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Abdelaziz Ed-Dra Team of Microbiology and Health, Laboratory of Chemistry-Biology Applied to the Environment, Moulay Ismail University Faculty of Sciences, BP. 11201 Zitoune Meknes, Morocco

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Fouzia Rhazi Filali Team of Microbiology and Health, Laboratory of Chemistry-Biology Applied to the Environment, Moulay Ismail University Faculty of Sciences, BP. 11201 Zitoune Meknes, Morocco

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Slimane Khayi Biotechnology Research Unit, National Institute for Agronomic Research (INRA), BP. 415, Avenue de la Victoire, Rabat, Morocco

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Said Oulghazi Cellular Genomics and Molecular Techniques of Investigations, Moulay Ismail University Faculty of Sciences, BP. 11201 Zitoune Meknes, Morocco

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Brahim Bouchrif Laboratory of Microbiology and Hygiene of Food and Water, Pasteur Institute Morocco, 1 place Louis Pasteur, Casablanca 20100, Morocco

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Abdellah El Allaoui Team of Microbiology and Health, Laboratory of Chemistry-Biology Applied to the Environment, Moulay Ismail University Faculty of Sciences, BP. 11201 Zitoune Meknes, Morocco

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Bouchra Ouhmidou Laboratory of Bioactive Molecules, Structures and Functions, Faculty of Sciences and Technologies, Sidi Mohamed Ben Abdallah University, Fes, Morocco

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Mohieddine Moumni Cellular Genomics and Molecular Techniques of Investigations, Moulay Ismail University Faculty of Sciences, BP. 11201 Zitoune Meknes, Morocco

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Salmonella is a major cause of morbidity and mortality in humans worldwide, and the infection with multidrug-resistant strains can cause severe diseases. This study was designed to evaluate the antimicrobial resistance, to detect the virulence genes, and to study the genetic diversity of isolated Salmonella strains using 16S rRNA sequences. For this, 34 Salmonella strains isolated from sausages were identified using biochemical and serological methods. Molecular tools were used to evaluate the presence of virulence genes (orgA, sitC, sipB, spiA, iroN, and sifA) using simplex and multiplex polymerase chain reaction (PCR) and to sequence 16S rRNA genes for phylogenetic analysis. The susceptibility to 24 selected antibiotics was also studied. The results of this study showed that all isolated Salmonella were positive for targeted virulence genes and were resistant to at least one antibiotic. However, the multidrug resistance was observed in 44% of isolated strains. The phylogenetic analysis of 16S rRNA sequences highlighted that Salmonella isolates were divided into 3 clusters and 3 sub-clusters, with a ≥98% similarity to Salmonella enterica species. From this study, we conclude that sausages are considered as a potential source of Salmonella, which could be a major risk to public health.

Abstract

Salmonella is a major cause of morbidity and mortality in humans worldwide, and the infection with multidrug-resistant strains can cause severe diseases. This study was designed to evaluate the antimicrobial resistance, to detect the virulence genes, and to study the genetic diversity of isolated Salmonella strains using 16S rRNA sequences. For this, 34 Salmonella strains isolated from sausages were identified using biochemical and serological methods. Molecular tools were used to evaluate the presence of virulence genes (orgA, sitC, sipB, spiA, iroN, and sifA) using simplex and multiplex polymerase chain reaction (PCR) and to sequence 16S rRNA genes for phylogenetic analysis. The susceptibility to 24 selected antibiotics was also studied. The results of this study showed that all isolated Salmonella were positive for targeted virulence genes and were resistant to at least one antibiotic. However, the multidrug resistance was observed in 44% of isolated strains. The phylogenetic analysis of 16S rRNA sequences highlighted that Salmonella isolates were divided into 3 clusters and 3 sub-clusters, with a ≥98% similarity to Salmonella enterica species. From this study, we conclude that sausages are considered as a potential source of Salmonella, which could be a major risk to public health.

Introduction

Salmonella species were discovered more than a century ago by Salmon, an American scientist. They are Gram-negative, motile, facultative anaerobic bacteria and classified within the Enterobacteriaceae family [1]. Salmonella are regarded as a major food-borne pathogen that causes an economic burden for health care systems worldwide [2]. The consumption of animal products contaminated with Salmonella is the leading cause of human Salmonellosis [3]. Globally, 94 million cases of gastroenteritis were caused by Salmonella with 155,000 deaths each year, knowing that 85% of them were related to food [4]. In the United States, a study estimated that nontyphoidal Salmonella were responsible for 1,027,000 cases of food-borne illness each year, with 19,586 hospitalizations and 378 deaths [5]. In Morocco, Salmonella are responsible for 42.8% of food-borne diseases [6].

