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. 2021 May 4;59(3):1097–1103. doi: 10.1007/s13197-021-05113-5

Virulence genes and sanitizers resistance in Salmonella isolates from eggs in southern Brazil

Louise Haubert 1, Darla Silveira Volcan Maia 1, Simone de Fátima Rauber Würfel 2, Cristiane Vaniel 1, Wladimir Padilha da Silva 1,3,✉
PMCID: PMC8814091  PMID: 35153327

Abstract

Salmonella spp. causes foodborne diseases related to the consumption of contaminated foods, especially poultry products. This study aimed to investigate the occurrence of Salmonella spp. serovars in raw eggs from supermarkets and street food markets in southern Brazil, to analyze virulence genes, resistance profiling to antimicrobials and sanitizers, and to determine the susceptibility of the isolates to Butia odorata extract. Among 160 samples analyzed, just two (1.25%) were positive for Salmonella spp.. One positive sample was from egg yolk (S. enterica serovar Gallinarum, isolate S28), and another one was from eggshell (S. enterica serovar Panama, isolate S37). Regarding the virulence genes, the isolate S37 harbored all the genes evaluated (hilA, invA, spvC, sefA, and pefA), while the isolate S28 did not harbor the pefA gene. The isolate S28 was resistant to tobramycin, azithromycin, and trimethoprim, while the isolate S37 showed resistance profile just to nalidixic acid. However, none of the resistance genes evaluated were identified. Both isolates showed resistance to benzalkonium chloride, chlorhexidine digluconate, sodium hypochlorite, and peracetic acid, presenting high MIC values for these sanitizers. In contrast, B. odorata extract showed antimicrobial activity against the isolates S28 and S37, however, more studies are needed to prove its potential as a natural antimicrobial compound.

Electronic supplementary material

The online version of this article (10.1007/s13197-021-05113-5) contains supplementary material, which is available to authorized users.

Keywords: S. Gallinarum, S. Panama, Virulence genes, Sanitizers resistance, Plant extract

Introduction

Salmonella spp. is a pathogenic microorganism very often found in eggs and in raw meat from pigs, turkeys, and chickens (EFSA 2018). Regarding eggs, Salmonella spp. can contaminate following oviposition, penetrating the eggshell and membrane, or during egg formation (Gantois et al. 2009). In Brazil, eggs and egg products represented a considerable number — around 7.3% — of food categories involved in foodborne diseases outbreaks between 2000 and 2017 (Brasil 2018).

Among the common enteric illnesses, salmonellosis has high rates of mortality (Besser 2018). The pathogenicity of Salmonella spp. has been associated with genes present in pathogenicity islands (SPI), located in chromosomal DNA, and high-molecular-mass virulence-associated plasmid (pSTV) (Campioni et al. 2012).

The extensive administration of antimicrobials in livestock as growth promoters and in veterinary therapeutics as well as the widespread use of antimicrobials compounds as therapeutic choices in human populations have contributed to the emergence of antimicrobial resistance in foodborne microorganisms, such as Salmonella spp. (Thames et al. 2012). Moreover, the spreading of multidrug resistant Salmonella isolates (resistance to ≥ 3 antimicrobial classes) is considered a severe concern for public health (Anjum et al. 2011).

Considering that Salmonella infections can be severe and fatal, especially at risk groups such as elderly, children and immunocompromised individuals (Arshad, et al. 2008), the administration of antimicrobials is crucial in these cases, and the antimicrobial resistance can hinder the treatment of the infection (Arshad et al., 1995). For this, epidemiologic studies regarding resistance profile and even studies about resistance genes have particular relevance to establish control procedures (Anjum et al. 2011). Also, the sanitizers’ resistance is an important issue in view of some isolates harbor cross-resistance to several antimicrobial compounds, increasing this public health concern (Long et al. 2016).

In this context, in the last years, some studies have been performed regarding the antimicrobial potential of plants as an alternative to synthetic compounds, including fruits, such as butiá (Butia odorata Barb. Rodr). This native fruit of South America, has antimicrobial activity against foodborne pathogens, such as Salmonella spp. (Haubert et al. 2019; Maia, et al. 2017).

