Abstract
Genetic profiles of Salmonella Minnesota isolates were analyzed using pulsed-field gel electrophoresis (PFGE). In total, 13 isolates obtained from the broiler industry collected in the states of Minas Gerais (11) and São Paulo (2), as well as five recovered from cases of foodborne infections in humans in the states of Minas Gerais (2), Santa Catarina (1), and Rio Grande do Sul (2), were submitted to PFGE. These 18 S. Minnesota isolates together with other 12 of poultry origin were also subjected to antimicrobial susceptibility testing. The PFGE analysis of 18 strains of S. Minnesota generated a dendrogram that grouped the isolates with 83–90% similarity into four main clusters. Among them, cluster “A” grouped the majority of isolates (13), including two of human origin that showed 90% similarity with a broiler isolate, both recovered in Minas Gerais. The S. Minnesota isolates showed resistance to tetracycline (80%), cefoxitin (80%), ceftazidime (46.7%), nalidixic acid (23.3%), ciprofloxacin (13.3%), and streptomycin (10%). No resistance to gentamicin, chloramphenicol, meropenem, nitrofurantoin, and sulfamethoxazole-trimethoprim was found. Moreover, 23.3% of the evaluated isolates presented multi-resistance profile, all from Minas Gerais. The results highlight the importance of further studies involving S. Minnesota, which is prevalent in the Brazilian broiler flocks and could provoke foodborne infection in humans.
Keywords: Salmonellosis, PFGE, Multi-resistance, Foodborne infection, Public health
Introduction
Salmonella is a genus of bacteria belonging to the Enterobacteriaceae family, capable of causing infections in humans and animals [1–3]. According to a technical note published by the Ministry of Agriculture, Livestock and Supply (MAPA), Salmonella Heidelberg and Salmonella Minnesota were the main serovars isolated from chicken carcasses slaughtered in Brazilian slaughterhouses in 2017, representing 56% and 19% of positive samples, respectively [4].
Although there are studies addressing aspects of the epidemiology, antimicrobial and genomic resistance of SH in samples from poultry production, or in those recovered from outbreaks of food infection in humans [5, 6], little has been investigated regarding S. Minnesota isolates. Despite being considered of lesser relevance in public health, S. Minnesota has genetic traits that confer ability to cause infection in hosts [7]. Moreover, it can act by exchanging antimicrobial resistance genes with other enterobacteria, contributing to the worsening of this problem in the poultry production environment [8].
Considering the relevance of Salmonella spp. for public and veterinary health and that poultry products (including chicken meat) are implicated in its transmission to consumers [1, 2], the present study was carried out to investigate the antimicrobial resistance and genetic relatedness among S. Minnesota strains isolated from the poultry production chain and foodborne infections in Southeast Brazil.
Material and methods
In total twenty-five isolates of Salmonella enterica subsp. enterica serovar Minnesota were selected from the collection of TECSA Laboratory that is accredited by MAPA to carry out official diagnosis for the National Poultry Health Program (PNSA). These strains were isolated in 2019 from poultry feces of broiler chicken farms located in the states of Minas Gerais (MG), Espírito Santo (ES), and São Paulo (SP). The isolates were serotyped at the Laboratory of Enterobacteria of the Oswaldo Cruz Foundation (FioCruz) being subsequently subjected to antimicrobial susceptibility testing and genotyped by using pulsed-field gel electrophoresis (PFGE) at the same institution. Other five S. Minnesota isolates from human samples (feces or urine) recovered between 2019 and 2020 were provided by FioCruz which were also included in the PFGE analysis as outgroup (Table 1).
Table 1.