The pathogenicity of Salmonella is influenced by a variety of virulence factors that play an important role in a wide range of pathogenic mechanisms, such as adhesion, invasion, intracellular survival, toxin production, and iron acquisition [7]. However, the presence of virulence genes in multidrug-resistant strains of Salmonella is associated with a severe infection and is a major public health concern [8].

The identification of Salmonella is subjected to various constraints due to the greater diversity of its species and serovars. The Salmonella genus contains two species, Salmonella bongori and Salmonella enterica, which is divided into six subspecies with the presence of more than 2600 serotypes [9]. Nowadays, it is agreed that the identification of Salmonella by biochemical and serological techniques requires about a week [10]. Hence, molecular methods based on DNA sequences represent the best alternatives for accurate and rapid bacterial identifications.

In the last years, the use of DNA sequencing has increased in the determination of the evolutionary relationships of different bacteria [11, 12]. In relation to Salmonella, phylogenetic studies includes sequencing of 16S rRNA, 23S rRNA, housekeeping genes, virulence genes, and inv-spa invasion gene complex [12]. It has been shown that genetic analysis of 16S rRNA gene increases the resolution between genus and species of Salmonella enterica and has a major role in bacterial phylogeny and taxonomic studies [13].

In Africa, specifically in Morocco, we noticed a lack of information for Salmonella pathogenicity and molecular identification. Thus, in this context, the objectives of this study were (i) to analyze the 16S rRNA sequences of 34 Salmonella strains isolated from sausages and determine their phylogenetic relationship, (ii) to study the distribution of 6 virulence genes among the isolated strains, and (iii) to assess their antimicrobial resistance using 26 antibiotics.

Materials and Methods

Isolation, Identification and Antimicrobial Susceptibility Testing

Thirty four Salmonella enterica belonging to 12 serotypes were isolated from sausages (beef sausages, turkey sausages, and artisanal sausages “merguez”) sold in Meknes city in Morocco and confirmed by biochemical, serological, and molecular tests [10]. The disc diffusion method on Mueller–Hinton agar was used to study the antimicrobial susceptibility profiles of isolated Salmonella against 26 antibiotics (Table 1). Results were interpreted according to the recommendation of the Clinical and Laboratory Standards Institute [14]. E. coli ATCC 25922 was used as a positive control of this study, and the isolated Salmonella strains showing a decrease in susceptibility (intermediate) were considered as resistant.

Table 1.

The antimicrobial agents used in this study

Antimicrobial agents Code Disk Content
Ampicillin AMP 10 µg
Amoxicillin AML 25 µg
Amoxicillin–clavulanic acid AMC 20 µg/10 µg
Imipenem IPM 10 µg
Ceftriaxone CRO 30 µg
Cefuroxime sodium CXM 30 µg
Ceftazidime CAZ 30 µg
Cefamandole MA 30 µg
Cefotaxime CTX 30 µg
Cefoxitin FOX 30 µg
Aztreonam ATM 30 µg
Sulfamethoxazole SMX 200 µg
Amikacin AK 30 µg
Colistin sulfate CT 50 µg
Kanamycin K 30 µg
Ofloxacin OFX 5 µg
Enrofloxacin ENR 5 µg
Ciprofloxacin CIP 5 µg
Nalidixic acid NA 30 µg
Flumequine UB 30 µg
Sulfonamide SSS 200 µg
Gentamicin CN 30 µg
Chloramphenicol C 30 µg
Tetracycline TE 30 µg
Streptomycin S 10 µg
Trimethoprim–sulfamethoxazole SXT 1.25 µg/23.75 µg

Amplification of the Virulence Genes Using Multiplex Polymerase Chain Reaction (PCR)

Simplex and multiplex PCR methods were used to examine the presence of 6 virulence genes in the isolated Salmonella (Table 2), using their gene specific primers as described in Table 3. The simplex PCR method was used to amplify the genes spiA, iroN, and sifA as described previously by Mezal et al. [15]. Meanwhile, the multiplex PCR method was used to amplify the genes orgA, sipB, and sitC as described by Skyberg et al. [7]. The amplification was done in a Mastercycler gradient (Perkin-Elmer, Boston, MA) under the following conditions: 5 min at 95 °C, 30 cycles of 30 s at 94 °C, 30 s at 66.5°C, and 2 min at 72 °C, with a final cycle of 10 min at 72 °C. The isolated strains were considered positive for the tested virulence genes if they produce an amplicon with the expected size (Table 3). Salmonella enterica serovar typhimurium DT104 was used as positive control.

