The Open Microbiology Journal




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

Molecular Study of Enterotoxins Genes of Staphylococcus aureus Isolated from Patients in Intensive Care Units



Maysaa El Sayed Zaki1, *, Mohamed A. Rizk1, Asmaa O. Bakr2
1 Clinical Pathology Department, Mansoura Faculty of Medicine, Mansoura, Egypt
2 Clinical Pathology Department, Aswan Faculty of Medicine, Aswan, Egypt

Abstract

Introduction:

Staphylococcus aureus is responsible for healthcare-associated sepsis. Various virulence genes may be responsible for the severity of the outcome of this infection.

Aims & objectives:

Therefore, the aim of the present study was to investigate the prevalence of enterotoxin genes in S .aureus associated with HCA sepsis affecting adult's patients in Intensive Care Units (ICU).

Materials & Methods:

The study is a cross-sectional observational study included 432 patients admitted to intensive care units with Healthcare-Associated Infections (HCAIs). The patients were subjected to blood culture and identification of the isolated bacteria according to the standard microbiological method. Isolates identified as S. aureus were subjected to molecular studies for the detection of meca gene and enterotoxins genes by multiplex Polymerase Chain Reaction (PCR).

Results & Discussion:

Blood culture was positive in 170 of the patients (39.3%). 47 of the blood culture yield S. aureu. Regarding studies of virulence genes in isolated S. aureus, the most frequent genes were seg (61.7%), mecA (46.8%) and sea (42.6%). The less frequent genes were tst and eta 6.4% for each. Analysis of demographic, clinical and virulence genes of isolated S. aureus to HAIs outcome reveals that the virulence genes namely mec, sei and tst of S. aureus were the only significant factors associated with death The distribution of enterotoxigenic genes among MRSA and MSSA shows a significant association between seg and sei genes in MRSA isolates.

Conclusion:

The present study highlights the prevalence of enterotoxin genes in isolated S.aureus from patients with hospital-acquired infections in intensive care units in a tertiary hospital. There was high prevalence as about two-thirds of the isolates harbor seg and sea genes in addition to methicillin resistance gene mecA. The fatal outcome of sepsis in those patients was associated with the presence of enterotoxin genes sei and tst. There is a need for screening patients admitted to intensive care units for S. aureus harboring these genes for proper management and application of isolation and contact guidelines of infection control

Keywords: MRSA, Enterotoxins, Multiplex PCR, Proper management, S. aureus, Enterotoxin genes.


Article Information


Identifiers and Pagination:

Year: 2018
Volume: 12
First Page: 381
Last Page: 389
Publisher Id: TOMICROJ-12-381
DOI: 10.2174/1874285801812010381

Article History:

Received Date: 28/7/2018
Revision Received Date: 1/11/2018
Acceptance Date: 13/11/2018
Electronic publication date: 30/11/2018
Collection year: 2018

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© 2018 Zaki 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 Clinical Pathology, Director of Infection Control Unit-Mansoura University Hospitals, Mansoura Faculty of Medicine, Mansoura city, ElGomhoria, Egypt; Tel: 0020502258877; E-mail: may_s65@hotmail.com




1. INTRODUCTION

Staphylococcus aureus (S.aureus) is a widely distributed pathogen, while it represents important colonizing bacteria in the anterior nares of about one-third healthy population [1Moran GJ, Krishnadasan A, Gorwitz RJ, et al. Emergency ID net study group. Methicillin-resistance S. aureus infections among patients in the emergency department. N Engl J Med 2006; 355: 666-74.[http://dx.doi.org/10.1056/NEJMoa055356] [PMID: 16914702] ]. S. aureus represents a major cause of infections in community-acquired and in Healthcare-Associated Infections (HCAIs) such as sepsis, endocarditis and soft tissue infections [2Valaperta R, Tejada MR, Frigerio M, et al. Staphylococcus aureus nosocomial infections: The role of a rapid and low-cost characterization for the establishment of a surveillance system. New Microbiol 2010; 33(3): 223-32.[PMID: 20954440] , 3Naimi TS, LeDell KH, Como-Sabetti K, et al. Comparison of community- and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA 2003; 290(22): 2976-84.[http://dx.doi.org/10.1001/jama.290.22.2976] [PMID: 14665659] ]. The consequences of the infections by S. aureus have increased by the development of antibiotics resistance especially to methicillin with widespread Methicillin-Resistant S. Aureus (MRSA) among HCAI [4Yao Z, Peng Y, Chen X, et al. Healthcare associated infections of methicillin-resistant Staphylococcus aureus: A case-control-control study. PLoS One 2015; 10(10): e0140604.[http://dx.doi.org/10.1371/journal.pone.0140604] [PMID: 26470023] ].

