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Research Article| Volume 8, ISSUE 4, P1043-1046, December 2020

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Frequency of methicillin-resistant Staphylococcus aureus (MRSA) in nose and cellular phone of medical and non-medical personnel of emergency departments of Ghaem hospital in Mashhad city

Published:March 29, 2020DOI:https://doi.org/10.1016/j.cegh.2020.03.017

      Abstract

      Background

      Staphylococcus aureus is one of the commensal bacteria and components of nose normal flora in 30–40% of people. The cellular phone is infected through the hands of a person who has already been infected with nasal discharge, in the hospital. Patients and family members with a weakened immune system are at high risk of contamination; the treatment procedure is difficult.

      Materials and methods

      200 individuals who were working in the emergency departments of Ghaem were included in the study. Sampling was done by three sterile swabs; two swabs from the nose and one from the surface of the cellular phone. The diagnosis was done according to the staphylococcus biochemical tests. Beta-lactamase positive staphylococcus was identified by nitrocefin. MIC method was performed using E-test strips and agar dilution for detecting the MRSA.

      Results

      86 out of 200 nasal, and 200 cellular phone samples were diagnosed as beta-lactamase positive staphylococci and sensitivity test was done. 17 out of 86 beta-lactamase positive Staphylococcus aureus samples were resistant to cefoxitin, piperacillin, ceftriaxone, and cefotaxime; just one of these 17 samples was resistant to vancomycin. 24 samples were contaminated with healthcare-associated MRSA (HA-MRSA). Totally, cellular phone and nasal discharge of 12% of studied individuals were infected with the HA-MRSA.

      Conclusion

      Cell phone usage should be prohibited in the hospital sections. Disinfection of the mobile phone should be taken when leaving the hospital, along with hand, face, and nose washing seriously. It is suggested to evaluate all persons working in hospitals regarding the contamination to MRSA.

