The Open Microbiology Journal




ISSN: 1874-2858 ― Volume 13, 2019
RESEARCH ARTICLE

Distribution of Class 1 and 2 Integrons Among Salmonella Enterica Serovars Isolated from Iranian Patients



Reza Ranjbar1, *, Fatemeh Taghipour2, Davoud Afshar3, Shohreh Farshad4
1 Molecular Biology Research Center, Systems Biology and Poisonings Institute, Baqiyatallah University of Medical Sciences, Tehran, Iran
2 Department of Microbiology, Islamic Azad University, Damghan Branch, Damghan, Iran
3 Department of Microbiology and Virology, School of Medicine, Zanjan University of Medical Sciences, Zanjan, Iran
4 Professor Alborzi Clinical Microbiology Research Center, Nemazi Hospital, Shiraz University of Medical Science, Shiraz, IR Iran

Abstract

Background:

Salmonella enterica has become increasingly resistant to antimicrobial agents, partly as a result of genes carried by integrons.

Objective:

The aim of the present study was to investigate the prevalence of class 1 and 2 integrons and resistance to antimicrobial agents in clinical isolates of S. enterica.

Methods:

This study included all Salmonella isolates, recovered from patients with salmonellosis, admitted to Medical Children Hospital, Tehran, Iran during 2015-2016. Bacterial isolates were identified using standard biochemical and agglutination tests. Antimicrobial susceptibility testing was performed according to the Clinical and Laboratory Standards Institute guidelines. The presence of class 1 and 2 integrons was investigated by Polymerase Chain Reaction (PCR) assay, using specific primers.

Results:

A total of 138 Salmonella strains were isolated and included in this study. Integrons were detected in 45 (32%) isolates. Class 1 and 2 integrons were detected in 24 (17.3%) and 21 (15.2%) isolates, respectively. All integron-positive isolates showed multidrug-resistant phenotypes. Resistance to more than three antimicrobial agents was observed in integron-positive isolates.

Conclusions:

Our findings showed that integrons were widely distributed among S. enterica isolates in Tehran. Class 1 integrons are more prevalent than class 2 integrons in Salmonella isolates, and there is an association with MDR patterns. Therefore, these integrons are more likely to be involved in the distribution of resistant phenotypes in Salmonella strains.

Keywords: Antibiotic resistance, Integrons, Multidrug-Resistant (MDR), Salmonella enterica, Antimicrobial agents, Phenotypes.


Article Information


Identifiers and Pagination:

Year: 2019
Volume: 13
First Page: 63
Last Page: 66
Publisher Id: TOMICROJ-13-63
DOI: 10.2174/1874285801913010063

Article History:

Received Date: 26/11/2018
Revision Received Date: 06/02/2019
Acceptance Date: 12/02/2019
Electronic publication date: 28/02/2019
Collection year: 2019

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© 2019 Ranjbar et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: (https://creativecommons.org/licenses/by/4.0/legalcode). This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Molecular Biology Research Center, Systems Biology and Poisonings Institute, Baqiyatallah University of Medical Sciences, Tehran, Iran; Tel: +982188039883; Fax: +982188039883; E-mail: ranjbarre@gmail.com




1. INTRODUCTION

Gastroenteritis and diarrheal diseases are among the most important health problems worldwide, especially in developing countries [1Ranjbar R, Salimkhani E, Sadeghifard N, et al. An outbreak of gastroenteritis of unknown origin in Tehran, July 2003. Pak J Biol Sci 2007; 10(7): 1138-40.
[http://dx.doi.org/10.3923/pjbs.2007.1138.1140] [PMID: 19070067]
]. Salmonella remains one of the most common causes of acute gastroenteritis and food-borne infections around the world [2Ranjbar R, Ahmadi M, Memariani M. Multiple-locus variable-number tandem repeat analysis (MLVA) for genotyping of Salmonella enterica subspecies enterica serotype Infantis isolated from human sources. Microb Pathog 2016; 100: 299-304.
[http://dx.doi.org/10.1016/j.micpath.2016.10.012] [PMID: 27765620]
]. Different species of this bacterium are frequently encountered in different countries, including Iran [3Mulvey MR, Soule G, Boyd D, Demczuk W, Ahmed R. Characterization of the first extended-spectrum beta-lactamase-producing Salmonella isolate identified in Canada. J Clin Microbiol 2003; 41(1): 460-2.
[http://dx.doi.org/10.1128/JCM.41.1.460-462.2003] [PMID: 12517 894]
]. Antibiotic resistance is common among these serovars, and a high prevalence of multidrug-resistance (MDR) isolates has also been reported [4Wang Y, Cao C, Alali WQ, et al. Distribution and antimicrobial susceptibility of foodborne Salmonella Serovars in eight provinces in China from 2007 to 2012 (Except 2009). Foodborne Pathog Dis 2017; 14(7): 393-9.
[http://dx.doi.org/10.1089/fpd.2016.2237] [PMID: 28375673]
].

