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The multidrug-resistant (MDR) Salmonella enterica serotype Newport strain that produces CMY-2 [beta]-lactamase (Newport MDR-AmpC) was the source of sporadic cases and outbreaks in humans in France during 2000-2005. Because this strain was not detected in food animals, it was most likely introduced into France throuqh imported food products.
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Third-generation cephalosporins are drugs of choice for treatment of persons with nontyphoidal Salmonella infections that require chemotherapy or when fluoroquinolones are contraindicated. A new public health concern is the emergence of third-generation cephalosporin–resistant Salmonella isolates (1). Multidrug-resistant (MDR) Salmonella enterica serotype Newport isolates that produce CMY-2, a [beta]-lactamase that inactivates third-generation cephalosporins, were first reported in the United States in 1998 (2). These isolates, known as Newport MDR-AmpC, have quickly spread through the United States in cattle and humans (3-5). It has been hypothesized that use of ceftio-fur, a third-generation cephalosporin licensed in the United States for use in cattle, could have selected for Newport MDR-AmpC (2-4, 7). Several observations and case-control studies suggested beef and milk from dairy cattle were substantial sources of Newport MDR-AmpC infection in humans (6-8).
These isolates seem to be extremely rare in Europe. Two surveys performed in England and Wales (278,308 human Salmonella isolates tested, 1992-2003) and Spain (959 human Salmonella isolates, 1999-2000) did not detect New port MDR-AmpC (9,10). In St. Petersburg, Russia, only 1 Newport MDR-AmpC isolate was reported among 1,078 Salmonella isolates during 2002-2005 (11). In France, a small outbreak (14 cases) of Newport MDR-AmpC was detected in 2003 and linked to consumption of imported horse meat (12). We undertook the present study to acquire more knowledge on circulation of Newport MDR-AmpC in humans, animals, and animal-derived food in France.
The Study
From 2000 through 2005, the French National Reference Centre for Salmonella at the Institut Pasteur in Paris reported 829 Newport isolates among 69,759 Salmonella clinical isolates. During this period and depending on the year, serotype Newport ranked between 6th and 10th in prevalence among human serotyped isolates. From 2000 through 2005, the Agence Francaise de Securite Sanitaire des Aliments reported 2,160 Newport isolates among 101,791 Salmonella isolates collected from animals and food products.
Antimicrobial drug susceptibility testing was performed on 585 human Newport isolates and 342 nonhuman Newport isolates by disk diffusion with 32 antimicrobial drugs (additional information available from fxweill@ pasteur.fr). Data for Newport human isolates are shown in the Table. Of 585 isolates tested, 46 (7.9%) were resistant to third-generation cepalosporins. The geographic origin of the isolates was mainly the Paris metropolitan area and northern France (online Appendix Table, available from www.cdc.gov/EID/content/14/6/954-appT.htm). There was a high prevalence of third-generation cephalosporin–resistant isolates during 2000 (15%) and 2003 (17.5% caused by a small outbreak). No third-generation cephalosporin resistance was detected in any of the nonhuman Newport isolates tested.
Experiments were performed on the 46 third-generation cephalosporin–resistant Newport isolates (additional information available from fxweill@pasteur.fr). All but 1 of the Newport isolates were resistant to cefoxitin (online Appendix Table). These isolates showed 4 resistance phenotypes; most (41, 89.1%) were resistant to streptomycin, sulfonamides, chloramphenicol, and tetracycline. PCR and sequencing showed that the 45 isolates resistant to cefoxitin were positive for the [bla.sub.cMY-2] gene, and cefoxitin-susceptible isolates contained the extended-spectrum [beta]-1actamase gene [bla.sub.CTX-M-1]. Ceftriaxone MICs of Newport MDR-AmpC isolates ranged from 32 mg/L to >256 mg/L, and ceftazidime MICs ranged from 64 mg/L to >256 mg/L. No [bla.sub.TEM] genes were detected. Three isolates with additional resistance to aminoglycosides contained a class 1 integron with the 1-kb gene cassette aadA24 (known to encode resistance to streptomycin and spectinomycin) (11). The chloramphenicol/ florfenicol resistance gene floR was detected in all but 1 CMY-2–producing Newport isolate.
Clonal relatedness of Newport isolates was assessed by multilocus sequence typing (MLST) and PulseNet standard method pulsed-field gel electrophoresis (PFGE) (Figure 1). All 16 Newport MDR-AmpC isolates tested had a common sequence type (ST), ST45. XbaI-PFGE identified 10 distinct profiles (similarity 76.7%) among all 45 Newport MDR-AmpC isolates. Single enzyme matches were found for 3 of the profiles (15 isolates) in the US PulseNet national database (www.cdc.gov/pulsenet; online Appendix Table; Figure 2). Two PFGE types (New6 and New8) were divided into 2-4 subtypes because of additional band(s)