Emergence and Diversity of Salmonella enterica Serovar Indiana Isolates with Concurrent Resistance to Ciprofloxacin and Cefotaxime from Patients and Food-Producing Animals in China

Abstract

e Salmonellosis is a major global foodborne infection, and strains that are resistant to a great variety of antibiotics have become a major public health concern. The aim of this study was to identify genes conferring resistance to fluoroquinolones and extendedspectrum ␤-lactams in nontyphoidal Salmonella (NTS) from patients and food-producing animals in China. In total, 133 and 21 NTS isolates from animals and humans, respectively, exhibiting concurrent resistance to ciprofloxacin and cefotaxime were cultured independently from 2009 to ϳ2013. All of the isolates were identified, serotyped, and subjected to antimicrobial susceptibility testing. Importantly, the isolates with concurrent resistance to ciprofloxacin and cefotaxime all were confirmed as S. enterica serovar Indiana. The presence of fluoroquinolone resistance genes and extended-spectrum ␤-lactamases (ESBLs) was established by PCR and DNA sequencing. The occurrence and diversity of different genes conferring fluoroquinolone resistance [qepA, oqxAB, and aac(6=)-Ib-cr] with mutations in topoisomerase-encoding genes (gyrA and parC) and several ESBLs (including CTX-M-65, CTX-M-27, CTX-M-15, CTX-M-14, and CTX-M-14/CTX-M-15) were noteworthy. Genes located on mobile genetic elements were identified by conjugation and transformation. Pulsed-field gel electrophoresis, used to determine the genetic relationships between these isolates, generated 91 pulsotypes from 133 chicken isolates and 17 pulsotypes from the 21 clinical isolates that showed considerable diversity. Analysis of the pulsotypes obtained with the isolates showed some clones appeared to have existed for several years and had been disseminating between humans and food-producing animals. This study highlights the emergence of ciprofloxacin-and cefotaxime-resistant S. enterica serovar Indiana, posing a threat to public health.

Comparative Analysis of Extended-Spectrum-β-Lactamase CTX-M-65-Producing Salmonella enterica Serovar Infantis Isolates from Humans, Food Animals, and Retail Chickens in the United States

“…We examined select bla CTX-M-65 -positive isolates with PFGE pattern JFXX01.0787. The bla CTX-M-65 gene has been well described in E. coli, Klebsiella pneumoniae, Salmonella enterica serovar Indiana, and Salmonella enterica serovar Typhimurium isolated from humans and healthy animals in China and Korea (12)(13)(14)(15)(16). It has also been found in commensal bacteria in pediatric populations in Bolivia (17) and produce imported to Switzerland from the Dominican Republic and Vietnam (18).…”

Prevalence and Antimicrobial Resistance of Salmonella enterica Serovar Indiana in China (1984–2016)

“…Indiana strains were resistant divided by the total number of tested drugs) in the 22 reported studies, in the five studies of animals they were all over 70% (range 71–97%), mainly 97% (14.5/15) (Lai et al., ), 87% (13.9/16) (Gong et al., ), 83% (15/18) (Zhang et al., ), 79% (14.3/18) (Lu et al., ) and 71% (11.3/16) (Zhang et al., ). There was a greater difference in resistance rates in the eight studies of people (range 17–100%) mainly 100% (12/12) (Zhang et al., ), 90% (14.4/16) (Gong et al., ), 80% (8.0/10) (Bai et al., ), 79% (10.3/13) (Li et al., ), 76% (11.4/15) (Xia et al., ), 54% (12.4/23) (Wang et al., b), 44% (7/16) (Wang et al., ) and 17% (2/12) (Cui et al., ). The resistance rates in the 12 studies of food varied from 50% to 91%, mainly 91% (12.2/14) (Lin et al., ), 90% (9/10) (Li et al., ), 89% (15.1/17) (Yang et al., ), 83% (10/12) (Lei et al., ), 78% (11.7/15) (Yang et al., ), 76% (7.6/10) (Bai et al., ), 76% (8.4/11) (Bai et al., ), 75% (6/8) (Cui et al., ), 72% (6.5/9) (Wang et al., ), 68% (7/11) (Wang et al., ), 60% (16.7/28) (Yan et al., ) and 50% (8/16) (Wang et al., ).…”

“…In total, S . Indiana was reported in people from 10 provinces (Table , Table S1) with Henan reporting the most cases, 41 in six cities (Jiyuan, Suixian, Zhoukou, Shangqiu, Zhenzhou and Dengfeng) (Lu et al., ; Zhang et al., ; Bai et al., ; Xia et al., 2019). With regard to other serovars found, the isolation rate of S .…”

“…Further, numerous S . Indiana isolates from multiple sources have been shown to be highly drug resistant with concurrent resistance to ciprofloxacin and ceftriaxone/cefotaxime (Jiang et al., ; Bai et al., , ; Gong et al., ). With the difficulties associated with treating multi‐drug‐resistant strains of Salmonella , there has thus been increasing concern about S .…”

Antimicrobial resistant and extended‐spectrum β‐lactamase producing Escherichia coli in common wild bird species in Switzerland

“…Similarly, CTX‐M‐65 is a prevalent ESBL in animal and human E. coli strains and Salmonella spp. in China (Bai et al., ). By contrast, CTX‐M‐1 is prevalent within the poultry industry and other livestock in Europe (Zurfluh et al., ).…”