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Brazilian Journal of Microbiology logoLink to Brazilian Journal of Microbiology
. 2023 Jan 6;54(1):469–474. doi: 10.1007/s42770-022-00893-0

The rise of multidrug resistant Salmonella isolates in healthy chickens in Brazil by successful establishment of plasmid IncHI2A carrying several antibiotic resistance genes

Rafael Antonio Casarin Penha Filho 1,✉, Joseane Cristina Ferreira 2, Renata Galetti 2, Ana Maria Iba Kanashiro 3, Angelo Berchieri Jr 1, Ana Lúcia da Costa Darini 2
PMCID: PMC9944584  PMID: 36607526

Abstract

Salmonella spp. is an important global issue in food-producing animals. The present study evaluated antimicrobial resistance and virulence profiles in Salmonella spp. isolates from chickens in Brazil. Identification of serotypes, virulence and antimicrobial resistance genes, and plasmid profiles were performed. Three different serovars were found, S. Schwarzengrund, S. Newport and S. Kentucky. All isolates were considered Multidrug- resistance (MDR). Among the 32 Salmonella spp. isolates analysed, 29 isolates carried blaCTX-M-2 gene and showed the insertion sequence ISCR1 and a class 1 integron structure upstream from blaCTX-M-2. This gene was harboured in large IncHI2A plasmids with approximately 280kb. Furthermore, 30 isolates harboured tetA and tetB genes and 25 also harboured qnrB. The virulence genes invA, misL, orfL, spiC and pipD were detected in all isolates. The study shows a high prevalence of MDR Salmonella isolates disseminated in poultry farms. The association of the replicon IncHI2A with the resistance genes found, elevate the risk of foodborne disease outbreaks.

Keywords: Brazil, ESBL, poultry, food-producing animals

Introduction

Salmonella spp. is a frequent etiological agent of foodborne infections. The intestinal tract of food-producing animals can be a reservoir of Salmonella spp., which may consequently lead to contamination of diverse derived food products. Foodborne salmonellosis has a high global impact in human health [1, 2]. The increasing global trade of food, especially unprocessed or raw meat and vegetables, new issues might arise regarding salmonellosis control. The presence of Salmonella spp. in healthy poultry represents a high risk factor, considering that poultry may be an important carrier for the transmission to humans through the consumption of contaminated derived food [3]. The combination of the previous factors to the presence of antimicrobial resistance genes on this bacteria genus aggravates the outcome of infections in both animals and humans [4].

Although there are more than 2600 different Salmonella serovars described, there is a tendency over time that few serovars stablish higher epidemiological relevance. In the Unites States, the CDC reported that only 5 serovars, including S. Enteritidis and S. Typhimurium, are responsible for more than 40% of all human salmonelosis cases [5, 6], during the last decade. The emergence of novel serovars with higher epidemiological relevance in the poultry production systems has ocurred throughout this period, and many factors are involved in this relevance dynamics, such as virulence factors, environmental adaptability or resistance to antimicrobials. Among these factors, the use of antimicrobials is the only influenced by humans, and it is important to control the use to minimize the election of resistant Salmonella isolates and also to control the spread of MDR clones by improving biosecurity measures throughout the food production chain and guarantee the quality of globally traded food [4].

Currently, the resistance genes that have been found in Salmonella isolates of animal origin, show that these genes are mostly associated to mobile genetic elements and confer resistance to important classes available for both humans and animal therapies. These genes are not Salmonella spp. specific, but can be aquired by a wide range of Enterobacteriaceae and Nonfermenting Gram-Negative Bacilli [7]. The dissemination of antimicrobial resistance often occurs via mobile genetic elements such as plasmids, transposons and gene cassettes harboured in integrons [8]. The most common integrons involved in antimicrobial resistance are class 1 integrons that are abundant in the genomes of many bacterial species [9]. The emergence and spread of Salmonella isolates presenting resistance to different antimicrobials is concerning because these drugs are crucial to the successful treatment of invasive and complicated infections [4, 10].