Table 2.

Description of genes functions used in this study

Genes Virulence-related function References
orgA Host recognition/invasion [35]
sipB Entry into nonphagocytic cells, killing of macrophages [36]
sitC Iron acquisition [37]
spiA Survival within macrophage [30]
iroN Iron acquisition [27]
sifA Filamentous structure formation [29]
Table 3.

Primers sequences used to amplify the virulence genes of isolated Salmonella

Virulence genes Primer sequence (5′-3′)a Size (bp) GenBank no. References
orgA F: TTTTTGGCAATGCATCAGGGA

R: GGCGAAAGCGGGGACGGTATT
255 NC003197 [7]
sitC F: CAGTATATGCTCAACGCGATGTGGGTCTCC

R: CGGGGCGAAAATAAAGGCTGTGATGAAC
768 NC003197 [7]
sipB F: GGACGCCGCCCGGGAAAAACTCTC

R: ACACTCCCGTCGCCGCCTTCACAA
875 NC003197 [7]
spiA F: CCAGGGGTCGTTAGTGTATTGCGTGAGATG

R: CGCGTAACAAAGAACCCGTAGTGATGGATT
550 NC003197 [7]
iroN F: ACTGGCACGGCTCGCTGTCGCTCTAT

R: CGCTTTACCGCCGTTCTGCCACTGC
1205 NC003197 [7]
sifA F: TTTGCCGAACGCGCCCCCACACG

R: GTTGCCTTTTCTTGCGCTTTCCACCCATCT
449 NC003197 [7]

F = forward; R = reverse.

Amplification and Sequencing of the 16S rRNA Genes

DNA was extracted from a culture on liquid medium using DNA Isolation Kit (Gen Elute Bacterial Genomic DNA kit, Sigma) according to the manufacturer's instructions. The amplification of 16S rRNA gene was performed in a reaction mixture of 25 µL, with 12.5 µL of ddH2O, 2.5 µL of 10x PCR buffer, 3.0 µL of 50 mM MgCl2, 0.5 µL of 10 mM dNTPs (KAPA Biosystems, USA), 2 µL of template DNA (70 ng/µL), 0.2 µL of Taq DNA polymerase enzyme (5 U/µL; KAPA Biosystems, USA), and 1.25 µL of 10 µM from each primer: fD1 (AGAGTTTGATCCTGGCTCAG) and rP2 (ACGGCTACCTTGTTACGACTT) [16]. The amplification was performed in “Veriti” thermal cycler (Applied Biosystems, USA) under the following conditions: 10 min at 94 °C, 36 cycles of 1 min at 94 °C, 30 s at 52 °C, 2 min at 72 °C, and a final cycle of 10 min at 72 °C. Electrophoresis migration was done in 1% agarose (Sigma) for 1 h at 100 V. Then, gel was stained in ethidium bromide with a concentration of 0 .5 µg/mL for 20 min, rinsed, and visualized using «G Box» system (Applied Biosystems, USA).

The obtained PCR products were purified by QIAquick PCR purification kit (ExoSAP-IT Affymetrix, USA), and sequenced bi-directionally using Big Dye Terminator Kit version 3.1 (Applied Biosystems) to prepare sequencing reactions. The sequencing procedure was conducted by 3130 XL Genetic Analyzer according to the manufacturer's instructions (Applied Biosystems, USA). Then, the collected data were analyzed by data collection software version 3.0 and sequencing analysis software version 5.3.1 (Applied Biosystems, USA). The sequences were manually trimmed and analyzed with the Basic Local Alignment Search Tool (BLAST).

Phylogenetic Analysis

The sequences were aligned with ClustalW, the evolutionary history was inferred using the neighbor-joining method, and the evolutionary distances were computed using the maximum composite likelihood method (Mega7 software) with 1000 bootstrap replications. Salmonella enterica str. 08-00436, Salmonella Mbandaka str. SA20026234, Salmonella Agona str. 460004 2-1, and Salmonella Typhi str. CT18 were used as in-group strains, and Escherichia coli ATCC 8739 was used as an out-group strain to root the phylogenetic tree.

