The Open Microbiology Journal




ISSN: 1874-2858 ― Volume 14, 2020
RESEARCH ARTICLE

Antibiotic Resistance Pattern and Frequency of PER-1, SHV-1 and AMPC Type B-Lactamase Genes in Pseudomonas aeruginosa Isolated from Clinical Samples



Fatemeh F. Amoudizaj1, *, Elnaz Aghayi2, Milad G. Matin3, Nayemeh Soltani3, Pejman Mala3
1 Department of Genetic, Tabriz Branch, Islamic Azad University, Tabriz, Iran
2 Department of Molecular Biology, Bonab Branch, Islamic Azad University, Bonab, Iran
3 Department of Microbiology, Urmia Branch, Islamic Azad University, Urmia, Iran

Abstract

Background:

The existence of Extended Spectrum B-lactamase (ESBL) genes plays an important role in spreading B-lactam antibiotic resistance in the producing strains of these enzymes. The resistance of gram-negative bacteria, such as Pseudomonas aeruginosa, to different antimicrobial agents, especially B-lactams, has increasingly been reported.

Objective:

This study was conducted to determine the prevalence of TEM-1and VEB-1 beta-lactamases gene in P. aeruginosa isolates through Polymerase Chain Reaction (PCR) method.

Methods:

100 clinical isolates of P. aeruginosa were collected from different clinical samples. The antibiotic susceptibility was examined by the disc diffusion method. The presence of PER-1, SHV-1 and AMPC genes was detected by PCR method.

Results:

Out of the studied P. aeruginosa isolates, 7, 9 and 37 isolates were positive for PER-1, SHV-1 and AMPC B-lactamases resistance genes, respectively. Patients with urinary infection had the most resistant isolates. All isolates (100%) were sensitive to polymyxin B.

Conclusion:

Antibiotic resistance in isolates of Pseudomonas can be caused by B-lactamases resistance genes. Noticing the increasing rate of the ESBLs producing strains, using the appropriate treatment protocol based on the antibiogram pattern of the strains is highly recommended.

Keywords: Pseudomonas aeruginosa, B-Lactamase, PER-1 gene, SHV-1 gene, AMPC gene, Antibiotic resistance, Polymerase chain reaction.


Article Information


Identifiers and Pagination:

Year: 2019
Volume: 13
First Page: 308
Last Page: 312
Publisher Id: TOMICROJ-13-308
DOI: 10.2174/1874285801913010308

Article History:

Received Date: 18/09/2019
Revision Received Date: 14/12/2019
Acceptance Date: 18/12/2019
Electronic publication date: 31/12/2019
Collection year: 2019

© 2019 Amoodizaj 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 Department of Genetic, Tabriz Branch, Islamic Azad University, Tabriz, Iran; E-mail: fatemeh.firoozi96@ yahoo.com; Tel: +98-9395572387