There are many mechanisms of antibiotic resistance through which bacteria exhibit resistance to antibiotics. Acquisition of genetic elements is one of the major mechanisms, which frequently occurs in both Gram-positive and Gram-

Table 1
Oligonucleotides used in the study.


Table 2
Antimicrobial susceptibility of Salmonella enterica isolates from different serogroups.


negative bacteria. Integrons are DNA elements with major involvement in the spread of antibiotic-resistant genes through horizontal or vertical gene transfer mechanisms [5Mazel D. Integrons: agents of bacterial evolution. Nat Rev Microbiol 2006; 4(8): 608-20.
[http://dx.doi.org/10.1038/nrmicro1462] [PMID: 16845431]
]. Although at least six classes of integrons have been reported, there is limited data about these integrons classes, and only classes 1, 2, and 3 are well-studied [6Ploy M-C, Lambert T, Couty J-P, Denis F. Integrons: an antibiotic resistance gene capture and expression system. Clin Chem Lab Med 2000; 38(6): 483-7.
[http://dx.doi.org/10.1515/CCLM.2000.070] [PMID: 10987194]
].

Integrons are very common in S. enterica serovars and seem to be significantly involved in the advent of antibiotic-resistant phenotypes in the strains [7Lopes GV, Michael GB, Cardoso M, Schwarz S. Antimicrobial resistance and class 1 integron-associated gene cassettes in Salmonella enterica serovar Typhimurium isolated from pigs at slaughter and abattoir environment. Vet Microbiol 2016; 194: 84-92.
[http://dx.doi.org/10.1016/j.vetmic.2016.04.020] [PMID: 27142182]
]. The presence of integrons in the strains increases resistance to fluoroquinolones, which are very effective in the treatment of salmonellosis [8Vo AT, van Duijkeren E, Gaastra W, Fluit AC. Antimicrobial resistance, class 1 integrons, and genomic island 1 in Salmonella isolates from Vietnam. PLoS One 2010; 5(2): e9440.
[http://dx.doi.org/10.1371/journal.pone.0009440] [PMID: 20195474]
]. In addition to fluoroquinolone resistance, resistance to cephalosporins has been also associated with integron cassettes. It is clear that veb-1 gene, encoding resistance to cephalosporins, is a part of integron cassettes. Fluoroquinolones and cephalosporins are two main classes of antibiotics, frequently used to treat Salmonella infections. The prevalence of resistant genes in association with integron cassettes can be a new challenge in the treatment of salmonellosis and its rate is increasing; therefore, it is necessary to determine different classes of integrons in the strains [9Naghoni A, Ranjbar R, Tabaraie B, et al. High prevalence of integron-mediated resistance in clinical isolates of Salmonella enterica. Jpn J Infect Dis 2010; 63(6): 417-21.
[PMID: 21099092]
].

The aim of the current study was to investigate the prevalence of integrons and resistance to antimicrobial agents in clinical isolates of S. enterica, isolated from patients admitted to the Medical Children Hospital of Tehran, Iran.

2. MATERIALS AND METHODS

2.1. Bacterial Isolates

This study included all recovered Salmonella isolates from patients with Salmonella infections, who were admitted to the Children Medical Center of Tehran, Iran during 2015-2016. The isolates were identified by standard biochemical and agglutination tests using commercial antisera (Staten Serum Institute, Copenhagen, Denmark), according to the manufacturer’s instructions.