Considering that there are few or even no data about the presence of Salmonella spp. in eggs in Brazil, this study aimed to investigate the occurrence of Salmonella spp. serovars in raw eggs from supermarkets and street food markets in southern Brazil. Furthermore, virulence genes, resistance profiling to antimicrobials and sanitizers, and the susceptibility of the isolates to Butia odorata extract were evaluated.

Material and methods

Sampling

Raw eggs available at eight establishments (four supermarkets and four street food markets) of Pelotas city, Rio Grande do Sul State, Brazil, were evaluated for the presence of Salmonella spp. in yolk and eggshell. One pack containing 12 eggs was purchased per establishment — as a normal consumer would do, without providing any special instructions to the seller — and transported to the microbiology laboratory. Six randomly eggs, out of the 12 purchased, were combined to make two samples for analysis (yolk and eggshell were evaluated separately). A total of 10 collections were performed, totalizing 160 samples and 480 eggs evaluated.

Isolation of Salmonella spp.

The yolk and eggshell were tested separately and the standard method described by the International Organization for Standardization (ISO-6579) was used with some modifications. Briefly, the yolk and eggshell were weighted (25 g) and immersed in 225 mL of Buffered Peptone Water (BPW) (Oxoid, UK) in separate bags, and were incubated at 37 °C for 24 h. After incubation, samples were selectively enriched in Rappaport Vassiliadis broth (RV) (Acumedia, Brazil) and Selenite Cystine broth (SC) (Himedia, India) and incubated again at 42 °C for 24 h. Cultures were then streaked onto Brilliant Green agar base modified (BPLS) (Himedia, India) and Xylose Lysine Deoxycholate agar (XLD) (Kasvi, Brazil) and incubated at 37 °C for 24 h. The suspected colonies were cultured on Tryptone Soya agar (TSA) (Kasvi, Brazil) and subjected to phenotypic tests which included biochemical reactions on Triple Sugar Iron agar (TSI) (Acumedia, Brazil), Lysine Iron agar (LIA) (Acumedia, Brazil), Urease (Vetec Quimica Fina Ltda, Brazil), Indole (SIM) (Vetec Quimica Fina Ltda, Brazil), and oxidase tests (Laborclin Produtos para Laboratórios Ltda, Brazil). The isolates with typical Salmonella spp. biochemical reactions in the phenotypic tests cited above were subjected to serology tests with somatic polyvalent anti-Salmonella serum (Probac, Brazil) and flagellar polyvalent anti-Salmonella serum (Probac, Brazil). For all the steps, the strain S. Typhimurium ATCC® 14028 was used as positive control.

Serotyping

In order to characterize the serotype of the isolates, serological tests were performed at the National Reference Center, Fundação Instituto Oswaldo Cruz, Rio de Janeiro, Brazil, by standard slide agglutination using commercially available antisera.

Molecular confirmation and detection of virulence genes

Firstly, genomic DNA was extracted according to the protocol recommended by Green and Sambrook (2012) with minor modifications. The identification of suspect Salmonella isolates at genus level by the detection of hilA gene and the detection of virulence genes (invA, spvC, sefA, and pefA) were performed by Polymerase Chain Reaction (PCR) assays. The oligonucleotides used are shown in the Table S1 in the supplementary material. The reaction mixtures contained 12.5 μL of GoTaq® Green Master Mix 2x (Promega, USA), 1 μL of each primer at a concentration of 10 ρmol, 2 μL of DNA (10 ng), and 8.5 μL of ultra-pure water (Promega, USA) to a total volume of 25 μL. The mixtures were subjected to a thermocycler MJ Research® PTC 100. Salmonella Enteritidis ATCC® 13076 and S. Typhimurium ATCC® 14028 were used as positive controls. Afterwards, the PCR products were subjected to 1.5% (w/v) agarose gel (Invitrogen, USA) electrophoresis at 80 V for 70 min in a 0.5 Tris/Acetate/EDTA buffer (TAE) using a molecular weight marker of 1 Kb (Invitrogen, USA). The amplified products were visualized in an UV transilluminator (Loccus, Brazil).