1. INTRODUCTION

Pseudomonas aeruginosa is a remarkably adaptive bacterial pathogen which can cause persistent infections in burn patients, immune-compromised patients, and individuals with the genetic disease cystic fibrosis. It is one of the most prevalent nosocomial pathogens, and the infections caused by P. aeruginosa can be very serious and life-threatening [1Zowawi HM, Harris PN, Roberts MJ, et al. The emerging threat of multidrug-resistant Gram-negative bacteria in urology. Nat Rev Urol 2015; 12(10): 570-84.
[http://dx.doi.org/10.1038/nrurol.2015.199] [PMID: 26334085]
]. P. aeruginosaisresponsible for 9% of all healthcare-associated infections, and the resistance to P. aeruginosa is increasing [2Crivaro V, Di Popolo A, Caprio A, et al. Pseudomonas aeruginosa in a neonatal intensive care unit: Molecular epidemiology and infection control measures. BMC Infect Dis 2009; 9(1): 70-4.
[http://dx.doi.org/10.1186/1471-2334-9-70] [PMID: 19463153]
, 3Tsakris A, Poulou A, Kristo I, et al. Large dissemination of VIM-2-metallo-β-lactamase-producing Pseudomonas aeruginosa strains causing health care-associated community-onset infections. Clin Microbiol Rev 2009; 47(11): 3524-9.
[http://dx.doi.org/10.1128/CMR.00040-09] [PMID: 19822890]
]. One of the most prominent attributes of these strains is their resistance to multiple clinically important antibiotics like the third generation of cephalosporins, imipenem and aztreonam. A great number of P. aeruginosa strains generate various classes of Extended Spectrum β-Lactamases (ESBLs) which allow the bacterium to tolerate against extended spectrum cephalosporins, such as cefotaxime, ceftriaxone and ceftazidime and they have been reported with a developing frequency [4Shacheraghi F, Shakibaie MR, Noveiri H. Molecular identification of ESBL Genes blaGES-blaVEB-blaCTX-M blaOXA-blaOXA-4, blaOXA-10 andblaPER-in Pseudomonas aeruginosa strains isolated from burn patients by PCR, RFLP and sequencing techniques. Int. J Biol Life Sci 2010; 3(6): 138-42.].

Beta-lactam antimicrobial agents exhibit the most common treatment for bacterial infections and continue to be the prominent cause of resistance to b-lactam antibiotics among Gram-negative bacteria worldwide. The persistent exposure of bacterial strains to a multitude of b-lactams has induced dynamic and continuous production and mutation of b-lactamases in these bacteria, expanding their activity even against the newly developed b-lactam antibiotics [5Mahdavi S, Isazadeh A. Lactobacillus casei suppresses hfq gene expression in Escherichia coli O157:H7. Br J Biomed Sci 2019; 76(2): 92-4.
[http://dx.doi.org/10.1080/09674845.2019.1567903] [PMID: 30633636]
, 6Mahdavi S, Azizi Dehbokri M, Isazadeh A. Contamination of chicken meat with salmonella spp distributed in mahabad city, iran. Int J Enteric Pathog 2018; 6(3): 65-8.
[http://dx.doi.org/10.15171/ijep.2018.18]
].

Resistance to ESBLs in P. aeruginosa is associated in most cases with the overproduction of AmpC [7Lister PD, Wolter DJ, Hanson ND. Antibacterial-resistant Pseudomonas aeruginosa: clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clin Microbiol Rev 2009; 22(4): 582-610.
[http://dx.doi.org/10.1128/CMR.00040-09] [PMID: 19822890]
]. However, a growing number of Ambler class A ESBLs, class B metallo-b-lactamases (MBLs), and class D extended spectrum oxacillinases (ES-OXAs) have been reported in P. aeruginosa clinical isolates [8Fournier D, Hocquet D, Dehecq B, Cholley P, Plésiat P. Detection of a new extended-spectrum oxacillinase in Pseudomonas aeruginosa. J Antimicrob Chemother 2010; 65(2): 364-5.
[http://dx.doi.org/10.1093/jac/dkp438] [PMID: 20008045]
]. Class A ESBLs reported in P. aeruginosa include PER, SHV, TEM, VEB, BEL, GES and CTX-M type [9Picão RC, Poirel L, Gales AC, Nordmann P. Diversity of β-lactamases produced by ceftazidime-resistant Pseudomonas aeruginosa isolates causing bloodstream infections in Brazil. Antimicrob Agents Chemother 2009; 53(9): 3908-13.
[http://dx.doi.org/10.1128/AAC.00453-09] [PMID: 19596871]
]. PER-1 was first identified in a P. aeruginosa clinical isolate recovered from a Turkish patient in France, in 1991 [10Nordmann P, Ronco E, Naas T, Duport C, Michel-Briand Y, Labia R. Characterization of a novel extended-spectrum beta-lactamase from Pseudomonas aeruginosa. Antimicrob Agents Chemother 1993; 37(5): 962-9.
[http://dx.doi.org/10.1128/AAC.37.5.962] [PMID: 8517722]
]. Later, PER-1 was found in European and Asian countries [11Akinci E, Vahaboglu H. Minor extended-spectrum β-lactamases. Expert Rev Anti Infect Ther 2010; 8(11): 1251-8.
[http://dx.doi.org/10.1586/eri.10.119] [PMID: 21073290]
].