Antimicrobial susceptibility testing was performed according to the Clinical and Laboratory Standards Institute (CLSI) guidelines and Kirby-Bauer disc diffusion method. The tested antibiotics included cotrimoxazole (1.25/23.75 μg), gentamicin (10 μg), ampicillin (10 μg), streptomycin (10 μg), and tetracycline (30 μg).

2.2. DNA Extraction

DNA extraction was carried out using a previously described method, with some modifications [10Hassanzadeh S, Pourmand MR, Afshar D, Dehbashi S, Mashhadi R. TENT: A rapid DNA extraction method of Staphylococcus aureus. Iran J Public Health 2016; 45(8): 1093-5.
[PMID: 27928541]
]. Briefly, overnight bacterial cultures were separately suspended in 250 μL of lysis buffer (10 mM tris-HCl, 0.1 M NaCl, 1 mM EDTA, and 5% [v/v] Triton X100; pH, 8.0) and boiled at 100°C for three minutes. The suspensions were centrifuged at 10 000 rpm for 10 minutes, and the supernatants were transferred to new sterile microtubes. Then, 250 μL of ethanol 95% was added to each microtube and kept at −20°C for 30 minutes. The solutions were centrifuged at 14 000 rpm for 20 minutes, and then, the sediments were dissolved in 100 μL of sterile distilled water and stored at −20°C. DNA concentration was measured using Thermo Scientific NanoDrop spectrophotometers.

2.3. Polymerase Chain Reaction (PCR) Assay

The PCR assay was carried out for the reaction mixture in a final volume of 25 uL, containing 12.5 μL of 2X PCR Master Mix (CinnaGen, Iran), 10 pmol of forward and reverse primers (Bioneer, Korea) (Table 1), and 50 ng DNA. The PCR conditions were as follows: initial denaturation at 94°C for five minutes; 30 cycles of 94°C for 50 seconds; annealing at 60°C and 72°C for one minute; and a final extension at 72°C for 10 minutes using a thermocycler (Eppendorf Thermal Cycler, Germany). The PCR products were electrophoresed on 1% (W/V) Agarose gel (Sigma-Aldrich, USA) and visualized under UV light after staining with a DNA Safe Stain (CinnaGen, Iran).

3. RESULTS

Among 138 Salmonella isolates, 1, 18, 41, and 78 isolates belonged to serogroups A, B, C, and D, respectively. The results of the antimicrobial susceptibility test, based on the serogroup categories, are presented in Table (2). As shown in this Table, 55 isolates were resistant to tetracycline, while only nine isolates had resistant phenotypes to ampicillin.

Fig. (1)
Agarose gel electrophoresis of Int1 amplicons. Lane M, 100-bp DNA ladder; lanes 1-5, Salmonella enterica isolates; lane 6, positive control; lane 7, negative control.


Fig. (2)
Agarose gel electrophoresis of Int2 amplicons. Lane M, 100-bp DNA ladder; lane 1, positive control; lanes 2-7, Salmonella enterica isolates; lane 8, negative control.


A total of 138 isolates were screened for int1 and int2 genes. Integron classes 1 and 2 were only detected in 45 isolates (class 1: 24 isolates (17.3%); class 2: 21 isolates (15.2%)). Figs. (1 and 2) demonstrate the amplicons of class 1 and 2 integrons, respectively.

4. DISCUSSION

Different levels of antimicrobial resistance to several antibiotics are common among bacteria worldwide [12Hendriksen RS, Mevius DJ, Schroeter A, et al. Occurrence of antimicrobial resistance among bacterial pathogens 2008.]. Integrons are genetic elements associated with resistance to antimicrobial agents. They are categorized into more than six classes, based on the intI gene sequence [13Domingues S, da Silva GJ, Nielsen KM. Integrons: Vehicles and pathways for horizontal dissemination in bacteria. Mob Genet Elements 2012; 2(5): 211-23.
[http://dx.doi.org/10.4161/mge.22967] [PMID: 23550063]
]. Transferability of integrons, especially class 1 integrons, has been found to be common among bacteria through the horizontal gene transfer mechanism [14van Essen-Zandbergen A, Smith H, Veldman K, Mevius D. Occurrence and characteristics of class 1, 2 and 3 integrons in Escherichia coli, Salmonella and Campylobacter spp. in the Netherlands. J Antimicrob Chemother 2007; 59(4): 746-50.
[http://dx.doi.org/10.1093/jac/dkl549] [PMID: 17307772]
]; our findings are consistent with the literature.