Antimicrobial susceptibility testing

The antimicrobial susceptibility of the Salmonella spp. isolates was tested by the agar disk diffusion method, according to the Clinical and Laboratory Standards Institute for the Enterobacteriaceae group (CLSI 2017). Twenty one antimicrobials were evaluated: ampicillin 10 μg (AMP), amoxicillin/clavulanic acid 30 μg (AMC), cefoxitin 30 μg (CFO), cefotaxime 30 μg (CTX), cephalothin 30 μg (CFL), imipenem 10 µg (IMP), amikacin 30 μg (AMI), kanamycin 30 μg (K), gentamicin 10 μg (GEN), tobramycin 10 μg (TOB), streptomycin 10 µg (STR), azithromycin 15 µg (AZI), tetracycline 30 μg (TET), minocycline 30 μg (MIN), nalidixic acid 30 μg (NAL), ciprofloxacin 5 μg (CIP), sulfonamide 300 μg (SUL), trimethoprim/sulfamethoxazole 1.25/23.75 μg (SUT), trimethoprim 5 μg (TRI), chloramphenicol 30 μg (CHL), and nitrofurantoin 300 µg (NIT), acquired from Laborclin (Laborclin Produtos para Laboratórios Ltda, Brazil). The strain Escherichia coli ATCC® 25922 was used as positive control.

Determination of minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) of sanitizers

The MIC of benzalkonium chloride (BC) (Sigma-Aldrich, UK), chlorhexidine digluconate (CHL) (Sigma-Aldrich, UK), sodium hypochlorite (SH) (Dinâmica Química Contemporânea, Brazil), and peracetic acid (PA) (Proc9, Brazil) were evaluated using the broth microdilution method in accordance with CLSI guidelines (CLSI 2017). Firstly, isolates S28 and S37 were incubated on TSA at 37 °C for 24 h. After incubation, the isolates were suspended in 0.85% (w/v) saline solution (SS) (Synth, Brazil) to achieve a turbidity equivalent to 0.5 McFarland standard and 10 µL was added with 90 µL Mueller–Hinton broth (MH) (Oxoid, UK) in a microdilution plate, using variable concentrations of the compounds (ranging from 0.5 to 128 µg.mL−1) with incubation at 37 °C for 24 h. The MICs were defined as the lowest concentration that prevented visible growth of the isolates.

The minimum bactericidal concentration (MBC) was evaluated from wells with no visible microbial growth. Aliquots of 100 µL were seeded on Petri dishes containing TSA and incubated at 37 °C for 24 h. The MBC was defined as the lowest concentration at which 99.9% of the initially inoculated cells were killed.

Detection of antimicrobial resistance genes

The isolates that presented antimicrobial resistance in the agar disk diffusion method were evaluated for the presence of resistance genes. The coding resistance genes to macrolides (ereB, ermB, and ermC), aminoglycosides (aadA, aadB, and aac(6′)-Ib) and folate pathway inhibitors (dfrA, and dfrD) were investigated by PCR assays using the oligonucleotides listed in Table S1. The cycling conditions of the PCR assays followed the recommendations of the referenced authors’ studies.

Susceptibility of Salmonella spp. isolates to Butia odorata extract

B. odorata extract preparation

A methanolic extract from B. odorata was prepared according to the method proposed by Shen et al. (2014). The chemical characterization of the methanolic B. odorata extract was described in a previous study (Haubert et al. 2019).

MIC and MBC of B. odorata extract

The MIC and MBC were performed using the broth microdilution method in accordance to CLSI guidelines (CLSI 2017). Previously, the isolates were incubated on TSA at 37 °C for 24 h. After incubation, the isolates were suspended in SS to achieve a turbidity equivalent to 0.5 McFarland standard and 10 µL was added with 100 µL MH in a microdilution plate, using variable concentrations of the compounds (ranging from 2.3 mg.mL−1 to 300 mg.mL−1) with incubation at 37 °C for 24 h. The MICs were defined as the lowest concentration that prevented visible growth of the isolates. The MBC was evaluated and defined as cited above.

Results and discussion

Based on the usual practices in eggs storage in supermarkets as well as in street food markets in Brazil (without refrigeration), we hypothesized that the consumption of eggs is a matter of concern to public health, and there is a risk of human salmonellosis due to the consumption of this food. Thus, raw eggs available at eight establishments (four supermarkets and four street food markets) were evaluated, totalizing 480 eggs. Of 160 samples, just two (1.25%) were positive for Salmonella spp.. One positive sample was from the egg yolk (S. enterica serovar Gallinarum, isolate S28), and another one was from the eggshell (S. enterica serovar Panama, isolate S37). Interestingly, the two positive samples were from supermarkets and not from street food markets, where there is neither sanitary inspection nor quality control.