AmpC contributes to the natural resistance of the microorganism toward labile and inducing molecules, such as aminopenicillins, first and second-generation cephalosporins [12Mahdavi S, Isazadeh AR. Investigation of contamination rate and determination of pattern of antibiotic resistance in coagulase positive staphylococcus aureus isolated from domestic cheeses in maragheh. Iran Pathobiol Res 2019; 22(2): 85-9.]. More importantly, when overproduced as a result of mutations altering the peptidoglycan recycling process, AmpC becomes a major cause of resistance to widely used anti-pseudomonal penicillins (ticarcillin and piperacillin), monobactams (aztreonam), and third-generation (ceftazidime) and fourth-generation (cefepime) cephalosporins [13Yari Z, Mahdavi S, Khayati S, Ghorbani R, Isazadeh A. Evaluation of antibiotic resistance patterns in Staphylococcus aureus isolates collected from urinary tract infections in women referred to Shahid Beheshti educational and therapeutic center in Maragheh city. Med J Tabriz Uni Med Sciences Health Services 2020; 41(6): 106-12.].

The purpose of this study was to investigate the frequency of PER-1, SHV-1 and AMPC type B-Lactamase genes in isolated P. aeruginosa strains from clinical samples in Tabriz hospitals, Iran

2. MATERIALS AND METHODS

2.1. Bacterial Isolates

In this descriptive study, 100 isolates of P. aeruginosa were isolated from clinical specimens (burn, urinary tract infection, ulcers, lung secretions and eyes) in Asadabadi hospital in Tabriz in 2018. The standard tests, including oxidase, catalase, oxidation/fermentation (OF), arginine dehydrogenase, pigment production in the Muller Hinton Agar medium and growth ability at 42°C were performed to confirm the P. aeruginosa isolates. Then, obtained isolates stored in the BHI medium containing 18% glycerol for further experiments. Ethical approval to perform the study was obtained from the institutional review board of Tabriz University of Medical Sciences. Written informed consent was obtained from all patients included in the study.

2.2. Antimicrobial Susceptibility Testing

Antibiotic resistance of isolated P. aeruginosa was investigated using a disc diffusion (Kirby-Bauer) method based on CLSI (Clinical and Laboratory Standard Institute) standards. The antimicrobial discs were as following: Polymexin B, Gentamicin, Tobramycin, Amikacin, Ceftazidime, Ciprofloxacin, Piperacillin, Piperacillin-Tazobactam and Tricarcin. P. aeruginosa ATCC 27853 was used as the control strain for susceptibility testing [14Mahdavi S, Kheyrollahi M, Sheikhloei H, Isazadeh A. Antibacterial and antioxidant activities of nasturtium officinale essential oil on food borne bacteria. Open Microbiol J 2019; 13: 81-5.
[http://dx.doi.org/10.2174/1874285801913010081]
,15Mahdavi S, Zali MS, Farajnia S, Mehmannavaz Y, Isazadeh A. The comparison of bovine fecal and buffy coat samples for diagnosis of Johne’s disease based on pcr. gene. Cell Tissue 2018; 5(2)e79745].

