact.


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Emilio Valverde Romero
Trinidad Parras Padilla
M. Inmaculada García García
Departamento de Microbiología
Hospital Universitario de Salamanca
P.O. de San Vicente 108
37007 Salamanca, Spain

Nuria Delgado Ronda
Departamento de Medicina Preventiva
Salud Pública y Microbiología Médica
Universidad de Salamanca
Salamanca, Spain

Ana Herrero
Departamento de Microbiología
Hospital Universitario de Salamanca
P.O. de San Vicente 108
37007 Salamanca, Spain

Juan Luis Muñoz Bellido
Departamento de Medicina Preventiva
Salud Pública y Microbiología Médica
Universidad de Salamanca
Salamanca, Spain

José Ángel García Rodríguez*
Departamento de Microbiología
Hospital Universitario de Salamanca
P.O. de San Vicente 108
37007 Salamanca, Spain

* Phone: 34923264825, Fax: 34923262261, E-mail: jagarrod{at}usal.es

Antimicrobial Agents and Chemotherapy, May 2005, p. 2142-2143, Vol. 49, No. 5
0066-4804/05/$08.00+0     doi:10.1128/AAC.49.5.2142-2143.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.




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