Sepsis caused by MRSA is defined as the second common cause of death in Europe and representing around 25% of death in the United States of America [4Yao Z, Peng Y, Chen X, et al. Healthcare associated infections of methicillin-resistant Staphylococcus aureus: A case-control-control study. PLoS One 2015; 10(10): e0140604.[http://dx.doi.org/10.1371/journal.pone.0140604] [PMID: 26470023] ].

The pathogenicity of S. aureus is associated by many factors such as multiple antibiotics resistance pattern especially of MRSA strains and the presence of several virulence factors and toxins production associated with some strains. The risk factors for acquiring HCAI associated with virulent S.aureus strains include prolonged hospitalization, prior antibiotics use, presence of prosthetic or central line, presence of immunocompromizing conditions such as diabetes mellitus and malignancy [5Morin CA, Hadler JL. Population-based incidence and characteristics of community-onset Staphylococcus aureus infections with bacteremia in 4 metropolitan Connecticut areas, 1998. J Infect Dis 2001; 184(8): 1029-34.[http://dx.doi.org/10.1086/323459] [PMID: 11574918] ].

Staphylococcus aureus has several virulence factors such as the microbial surface components that facilitate the adhesion of the bacteria to the prosthetic surfaces in addition to the secreted toxins and adhesion factors like hemolysins, leukocidins, enterotoxins, and exfoliative toxins that aid in invasion and spread of infection [6Schlievert PM, Strandberg KL, Lin YC, Peterson ML, Leung DY. Secreted virulence factor comparison between methicillin-resistant and methicillin-sensitive Staphylococcus aureus, and its relevance to atopic dermatitis. J Allergy Clin Immunol 2010; 125(1): 39-49.[http://dx.doi.org/10.1016/j.jaci.2009.10.039] [PMID: 20109735] ].

The toxicity of the produced toxins from S. aureus is associated with superantigens properties that lead to massive immune reactions such as that associated with enterotoxins production. The superantigens act by the release of massive proinflammatory cytokines that lead to massive inflammatory reactions. Superantigens act by direct strong activation of T lymphocytes without prior antigen presentation; it acts by binding to a specific variable region of the T cell antigen receptor-β-chain [7Llewelyn M, Cohen J. Superantigens: Microbial agents that corrupt immunity. Lancet Infect Dis 2002; 2(3): 156-62.[http://dx.doi.org/10.1016/S1473-3099(02)00222-0] [PMID: 11944185] ]. This leadsto a massive release of proinflammatorycytokines such as TNF-α, IL-6, and IFN-γ [8McCormick JK, Yarwood JM, Schlievert PM. Toxic shock syndrome and bacterial superantigens: An update. Annu Rev Microbiol 2001; 55: 77-104.[http://dx.doi.org/10.1146/annurev.micro.55.1.77] [PMID: 11544350] , 9Stevens DL. The toxic shock syndromes. Infect Dis Clin North Am 1996; 10(4): 727-46.[http://dx.doi.org/10.1016/S0891-5520(05)70324-X] [PMID: 8958166] ]. This systemic inflammatory reaction can contribute to the severity of S. aureus sepsis [10Holtfreter S, Bröker BM. Staphylococcal superantigens: Do they play a role in sepsis? Arch Immunol Ther Exp (Warsz) 2005; 53(1): 13-27.[PMID: 15761373] ].

Therefore, the aim of the present study was to investigate the prevalence of enterotoxin genes in S. aureus associated with HCA sepsis affecting adult's patients in Intensive Care Units (ICU) from Mansoura University Hospital, Egypt from May 2017 till April 2018.

2. MATERIALS AND METHODS

The study is a cross-sectional observational study conducted on Mansoura University Hospital, Egypt from May 2017 till April 2018. Patients were admitted to intensive care units in the hospital during this period. The study was approved by Mansoura Faculty of Medicine ethical committee and approval consents were obtained from the patients.

The patients were subjected to full clinical history registration by smartphone as a part of the national surveillance system of the infection control committee of Universities hospitals in cooperation with Center of Disease Control (CDC)-USA for hospital-acquired infections-phase 3. The registered data included demographic data, presence of comorbidity, cause of admission, presence of organ failure associated with sepsis, the signs associated with sepsis and the outcome either by discharge or death. The sepsis was identified as primary sepsis with no signs of other focus of infections; device associated bloodstream infections associated with the use of the devices such as a central venous catheter and secondary sepsis if there was the primary focus of infection.