2.3. Molecular Detection

Extraction kit (Jena Bioscience) was used to extract DNA from isolated P. aeruginosa. The quantity and quality of extracted DNA were investigated nanodrop instrument and electrophoresis on 1% agarose gel, respectively. The sequence of primers for the detection of PER-1, SHV-1 and AMPC genes was selected from references and synthesized with Sina Clone Company (Table 1),[16Fazeli H, Fatahi Bafghi M, Faghri M, Akbari R. Molecular study of PER and VEB genes is multidrug resistant Pseudomonas aeroginosa isolated from clinical specimens in Isfahan/Iran and their antibiotic resistance patterns. J Kerman Univ Med Sci 2012; 19(4): 345-53.-18Quale J, Bratu S, Gupta J, Landman D. Interplay of efflux system, ampC, and oprD expression in carbapenem resistance of Pseudomonas aeruginosa clinical isolates. Antimicrob Agents Chemother 2006; 50(5): 1633-41.
[http://dx.doi.org/10.1128/AAC.50.5.1633-1641.2006] [PMID: 16641429]
]. The polymerase chain reaction (PCR) was carried out to detect the PER-1, SHV-1 and AMPC genes. For this purpose, the Amplicon kit (Pishgam Co.) was used according to the manufacturer's protocol. The master mix of PCR reaction with a final volume of 25μl was prepared (2μl of MgCl2, 2.5μl PCR buffer, 0.5μl dNTPs, 17.3μl distilled water, 1μL forward primer, 1μL reverse primer, 0.1μl Taq polymerase). Finally, 1μL of DNA template was added to each micro tubes. The temperature and cycle's program was as following: 1 cycle initial denaturation (95°C for 3 min), 35 cycle denaturation (93°C for 45 sec), 35 cycle annealing (30 sec), 35 cycle extension (72°C for 25 seconds) and 1 cycle final extension (72°C for 1 min). The PCR products were electrophoresed by agarose gel 1% containing ethidium bromide for one hour. The products were examined by a gel doc instrument [15Mahdavi S, Zali MS, Farajnia S, Mehmannavaz Y, Isazadeh A. The comparison of bovine fecal and buffy coat samples for diagnosis of Johne’s disease based on pcr. gene. Cell Tissue 2018; 5(2)e79745].

3. RESULTS

In this study, 100 samples of P. aeruginosa were isolated from different clinical specimens. Antibiogram tests showed that the highest resistance to the antibiotic was related to Piperacillin (88%), Ceftazidime (76%) and Amikacin (71%). The results of antibiogram tests are shown in Table 2.

The obtained results showed that among 100 tested isolates, 18 (18%) cases had PER-1 gene, 21 (21%) isolates had SHV-1 gene, and 61 cases (61%) had AMPC gene. The results showed that 17 (17%) isolated strains had two resistance genes at the same time. Also, 1 (1%) isolated strain had three resistance genes at the same time.

Results showed that the highest and lowest isolated positive samples related to patients with urinary tract infection and patients with eye infection, respectively. The frequency of PER-1, SHV-1 and AMPC genes based on the type of clinical specimen is shown in Table 3.

4. DISCUSSION

The identification of antibiotic-resistant strains in hospitals seems necessary to prevent the release of genes resistant [19Mahdavi S, Tanhaeivash E, Isazadeh A. Investigating the Presence and Expression of stx1 Gene in Escherichia coli Isolated From Women With Urinary Tract Infection Using Real-Time PCR in Tabriz, Iran. Int J Enteric Pathog 2018; 6(4): 104-7.
[http://dx.doi.org/10.15171/ijep.2018.26]
]. Today, due to the high prevalence of antibiotic-resistant bacteria, controlling infectious diseases often fail [20Chanwit Tribuddharat MD, Somporn S, Wararat C. A correlation between phenotypes and genotypes of Extended- Spectrum Beta-Lactamase (ESBL)- producing klebsiella pneumoniae in a University Hospital Thailand. J Infect Dis Antimicrob Agents 2007; 24(3): 117-23.]. This may be due to a lack of sufficient information about dominant flora of hospitals and the origin of antibiotic resistance in hospitalized patients. Therefore, the study of antibiotic resistance in hospital strains gives us a clear view of the challenges [21Tan J, Pitout JD, Guttman DS. New and sensitive assay for determining Pseudomonas aeruginosa metallo-beta-lactamase resistance to imipenem. J Clin Microbiol 2008; 46(5): 1870-2.
[http://dx.doi.org/10.1128/JCM.02175-07] [PMID: 18337388]
, 22Jamali SH, Bahar MA, Hoshmand M. Prevalence of VIM & IMP metallobetalactamase in imipenem resistant Pseudomonas aeroginosa isolated from burn patients. Knowledge Microbial 2009; 1(1): 19-25.]. Determination of antibiotic resistance of P. aeruginosa in the present study showed that resistance to ciprofloxacin is increasing, while a high sensitivity was observed to Polymyxin B.