Currently, a large percentage of Salmonella isolates from domestic animals, isolated from clinical or non-clinical origin carry antibiotic resistance genes and resistance profile against antimicrobials, commonly used in hospital care. Food-production animals, especially those in intensive farming systems, such as poultry, swines and dairy cattle, have shown the presence of relevant resistance genes in pathogenic or microbiota bacteria [11]. Resistance genes for 3rd and 4th generation beta-lactams, which are crucial antibiotics in human medicine, are increasinlgy described in these animals. Resistance to these antibiotics are mediated by the AmpC and Extended Spectrum Beta-lactamase (ESBL) families and these are often found in E. coli and Salmonella spp. [12].

The spread and the global persistence of serotype S. Kentucky reflect a particular situation related to the increased globalization of travel and the food/animal trade in different geographical regions. This serotype has been recovered from several poultry farms worldwide, and has shown a high potential to cause human infection [13, 14]. The acquisition of an E. coli ColV virulence plasmid by S. Kentucky was also associated with enhanced colonization ability in chickens [15].

The increasing concern with antimicrobial resistance and food safety has been recognized by various international organizations [9, 16]. Considering the complex epidemiology of this issue, the investigation of genes, elements and sources involved in the dissemination are highly relevant at this moment to overcome or manage this problem. Thus, the present study evaluated antimicrobial resistance and virulence profile in different Salmonella isolates from chickens in Brazil, to determine the prevalence of resistance elements and characterize the resistance profile of these bacteria.

Material and methods

Bacterial isolates

In 2013, drag swabs were collected from 23 chicken farms, located in Goias, Brazil. Thirty-two Salmonella spp. isolates were obtained. Isolates were characterized with biochemical tests using API 20E strips (bioMérieux, France) and the serotyping method follow the Kaufmann-White Le Minor scheme.

Antimicrobial susceptibility

The antimicrobial susceptibility of the isolates was determined by using the disk diffusion methods [17], and the results were interpreted according to recommendations of the Clinical and Laboratory Standards Institute [18]. Antimicrobial agents were tested: amoxicillin-clavulanic acid (AMC), piperacillin/tazobactam (TZP), cefotaxime (CTX), ceftazidime (CAZ), ceftiofur (EFT), cefoxitin (FOX), cefepime (FEP), aztreonam (ATM), ertapenem (ETP), nalidixic acid (NAL), ciprofloxacin (CIP), enrofloxacin (ENR), tetracycline (TET), gentamicin (GEN), trimethoprim-sulfamethoxazole (SXT) and chloramphenicol (CHL). ESBL-producing isolates were screened by double disk synergism (DDS) using CTX and CAZ with AMC.

Pulsed-field gel electrophoresis (PFGE)

Genetic relationship among 32 MDR isolates was determined by analysis of XbaI-digested genomic DNA on pulsed field gel electrophoresis (PFGE), performed in CHEF DRIII System (Bio-Rad, USA) [19]. Gels were analysed with the BioNumerics fingerprinting software (Applied Maths, Belgium) and the normalized profiles were compared using the Dice similarity index. The dendrogram was constructed using the unweighted-pair group method using average linkage algorithm (UPGMA).

Investigation of resistance and virulence genes

The investigation of blaTEM, blaSHV, blaCTX-M (groups 1, 2, 8, 9 and 25), PMQR genes and tet genes (A, B, C, D, E and G) was carried out by PCR and sequencing [20–23]. The DNA sequences and translated amino acid sequences obtained were compared with references found in the LAHEY home page (http://www.lahey.org/Studies/). The presence of virulence genes invA (invasion protein), misL (involved in intramacrophage survival), orfL (adhesin/autotransporter), spiC (type III secretion system) and pipD (type III secretion effector associated with SPI-1 system) was evaluated by PCR [24, 25].

Characterization of genetic environment of resistance

After identification of β-lactamase genes in resistant isolates, the genetic environment of β-lactamase genes was determined by PCR of upstream and downstream regions, as described previously [26]. Plasmids were investigated and characterized by the PBRT scheme, as previously described [27]. Southern blot and hybridization methods were performed to locate the replicon type carrying the ESBL-encoding gene. Briefly, plasmid DNA was digested with S1 nuclease and analysed on PFGE gels (S1-PFGE). The PFGE gel was transferred to the nylon membrane (Hybond-N+, GE Healthcare Life Sciences, USA) and hybridization with specific probes for detection of the resistance gene and the incompatibility (Inc) groups. The identification of the replicon type harbouring the resistance gene was determined when these probes hybridized in the same position.