In the present study, the prevalence of antibiotic resistance among Salmonella isolates was determined. The results showed that most isolates were resistant and susceptible to tetracycline and ampicillin, respectively. In accordance with our findings, Jackson et al. showed that S. typhimurium isolates are resistant to tetracycline, ampicillin, and cotrimoxazole [15Onyuka JH, Kakai R, Onyango DM, Arama PF, Gichuki J. Prevalence and antimicrobial susceptibility patterns of enteric bacteria isolated from water and fish in lake victoria basin of western 2011.]. In a previous study, we revealed that Salmonella isolates had high levels of resistance to doxycycline, tetracycline, and strepto mycin [16Ranjbar R, Giammanco GM, Farshad S, Owlia P, Aleo A, Mammina C. Serotypes, antibiotic resistance, and class 1 integrons in Salmonella isolates from pediatric cases of enteritis in Tehran, Iran. Foodborne Pathog Dis 2011; 8(4): 547-53.
[http://dx.doi.org/10.1089/fpd.2010.0736] [PMID: 21204690]
]. Our findings, in line with previous studies, indicate that resistance to tetracycline is common among isolates, and this agent seems to be ineffective in the treatment of Salmonella infections.

In this study, resistance to antimicrobial agents varied among Salmonella serogroups; this finding is predictable due to the presence of different strains in these groups. These serogroups were formerly classified as Salmonella species. Also, different patterns of antibiotic resistance have been reported among Salmonella species by other researchers [17Busani L, Graziani C, Battisti A, et al. Antibiotic resistance in Salmonella enterica serotypes typhimurium, enteritidis and infantis from human infections, foodstuffs and farm animals in Italy. Epidemiol Infect 2004; 132(2): 245-51.
[http://dx.doi.org/10.1017/S0950268803001936] [PMID: 15061499]
, 18Tassios PT, Markogiannakis A, Vatopoulos AC, et al. Molecular epidemiology of antibiotic resistance of Salmonella enteritidis during a 7-year period in Greece. J Clin Microbiol 1997; 35(6): 1316-21.
[PMID: 9163436]
].

In the present study, we characterized two classes of integrons, and 45 out of 138 isolates harbored class 1 (17.3%) and class 2 (15.2%) integrons. In a previous study, Asgharpour et al. showed that 36% of S. infantis isolates were positive for class 1 integrons, and all these isolates were also resistant to nalidixic acid, tetracycline, and streptomycin [19Asgharpour F, Rajabnia R, Ferdosi Shahandashti E, Marashi MA, Khalilian M, Moulana Z. Investigation of class I integron in Salmonella infantis and its association with drug resistance. Jundishapur J Microbiol 2014; 7(5): e10019.
[http://dx.doi.org/10.5812/jjm.10019] [PMID: 25147710]
]. In comparison with our study, the higher prevalence of class 1 integrons in the mentioned study shows that application of antibiotics in the poultry industry may increase antibiotic resistance [20Bada-Alambedji R, Fofana A, Seydi M, Akakpo AJ. Antimicrobial resistance of Salmonella isolated from poultry carcasses in Dakar (Senegal). Braz J Microbiol 2006; 37(4): 510-5.
[http://dx.doi.org/10.1590/S1517-83822006000400020]
]. In another study, 45% of S. enterica serotypes, including Mbandaka, Brandenburg, Agona, Alachua, and Panama serotypes, harbored class 1 integron genes [21Ribeiro VB, Lincopan N, Landgraf M, Franco BD, Destro MT. Characterization of class 1 integrons and antibiotic resistance genes in multidrug-resistant Salmonella enterica isolates from foodstuff and related sources. Braz J Microbiol 2011; 42(2): 685-92.
[http://dx.doi.org/10.1590/S1517-83822011000200033] [PMID: 24031 680]
].