Table 1
The sequence and characteristics of used primers.


Table 2
Antibiotic resistance pattern of isolates of P. aeruginosa isolated from clinical samples.


Table 3
Frequency of PER-1, SHV-1 and AMPC genes in isolates of P. aeruginosa isolated from clinical samples.


In a study conducted by Ranjbar et al. (2011) in Tehran hospitals, the resistance to amikacin and imipenem was reported 97.5% and 90%, respectively [23Ranjbar R, Owlia P, Saderi H, et al. Characterization of Pseudomonas aeruginosa strains isolated from burned patients hospitalized in a major burn center in Tehran, Iran. Acta Med Iran 2011; 49(10): 675-9.
[PMID: 22071644]
]. In a study by Rajaie et al. (2015) showed that the resistance to amikacin, tobramycin, ciprofloxacin, gentamicin and ceftazidime was 92%, 88%, 88%, 96% and 96%, respectively [24Rajaie S, Mohammadi Sichani M, Mohammad Yousefi H. Study on the inhibitory activity of zinc oxide nanoparticles against Pseudomonas aeruginosa isolated from burn wounds. Qom Univ Med Sci J 2015; 9(1): 30-7.]. In the study by Fazeli et al. (2013) The rate of resistance to amikacin, gentamicin, ciprofloxacin was 60, 50, 65%, respectively [25Fazeli H, Havaei SA, Solgi H, Shokri D, Motallebirad T. Pattern of Antibiotic Resistance in Pesudomonas Aeruginosa Isolated from Intensive Care Unit, Isfahan, Iran. Majallah-i Danishkadah-i Pizishki-i Isfahan 2013; 31(232): 433-8.]. In another study by Adabi et al. (2015) antibiotic resistant pattern to amikacin, ciprofloxacin, gentamicin and amikacin was reported 86%, 87%, 88% and 96%, respectively [26Adabi M, Talebi Taher M, Arbabi L, et al. Determination of antibiotic resistance pattern of Pseudomonas aeruginosa strains isolated from patients with burn wounds. J Ardabil Univ Med Sci 2015; 15(1): 66-74.]. In the present study, 67% of the studied samples were sensitive to polymyxin B, which Rostampour et al. (2015) reported similar results [27Rostam Pour S, Gorzin AA. Motamedi Gh. Frequency of blaKHM-1, blaIMP-1, 2 and blaSPM-1 genes in clinical isolates of metallo β-lactamase producing Pseudomonas aeruginosa in hospitalized burned patients in Ghotbeddin Shirazi Hospital. J Qazvin Univ Med Sci 2015; 19(2): 21-9.]. Our results showed that most of the isolated P. aeruginosa was resistance to the ceftazidime, ciprofloxacin, amikacin, tobramycin, gentamicin, piperacillin, piperacillin-tazobactam and ticarcillin. Generally, with a glimpse of previous studies, it can be concluded that the resistance of P. aeruginosa strains to different antibiotics is relatively high. On the other hand, resistance patterns are constantly changing, which should be considered. According to our results, the polymyxin B is currently the best choice for antibiotic therapy of P. aeruginosa infections.