Results

Bacterial isolates

Salmonella spp. isolates were serotyped and classified among three different serovars S. Schwarzengrund (17/32), S. Newport (13/32) and S. Kentucky (2/32) (Table 1).

Table 1.

Microbiological and molecular characteristic of MDR Salmonella isolates from poultry farms

Isolates Serovar Farm Phenotype of resistance Resistance genes Plasmid content (Inc/kb) Genetic environment PFGE type
12406 Newport 1 CTX,FEP,ATM,EFT,NAL,CIP,ENR,TET,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/280 Int class1+ISCR1 B
12407 Schwarzengrund 2 CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,TET,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A,NT/280, 60 Int class1+ISCR1 A
12408 Newport 2 AMC, CTX,CAZ,FEP,ATM,EFT,TET,SXT blaCTX-M-2, tetA, tetB HI2A,NT/280, 40 Int class1+ISCR1 B
12410 Newport 3 AMC, CTX,CAZ,FEP,ATM,EFT,TET,SXT blaCTX-M-2, tetA, tetB HI2A,NT/280, 40 Int class1+ISCR1 B
12411 Newport 4 CTX,CAZ,FEP,ATM,EFT,TET SXT blaCTX-M-2, tetA, tetB HI2A/280 Int class1+ISCR1 B
12416 Schwarzengrund 5 AMC,CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,TET,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/280 Int class1+ISCR1 A
12818 Schwarzengrund 6 CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,TET,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/280 Int class1+ISCR1 A
12819 Schwarzengrund 6 CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,TET,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/280 Int class1+ISCR1 A
12824 Schwarzengrund 7 CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,TET,SXT blaCTX-M-2, qnrB5, tetA ,tetB HI2A/280 Int class1+ISCR1 A
12825 Schwarzengrund 7 CTX,FEP,ATM,EFT,NAL,CIP,ENR,TET,SXT blaCTX-M-2, tetA, tetB HI2A/280 Int class1+ISCR1 A
12828 Schwarzengrund 8 TET,CHL,SXT tetA, tetB HI2A/280 ND A
13206 Newport 9 AMC,CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,TET,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/280 Int class1+ISCR1 B
13207 Newport 9 AMC,CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,TET,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/280 Int class1+ISCR1 B
13210 Schwarzengrund 10 CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,SXT blaCTX-M-2, qnrB5 HI2A/280 Int class1+ISCR1 A
13211 Schwarzengrund 10 CTX,CAZ,FEP,ATM,EFT,TET,SXT blaCTX-M-2, tetA, tetB HI2A/280 Int class1+ISCR1 A
13213 Schwarzengrund 11 NAL,CIP,ENR,TET,SXT,CHL,FLO qnrB5, tetA HI2A,A-C/280, 150 ND A
13214 Newport 11 CTX,ATM,EFT,TET,SXT blaCTX-M-2, tetA, tetB HI2A,P/280, 25 Int class1+ISCR1 B
13766 Schwarzengrund 12 AMC,CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,TET,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/280 Int class1+ISCR1 A
13771 Schwarzengrund 13 CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/280 Int class1+ISCR1 A
14289 Schwarzengrund 14 AMC,CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,TET,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/280 Int class1+ISCR1 A
14290 Schwarzengrund 15 CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/300 Int class1+ISCR1 A
14292 Newport 16 AMC,CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,TET,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A,NT/280, 35 Int class1+ISCR1 B
14296 Schwarzengrund 17 CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/300 Int class1+ISCR1 A
14297 Schwarzengrund 18 CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A,NT/280, 60 Int class1+ISCR1 A
14298 Schwarzengrund 18 CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/280,35 Int class1+ISCR1 A
14302 Newport 19 NAL,CIP,ENR,TET,CHL qnrB5 NT/200 ND B
14995 Newport 20 CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/300 Int class1+ISCR1 B
14996 Newport 20 CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/280 Int class1+ISCR1 B
14998 Kentucky 21 CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/300 Int class1+ISCR1 C
14999 Kentucky 21 AMC,CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,TET,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/280 Int class1+ISCR1 C
15007 Newport 22 AMC,CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,TET,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/280 Int class1+ISCR1 B
15009 Newport 23 AMC,CTX,CAZ,FEP,ATM,EFT,NAL,CIP,ENR,TET,SXT blaCTX-M-2, qnrB5, tetA, tetB HI2A/280 Int class1+ISCR1 B
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AMC amoxicillin-clavulanic acid, CTX cefotaxime, CAZ ceftazidime, FEP cefepime, ATM aztreonam, EFT ceftiofur, NAL nalidixic acid, CIP ciprofloxacin, ENR enrofloxacin, TET: tetracycline, CHL chloramphenicol, SXT trimethoprim-sulfamethoxazole. NT plasmids non-typeable by PBRT, ND not determined