Different results were found by Kalupahana et al. (2017) that evaluated the occurrence of nontyphoidal Salmonella in retail table eggs in Sri Lanka. Salmonella spp. was isolated from 15 of the 100 retail outlets, being that 12 showed Salmonella spp. in the shell washings and three in the egg contents. The serovars identified were S. Mbandaka, S. Braenderup, S. Corvallis, and S. Emek. On the other hand, Singh et al. (2010) isolated Salmonella spp. in 4.82% of egg samples from India, being S. Typhimurium the prevalent serovar. However, the data observed in this study are of concern because, despite the low contamination of Salmonella spp. found in the eggs, raw eggs are ingredients used in many dishes, therefore, can generate a high number of infections by this microorganism (Ethelberg et al. 2014).

In this study, S. Gallinarum was isolated from yolk. Salmonella spp. can colonize reproductive organs of the poultries, and can contaminate the egg during its formation, occurring, therefore, vertical contamination of the yolk (Gantois et al. 2009; Martelli and Davies 2012; Poppe et al. 1998). It is interesting to highlight that some Salmonella serovars are almost exclusively related to one particular host species, such as S. Gallinarum with poultry (Uzzau et al. 2000).

Salmonella Panama was isolated from eggshell. Eggs can also be contaminated by horizontal transmission, where Salmonella spp. reaches the eggshell from the colonized gut or from contaminated feces during or after eggs laying. Besides that, after laying into the contaminated environment, the outer shell surface can also be contaminated (Gantois et al. 2009). Additionally, the presence of Salmonella spp. in eggshells can cross-contaminate food surfaces and other food. From our point of view, it is the first report of S. Panama in eggshell in Brazil, and it demonstrates the environmental contamination even in eggs subjected to sanitary inspection.

Regarding the virulence genes, S. Panama (S37) harbored all the genes evaluated (hilA, invA, spvC, sefA, and pefA), while S. Gallinarum (S28) did not harbor the pefA gene (Table 1). This result is in accordance with the literature, which reports that this serovar does not carry the pef locus, contained in a plasmid that encodes for fimbriae (Rychlik et al. 2006). On the other hand, the sefA gene, identified in both isolates, is located in the chromosome and encode for structural subunit of SEF14 fimbriae (Clouthier et al. 1993).

Table 1.

Characteristics of the Salmonella spp. isolates of this study

Isolate ID Source Isolation date Serovar Virulence genes Antimicrobial resistancea Sanitizers resistanceb MIC of BEc(mg.mL−1) MBC of BEd(mg.mL−1)
S28 Egg yolk 2013.03.19 Gallinarum hilA, invA, sefA,spvC TOB-AZI-TRI BC-CHL- SH-PE 37.5 150
S37 Eggshell 2013.04.22 Panama hilA,invA, sefA,spvC, pefA NAL BC-CHL- SH-PE 37.5 37.5
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TOB tobramycin, AZI azithromycin, TRI trimethoprim, NAL nalidixic acid, BC benzalkonium chloride, CHL chlorhexidine digluconate, SH sodium hypochlorite, PA peracetic acid, MIC of BE Minimum inhibitory concentration of Butia odorata extract, MBC of BE Minimum bactericidal concentration of Butia odorata extract

The hilA gene is related to cell invasion (Cardona-Castro et al. 2002) as well as the invA gene (Swamy et al. 1996). Already the spv (Salmonella plasmid virulence) genes are involved in intra-macrophage survival of Salmonella (Rychlik et al. 2006), spvC is one of the central effectors of spvRABCD operon (Matsui et al. 2001).