2.1. Microbiological Culture

Ten Milliliter blood samples were collected from each patient completely under sterile conditions. Five milliliters of the blood was inoculated to aerobic blood culture and the other five was inoculated to the anaerobic blood culture bottles (BD BACTEC™ FX blood culture system). Positive blood culture bottles were subjected to subculture on blood agar at 37ºC for 24-48 hours. Colonies were subjected to identification by gram stain, coagulase and catalase tests for identification of S. aureus.

Antibiotics susceptibility tests were performed by disc diffusion method on Muller –Hinton agar according to the Clinical and Laboratory Standards Institute (CLSI) 2013 [11Clinical and Laboratory Standards Institute (CLSI) M100-S23 Wayne, Pa, USA: CLSI; 2013 Performance standards for antimicrobial susceptibility testing; twenty third informational supplement 2013. Available from: https://clsi.org/standards/products/microbiology/documents/m100/]. The used discs were imipenem (10μg/disk), amikacin (30µg), amoxicillin/clavulinic acid (30µg), ampicillin(10µg),ciprofloxacin (10μg), cefotaxime (30µg), ceftazidime (10µg), cefoxitin (10µg), trimethoprim/sulfamethaxone (25µg) erythromycin (15µg) (Oxoid-Thermo Fisher Scientific- Thermo Fisher Scientific 168 Third Avenue,Waltham, MA USA 02451). MRSA was defined as S. aureus resistant to cefoxitin.

2.2. Molecular Studies of Isolated S. aureus

2.2.1. DNA Extraction

The colonies that were identified to be S. aureus were subcultured on blood agar plates at 37ºC for overnight and the colonies were obtained and DNA was extracted by the boiling method as described previously [12Fitzgerald JR, Reid SD, Ruotsalainen E, et al. Genome diversification in Staphylococcus aureus: Molecular evolution of a highly variable chromosomal region encoding the Staphylococcal exotoxin-like family of proteins. Infect Immun 2003; 71(5): 2827-38.[http://dx.doi.org/10.1128/IAI.71.5.2827-2838.2003] [PMID: 12704157] ].

DNA was kept frozen at -20ºC till PCR.

2.2.2. Duplex PCR for Identification of MRSA

Identification of MRSA was performed by rapid duplex PCR described previously by Jonas et al., 2002 [13Jonas D, Speck M, Daschner FD, Grundmann H. Rapid PCR-based identification of methicillin-resistant Staphylococcus aureus from screening swabs. J Clin Microbiol 2002; 40(5): 1821-3.[http://dx.doi.org/10.1128/JCM.40.5.1821-1823.2002] [PMID: 11980967] ]. The principle of PCR is the use of four primers for mecA and femB in PCR. Positive isolates for both genes indicated MRSA. The sequences of the used primers were listed in Table 1.

Table 1
Genes, sequences of the used primers and the bp of the products.


The amplification process included denaturation at 94°C for 4 minutes (min), followed by 30 cycles of 45 seconds at 94°C, 45 seconds at 50°C, and 60 seconds at 72°C, with a final extension step at 72°C for 2 min. Ten microliter aliquots were loaded onto agarose gel electrophoresis 90 V for 90 minutes and stained with 10 μg of ethidium bromide/ml after electrophoresis.

2.2.3. Multiplex PCR for Enterotoxins Detection

Multiplex PCR was used by preparing a mixture A set with the primers mentioned in Table 1 and primers mixture B (Qiagen). The first reaction of PCR contained 10ng of template DNA with 20picomol (each) of sea, seb, sec, see, and femA primers in amplification mixture of 50 μl of the ready to use Qiagen amplification mixture. The second round of PCR, the primers used, were those for B mixture at a concentration of 20 pmol each for etb, tst, and femA and 50 pmol for eta. The following amplification steps were carried out in the first round and in the second round of PCR; denaturation at 94°C for 5 min was followed by 35 cycles of amplification (denaturation at 94°C for 2 min, annealing at 57°C for 2 min, and extension at 72°C for 1 min), ending with a final extension at 72°C for 7 min [14Mehrotra M, Wang G, Johnson WM. Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. J Clin Microbiol 2000; 38(3): 1032-5.[PMID: 10698991] ].