Antimicrobial susceptibility

In the present study, among the 32 isolates analysed, 29 (90.6%) showed ESBL phenotype. These same 29 Salmonella spp. isolates showed resistance to CTX, EFT and ATM. Additionally, some isolates also showed resistance to other β-lactams tested, including 34% resistance to AMC, 80% to CAZ and 87% to FEP. However, 100% were susceptible to FOX, TZP and ETP. Furthermore, 81% (26/32) of the isolates were also resistant to the non-beta-lactam antibiotics NAL, CIP and ENR, 72% to TET and 97% to SXT and 9% were resistant to CHL (Table 1). Thus, all isolates were considered MDR, not-susceptible to at least one agent in three or more antimicrobial categories [28]. The MDR Salmonella spp. were isolated in all farms (Table 1).

Pulsed-field gel electrophoresis (PFGE)

All 32 MDR Salmonella isolates were successfully typed by PFGE, 17 S. Schwarzengrund isolated from different farms belonged to the same PFGE-type A, 13 S. Newport isolated were classified as PFGE-type B and two S. Kentucky isolated belonged to PFGE-type C (Table 1).

Investigation of resistance and virulence genes

Investigation of β-lactamase groups by PCR revealed that all 29 ESBL-producing isolates (100%) carried the blaCTX-M-2 gene (Table 1). The qnrB gene was found in 25 isolates (Table 1) and 30 isolates harboured tetA and tetB genes (Table 1).

The genes invA, misL, orfL, spiC and pipD were evaluated and all these genes were detected in all isolates,

Characterization of genetic environment of resistance

The genetic environment characterized in CTX-M-producing isolates showed the insertion sequence ISCR1 and a class 1 integron structure with 7 kb upstream (5’ region) from blaCTX-M-2 in all encoding isolates (Table 1). The ISCR1 was found upstream of the blaCTX-M-2 and the resistance gene was associated with sul-1 type integron structure.

Plasmids replicons from groups IncHI2A were identified in 97% (31/32) of the isolates (31/32). Replicons IncP and IncA/C were found in 3% (1/32) of the isolates (Table 1). The hybridization showed that 29 Salmonella spp. isolates harboured blaCTX-M-2 gene in large IncHI2A plasmids with approximately 280kb to 300kb (Table 1).

Discussion

These findings bring important information about the maintenance and dissemination of the resistance genes in animal farms. The association of blaCTX-M-2 with ISCR1 and class 1 integron, increases the co-selection and maintenance risks of resistant bacteria, once these mobile genetic elements carries a resistance gene to quaternary ammonium disinfectants. Thus, the use of this antimicrobial alone, in poultry facilities and farms as a biosafety measure, may interfere in bacterial population in this environment.

Fluoroquinolones are extensively used as therapeutic drugs in veterinary medicine and the continuous use of subinhibitory antibiotic concentrations, in the poultry environment, may promote the genetic recombination and select resistant Salmonella isolates with reduced susceptibility [29, 30]. The quinolone resistance detected may be related to chromosomal mutations in quinolone-resistance-determining region (QRDR) or associated with other resistance mechanisms (e.g. porin deficiencies, overexpression of efflux systems). However, the presence of qnr genes in plasmids increases the risk of horizontal dissemination of co-resistance among enterobacteria [31]. In the present study, 81% (26/32) of the isolates were resistant to the most relevant therapeutic options, within these classes: NAL, CIP and ENR. Moreover, 25 of these isolates carried plasmidial qnrB5 gene, which could be easily transferred and contribute to reduce susceptibility to these antimicrobials.