The antimicrobial susceptibility testing of the two isolates showed a low level of resistance to the 21 antimicrobials evaluated. However, the isolate S28 was resistant to tobramycin, azithromycin and trimethoprim, while the isolate S37 revealed resistance profile to nalidixic acid only (Table 1). The aminoglycoside resistance rates in Salmonella spp. isolates from poultry and eggs varies according to studies. Cortes et al. (2017), for example, detected 100% of resistance to amikacin, gentamicin and tobramycin in Salmonella spp. isolates from broiler carcasses. Singh et al. (2010) found 66.7% of resistance to trimethoprim in Salmonella spp. isolates from eggs of wholesale markets, whereas the resistance profile in isolates from eggs of poultry farms and retail markets, for the same antimicrobial, was 0 and 9.9%, respectively, showing differences in resistance profile according to the origin of the samples. The resistance profile to azithromycin obtained in this study is relevant given that this antimicrobial is recommended for the therapeutic conduct of invasive salmonellosis (Sjolund-Karlsson et al. 2011). Therefore, more epidemiologic studies are necessary in this region to unravel this point.

A high prevalence of resistance to nalidixic acid (47%) was observed in the study of Fardsanei et al. (2017) in Salmonella spp. isolates from poultry meats and eggs in Iran. Resistance profile to nalidixic acid occurs due to the extensive usage of quinolones in veterinary medicine, given that the use of these compounds can select for mutant Salmonella strains resistant to nalidixic acid or with reduced susceptibility to fluoroquinolones class, such as ciprofloxacin (Rowlands et al. 2014).

High MIC values to sanitizers were detected in the present study, with the isolate S28 presenting MIC values of 64, 128, > 128 and > 128 μg.mL−1 for BC, CHL, SH, and PA, respectively. In the same way, the isolate S37 presented MIC of 64 μg.mL−1 for BC, and MIC > 128 μg.mL−1 for the others sanitizers. The MBC values found for the isolate S28 were 64 and 128 μg.mL−1 for BC and CHL, respectively, while isolate S37 showed MBC of 64 μg.mL−1 for BC, the same MIC value. Although resistance profile has been observed to all compounds evaluated, BC was the most effective sanitizer for these isolates in view of the lowest value of the MIC and MBC. Long et al. (2016) found similar results to those obtained in this study for BC, where MIC values ranged from 64 to 128 μg.mL−1, and for CHL, the values ranged from 32 to 64 μg.mL−1 in Salmonella spp. isolates from chicken and egg production chains. These results showed that the continuous contact of Salmonella spp. isolates to sanitizers in the chain production or even in the environment can be the cause of the high MIC values found. It is noteworthy that SH sanitizer is widely used in the washing process of eggs in Brazil and both isolates showed high resistance to this compound.

The antimicrobial resistance genes ereB, ermB, ermC, aadA, aadB, aac(6′)-Ib, dfrA, and dfrD were not identified in the isolates evaluated in this study. This suggests that other mechanisms or other resistance genes can contribute to antimicrobial resistance phenotypes in these isolates (Haubert et al. 2019). Point mutations in some constitutive genes, such as gyrA and parC, confer resistance to quinolones and can be responsible to express the resistance phenotype for nalidixic acid (Zhu et al. 2017). Moreover, integrons on plasmids can be involved in the resistance profiling to macrolides, aminoglycosides, and inhibitors of folate synthesis in Salmonella spp. isolates (Zhu et al. 2017).

The B. odorata extract revealed antimicrobial activity against the two Salmonella isolates, showing the MIC value of 37.5 mg.mL−1. In another study, Haubert et al. (2019) evaluated B. odorata extract against Salmonella isolates from food and food environments and found MIC values ranging from 10 to 19 mg.mL−1 for most isolates evaluated. Although the MIC values obtained in the present study are higher, the B. odorata extract presented antibacterial potential against the Salmonella isolates. The MBC value was 150 and 37.5 mg.mL−1 for isolates S28 and S37, respectively (Table 1). It is noteworthy that for isolate S37, the MIC and MBC was the same, therefore, needing a lower concentration of the compound to inhibit this isolate. These findings point out that this plant extract could be an effective strategy to inhibit the growth of Salmonella spp. isolates from eggs, with potential to be used as an alternative to common sanitizers used in the food industry.