2.2.4. Quality Control for PCR

The strains used as positive control for PCR reactions were S. aureus ATCC 13565 (SEA), S. aureus ATCC 14458 (SEB), S. aureus ATCC 19095 (SEC), S. aureus90-S-1025 (SED), S. aureusATCC 27664 (SEE), S. aureus 88-S-8902 (ETA), S. aureus 88-S-8620 (ETB), S. aureus 92-S-1344 (TSST-1), and S. aureus 95-S-739 (mecA). Sterile distilled water was used as negative control.

2.2.5. Statistical Analysis

Data were collected, revised, coded and entered to the statistical package for social science (SPSS) version 20. The quantitative data were presented as mean, standard deviations and ranges. The comparison between the studied groups was done by using Chi-Square and P was considered significant when < 0.05.

3. RESULTS

The study included 432 patients admitted to intensive care units and suspected to have HCAIs. Blood culture was positive in 170 of the patients (39.3%). 47 of the blood culture yield S .aureus, data not shown.

The study of demographic and clinical data associated with HAIs due to S. aureus was summarized in Table 2. The patients were mainly female patients (53.2%) with mean age 52.6± 11.3 years. The main diagnostic sign was fever (80.9%) and hypotension (46.8%). The infection was associated with the presence of central venous catheter in 14.9% of the patients, ventilator in 4.3% and urinary catheter in 2.1%. The type of the HAIs was primary sepsis in 48.9% of the patients followed by secondary sepsis due to pneumonia in 34% of the patients and urinary tract infections in 17% of the patients. The outcome of the patients discharged in 61.7% and death in 38.3% of the patients, Table 2.

Table 2
Demographic, clinical data of patients with positive blood culture for S. aureus.


Regarding studies of virulence genes in isolated S. aureus, the most frequent genes were seg (61.7%), mecA (46.8%) and sea (42.6%). The less frequent genes were tst and eta (6.4%) for each, Table 3.

Table 3
Prevalence of mecA, and enterotoxins genes among S. aureus.


Analysis of demographic, clinical and virulence genes of isolated S. aureus to HAIs outcome reveals that the virulence genes namely mec, sei and tst of S.aureus were the only significant factors associated with death (P=0.0001, P=0.0001, P=0.05 respectively), Table 4.

Table 4
Comparative study between demographic, clinical and S. aureus genes among patients with fatal outcome and survivors.


The distribution of enterotoxigenic genes among MRSA and MSSA shows a significant association between seg and sei genes in MRSA isolates, Table 5.

Table 5
Distribution of enterotoxins genes among MRSA and MSSA.


Isolated S. aureus from blood culture had high resistance to betalactam antibiotics, ampicillin, amoxicillin/clavulinic acid (66%, 61.7% respectively). The lowest resistance was for imipenem followed amikacin (6.4%, 12.8% respectively), (Fig. 1).

4. DISCUSSION

The site of infections in ICU depends upon different factors such as the type of ICUs, the type of the patients served by the hospital and the method of surveillance depending method for identification of HAIs [15Gastmeier P, Sohr D, Just HM, Nassauer A, Daschner F, Rüden H. How to survey nosocomial infections. Infect Control Hosp Epidemiol 2000; 21(6): 366-70.[http://dx.doi.org/10.1086/501774] [PMID: 10879565] ]. In the present study, the surveillance method was performed by active detection of the clinical signs of infections for patients admitted to ICUs associated with laboratory diagnosis. The rate of positive blood culture for those patients(39.3%) was higher than the previously reported rate [16Braga IA, Campos PA, Gontijo-Filho PP, Ribas RM. Multi-hospital point prevalence study of healthcare-associated infections in 28 adult intensive care units in Brazil. J Hosp Infect 2018; 6701(18): 30141-5.]. However, the results were consistent with the reports determining that sepsis as one of the common hospital-acquired infections with pneumonia and urinary tract infections [16Braga IA, Campos PA, Gontijo-Filho PP, Ribas RM. Multi-hospital point prevalence study of healthcare-associated infections in 28 adult intensive care units in Brazil. J Hosp Infect 2018; 6701(18): 30141-5., 17Cairns S, Reilly J, Booth M. Prevalence of healthcare-associated infection in Scottish intensive care units. J Hosp Infect 2010; 76(4): 308-10.[http://dx.doi.org/10.1016/j.jhin.2010.05.010] [PMID: 20970880] ].

Fig. 1
Antibiotics resistance of isolated S.aureus.