      Keywords

      1. Introduction

      Staphylococcus aureus is a member of the micrococci family which is coagulase-positive; it is positive in gram staining too. Staphylococcus aureus is the main cause of septicemia, endocarditis, osteomyelitis, pneumonia, toxic shock syndrome, food poisoning, carbuncle, and furuncle. These complications are more prevalent among patients with a weakened immune system. It is found in the anterior part of the nose in adults and pediatrics as the primary source; it is found in the nose of 20–40% of healthy individuals too. The number of bacteria is higher in people who work in the hospital sectors. Staphylococcus aureus carriers are the main cause of Staphylococcal infections.
      • Ramana K.V.
      • Mohanty S.K.
      • Wilson C.G.
      Staphylococcus aureus colonization of anterior nares of school going children.
      ,
      • Klein E.
      • Smith D.L.
      • Laxminarayan R.
      Community-associated methicillin-resistant Staphylococcus aureus in outpatients, United States, 1999–2006.
      Staphylococci were sensitive to penicillin before 1940. It was the first antibiotic that was used for treatment in 1941. After a short time, strains containing beta-lactamase enzymes were generated in Staphylococcus aureus and resistance was spread in the environment. The lack of binding of β-lactams to Penicillin-Binding proteins (PBPs) is the main cause of Staphylococcus aureus resistance to the antibiotics. These proteins are responsible for building the bacterial cell wall; they are targeted by beta-lactam antibiotics. PBP2a is one of the subgroups of mutant PBPs; it is 78 kDa. It increases the resistance of Staphylococcus aureus to beta-lactams due to the high expression and low binding to beta-lactams.
      • Rahimi F.
      • Karimi S.
      Antibiotic resistance pattern and prophage typing of methicillin resistant Staphylococcus aureus strains isolated from chicken husbandries in tehran.
      ,
      • Plata K.
      • Rosato A.E.
      • Wegrzyn G.
      Staphylococcus aureus as an infectious agent: overview of biochemistry and molecular genetics of its pathogenicity.
      The production of this new protein is linked to the mec genes which are found in the bacterium genome. The emergence of MRSA strains is a therapeutic problem in patients. PBP2a is encoded by the mecA gene and transported by the SCCmec (Staphylococcal Cassette Chromosome mec) large cassette gene. This cassette consists of three parts: ccr complex, mec complex, and J regions. There are five main types of SCCmec (types VI-I), based on the characteristics of this genetic region. Mainly, it causes resistance to methicillin and other beta-lactams. The presence or the absence of the mecA gene determine methicillin resistance or susceptibility. MRSA is resistant to beta-lactam antibiotics such as penicillin, methicillin, nafcillin, and oxacillin. MRSA is one of the most prevalent pathogens in the world that is responsible for a wide range of nosocomial infections.
      • Havaei S.A.
      • Vidovic S.
      • Tahmineh N.
      • et al.
      Epidemic methicillin-susceptible Staphylococcus aureus lineages are the main cause of infections at an Iranian university hospital.
      ,
      • Havaei S.A.
      • Halaji M.
      • Vidovic S.
      • et al.
      Prevalence and genotyping of methicillin-resistant and-susceptible Staphylococcus aureus strains isolated from patients in a university hospital, Isfahan, Iran.
      Studies have shown that contaminated medical staff (including doctors, nurses, and even service personnel in departments) are common sources of antibiotic-resistant Staphylococcus aureus epidemics in the hospital. MRSA which are separated from hospitals are called Healthcare-associated MRSA (HA-MRSA), and those which are separated from the community are named Community-Acquired MRSA (CA-MRSA). When you use a mobile phone, nose colonized staphylococci are placed on the mobile surface. According to the drought resistance of bacterium, it will be able to survive on the mobile surface. Mobile reuse will contaminate the fingers and then other consumables, and eventually will transfer to the next person. Hospital staff including physicians, nurses, health care providers, and even service personnel, are at risk.
      • Rezazadeh M.
      • Yousefi M.R.
      • Sarmadian H.
      • Ghaznavirad E.
      Antibiotic Profile of Methicillin-Resistant Staphylococcus aureus with Multiple-Drug Resistances Isolated from Nosocomial Infections in Vali-Asr Hospital of Arak.
      • Sobhani Poor M.H.
      • Mansouri S.
      • Saeidadeli N.
      Prevalence of methicillin-resistant Staphylococcus aureus (MRSA) and antibiotic resistance patterns of the isolates from the nose of training soldiers in kerman in 2012.
      • Otter J.A.
      • French G.L.
      Molecular epidemiology of community-associated meticillin-resistant Staphylococcus aureus in Europe.
      Today, despite therapeutic antibiotics, MRSA strains have spread in many parts of the world, especially in hospitals and health centers.
      • Feßler A.T.
      • Schünemann R.
      • Kadlec K.
      • et al.
      Methicillin-resistant Staphylococcus aureus (MRSA) and methicillin-resistant Staphylococcus pseudintermedius (MRSP) among employees and in the environment of a small animal hospital.
      Therefore, we aimed to obtain samples from nasal discharge and cell phones in the emergency Departments of Ghaem Hospital in Mashhad city, Iran. The isolates of MRSA-HA were examined for antibiotic resistance.

      2. Material and methods

      In the present study, 200 medical personnel of Ghaem hospital of Mashhad were selected from five emergency departments including internal, neurosurgery, surgery, pediatrics and heart. Sampling was done during May–November 2017.146 out of studied individuals were female (85.6%), and 17 (14.2%) were male. Sampling was done by three swabs from each of the subjects. Samples were taken from each nostril using two sterile wet swabs. The swab was passed about one cm in the nostril and rotated; the rotation was done five times. The third swap was used for the cellphone surface. Totally, 400 samples were assessed by swab for the presence of HA-MRSA in this study. The samples were cultivated at nutrient broth medium at 37 °C for 24 h; then recultivated on the agar medium. After 18 h of incubation, the colonies were stained by gram method. Gram-positive cocci were detected, and Staphylococcus aureus was evaluated by biochemical tests such as catalase, coagulase, Mannitol, DNase and Novobiocin Test. Also, the Nitrocefin test was used for identifying the beta-lactamase positive Staphylococcus.
      • Safdari H.
      • Neshani A.
      • Sadeghian A.
      • Ebrahimi M.
      • Iranshahi M.
      • Sadeghian H.
      Potent and selective inhibitors of class A β-lactamase: 7-prenyloxy coumarins.
      To identify Staphylococcus aureus resistance to methicillin (MRSA), the concentration equivalent to 0.5 McFarland standard was used to cultivate on Müller Hinton agar. The Kirby-Bauer method test was performed for antibiotics including ceftriaxone, vancomycin, piperacillin, imipenem, cefoxitin, cefotaxime.
      • Hudzicki J.
      Kirby-Bauer Disk Diffusion Susceptibility Test Protocol.