Features of Salmonella Minnesota (n = 30) strains isolated from poultry and humans
| SM strains | Year of isolation | Source | Location | Resistant pattern |
|---|---|---|---|---|
| SM A01 | 2019 | Poultry feces | Minas Gerais | TCY, FOX, CAZ |
| SM A02 | 2019 | Poultry feces | São Paulo | TCY, FOX, CAZ |
| SM A03 | 2019 | Poultry feces | Minas Gerais | TCY, FOX, CAZ |
| SM A04 | 2019 | Poultry feces | Minas Gerais | TCY, FOX, CAZ |
| SM A05 | 2019 | Poultry feces | Minas Gerais | TCY, FOX, CAZ |
| SM A06 | 2019 | Poultry feces | São Paulo | TCY, FOX |
| SM A07 | 2019 | Poultry feces | Minas Gerais | TCY, FOX |
| SM A08 | 2019 | Poultry feces | Minas Gerais | TCY, FOX, CAZ, CIP, NAL |
| SM A09 | 2019 | Poultry feces | Minas Gerais | TCY, FOX, CAZ |
| SM A10 | 2019 | Poultry feces | Minas Gerais | TCY, FOX, CAZ, NAL, STR |
| SM A11 | 2019 | Poultry feces | Minas Gerais | TCY, FOX, CAZ, NAL, STR |
| SM A12 | 2019 | Poultry feces | Minas Gerais | TCY, FOX, CAZ, NAL |
| SM A13 | 2019 | Poultry feces | Minas Gerais | TCY, FOX, CAZ |
| SM A14 | 2019 | Poultry feces | Minas Gerais | TCY, FOX, CAZ |
| SM A15 | 2019 | Poultry feces | Minas Gerais | TCY, FOX |
| SM A16 | 2019 | Poultry feces | Minas Gerais | TCY, FOX |
| SM A17 | 2019 | Poultry feces | Minas Gerais | TCY, FOX, CAZ |
| SM A18 | 2019 | Poultry feces | Espírito Santo | NAL |
| SM A19 | 2019 | Poultry feces | Minas Gerais | TCY, FOX, CAZ, NAL |
| SM A20 | 2019 | Poultry feces | Minas Gerais | TCY, FOX |
| SM A21 | 2019 | Poultry feces | Minas Gerais | TCY, FOX |
| SM A22 | 2019 | Poultry feces | Minas Gerais | TCY, FOX, NAL |
| SM A23 | 2019 | Poultry feces | Minas Gerais | TCY, FOX, CIP |
| SM A24 | 2019 | Poultry feces | Minas Gerais | CIP |
| SM A25 | 2019 | Poultry feces | Minas Gerais | CIP |
| SM H01 | 2019 | Human feces | Santa Catarina | STR, NAL |
| SM H02 | 2020 | Human feces | Rio Grande do Sul | STR (I), CIP (I) |
| SM H03 | 2020 | Human urine | Rio Grande do Sul | CIP (I) |
| SM H04 | 2020 | Human feces | Minas Gerais | TCY, FOX |
| SM H05 | 2020 | Human feces | Minas Gerais | TCY, FOX |
NAL nalidixic acid, FOX cefoxitin, CAZ ceftazidime, CIP ciprofloxacin, STR streptomycin, TCY tetracycline, I intermediate resistance profile
Antimicrobial susceptibility test was carried out in twenty-five S. Minnesota isolates from poultry using the Kirby-Bauer disk-diffusion method following the interpretative criteria of the Clinical and Laboratory Standards Institute [9]. Pseudomonas aeruginosa ATCC 27,853 and Escherichia coli ATCC 25,922 were used as quality control strains. Critically important antimicrobials used in veterinary and human medicine were chosen for the antimicrobial susceptibility test. We included in this study 11 antimicrobial disks (Cefar Diagnóstica Ltda., São Paulo, Brazil) as gentamicin (GEN; 10 µg), streptomycin (STR; 10 µg), chloramphenicol (CHL; 30 µg), meropenem (MEM; 10 µg), cefoxitin (FOX; 30 µg), ceftazidime (CAZ; 30 µg), nitrofurantoin (NIT; 300 µg), ciprofloxacin (CIP; 5 µg), nalidixic acid (NAL; 30 µg), sulfamethoxazole-trimethoprim (SXT; 25 µg), and tetracycline (TCY; 30 µg).
In order to evaluate the genetic relatedness, S. Minnesota strains (13 of avian origin and five of human origin) were submitted to PFGE typing which was performed according to the standard PulseNet protocol for Salmonella serovars [10]. The analysis and construction of the similarity dendrogram were carried out using the Bionumerics software version 7.1 (Applied mathematics, Sint-Martens-Latem, Belgium), applying the Unweighted Pair Group Method using Arithmetic averages (UPGMA). The band patterns obtained in PFGE were compared using the Dice coefficient at 1% tolerance and 0.5% optimization.