Up to 17.39% of isolates harboring class 1 integrons were resistant to ampicillin (2.89%), gentamicin and trimethoprim / sulfamethoxazole (5.79%), tetracycline (10.14%), and streptomycin (7.97%), whereas resistance to these antibiotics in integron-negative isolates was 14.49%, 7.97%, 7.24%, 26.08%, and 22.46%, respectively. The low level of ampicillin resistance among integron-negative isolates suggests that resistance to this antibiotic is not associated with integrons and is commonly associated with TEM β-lactamases, as described in the literature [22Ebner P, Garner K, Mathew A. Class 1 integrons in various Salmonella enterica serovars isolated from animals and identification of genomic island SGI1 in Salmonella enterica var. Meleagridis. J Antimicrob Chemother 2004; 53(6): 1004-9.
[http://dx.doi.org/10.1093/jac/dkh192] [PMID: 15117931]
].

The prevalence of class 2 integrons was found to be 15.21% among the studied isolates, indicating the low prevalence of this class of integrons. In studies by other researchers, the prevalence of class 2 integrons was also lower than our study [23Antunes P, Machado J, Peixe L. Characterization of antimicrobial resistance and class 1 and 2 integrons in Salmonella enterica isolates from different sources in Portugal. J Antimicrob Chemother 2006; 58(2): 297-304.
[http://dx.doi.org/10.1093/jac/dkl242] [PMID: 16782741]
, 24Peirano G, Agersø Y, Aarestrup FM, dos Reis EMF, dos Prazeres Rodrigues D. Occurrence of integrons and antimicrobial resistance genes among Salmonella enterica from Brazil. J Antimicrob Chemother 2006; 58(2): 305-9.
[http://dx.doi.org/10.1093/jac/dkl248] [PMID: 16782743]
]. In this regard, in a study by Jin et al., class 2 integrons were not detected even among 834 Salmonella isolates [25Jin Y, Ling JM. Prevalence of integrons in antibiotic-resistant Salmonella spp. in Hong Kong. Jpn J Infect Dis 2009; 62(6): 432-9.
[PMID: 19934534]
].

CONCLUSION

According to our findings, the prevalence of antibiotic resistance is high among Salmonella isolates, and screening for integrons, as likely indicators of antibiotic resistance, may be useful in detecting Salmonella organisms with antibiotic-resistance phenotypes. Although our study showed that integrons are associated with antibiotic-resistance phenotypes, further studies are needed to determine the exact relationship between classes of integrons and resistance to different antibiotics.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This study was approved in Ethical Committee No.33 in Baqiyatallah University of Medical Sciences, Tehran.

HUMAN AND ANIMAL RIGHTS

No animals/humans were used for studies that are the basis of this research.

CONSENT FOR PUBLICATION

Informed consent was obtaind from all the participants.

CONFLICT OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENT

We would like to thank the “Clinical Research Development Center of Baqiyatallah hospital” for their kind cooperation. This study was financially supported in part by “Clinical Research Development Center of Baqiyatallah hospital”.

