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. 2023 Aug 31;13(17):2770.
doi: 10.3390/ani13172770.

Association between Phenotypes of Antimicrobial Resistance, ESBL Resistance Genes, and Virulence Genes of Salmonella Isolated from Chickens in Sichuan, China

Gang Shu  1 , Jianyu Qiu  1 , Yilei Zheng  2 , Lijen Chang  3 , Haohuan Li  1 , Funeng Xu  1 , Wei Zhang  1 , Lizi Yin  1 , Hualin Fu  1 , Qigui Yan  1 , Ting Gan  1 , Juchun Lin  1
Affiliations

Association between Phenotypes of Antimicrobial Resistance, ESBL Resistance Genes, and Virulence Genes of Salmonella Isolated from Chickens in Sichuan, China

Gang Shu et al. Animals (Basel). .

Abstract

The aim of this study was to explore the association between antimicrobial resistance, ESBL genes, and virulence genes of Salmonella isolates. From 2019 to 2021, a total of 117 Salmonella isolates were obtained from symptomatic chickens in Sichuan Province, China. The strains were tested for antimicrobial resistance and the presence of ESBL according to the Clinical and Laboratory Standards Institute (CLSI) instructions. The presence of ESBL genes and genes for virulence was determined using Polymerase Chain Reaction (PCR). In addition, Multilocus Sequence Typing (MLST) was applied to confirm the molecular genotyping. Moreover, the mechanism of ESBL and virulence gene transfer and the relationships between the resistance phenotype, ESBL genes, and virulence genes were explored. The isolates exhibited different frequencies of resistance to antibiotics (resistance rates ranged from 21.37% to 97.44%), whereas 68.38% and 41.03% of isolates were multi-drug resistance (MDR) and ESBL-producers, respectively. In the PCR analysis, blaCTX-M was the most prevalent ESBL genotype (73.42%, 58/79), and blaCTX-M-55 showed the most significant effect on the resistance to cephalosporins as tested by logistic regression analysis. Isolates showed a high carriage rate of invA, avrA, sopB, sopE, ssaQ, spvR, spvB, spvC, stn, and bcfC (ranged from 51.28% to 100%). MLST analysis revealed that the 117 isolates were divided into 11 types, mainly ST92, ST11, and ST3717. Of 48 ESBL-producers, 21 transconjugants were successfully obtained by conjugation. Furthermore, ESBL and spv virulence genes were obtained simultaneously in 15 transconjugants. These results highlighted that Salmonella isolates were common carriers of ESBLs and multiple virulence genes. Horizontal transfer played a key role in disseminating antimicrobial resistance and pathogenesis. Therefore, it is necessary to continuously monitor the use of antimicrobials and the prevalence of AMR and virulence in Salmonella from food animals and to improve the antibiotic stewardship for salmonellosis.

Keywords: ESBL genes; MLST; Salmonella; antimicrobial resistance; chicken; virulence genes.

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Conflict of interest statement

The authors have no conflict of interest to declare.

Figures

Figure 1
Figure 1
The rate of multidrug-resistant Salmonella isolates. AMP, ampicillin; CFZ, cefazolin; CRO, ceftriaxone; CTX, cefotaxime; GEN, gentamicin; KAN, kanamycin; DOX, doxycycline; NAL, nalidixic acid; CIP, ciprofloxacin; COL, colistin sulfate; 3—resistance to 3 antimicrobials; 4—resistance to 4 antimicrobials; 5—resistance to 5 antimicrobials; 6—resistance to 6 antimicrobials; 7—resistance to 7 antimicrobials; 8—resistance to 8 antimicrobials; 9—resistance to 9 antimicrobials; 10—resistance to 10 antimicrobials; red, resistance; white, intermediate or susceptible.
Figure 2
Figure 2
Comparison of multidrug-resistance rate between ESBL+ and ESBL− isolates. 3—resistance to 3 antimicrobials; 4—resistance to 4 antimicrobials; 5—resistance to 5 antimicrobials; 6—resistance to 6 antimicrobials; 7—resistance to 7 antimicrobials; 8—resistance to 8 antimicrobials; 9—resistance to 9 antimicrobials; 10—resistance to 10 antimicrobials; ESBL+ vs. ESBL− multidrug-resistance rate, * p < 0.05.
Figure 3
Figure 3
The detection of virulence genes in ESBL− and ESBL+ isolates. The detection rates of virulence genes in ESBL+ vs. ESBL−, * p < 0.05.
Figure 4
Figure 4
Minimum spanning tree analysis of 117 Salmonella isolates based on allelic profiles of 7 housekeeping genes. Each circle corresponds to a ST and the number of each ST is given beside the circle. The circle size depends on the number of isolates found within that profile, and the width of the line connecting 2 strains indicates the genetic variation in these isolates.
Figure 5
Figure 5
The occurrence of ST among the ESBL− and ESBL+ isolates. The detection rates of ST in ESBL+ vs. ESBL−, * p < 0.05.
Figure 6
Figure 6
The distribution of AMR in different STs of Salmonella isolates. The distribution of the average antimicrobial resistance (in percent) of various STs towards 10 antimicrobials. The color of individual cells varies with the percentage of antimicrobial resistance shown in the cells. * ST containing only one strain.
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References

    1. Zhou C., Liang J., Jiang W., He X., Liu S., Wei P. The effect of a selected yeast fraction on the prevention of pullorum disease and fowl typhoid in commercial breeder chickens. Poult. Sci. 2020;99:101–110. doi: 10.3382/ps/pez567. - DOI - PMC - PubMed
    1. Chlebicz A., Slizewska K. Campylobacteriosis, Salmonellosis, Yersiniosis, and Listeriosis as Zoonotic Foodborne Diseases: A Review. Int. J. Environ. Res. Public Health. 2018;15:863. doi: 10.3390/ijerph15050863. - DOI - PMC - PubMed
    1. Ma Y., Xu X., Gao Y., Zhan Z., Xu C., Qu X., Chen Z., Bai J., Liao M., Zhang J. Antimicrobial resistance and molecular characterization of Salmonella enterica serovar Corvallis isolated from human patients and animal source foods in China. Int. J. Food Microbiol. 2020;335:108859. doi: 10.1016/j.ijfoodmicro.2020.108859. - DOI - PubMed
    1. Sahan Yapicier O., Ozturk D. Characterization of class 1, 2, 3 integrons, ESBL genes and antibiotic susceptibility of Salmonella serotypes from broiler and cattles in Turkey. Pol. J. Vet. Sci. 2022;25:345–355. doi: 10.24425/pjvs.2022.141820. - DOI - PubMed
    1. Wang J., Zhu X., Zhao Y., Liu H., Zhang Z., Yan L., Chen Y., Robertson I.D., Guo A., Aleri J.W. Prevalence and antimicrobial resistance of Salmonella and ESBL E. coli isolated from dairy cattle in Henan Province, China. Prev. Vet. Med. 2023;213:105856. doi: 10.1016/j.prevetmed.2023.105856. - DOI - PubMed

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