Results and discussion
The antimicrobial susceptibility analysis of the poultry isolates of S. Minnesota resulted in nine profiles of antimicrobial resistance (numbers 1 to 9) which are shown in Table 2. The most frequent profiles were “4,” which grouped nine strains resistant to tetracycline, cefoxitin, and ceftazidime (TCY-FOX-CAZ), and “3,” with six strains resistant to tetracycline and cefoxitin (TCY-FOX). All S. Minnesota strains were resistant to at least one antimicrobial as summarized in Table 1. In addition, three S. Minnesota strains (10%) showed reduced susceptibility, three (10%) were resistant to only one antimicrobial, while 18 strains (60%) were resistant to antimicrobials of two classes, and seven S. Minnesota strains (23.3%) were multidrug resistant, since they were resistant to at least one antimicrobial from three or more distinct classes [11].
Table 2.
Resistance patterns of Salmonella Minnesota strains (n = 25) recovered from poultry feces
| Profile | Resistance pattern | Strain number | Strain percentage | Classes | Multidrug resistance |
|---|---|---|---|---|---|
| 1 | CIP | 2 | 8.0% | 1 | No |
| 2 | NAL | 1 | 4.0% | 1 | No |
| 3 | TCY, FOX | 6 | 24.0% | 2 | No |
| 4 | TCY, FOX, CAZ | 9 | 36.0% | 2 | No |
| 5 | TCY, FOX, CIP | 1 | 4.0% | 3 | Yes |
| 6 | TCY, FOX, NAL | 1 | 4.0% | 3 | Yes |
| 7 | TCY, FOX, CAZ, CIP, NAL | 1 | 4.0% | 3 | Yes |
| 8 | TCY, FOX, CAZ, NAL | 2 | 8.0% | 3 | Yes |
| 9 | TCY, FOX, CAZ, NAL, STR | 2 | 8.0% | 4 | Yes |
NAL nalidixic acid, FOX cefoxitin, CAZ ceftazidime, CIP ciprofloxacin, STR streptomycin, TCY tetracycline
In the present study, resistance to gentamicin, chloramphenicol, meropenem, nitrofurantoin, and sulfamethoxazole-trimethoprim was not observed. In turn, the strains of S. Minnesota evaluated showed resistance to tetracycline (80%), cefoxitin (80%), ceftazidime (46.7%), nalidixic acid (23.3%), ciprofloxacin (13.3%), and streptomycin (10%). Most of these drugs are used in healthy animals prophylactically to prevent infections or as growth promoters [12]. The last is even more controversial, since it is based on the use of subtherapeutic doses to accelerate animal weight gain, which can lead to the selection of resistant bacteria [13].
Despite the fact that it is not possible to state that the misuse of antibiotics has influenced the resistance profiles of the strains evaluated in the present study, it was observed that 23.3% of the tested strains were multidrug resistant. This is an important aspect, which added to the several virulence factors and pathogenicity mechanisms of Salmonella spp., making more difficult to treat some cases of the foodborne salmonellosis [7, 14].
Tetracycline was one of the first antimicrobials adopted for use in animal production, being common a high frequency of resistance to this drug [7, 15]. Even though they were banned in 1998 in Brazil as additives for animal feed, they are still used therapeutically, thus exerting some selective pressure on microorganisms [16].
Another crucial point to be emphasized is that the currently recommended treatment options for salmonellosis in humans include fluoroquinolones and third-generation cephalosporins [17]. However, due to their broad spectrum of action, these drugs are also frequently used in veterinary medicine. This is particularly worrying, given that the present study demonstrated the presence of strains resistant to these two classes. Thus, it is highlighted that the circulation of Salmonella isolates resistant to these antimicrobials in the Brazilian broiler chain constitutes a risk to public health [1]. Is noteworthy that twenty-four (80%) S. Minnesota strains displayed resistant to cefoxitin (FOX). This phenotypic resistance is most likely encoded by the overproduction of AmpC exhibiting resistance to broad-spectrum second-generation cephalosporins, such as cefoxitin. This finding is consistent with previous surveys that reported the presence of Salmonella enterica serovars phenotypically resistant to cefoxitin associated with the presence of blaCMY-2 gene [14, 18, 19]. These data are particularly worrisome, because AmpC genes in salmonellae may indicate impermeability and/or plasmid-mediated AmpCs expression that is acquired via horizontal gene transfer. In addition, this plasmid is not restricted to encode resistance to cephamycins but also can harbor a wide variety of resistance genes conferring multidrug resistance phenotype, which raises a public health concern as treatment options become limited [18, 19]. Furthermore, Salmonella enterica serovars displaying resistance to these β-lactams appear to be endemic in both North and South American countries [6, 14, 19–21]. In this regard, considering the potential transmission to humans, surveillance of cefoxitin-resistant S. Minnesota in the poultry production chain needs to be monitored to prevent their spread.