The practice of patients care has many advances in the last decades among which are the use of invasive devices. The invasive devices such as central venous line and urinary catheters are associated with the introduction of virulent pathogens from the surrounding environment to patients with reduced immune states due to their diseases and associated comorbidity [18Hynes-Gay P, Lalla P, Leo M, Merrill-Bell A, Nicholson M, Villaruel E. Understanding sepsis: From SIRS to septic shock. Dynamics 2002; 13(1): 17-20.[PMID: 11951322] ]. In the present study, the sepsis was associated with a central venous catheter in 14.9%, ventilator in 4.3% and urinary catheter in 2.1%. These rates were higher than that reported previously by Sato et al., 2016 [19Sato R, Kuriyama A, Takada T, Nasu M, Luthe SK. Prevalence and risk factors of sepsis-induced cardiomyopathy: A retrospective cohort study 2016.] (3.4%) and lower than that reported by Braga et al. [17Cairns S, Reilly J, Booth M. Prevalence of healthcare-associated infection in Scottish intensive care units. J Hosp Infect 2010; 76(4): 308-10.[http://dx.doi.org/10.1016/j.jhin.2010.05.010] [PMID: 20970880] ], (87.%). The differences may be attributed to the difference in the site of infections and the types of ICUs. Moreover, there are differences in the compliance of healthcare workers to guidelines for infection control.

In the present study, S. aureus was isolated from 27.6% of positive blood culture. S. aureus is considered one of the most important pathogens, responsible for nosocomial infections. The prevalence rate of S. aureus was similar to a previous report [20Kao CH, Kuo YC, Chen CC, et al. Isolated pathogens and clinical outcomes of adult bacteremia in the emergency department: A retrospective study in a tertiary Referral Center. J Microbiol Immunol Infect 2011; 44(3): 215-21.[http://dx.doi.org/10.1016/j.jmii.2011.01.023] [PMID: 21524617] ].

The prevalence of MRSA strains among isolated S. aureus was around half of the isolates. This finding is online with the previous report from USA with rates up to 55% of isolated S.aureus defined as MRSA [21Cosgrove SE, Qi Y, Kaye KS, Harbarth S, Karchmer AW, Carmeli Y. The impact of methicillin resistance in Staphylococcus aureus bacteremia on patient outcomes: Mortality, length of stay, and hospital charges. Infect Control Hosp Epidemiol 2005; 26(2): 166-74.[http://dx.doi.org/10.1086/502522] [PMID: 15756888] ]. MRSA is associated with high mortality rates among patients admitted to ICUs, higher costs and prolonged hospital stay [21Cosgrove SE, Qi Y, Kaye KS, Harbarth S, Karchmer AW, Carmeli Y. The impact of methicillin resistance in Staphylococcus aureus bacteremia on patient outcomes: Mortality, length of stay, and hospital charges. Infect Control Hosp Epidemiol 2005; 26(2): 166-74.[http://dx.doi.org/10.1086/502522] [PMID: 15756888] ].

Regarding studies of virulence genes in isolated S. aureus, the most frequent genes were seg (61.7%), and sea (42.6%). The less frequent genes were tst and eta (6.4% for each). Different reports defined sea and seg genes as the most frequent enterotoxins genes associated with hospital-acquired sepsis [22Deodhar D, Varghese G, Balaji V, et al. Prevalence of toxin genes among the clinical isolates of Staphylococcus aureus and its clinical impact. J Glob Infect Dis 2015; 7(3): 97-102.[http://dx.doi.org/10.4103/0974-777X.162234] [PMID: 26392716] ]. Other report found tst and txt as the common enterotoxin genes in S. aureus isolates [23Abiri P. AkhavanSepahi A, Goudarzi H, Goudarzi M. Distribution of genes encoding toxin, adhesion, and antibacterial resistance among various sccmec types of methicillin-resistant Staphylococcus aureus isolated from intensive care unit, Tehran, Iran. Jundishapur J Microbiol 2017; 10(12): e14477.[http://dx.doi.org/10.5812/jjm.14477] ]. The distribution of enterotoxin genes differs according to geographic regions and types of studied patients.

The distinguished findings of the present study were the statistically significant association of the virulent genes mec, sei and tst of S. aureus with death.