REFERENCES

[1] Ranjbar R, Salimkhani E, Sadeghifard N, et al. An outbreak of gastroenteritis of unknown origin in Tehran, July 2003. Pak J Biol Sci 2007; 10(7): 1138-40.
[http://dx.doi.org/10.3923/pjbs.2007.1138.1140] [PMID: 19070067]
[2] Ranjbar R, Ahmadi M, Memariani M. Multiple-locus variable-number tandem repeat analysis (MLVA) for genotyping of Salmonella enterica subspecies enterica serotype Infantis isolated from human sources. Microb Pathog 2016; 100: 299-304.
[http://dx.doi.org/10.1016/j.micpath.2016.10.012] [PMID: 27765620]
[3] Mulvey MR, Soule G, Boyd D, Demczuk W, Ahmed R. Characterization of the first extended-spectrum beta-lactamase-producing Salmonella isolate identified in Canada. J Clin Microbiol 2003; 41(1): 460-2.
[http://dx.doi.org/10.1128/JCM.41.1.460-462.2003] [PMID: 12517 894]
[4] Wang Y, Cao C, Alali WQ, et al. Distribution and antimicrobial susceptibility of foodborne Salmonella Serovars in eight provinces in China from 2007 to 2012 (Except 2009). Foodborne Pathog Dis 2017; 14(7): 393-9.
[http://dx.doi.org/10.1089/fpd.2016.2237] [PMID: 28375673]
[5] Mazel D. Integrons: agents of bacterial evolution. Nat Rev Microbiol 2006; 4(8): 608-20.
[http://dx.doi.org/10.1038/nrmicro1462] [PMID: 16845431]
[6] Ploy M-C, Lambert T, Couty J-P, Denis F. Integrons: an antibiotic resistance gene capture and expression system. Clin Chem Lab Med 2000; 38(6): 483-7.
[http://dx.doi.org/10.1515/CCLM.2000.070] [PMID: 10987194]
[7] Lopes GV, Michael GB, Cardoso M, Schwarz S. Antimicrobial resistance and class 1 integron-associated gene cassettes in Salmonella enterica serovar Typhimurium isolated from pigs at slaughter and abattoir environment. Vet Microbiol 2016; 194: 84-92.
[http://dx.doi.org/10.1016/j.vetmic.2016.04.020] [PMID: 27142182]
[8] Vo AT, van Duijkeren E, Gaastra W, Fluit AC. Antimicrobial resistance, class 1 integrons, and genomic island 1 in Salmonella isolates from Vietnam. PLoS One 2010; 5(2): e9440.
[http://dx.doi.org/10.1371/journal.pone.0009440] [PMID: 20195474]
[9] Naghoni A, Ranjbar R, Tabaraie B, et al. High prevalence of integron-mediated resistance in clinical isolates of Salmonella enterica. Jpn J Infect Dis 2010; 63(6): 417-21.
[PMID: 21099092]
[10] Hassanzadeh S, Pourmand MR, Afshar D, Dehbashi S, Mashhadi R. TENT: A rapid DNA extraction method of Staphylococcus aureus. Iran J Public Health 2016; 45(8): 1093-5.
[PMID: 27928541]
[11] Mazel D, Dychinco B, Webb VA, Davies J. Antibiotic resistance in the ECOR collection: integrons and identification of a novel aad gene. Antimicrob Agents Chemother 2000; 44(6): 1568-74.
[http://dx.doi.org/10.1128/AAC.44.6.1568-1574.2000] [PMID: 10817 710]
[12] Hendriksen RS, Mevius DJ, Schroeter A, et al. Occurrence of antimicrobial resistance among bacterial pathogens 2008.
[13] Domingues S, da Silva GJ, Nielsen KM. Integrons: Vehicles and pathways for horizontal dissemination in bacteria. Mob Genet Elements 2012; 2(5): 211-23.
[http://dx.doi.org/10.4161/mge.22967] [PMID: 23550063]
[14] van Essen-Zandbergen A, Smith H, Veldman K, Mevius D. Occurrence and characteristics of class 1, 2 and 3 integrons in Escherichia coli, Salmonella and Campylobacter spp. in the Netherlands. J Antimicrob Chemother 2007; 59(4): 746-50.
[http://dx.doi.org/10.1093/jac/dkl549] [PMID: 17307772]
[15] Onyuka JH, Kakai R, Onyango DM, Arama PF, Gichuki J. Prevalence and antimicrobial susceptibility patterns of enteric bacteria isolated from water and fish in lake victoria basin of western 2011.
[16] Ranjbar R, Giammanco GM, Farshad S, Owlia P, Aleo A, Mammina C. Serotypes, antibiotic resistance, and class 1 integrons in Salmonella isolates from pediatric cases of enteritis in Tehran, Iran. Foodborne Pathog Dis 2011; 8(4): 547-53.
[http://dx.doi.org/10.1089/fpd.2010.0736] [PMID: 21204690]
[17] Busani L, Graziani C, Battisti A, et al. Antibiotic resistance in Salmonella enterica serotypes typhimurium, enteritidis and infantis from human infections, foodstuffs and farm animals in Italy. Epidemiol Infect 2004; 132(2): 245-51.
[http://dx.doi.org/10.1017/S0950268803001936] [PMID: 15061499]
[18] Tassios PT, Markogiannakis A, Vatopoulos AC, et al. Molecular epidemiology of antibiotic resistance of Salmonella enteritidis during a 7-year period in Greece. J Clin Microbiol 1997; 35(6): 1316-21.
[PMID: 9163436]
[19] Asgharpour F, Rajabnia R, Ferdosi Shahandashti E, Marashi MA, Khalilian M, Moulana Z. Investigation of class I integron in Salmonella infantis and its association with drug resistance. Jundishapur J Microbiol 2014; 7(5): e10019.
[http://dx.doi.org/10.5812/jjm.10019] [PMID: 25147710]
[20] Bada-Alambedji R, Fofana A, Seydi M, Akakpo AJ. Antimicrobial resistance of Salmonella isolated from poultry carcasses in Dakar (Senegal). Braz J Microbiol 2006; 37(4): 510-5.
[http://dx.doi.org/10.1590/S1517-83822006000400020]
[21] Ribeiro VB, Lincopan N, Landgraf M, Franco BD, Destro MT. Characterization of class 1 integrons and antibiotic resistance genes in multidrug-resistant Salmonella enterica isolates from foodstuff and related sources. Braz J Microbiol 2011; 42(2): 685-92.
[http://dx.doi.org/10.1590/S1517-83822011000200033] [PMID: 24031 680]
[22] Ebner P, Garner K, Mathew A. Class 1 integrons in various Salmonella enterica serovars isolated from animals and identification of genomic island SGI1 in Salmonella enterica var. Meleagridis. J Antimicrob Chemother 2004; 53(6): 1004-9.
[http://dx.doi.org/10.1093/jac/dkh192] [PMID: 15117931]
[23] Antunes P, Machado J, Peixe L. Characterization of antimicrobial resistance and class 1 and 2 integrons in Salmonella enterica isolates from different sources in Portugal. J Antimicrob Chemother 2006; 58(2): 297-304.
[http://dx.doi.org/10.1093/jac/dkl242] [PMID: 16782741]
[24] Peirano G, Agersø Y, Aarestrup FM, dos Reis EMF, dos Prazeres Rodrigues D. Occurrence of integrons and antimicrobial resistance genes among Salmonella enterica from Brazil. J Antimicrob Chemother 2006; 58(2): 305-9.
[http://dx.doi.org/10.1093/jac/dkl248] [PMID: 16782743]
[25] Jin Y, Ling JM. Prevalence of integrons in antibiotic-resistant Salmonella spp. in Hong Kong. Jpn J Infect Dis 2009; 62(6): 432-9.
[PMID: 19934534]