Regarding the molecular analysis, the band patterns obtained by PFGE for the 18 strains of S. Minnesota isolated from poultry (n = 13) and human (n = 5), a genetic similarity dendrogram is depicted in Fig. 1, whose cutoff point was 80% [6]. It was observed the clustering of four clonal groups (isolated with common ancestor) in the originated dendrogram, designated as A, B, C, and D. The S. Minnesota strains did not cluster by year, origin, source, or geographic location, whereas antimicrobial resistance profiles slightly varied by strains across the tree (Fig. 1).
Fig. 1.
Dendrogram of PFGE patterns of S. Minnesota strains obtained from poultry feces and human urine/feces samples collected in different Brazilian states. UPGMA clustering method, similarity based on the Dice coefficient (%), optimization, and tolerance set at 1.5%. Legend: Minas Gerais (MG), Rio Grande do Sul (RS), Santa Catarina (SC), and São Paulo (SP).
Cluster A encompasses 13 strains (11 from poultry and two from humans), one sample from broilers from São Paulo and the rest from Minas Gerais, which showed 86% similarity. In this group, there are nine pulse types, with emphasis on the pulse types BRJIGX01.033 and BRJIGX01.028, which presented, respectively, four and two representatives. Cluster A was divided into sub-clusters A1, A2, and A3 for better visualization. In sub-cluster A3, there are two human strains, SM H04/20 and SM H05/20, and these showed 90% similarity with a strain of animal origin (SM A03/19). The human strains in A3 still show 87% similarity with the other strains recovered from broilers presented in A2 and A1.
Cluster B has three strains with unique representative of their respective pulse types. In this cluster, there is a human strain (SM H03/20) from the state of Rio Grande do Sul, which nested with 83% of similarity with two strains of poultry origin, one from Minas Gerais (SM A01/19) and the other from São Paulo (SM A02/19). In turn, clusters C and D are represented by human samples collected in Santa Catarina and Rio Grande do Sul. However, they are unique representatives of their respective clusters, presenting < 70% similarity with the other samples evaluated.
The analysis of the dendrogram generated by PFGE of genomic DNA digested with XbaI of 13 strains of S. Minnesota allowed the identification of clusters with more than 80% similarity among strains isolated from samples of animals and humans. Clustering points to a close similarity among strains of S. Minnesota from humans and poultry. The data suggests that strains are closely related clonally and have a common origin, which has undergone changes and has spread over space and time [1, 15]. This is particularly noticed in three strains observed in cluster A (SM H04/20, SM H05/20, and SM A03/19) which in addition of presenting 90% similarity, all were isolated in Minas Gerais. Although the number of tested strains in this study illustrates a better representation to Minas Gerais state, the findings within this study substantially aid in the S. Minnesota genotyping, and these analysis should be expanded to a diverse set of S. Minnesota strains, as well as further studies are necessary to fully comprehend the epidemiology of S. Minnesota strains as emerging serovar carrying antimicrobial resistance markers and their potential to be spread throughout human-animal-environment interface.
Therefore, it is worth highlighting that official monitoring and surveillance of antimicrobial use is essential to reduce the continuous evolution of bacterial resistance in the poultry production system. The genetic characterization through molecular techniques, such as PFGE, represents an important auxiliary tool in the understanding of the origin and dynamics of the agent, as well as in the identification of circulating and emerging strains. These results also confirm that PFGE is still a suitable approach to genotype various Salmonella serovars, as previously established [22]. Moreover, knowledge about genetic profiles and antimicrobial resistance of S. Minnesota is of great value for a more detailed evaluation of the circulating pulse types in poultry and the risk represented by them to the public health.
Acknowledgements
We are grateful to TECSA Laboratory and to the staff of the Laboratory of Enterobacteria of the Oswaldo Cruz Foundation (FioCruz) for the strains and technical support.
Author contribution
All authors whose names appear on the submission made substantial contributions to the conception of the work, interpretation of data, and critical review, agreeing to be accountable for all aspects of the work.
Data availability
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Code availability
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Declarations
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Consent for publication
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Conflict of interest
The authors declare no competing interests.
Footnotes
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