Conclusion

In conclusion, out of the 160 egg samples evaluated, two were positive for Salmonella spp., indicating a potential hazard to public health. The serovars identified were S. Gallinarum and S. Panama and were isolated, respectively, from yolk and eggshell of purchased eggs from supermarkets in southern Brazil. Despite the low antimicrobial resistance profiling, the isolates were resistant to sanitizers evaluated and harbored important virulence genes, being able to cause salmonellosis in the consumers. In this way, the guarantee of microbiological security of raw eggs through application of proper food safety regulations is required to ensure consumer safety. Moreover, Butia odorata extract showed antimicrobial activity against Salmonella spp. isolates from eggs, and may be a new strategy to prevent this relevant foodborne pathogen.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 23 kb) (23.1KB, docx)

Acknowledgements

The authors thanks to the Laboratório de Enterobactérias—Fundação Instituto Oswaldo Cruz (FIOCRUZ) for serotyping Salmonella spp. isolates.

Funding

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001, Programa Nacional de Pós-Doutorado (PNPD), Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS), and by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (306367/2019-0).

Footnotes

Publisher's Note

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Contributor Information

Louise Haubert, Email: louisehaubert@hotmail.com.

Darla Silveira Volcan Maia, Email: darlavolcan@yahoo.com.br.

Simone de Fátima Rauber Würfel, Email: simone_rauber@hotmail.com.

Cristiane Vaniel, Email: cristianevaniel@yahoo.com.br.

Wladimir Padilha da Silva, Email: silvawp@ufpel.edu.br.