In this study, the presence of PER-1, SHV-1, and AMPC antibiotic resistance genes was investigated by PCR method. The enzymes produced by these genes are known as extended spectrum β-lactamase, which inhibits the function of antibiotics. The PER-1 Beta-lactamase was first reported in 1991 and is able to hydrolyze penicillins and cephalosporins. The PER-1 enzyme has been found on bacterial chromosome and plasmid [28Mantengoli E, Rossolini GM. Tn5393d, a complex Tn5393 derivative carrying the PER-1 extended-spectrum β-lactamase gene and other resistance determinants. Antimicrob Agents Chemother 2005; 49(8): 3289-96.
[http://dx.doi.org/10.1128/AAC.49.8.3289-3296.2005] [PMID: 16048938]
]. The SHV-1 enzyme is also a extended spectrum β-lactamase, which able to destroying extended spectrum cephalosporins, such as cefotaxime, ceftriaxone and ceftazidime [29Jacoby GA, Medeiros AA. More extended-spectrum beta-lactamases. Antimicrob Agents Chemother 1991; 35(9): 1697-704.
[http://dx.doi.org/10.1128/AAC.35.9.1697] [PMID: 1952834]
]. In the present study, all strains with SHV-1 enzyme showed a resistance to ceftazidime, which can be attributed to the presence of this enzyme. Another resistance mechanism in gram-negative bacteria is the production of chromosomal cephalosporins C, such as AMPC β-lactamases. Today, isolates that produce both AMPC and ESBLs are increasing, which has a high resistance to antimicrobial agents [30Kong KF, Schneper L, Mathee K. Beta-lactam antibiotics: from antibiosis to resistance and bacteriology. APMIS 2010; 118(1): 1-36.
[http://dx.doi.org/10.1111/j.1600-0463.2009.02563.x] [PMID: 20041868]
]. These enzymes can hydrolyze penicillins, cephalosporins, cefamixins, and beta-lactamase inhibitors, and have only a low affinity for carbapenem and cephapine [31Jacoby GA. Amp C β-lactamases. Clin Microbiol Rev 2009; 22(1): 161-82.
[http://dx.doi.org/10.1128/CMR.00036-08] [PMID: 19136439]
]. In the present study, high resistance to penicillin and cephalosporin antibiotics can be due to the expression of PER-1 and AMPC genes in the studied isolates.

CONCLUSION

Due to the increased antibiotic resistance in clinical specimens, physicians must be careful in selection of effective antibiotics. In strains with SHV-1 beta-lactamase, the use of ceftazidime does not have an effect on infection control. Also, strains with AMPC gene are increasing, which could be a problem in the future. Also, polymyxin B is an effective antibiotic for treatment of P. aeruginosa infections in hospitals.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

Ethical approval in this study was obtained from the institutional review board of Tabriz University of Medical Sciences, Iran.

HUMAN AND ANIMAL RIGHTS

No Animals were used in this research. All human research procedures followed were in accordance with the ethical standards of the committee responsible for human experimentation (institutional and national), and with the Helsinki Declaration of 1975, as revised in 2013.

CONSENT FOR PUBLICATION

Informed consent was obtained from all the participants prior to publication.

AVAILABILITY OF DATA AND MATERIALS

All relevant data and materials are provided within the manuscript.

FUNDING

None.

CONFLICT OF INTEREST

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

ACKNOWLEDGEMENTS

The authors would like to thank all the participants for taking part in this study.