Ethics

Ethical approval was not required in this study since no live animals or humans samples were used in the experiments.

Results

Isolation, Identification and Antimicrobial Susceptibility Testing

Among the 34 isolated Salmonella, 12 serotypes were identified (Table 4). In addition, the antimicrobial resistance analysis has shown a high rate of resistance to several antibiotics, with presence of 13 different phenotypic profiles (Table 4). Moreover, multidrug resistance (more than two antibiotics) was detected in 15 strains (44%). From them, one Salmonella typhimurium strain was considered as the highest by exerting resistance against 18 different antimicrobial compounds (Table 4).

Table 4.

Virulence genes and antimicrobial resistance profile of Salmonella serovars isolated from sausages

Code Serotypes Accession Number Resistant profiles Virulence genes
orgA sipB sitC spiA iroN sifA
8D Agona KX355299 AMP + + + + + +
63 D Muenster KX355305 AMP + + + + + +
55 MA Livingstone KX355303 AMP + + + + + +
57 B Anatum KX355304 AMP, S, CT + + + + + +
3MA Give KX355298 AMP, S + + + + + +
42MA Give MG869141 AMP, S + + + + + +
58MA Give MG869142 AMP, S + + + + + +
29MA Give MG869140 AMP, S + + + + + +
2B Bovismorbificans KX355297 AMP, S + + + + + +
12B Bovismorbificans MG869128 AMP, S + + + + + +
51B Mbandaka MG869131 AMP + + + + + +
31B Mbandaka MG869129 AMP + + + + + +
80B Mbandaka KX355306 AMP, S, CT + + + + + +
9MA Mbandaka MG869136 AMP, S, CT + + + + + +
17D Montevideo KX355301 AMP, S, CT + + + + + +
108D Montevideo MG869146 AMP, S, CT + + + + + +
72D Montevideo MG869143 AMP, S, CT + + + + + +
100MA Corvallis MG869133 AMP, S + + + + + +
97MA Corvallis KX355307 AMP, S + + + + + +
25B Corvallis MG869139 AMP, S + + + + + +
95D Corvallis MG869134 AMP, S + + + + + +
94MA Corvallis MG869144 AMP, CT + + + + + +
18B Corvallis MG869137 AMP, CT + + + + + +
19MA Corvallis MG869138 AMP, AML, SMX, SSS + + + + + +
113MA Corvallis KX355309 AMP, S, AML, CXM, + + + + + +
130 D Saintpaul KX355311 AMP, S, CT, SMX, SSS, SXT + + + + + +
104D Kentucky MG869145 AMP, S + + + + + +
143D Kentucky MG869135 AMP, S + + + + + +
30D Kentucky KX355302 AMP, S, TE, ENR, OFX, CIP, NA, UB + + + + + +
116B Kentucky KX355310 AMP, AML, MA, SMX, NA, ENR, UB, OFX, CIP, TE, S, SSS + + + + + +
1D Kentucky MG869130 AMP, AML, AMC, SMX, NA, ENR, UB, OFX, CIP, TE, S, SSS + + + + + +
14D Kentucky KX355300 AMP, AML, AMC, MA, SMX, NA, ENR, UB, OFX, CIP, TE, S, SSS + + + + + +
102D Typhimurium MG869132 AMP, AML, AMC, CRO, MA, CXM, CTX, SXT, SMX, K, AK, CT, TE, S, C, SSS + + + + + +
105D Typhimurium KX355308 AMP, AML, AMC, CRO, MA, CXM, CTX, SXT, SMX, NA, UB, K, AK, CT, TE, S, C, SSS + + + + + +

Amplification of Virulence Genes Using Multiplex PCR

In order to evaluate the pathogenicity of Salmonella strains and to have an idea about its capacity to survive in host environments, simplex and multiplex PCR methods were used to detect 6 virulence genes, namely, orgA, sipB, sitC, spiA, iroN, and sifA (Figures 1 and 2), involved in its virulence system. The results showed that all isolated strains contain the 6 virulence genes (Table 4).

Figure 1.
Figure 1.

PCR products amplified with the universal virulence gene primers (orgA, sipB, and sitC). Lanes: (M) DNA ladder (GeneRuler 1Kb Plus), (1) negative control, (2) positive control, and (3–12) Salmonella tested.