Although the preventive use of tetracycline was banned in Brazil since 1998, in animal feed, this antimicrobial agent remains one of the most frequently used in therapeutics because it is easily accessible [32], which may explain the high levels of resistance found in our study. Both tetA and tetB genes were found in 30/32 (94%) of the Salmonella spp. isolates. This was similar to the findings in others studies reported [33].

The impacting data obtained herein show an alarming high rate of MDR, where 90% of the Salmonella spp. isolates from broilers were ESBL-producers. This results show that the resistant isolates circulating in the sampled flocks, have been successfully established within the poultry production sites. The gene blaCTX-M-2 was harboured in plasmids that simultaneously carried resistance genes to other antimicrobial classes. The large sized plasmids found, carrying different resistance genes, also belonged to the same replicon. The fact that these were present in different serovars relates to the relevant role of this plasmid for bacterial survival and persistence, to the point where it has been disseminated horizontally to different bacteria. Antimicrobial co-resistance to several drugs is concerning, considering the drastic reduction in therapeutic options available to treat such infections. Even though the risk of foodborne infections is not easily estimated and non-typhoidal Salmonella are most related to intestinal infections, MDR isolates could increase morbidity and mortality especially in susceptible more hosts [34].

The invA is conserved among Salmonella serotypes and is a useful marker for molecular detection of this pathogen by PCR. However, the presence of other additional virulence genes in all 3 different serovars studied, highlighted the virulence potential and showed the risk of Salmonella isolates to cause persistent infections in poultry and contaminate derived food. These genes have already been reported in Salmonella isolates from chickens and humans in Brazil and South Africa [33].

These data showed that antimicrobial resistance is still growing and evolving, considering characteristics and the level of dissemination of the mobile genetic elements found. The high rate of CTX resistant isolates (90.6%) revealed in the present study, demonstrated the successful establishment of isolates with improved survival and dissemination characteristics. In a previous study, among 83 Salmonella isolates from 2009 to 2012, 21.7% were considered MDR, and 13.5% carried blaCTX-M-2 or blaCMY-2 genes [35]. However, the present study showed an increased MDR rate and blaCTX-M-2 dissemination, reaching 100% (32/32) and 90% (29/32) of the isolates, respectively. Co-resistance to several drugs and virulence determinants may be present in the same plasmid, which may be co-selected by antibiotic pressure [36] resulting in increased morbidity, mortality, systemic infections and hospitalization rates with resistant non-typhoid Salmonella isolates [37]. Overall, the cooperation and the exchange of information between the sectors of agriculture, veterinary, food production and public health has become essential for the constant surveillance and control of antimicrobial resistance worldwide. The genetic mobile elements involved in the dissemination of antimicrobial resistance are able to spread not only among animal Salmonella spp. isolates, but in favourable environments the exchange of these genes may occur with other Enterobacteriaceae from animals and humans.

Conclusion

The molecular features presented by the Salmonella spp. isolates studied herein, showed the capacity of these pathogenic MDR bacteria to persist and disseminate resistance in animal environment. Thus, this study shed light on the high dissemination potential of resistance among different bacteria, allowing successful establishment of a mobile genetic element (MGE). The frequent association of the replicon IncHI2A with blaCTX-M-2, with slight variations on size and additional resistance genes co-inserted, found in 90% of the isolates from different farms has been shown to be established since 2009 and this fact may elevate the risk of outbreaks of foodborne infections, considering its prevalence.

Acknowledgements

We would like to thank Dr. Luke Richards for his kind review of the text. São Paulo Research Foundation (FAPESP) for the constant support for our research (Grant n. 2014/14494-8). Rafael. Penha Filho, (FAPESP, grant 2017/00620-0).

Authors’ contributions

R.A.C.P.F. and J.C.F. carried out the experiment and wrote the manuscript with support from A.B.Jr. and A.L.C.D, R.G. contributed to the interpretation of the results and A. M. I. K. contributed to sample preparation and isolation of samples. All authors contributed to the final version of the manuscript. A.L.C.D supervised the project.

Funding

This study was funded by São Paulo Research Foundation (FAPESP), Grant n. 2014/14494-8.

Declaration

Competing interest

The authors have no competing interests to declare

Footnotes

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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