REFERENCES

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[16] Fazeli H, Fatahi Bafghi M, Faghri M, Akbari R. Molecular study of PER and VEB genes is multidrug resistant Pseudomonas aeroginosa isolated from clinical specimens in Isfahan/Iran and their antibiotic resistance patterns. J Kerman Univ Med Sci 2012; 19(4): 345-53.
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[http://dx.doi.org/10.1128/AAC.50.5.1633-1641.2006] [PMID: 16641429]
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[http://dx.doi.org/10.15171/ijep.2018.26]
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[21] Tan J, Pitout JD, Guttman DS. New and sensitive assay for determining Pseudomonas aeruginosa metallo-beta-lactamase resistance to imipenem. J Clin Microbiol 2008; 46(5): 1870-2.
[http://dx.doi.org/10.1128/JCM.02175-07] [PMID: 18337388]
[22] Jamali SH, Bahar MA, Hoshmand M. Prevalence of VIM & IMP metallobetalactamase in imipenem resistant Pseudomonas aeroginosa isolated from burn patients. Knowledge Microbial 2009; 1(1): 19-25.
[23] Ranjbar R, Owlia P, Saderi H, et al. Characterization of Pseudomonas aeruginosa strains isolated from burned patients hospitalized in a major burn center in Tehran, Iran. Acta Med Iran 2011; 49(10): 675-9.
[PMID: 22071644]
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[26] Adabi M, Talebi Taher M, Arbabi L, et al. Determination of antibiotic resistance pattern of Pseudomonas aeruginosa strains isolated from patients with burn wounds. J Ardabil Univ Med Sci 2015; 15(1): 66-74.
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Endorsements



"Open access will revolutionize 21st century knowledge work and accelerate the diffusion of ideas and evidence that support just in time learning and the evolution of thinking in a number of disciplines."


Daniel Pesut
(Indiana University School of Nursing, USA)

"It is important that students and researchers from all over the world can have easy access to relevant, high-standard and timely scientific information. This is exactly what Open Access Journals provide and this is the reason why I support this endeavor."


Jacques Descotes
(Centre Antipoison-Centre de Pharmacovigilance, France)

"Publishing research articles is the key for future scientific progress. Open Access publishing is therefore of utmost importance for wider dissemination of information, and will help serving the best interest of the scientific community."


Patrice Talaga
(UCB S.A., Belgium)

"Open access journals are a novel concept in the medical literature. They offer accessible information to a wide variety of individuals, including physicians, medical students, clinical investigators, and the general public. They are an outstanding source of medical and scientific information."


Jeffrey M. Weinberg
(St. Luke's-Roosevelt Hospital Center, USA)

"Open access journals are extremely useful for graduate students, investigators and all other interested persons to read important scientific articles and subscribe scientific journals. Indeed, the research articles span a wide range of area and of high quality. This is specially a must for researchers belonging to institutions with limited library facility and funding to subscribe scientific journals."


Debomoy K. Lahiri
(Indiana University School of Medicine, USA)

"Open access journals represent a major break-through in publishing. They provide easy access to the latest research on a wide variety of issues. Relevant and timely articles are made available in a fraction of the time taken by more conventional publishers. Articles are of uniformly high quality and written by the world's leading authorities."


Robert Looney
(Naval Postgraduate School, USA)

"Open access journals have transformed the way scientific data is published and disseminated: particularly, whilst ensuring a high quality standard and transparency in the editorial process, they have increased the access to the scientific literature by those researchers that have limited library support or that are working on small budgets."


Richard Reithinger
(Westat, USA)

"Not only do open access journals greatly improve the access to high quality information for scientists in the developing world, it also provides extra exposure for our papers."


J. Ferwerda
(University of Oxford, UK)

"Open Access 'Chemistry' Journals allow the dissemination of knowledge at your finger tips without paying for the scientific content."


Sean L. Kitson
(Almac Sciences, Northern Ireland)

"In principle, all scientific journals should have open access, as should be science itself. Open access journals are very helpful for students, researchers and the general public including people from institutions which do not have library or cannot afford to subscribe scientific journals. The articles are high standard and cover a wide area."


Hubert Wolterbeek
(Delft University of Technology, The Netherlands)

"The widest possible diffusion of information is critical for the advancement of science. In this perspective, open access journals are instrumental in fostering researches and achievements."


Alessandro Laviano
(Sapienza - University of Rome, Italy)

"Open access journals are very useful for all scientists as they can have quick information in the different fields of science."


Philippe Hernigou
(Paris University, France)

"There are many scientists who can not afford the rather expensive subscriptions to scientific journals. Open access journals offer a good alternative for free access to good quality scientific information."


Fidel Toldrá
(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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