Citation: European Journal of Microbiology and Immunology EuJMI 9, 2; 10.1556/1886.2018.00035

Amplification and Sequencing of the 16S rRNA Genes

Amplification of 16S rRNA genes was performed on extracted genomic DNA of isolated Salmonella strains. The results showed that all examined strains generate an amplicon of 1500 bp (Figure 3). Then, PCR products were sequenced and analyzed by the online software “BLAST” (https://blast.ncbi.nlm.nih.gov/Blast.cgi?PAGE_TYPE=BlastSearch), and the obtained sequences were deposited in GenBank under the corresponding accession numbers (Table 4).

Figure 3.
Figure 3.

The amplification results of 16S rRNA genes using universal primers. Lanes: (1) S. Typhimirium, (2) S. Mbandaka, (3) S. Livingstone, (4), S. Muenster, (5) S. Give, (6) S. Bovismorbificans, (7–9) S. Kentucky, (10–11) S. Corvallis, (12) S. Montevideo, (13) S. Agona, (14) S. Anatum, (15) S. Saintpaul, and (M) 1Kb DNA ladder

Citation: European Journal of Microbiology and Immunology EuJMI 9, 2; 10.1556/1886.2018.00035

Phylogenetic Analysis and Identification Criteria

The phylogenetic analysis of 16S rRNA genes organized all the strains into 3 clusters (I, II, and III), and cluster I is divided into 3 sub-clusters (Ia, Ib, and Ic) (Figure 4). The analysis of 16S rRNA genes groups the serotypes Corvallis, Kentucky, Typhimurium, Anatum, Mbandaka, Livingstone, and Saintpau in cluster I, and cluster II is constituted by S. Montevideo, S. Bovismorbificans, S. Give, and S. Agona. However, cluster III is constituted by 2 strains, namely, S. Muenster and S. Kentucky, which are placed separately on side branches from the strains. Moreover, 16S rRNA based analysis showed that all 16S rRNA sequences possessed a ≥98% similarity to those of Salmonella enterica species.

Figure 4.
Figure 4.

Phylogenetic tree of isolated Salmonella enterica strains based on 16S rRNA sequences analysis using MEGA7

Citation: European Journal of Microbiology and Immunology EuJMI 9, 2; 10.1556/1886.2018.00035

Discussion

Worldwide, Salmonella are recognized as a major gastrointestinal pathogen for humans and animals, whereas, Salmonella typhimurium and Salmonella enteritidis were considered as the major serovars that can be infecting human after eating food of animal origin, but this data may be different over the years and countries.

In this study, the antimicrobial resistance analysis revealed the presence of Salmonella Kentucky resistant to quinolones and Salmonella Typhimurium resistant to multiple antibiotics including 3rd generation cephalosporins. Other studies showed that the resistance to quinolones, fluoroquinolones, and 3rd generation cephalosporins in Salmonella has recently increased [1720]. This resistance may be due to the intensive use of antibiotics in the veterinary and human fields by contributing to the acquisition of resistance genes and exerting a selective pressure for the development of resistant bacteria [21] and may change depending on serotype, time, source of microorganism, and geographic region of isolate [22].

The pathogenicity of Salmonella is influenced by various factors encoded by different virulence genes that play an important role in different steps of pathogenicity, such as adhesion, invasion, intracellular survival, systemic infection, toxin production, and iron acquisition [7]. In this study, the amplification of virulence genes by PCR showed that all isolated strains contain the 6 tested virulence genes (orgA, sitC, sipB, spiA, iroN, and sifA).

The host cell invasion and intracellular survival of Salmonella depend on several genes that are clustered on pathogenicity islands (PIs), and these effector proteins are transferred by 2 type III secretion systems, namely, T3SS1 and T3SS2 [23]. Moreover, Salmonella strains expresses several invasion genes located on the Salmonella pathogenicity islands 1 and 2 (SPI-1 and SPI-2), which promote bacterial uptake and invasion of non-phagocytic cells to cross the epithelial barrier [24]. Among these genes, orgA is required for invasion and secretion system [25]. Thus, the sipB gene is responsible for the entry into non-phagocytic cells and the killing of macrophages. It has been shown that the targeting of sipB by the inv-Spa type III secretion apparatus is necessary and sufficient for the induction of macrophage apoptosis [26].