References

  1. Anjum MF, Choudhary S, Morrison V, Snow LC, Mafura M, Slickers P, Ehricht R, Woodward MJ. Identifying antimicrobial resistance genes of human clinical relevance within Salmonella isolated from food animals in Great Britain. J Antimicrob Chem. 2011;66(3):550–559. doi: 10.1093/jac/dkq498. [DOI] [PubMed] [Google Scholar]
  2. Arshad MM, Wilkins MJ, Downes FP, Rahbar MH, Erskine RJ, Boulton ML, Younnus M, Saeed AM. Epidemiologic attributes of invasive non-typhoidal Salmonella infections in Michigan, 1995–2001. Int J Infec Dis. 1995;12:176–182. doi: 10.1016/j.ijid.2007.06.006. [DOI] [PubMed] [Google Scholar]
  3. Besser JM. Salmonella epidemiology: a whirlwind of change. Food Microbiol. 2018;71:55–59. doi: 10.1016/j.fm.2017.08.018. [DOI] [PubMed] [Google Scholar]
  4. Brasil. Surtos de Doenças Transmitidas por Alimentos no Brasil (2018) Available at: http://www.saude.gov.br/images/pdf/2018/julho/02/Apresentacao-Surtos-DTA-Junho-2018.pdf. Accessed 26 August 2019.
  5. Campioni F, Bergamini AMM, Falcão JP. Genetic diversity, virulence genes and antimicrobial resistance of Salmonella Enteritidis isolated from food and humans over a 24-year period in Brazil. Food Microbiol. 2012;32:254–264. doi: 10.1016/j.fm.2012.06.008. [DOI] [PubMed] [Google Scholar]
  6. Cardona-Castro N, Restrepo-Pineda E, Correa-Ochoa M. Detection of hilA Gene sequences in Serovars of Salmonella enterica subspecies Enterica. Mem Inst Osw Cruz. 2002;97(8):1153–1156. doi: 10.1590/S0074-02762002000800016. [DOI] [PubMed] [Google Scholar]
  7. Clouthier SC, Müller K-H, Doran JL, Collinson SK, Kay WW. Characterization of three fimbrial genes, sefABC, of Salmonella enteritidis. J Bact. 1993;175(9):2523–2533. doi: 10.1128/jb.175.9.2523-2533.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. CLSI (Clinical and Laboratory Standards Institute), (2017) Performance standards for antimicrobial susceptibility testing; twenty-seven informational supplement, CLSI document M100–S25. PA, USA
  9. Cortes VD, Rodriguez V, Verjan GN. Phenotypic and Genotypic Antibiotic Resistance of Salmonella from Chicken Carcasses Marketed at Ibague. Colombia Braz J Poul Sci. 2017;19(2):347–354. doi: 10.1590/1806-9061-2016-0405. [DOI] [Google Scholar]
  10. EFSA (European Food Safety Authority) (2018) Salmonella, 2018. Available at: http://www.efsa.europa.eu/en/topics/topic/salmonella. Accessed 12 september 2018.
  11. Ethelberg S, Mølbak K, Josefsen MH. Bacteria: Salmonella Non-Typhi. Encyc Food Saf. 2014;1:501–514. doi: 10.1016/B978-0-12-378612-8.00112-8. [DOI] [Google Scholar]
  12. Fardsanei F, Soltan Dallal MM, Douraghi M, Salehi TZ, Mahmoodi M, Memariani H, Nikkhahi F. Genetic diversity and virulence genes of Salmonella enterica subspecies enterica serotype Enteritidis isolated from meats and eggs. Microb Pathog. 2017;107:451–456. doi: 10.1016/j.micpath.2017.04.026. [DOI] [PubMed] [Google Scholar]
  13. Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Gast R, Humphrey TJ, Immerseel FV. Mechanisms of egg contamination by Salmonella Enteritidis. FEMS Microbiol Rev. 2009;33:718–738. doi: 10.1111/j.1574-6976.2008.00161.x. [DOI] [PubMed] [Google Scholar]
  14. Grape M, Sundström L, Kronvall G. Sulphonamide resistance gene sul3 found in Escherichia coli isolates from human sources. J Antimicrob Chemot. 2003;52(6):1022–1024. doi: 10.1093/jac/dkg473. [DOI] [PubMed] [Google Scholar]
  15. Green MR, Sambrook J. Molecular Cloning: A Laboratory Manual. 4. New York: Cold Spring Harbor Laboratory Press; 2012. [Google Scholar]
  16. Haubert L, Zehetmeyr ML, Pereira YMN, Kroning IS, Maia DSV, Sehn CP, Lopes GV, Lima AS, Silva WP. Tolerance to benzalkonium chloride and antimicrobial activity of Butia odorata Barb. Rodr. extract in Salmonella spp. isolates from food and food environments. Food Res Int. 2019;116:652–659. doi: 10.1016/j.foodres.2018.08.092. [DOI] [PubMed] [Google Scholar]
  17. Kalupahana RS, Rajapaksa DIG, Fernando PS, Thilakarathne DS, Abeynayake P. Occurrence and characterization of nontyphoidal Salmonella in retail table eggs in Kandy district of Sri Lanka. Food Cont. 2017;72:244–248. doi: 10.1016/j.foodcont.2016.04.024. [DOI] [Google Scholar]
  18. Kehrenberg C, Schwarz S. Occurrence and linkage of genes coding for resistance to sulfonamides, streptomycin and chloramphenicol in bacteria of the genera Pasteurella and Mannheimia. FEMS Microbiol Lett. 2001;205(2):283–290. doi: 10.1111/j.1574-6968.2001.tb10962.x. [DOI] [PubMed] [Google Scholar]