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(Instituto de Agroquimica y Tecnologia de Alimentos, Spain)

"Open access journals have become a fundamental tool for students, researchers, patients and the general public. Many people from institutions which do not have library or cannot afford to subscribe scientific journals benefit of them on a daily basis. The articles are among the best and cover most scientific areas."


M. Bendandi
(University Clinic of Navarre, Spain)

"These journals provide researchers with a platform for rapid, open access scientific communication. The articles are of high quality and broad scope."


Peter Chiba
(University of Vienna, Austria)

"Open access journals are probably one of the most important contributions to promote and diffuse science worldwide."


Jaime Sampaio
(University of Trás-os-Montes e Alto Douro, Portugal)

"Open access journals make up a new and rather revolutionary way to scientific publication. This option opens several quite interesting possibilities to disseminate openly and freely new knowledge and even to facilitate interpersonal communication among scientists."


Eduardo A. Castro
(INIFTA, Argentina)

"Open access journals are freely available online throughout the world, for you to read, download, copy, distribute, and use. The articles published in the open access journals are high quality and cover a wide range of fields."


Kenji Hashimoto
(Chiba University, Japan)

"Open Access journals offer an innovative and efficient way of publication for academics and professionals in a wide range of disciplines. The papers published are of high quality after rigorous peer review and they are Indexed in: major international databases. I read Open Access journals to keep abreast of the recent development in my field of study."


Daniel Shek
(Chinese University of Hong Kong, Hong Kong)

"It is a modern trend for publishers to establish open access journals. Researchers, faculty members, and students will be greatly benefited by the new journals of Bentham Science Publishers Ltd. in this category."


Jih Ru Hwu
(National Central University, Taiwan)


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