The iroN gene is implicated in iron acquisition [27]. However, the sitC gene encodes an important transporter of iron. Also, a study carried out by Boyer et al. on Salmonella Typhimurium showed that sitABCD is required for replication of Salmonella inside macrophages and for the creation of virulence in susceptible animals [28]. On the other hand, the sifA gene is required for the formation of filamentous structures in the lysosome vacuoles of infected epithelial cells [29].

A previous study conducted on Salmonella typhimurium showed that spiA gene codes for an outer membrane component that is essential for virulence in host cells [30]. Another study carried out by Dong et al. revealed that spiA gene is associated with biofilm formation mechanism [31]. It has been demonstrated that biofilm formation improves the ability of microorganisms to withstand stresses, such as desiccation, temperature extremes, antibiotics, and antiseptics [32], which allowed these bacteria to survive longer in animal farms and to contaminate meats and eggs, which remain the main vehicles of Salmonella transmission to humans.

In Morocco, it is a challenge for laboratories to systematically identify Salmonella isolates on the basis of biochemical and serological identification using Kaufmann White scheme because of the cost of reagents and the time needed to get the results. In this study, we conducted a rapid and cost-effective method to identify the isolated Salmonella strains using DNA sequencing tools. Furthermore, the sequence analysis of the 16S rRNA genes is being regularly used to identify bacterial species and to perform the taxonomic studies in clinical and scientific investigations [33]. However, the phylogenetic analyses can be used to understand the emergence of pathogenic bacteria and to study the relationship between isolated strains and other reference strains, implicated in animal or human diseases [12, 19, 34].

In this study, the analysis of phylogenetic tree showed the presence of different 16S rRNA profiles among the isolated Salmonella serovars, which are grouped into 3 clusters and 3 sub-clusters, suggesting the presence of different contamination sources due to the diversity of raw materials and manufacturing processes used for each type of sausages.

Conclusion

The results obtained in this study showed that the sequencing of 16S rRNA genes was a suitable tool for identification of Salmonella strains at the genus and species level. In addition, the phylogenic analysis showed a high diversity in all clusters of this bacterium. Furthermore, the antimicrobial resistance and the virulence gene analysis suggest that sausages are contaminated with Salmonella strains and present a major risk to public health.

Funding Sources

The authors declare that they did not have any funding source or grant to support their research work.

Authors' Contributions

This work was carried out in collaboration between all authors. FRF, BB and MM designed the experimental procedures. AED, BO and AE conducted the experimental analysis. SK and SO conducted the bio-informatics analysis. AED and FRF analyzed the data and wrote the manuscript. All authors read and approved the final manuscript.

Conflict of Interest

The authors declare no conflicts of interest.

Acknowledgement

The authors would like to express their sincere thanks to National Center for Scientific and Technical Research (CNRST) for sequencing the PCR products.

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    Acar S , Bulut E, Durul B, Uner I, Kur M, Avsaroglu MD, Kirmaci HA, Tel YO, Zeyrek FY, Soyer Y. Phenotyping and genetic characterization of Salmonella enterica isolates from Turkey revealing arise of different features specific to geography. Int J Food Microbiol. 2017;241:98107.

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    Ibarra JA , Steele-Mortimer O. Salmonella - the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell Microbiol. 2009;11:157986.

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    Bhunia A . Salmonella enterica. In: Foodborne Microbial Pathogens, New York: Springer; 2018. p. 271287

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    Klein JR , Fahlen TF, Jones BD. Transcriptional organization and function of invasion genes within Salmonella enterica serovar Typhimurium pathogenicity island 1, including the prgH, prgI, prgJ, prgK, orgA, orgB, and orgC genes. Infect Immun. 2000;68:336876.

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    Hersh D , Monack DM, Smith MR, Ghori N, Falkow S, Zychlinsky A. The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci USA. 1999;96:2396401.

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    Bäumler AJ , Norris TL, Lasco T, Voigt W, Reissbrodt R, Rabsch W, Heffron F. IroN, a novel outer membrane siderophore receptor characteristic of Salmonella enterica. J Bacteriol. 1998;180:144653.

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    • Export Citation
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    Boyer E , Bergevin I, Malo D, Gros P, Cellier MFM. Acquisition of Mn(II) in addition to Fe(II) is required for full virulence of Salmonella enterica serovar Typhimurium. Infect Immun. 2002;70:603242.