  19. Kerrn MB, Klemmensen T, Frimodt-Moller N, Espersen F. Susceptibility of Danish Escherichia coli strains isolated from urinary tract infections and bacteraemia, and distribution of sul genes conferring sulphonamide resistance. J Antimicr Chemot. 2002;50:513–516. doi: 10.1093/jac/dkf164. [DOI] [PubMed] [Google Scholar]
  20. Kikuvi GM, Schwarz S, Ombui JN, Mitema ES, Kehrenberg C. Streptomycin and chloramphenicol resistance genes in Escherichia coli isolates from cattle, pigs, and chicken in Kenya. Microb Drug Resist. 2007;13(1):62–68. doi: 10.1089/mdr.2006.9998. [DOI] [PubMed] [Google Scholar]
  21. Long M, Lai H, Deng W, Zhou K, Li B, Liu S, Fan L, Wang H, Zou L. Disinfectant susceptibility of different Salmonella serotypes isolated from chicken and egg production chains. J App Microbiol. 2016;121(3):672–681. doi: 10.1111/jam.13184. [DOI] [PubMed] [Google Scholar]
  22. Maia DSV, Aranha BC, Chaves FC, Silva WP. Antibacterial activity of Butia odorata Barb. Rodr extracts Trends Phyto Res. 2017;1(3):169–174. [Google Scholar]
  23. Martelli F, Davies RH. Salmonella serovars isolated from table eggs: an overview. Food Res Int. 2012;45:745–754. doi: 10.1016/j.foodres.2011.03.054. [DOI] [Google Scholar]
  24. Martineau F, Picard FJ, Grenier L, Roy PH, Ouellette M, Trial E, Bergeron MG. Multiplex PCR assays for the detection of clinically relevant antibiotic resistance genes in staphylococci isolated from patients infected after cardiac surgery. J Antimicr Chemot. 2000;46:527–533. doi: 10.1093/jac/46.4.527. [DOI] [PubMed] [Google Scholar]
  25. Matsui H, Bacot CM, Garlington WA, Doyle TJ, Roberts S, Gulig PA. Virulence Plasmid-Borne spvB and spvC Genes Can Replace the 90-Kilobase Plasmid in Conferring Virulence to Salmonella enterica Serovar Typhimurium in Subcutaneously Inoculated Mice. J Bac. 2001;183(15):4652–4658. doi: 10.1128/JB.183.15.4652-4658.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Poppe C, Duncan CL, Mazzocco A. Salmonella Contamination of Hatching and Table Eggs: a Comparison. Can J Vet Res. 1998;62:91–198. [PMC free article] [PubMed] [Google Scholar]
  27. Rychlik I, Gregorova D, Hradecka H. Distribution and function of plasmids in Salmonella enterica. Vet Microbiol. 2006;112:1–10. doi: 10.1016/j.vetmic.2005.10.030. [DOI] [PubMed] [Google Scholar]
  28. Singh S, Yadav AS, Singh SM, Bharti P. Prevalence of Salmonella in chicken eggs collected from poultry farms and marketing channels and their antimicrobial resistance. Food Res Int. 2010;43:2027–2030. doi: 10.1016/j.foodres.2010.06.001. [DOI] [Google Scholar]
  29. Rowlands REG, Ristori CA, Ikuno AA, Barbosa ML, Jakabi M, Franco BDGM. Prevalence of drug resistance and virulence features in Salmonella spp. isolated from foods associated or not with salmonellosis in Brazil. Rev Inst Med Trop São Paulo. 2014;56(6):461–467. doi: 10.1590/S0036-46652014000600001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shen X, Sun X, Xie Q, Liu H, Zhao Y, Pan Y, Hwang C, Wu VCH. Antimicrobial effect of blueberry (Vaccinium corymbosum L.) extracts against the growth of Listeria monocytogenes and Salmonella Enteritidis. Food Cont. 2014;35(1):159–165. doi: 10.1016/j.foodcont.2013.06.040. [DOI] [Google Scholar]
  31. Sjolund-Karlsson M, Joyce K, Blickenstaff K, Ball T, Haro J, Medalla FM, Fedorka-Cray P, Zhao S, Crump JA, Whichard JM. Antimicrobial susceptibility to azithromycin among Salmonella enterica Isolates from the United States. Antimicrob Agents Chemot. 2011;55(9):3985–3989. doi: 10.1128/AAC.00590-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Thames CH, Pruden A, James RE, Ray PP, Knowlton KF. Excretion of antibiotic resistance genes by dairy calves fed milk replacers with varying doses of antibiotics. Front Microbiol. 2012;3:1–12. doi: 10.3389/fmicb.2012.00139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Uzzau S, Brown DJ, Wallis T, Rubino S, Leori G, Bernard S, Casadesus J, Platt DJ, Olsen JE. Host adapted serotypes of Salmonella enterica. Epidemiol Infect. 2000;125:229–255. doi: 10.1017/S0950268899004379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Weerakkody NS, Caffin N, Turner MS, Dykes GA. In vitro antimicrobial activity of less-utilized spice and herb extracts against selected food-borne bacteria. Food Control. 2010;21(10):1408–1414. doi: 10.1016/j.foodcont.2010.04.014. [DOI] [Google Scholar]
  35. Zhu Y, Lai H, Zou L, Yin S, Wang C, Han X, Xia X, Hu K, He L, Zhou K, Chen S, Ao X, Liu S. Antimicrobial resistance and resistance genes in Salmonella strains isolated from broiler chickens along the slaughtering process in China. Int J Food Microbiol. 2017;259:43–51. doi: 10.1016/j.ijfoodmicro.2017.07.023. [DOI] [PubMed] [Google Scholar]

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