Enterotoxins in S. aureus are associated with septic shock as they are known to be a strong inducer of the adaptive immune system as they act as a superantigen [17Cairns S, Reilly J, Booth M. Prevalence of healthcare-associated infection in Scottish intensive care units. J Hosp Infect 2010; 76(4): 308-10.[http://dx.doi.org/10.1016/j.jhin.2010.05.010] [PMID: 20970880] ]. There are strong evidence for this action in animals models, however, human studies are scarce [24Becker K, Friedrich AW, Lubritz G, Weilert M, Peters G, Von Eiff C. Prevalence of genes encoding pyrogenic toxin superantigens and exfoliative toxins among strains of Staphylococcus aureus isolated from blood and nasal specimens. J Clin Microbiol 2003; 41(4): 1434-9.[http://dx.doi.org/10.1128/JCM.41.4.1434-1439.2003] [PMID: 12682126] , 25Ferry T, Thomas D, Genestier AL, et al. Comparative prevalence of superantigen genes in Staphylococcus aureus isolates causing sepsis with and without septic shock. Clin Infect Dis 2005; 41(6): 771-7.[http://dx.doi.org/10.1086/432798] [PMID: 16107972] ]. The prevalence of specific enterotoxines genes of S. aureus among patients in different geographic location is not well known [25Ferry T, Thomas D, Genestier AL, et al. Comparative prevalence of superantigen genes in Staphylococcus aureus isolates causing sepsis with and without septic shock. Clin Infect Dis 2005; 41(6): 771-7.[http://dx.doi.org/10.1086/432798] [PMID: 16107972] ].

Isolated S. aureus from blood culture had high resistance to beta-lactam antibiotics, ampicillin, amoxicillin/clavulinic acid (66%, 61.7% respectively). The lowest resistance was for imipenem followed amikacin (6.4%, 12.8% respectively).

Staphylococcus aureus and especially MRSA strains have shown an increase resistance towards currently available beta-lactam antimicrobial agents such as penicillin and cephalosporins [26Deng JJ, Zhu JN, Yang CL, et al. Clinical distribution and drug resistance of Staphylococcus aureus isolated from hospitalized children. Sichuan Da Xue Xue Bao Yi Xue Ban 2013; 44(1): 159-61.[PMID: 23600232] ]. The microbiological study of antibiotics susceptibility pattern is an important issue to control infection with ICU by use of empiric therapy based upon locally prepared antibiotics policy. Other measures to control the spread of S .aureus is good hand hygiene practice and proper isolation precautions for patients infected with MRSA with active surveillance of the patients admitted to ICU to enhance contact precautions [27Muto CA, Jernigan JA, Ostrowsky BE, et al. SHEA guideline for preventing nosocomial transmission of multidrug-resistant strains of Staphylococcus aureus and enterococcus. Infect Control Hosp Epidemiol 2003; 24(5): 362-86.[PMID: 12785411] , 28Widmer AF, Lakatos B, Frei R. Strict infection control leads to low incidence of methicillin-resistant Staphylococcus aureus bloodstream infection over 20 years. Infect Control Hosp Epidemiol 2015; 36(6): 702-9.[http://dx.doi.org/10.1017/ice.2015.28] [PMID: 25721306] ].

CONCLUSION

The present study highlights the prevalence of enterotoxin genes in isolated S. aureus from patients with hospital-acquired infections in intensive care units in a tertiary hospital. There was high prevalence as about two-thirds of the isolates harbor seg and sea genes in addition to methicillin resistance gene mecA. The fatal outcome of sepsis in those patients was associated with the presence of enterotoxin genes sei and tst. There is a need for screening patients admitted to intensive care units for S. aureus harboring these genes for proper management and application of isolation and contact guidelines of infection control.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

The study was approved by Mansoura Faculty of Medicine committee.

HUMAN AND ANIMAL RIGHTS

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

CONSENT FOR PUBLICATION

Informed consent were obtained.

CONFLICT OF INTEREST

The author declares no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

Declared none.

REFERENCES

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[13] Jonas D, Speck M, Daschner FD, Grundmann H. Rapid PCR-based identification of methicillin-resistant Staphylococcus aureus from screening swabs. J Clin Microbiol 2002; 40(5): 1821-3.[http://dx.doi.org/10.1128/JCM.40.5.1821-1823.2002] [PMID: 11980967]
[14] Mehrotra M, Wang G, Johnson WM. Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. J Clin Microbiol 2000; 38(3): 1032-5.[PMID: 10698991]
[15] Gastmeier P, Sohr D, Just HM, Nassauer A, Daschner F, Rüden H. How to survey nosocomial infections. Infect Control Hosp Epidemiol 2000; 21(6): 366-70.[http://dx.doi.org/10.1086/501774] [PMID: 10879565]
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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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