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    • Search Google Scholar
    • Export Citation
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    Stein MA , Leung KY, Zwick M, Garcia-del Portillo F, Finlay BB. Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells. Mol Microbiol. 1996; 20: 15164.

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    • Search Google Scholar
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    Ochman H , Soncini FC, Solomon F, Groisman EA. Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci USA. 1996;93:78004.

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    • Search Google Scholar
    • Export Citation
  • 31.

    Dong Y , Glasner JD, Blattner FR, Triplett EW. Genomic Interspecies Microarray Hybridization: Rapid Discovery of Three Thousand Genes in the Maize Endophyte, Klebsiella pneumoniae 342, by Microarray Hybridization with Escherichia coli K-12 Open Reading Frames. Appl Environ Microbiol. 2001;67:191121.

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    • Search Google Scholar
    • Export Citation
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    Marin C , Hernandiz A, Lainez M. Biofilm development capacity of Salmonella strains isolated in poultry risk factors and their resistance against disinfectants. Poult Sci. 2009;88:42431.

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    • Export Citation
  • 33.

    Petti CA , Polage CR, Schreckenberger P. The role of 16S rRNA gene sequencing in identification of microorganisms misidentified by conventional methods. J Clin Microbiol. 2005;43:61235.

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    • Search Google Scholar
    • Export Citation
  • 34.

    Ed-Dra A , Karraouan B, El Allaoui A, Khayatti M, El Ossmani H, Rhazi Filali F, ElMdaghri N, Bouchrif B. Antimicrobial resistance and genetic diversity of Salmonella Infantis isolated from foods and human samples in Morocco. J Glob Antimicrob Resist. 2018;14:297301.

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    • Export Citation
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    Jones BD , Falkow S. Identification and characterization of a Salmonella typhimurium oxygen-regulated gene required for bacterial internalization. Infect Immun. 1994;62:374552.

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    Chen LM , Kaniga K, Galan JE. Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol. 1996;21:110115.

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    • Crossref
    • Search Google Scholar
    • Export Citation
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    Karraouan B , Ziyate N, Ed-Dra A, Amajoud N, Boutaib R, Akil A, El Allaoui A, El Ossmani H, Zerouali K, Elmdaghri N, Bouchrif B. Salmonella Kentucky: Antimicrobial resistance and molecular analysis of clinical, animal and environment isolates, Morocco. J Infect Dev Ctries. 2017;11:36870.

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    Foley SL , Lynne AM. Food animal-associated Salmonella challenges: pathogenicity and antimicrobial resistance. J Anim Sci. 2008;86:E17387.

  • 22.

    Acar S , Bulut E, Durul B, Uner I, Kur M, Avsaroglu MD, Kirmaci HA, Tel YO, Zeyrek FY, Soyer Y. Phenotyping and genetic characterization of Salmonella enterica isolates from Turkey revealing arise of different features specific to geography. Int J Food Microbiol. 2017;241:98107.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Ibarra JA , Steele-Mortimer O. Salmonella - the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell Microbiol. 2009;11:157986.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24.

    Bhunia A . Salmonella enterica. In: Foodborne Microbial Pathogens, New York: Springer; 2018. p. 271287

  • 25.

    Klein JR , Fahlen TF, Jones BD. Transcriptional organization and function of invasion genes within Salmonella enterica serovar Typhimurium pathogenicity island 1, including the prgH, prgI, prgJ, prgK, orgA, orgB, and orgC genes. Infect Immun. 2000;68:336876.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    Hersh D , Monack DM, Smith MR, Ghori N, Falkow S, Zychlinsky A. The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci USA. 1999;96:2396401.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Bäumler AJ , Norris TL, Lasco T, Voigt W, Reissbrodt R, Rabsch W, Heffron F. IroN, a novel outer membrane siderophore receptor characteristic of Salmonella enterica. J Bacteriol. 1998;180:144653.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28.

    Boyer E , Bergevin I, Malo D, Gros P, Cellier MFM. Acquisition of Mn(II) in addition to Fe(II) is required for full virulence of Salmonella enterica serovar Typhimurium. Infect Immun. 2002;70:603242.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    Stein MA , Leung KY, Zwick M, Garcia-del Portillo F, Finlay BB. Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells. Mol Microbiol. 1996; 20: 15164.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30.

    Ochman H , Soncini FC, Solomon F, Groisman EA. Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci USA. 1996;93:78004.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Dong Y , Glasner JD, Blattner FR, Triplett EW. Genomic Interspecies Microarray Hybridization: Rapid Discovery of Three Thousand Genes in the Maize Endophyte, Klebsiella pneumoniae 342, by Microarray Hybridization with Escherichia coli K-12 Open Reading Frames. Appl Environ Microbiol. 2001;67:191121.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32.

    Marin C , Hernandiz A, Lainez M. Biofilm development capacity of Salmonella strains isolated in poultry risk factors and their resistance against disinfectants. Poult Sci. 2009;88:42431.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33.

    Petti CA , Polage CR, Schreckenberger P. The role of 16S rRNA gene sequencing in identification of microorganisms misidentified by conventional methods. J Clin Microbiol. 2005;43:61235.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Ed-Dra A , Karraouan B, El Allaoui A, Khayatti M, El Ossmani H, Rhazi Filali F, ElMdaghri N, Bouchrif B. Antimicrobial resistance and genetic diversity of Salmonella Infantis isolated from foods and human samples in Morocco. J Glob Antimicrob Resist. 2018;14:297301.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Jones BD , Falkow S. Identification and characterization of a Salmonella typhimurium oxygen-regulated gene required for bacterial internalization. Infect Immun. 1994;62:374552.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36.

    Chen LM , Kaniga K, Galan JE. Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol. 1996;21:110115.

  • 37.

    Janakiraman A , Slauch JM. The putative iron transport system SitABCD encoded on SPI1 is required for full virulence of Salmonella typhimurium. Mol Microbiol. 2000;35:114655.

    • Crossref
    • Search Google Scholar
    • Export Citation
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Senior editors

Editor(s)-in-Chief: Dunay, Ildiko Rita, Prof. Dr. Pharm, Dr. rer. nat., University of Magdeburg, Germany

Editor(s)-in-Chief: Heimesaat, Markus M., Prof. Dr. med., Charité - University Medicine Berlin, Germany

Editorial Board

  • Berit Bangoura, Dr. DVM. PhD,  University of Wyoming, USA
  • Stefan Bereswill, Prof. Dr. rer. nat., Charité - University Medicine Berlin, Germany
  • Dunja Bruder, Prof. Dr. rer. nat., University of Magdeburg, Germany
  • Jan Buer, Prof. Dr. med., University of Duisburg, Germany
  • Edit Buzas, Prof. Dr. med., Semmelweis University, Hungary
  • Renato Damatta, Prof. PhD, UENF, Brazil
  • Maria Deli, MD, PhD, DSc, Biological Research Center, HAS, Hungary
  • Olgica Djurković-Djaković, Prof. Phd, University of Belgrade, Serbia
  • Jean-Dennis Docquier, Prof. Dr. med., University of Siena, Italy
  • Zsuzsanna Fabry, Prof. Phd, University of Washington, USA
  • Ralf Ignatius, Prof. Dr. med., Charité - University Medicine Berlin, Germany
  • Achim Kaasch, Prof. Dr. med., Otto von Guericke University Magdeburg, Germany
  • Oliver Liesenfeld, Prof. Dr. med., Inflammatix, USA
  • Matyas Sandor, Prof. PhD, University of Wisconsin, USA
  • Ulrich Steinhoff, Prof. PhD, University of Marburg, Germany
  • Michal Toborek, Prof. PhD, University of Miami, USA
  • Susanne A. Wolf, PhD, MDC-Berlin, Germany

 

Dr. Dunay, Ildiko Rita
Magdeburg, Germany
E-mail: ildiko.dunay@med.ovgu.de

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2023  
Web of Science  
Total Cites
WoS
674
Journal Impact Factor 3.3
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without
Journal Self Cites
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0.601
Scimago Quartile Score Microbiology (medical) (Q2)
Microbiology (Q3)
Immunology and Allergy (Q3)
Immunology (Q3)
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Scopus
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Scopus
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Microbiology (medical) Q2
Scopus
SNIP
0.832

 

European Journal of Microbiology and Immunology
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European Journal of Microbiology and Immunology
Language English
Size A4
Year of
Foundation
2011
Volumes
per Year
1
Issues
per Year
4
Founder Akadémiai Kiadó
Founder's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Publisher Akadémiai Kiadó
Publisher's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Responsible
Publisher
Chief Executive Officer, Akadémiai Kiadó
ISSN 2062-509X (Print)
ISSN 2062-8633 (Online)

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