      3. Results

      After conducting biochemical tests, 251 positive samples of Staphylococcus aureus were detected; including 164 samples from nasal secretions and 87 from mobile phones. Data is provided in detail in table number 1. The rate of positive beta-lactamase staphylococci isolated from the nose and the cell phone was 31% (62) and 12%
      • Dibah S.
      • Arzanlou M.
      • Jannati E.
      • Shapouri R.
      Prevalence and antimicrobial resistance pattern of methicillin resistant Staphylococcus aureus (MRSA) strains isolated from clinical specimens in Ardabil, Iran.
      among the staff of the hospital, respectively (see Table 1).
      86 samples of beta-lactamase positive Staphylococcus aureus were evaluated from the point of the sensitivity test. 17 were resistant to cefoxitin, piperacillin, ceftriaxone, and cefotaxime; interestingly, one of these 17 samples showed resistance to vancomycin (Table 2). Also. In this study, 24 samples from the cell phone of the Emergency staff and their nasal swab was similar for the type of HA-MRSA bacteria and also for the antibiotic susceptibility. The surface of the mobile phone and nasal discharge of 12% of the studied personnel were infected with HA-MRSA. It is possible that the bacteria transmitted from the nasal discharge to the cellular phone surface, which leads to cell phone contamination. In this study, the prevalence of beta-lactamase positive Staphylococcus aureus (isolated from nasal discharge) was 31% in Ghaem Hospital emergency department staff.
      Table 1Frequency of β-lactamase positive Staphylococcus aureus from mobile samples and nasal secretions.
      Numberbeta-lactamase Positive
      Mobile surface samples20024 (12%)
      Nasal discharge samples20062 (31%)
      Table 2Antibiogram results of Staphylococcus aureus isolated from nasal secretion and phone surfaces.
      BacteriaNasal secretionPhone surface
      AntibioticnumberSensitive

      %))
      Resistant (%)numbersensitive (%)Resistant (%)
      S. aureusvancomycin6261 (98.84%)1 (1.16%)2424 (100%)100%
      S. aureusceftriaxone6262 (100%)100%2420 (83.3%)4 (16.6%)
      S. aureuscefotaxime6262 (100%)100%2420 (83.3%)4 (16.6%)
      S. aureuscefoxitin6260 (96.7%)2 (3.3%)2424 (100%)100%
      S. aureuspiperacillin6262 (100%)100%222 (91.6%)2 (8.4%)
      S. aureusimipenem6258 (93.54%)4 (6.46%)024 (100%)24 (100%)
      S. aureusaztreonam6258 (93.54%)4 (6.46%)024 (100%)24 (100%)

      4. Discussion

      Increasing antibiotic-resistant microorganisms is one of the most serious problems in health care systems.
      • Appelbaum P.C.
      Microbiology of antibiotic resistance in Staphylococcus aureus.
      • Khaledi A.
      • Esmaeili D.
      • Jamehdar S.A.
      • Esmaeili S.-A.
      • Neshani A.
      • Bahador A.
      Expression of MFS efflux pumps among multidrug resistant Acinetobacter baumannii clinical isolates.
      • Esmaeili D.
      • Daymad S.F.
      • Neshani A.
      • Rashki S.
      • Marzhoseyni Z.
      • Khaledi A.
      Alerting prevalence of MBLs producing Pseudomonas aeruginosa isolates.
      • Kholoujini M.
      • Karami P.
      • Khaledi A.
      • Neshani A.
      • Matin P.
      • Alikhani M.Y.
      Identification of Pathogenic Bacteria in Blood Cultures and Susceptibility Testing of Isolates with Various Antibiotics.
      • Neshani A.
      • Zare H.
      • Eidgahi M.R.A.
      • Khaledi A.
      • Ghazvini K.
      Epinecidin-1, a highly potent marine antimicrobial peptide with anticancer and immunomodulatory activities.
      • Mansury D.
      • Khaledi A.
      • Ghazvini K.
      • et al.
      Study of bacterial infections among patients receiving kidney transplant in Mashhad, Iran.
      One of the most common antibiotic-resistant bacteria is MRSA. Identification of MRSA contaminated staff in hospital wards can prevent the spread of this type of resistance.
      • Feßler A.T.
      • Schünemann R.
      • Kadlec K.
      • et al.
      Methicillin-resistant Staphylococcus aureus (MRSA) and methicillin-resistant Staphylococcus pseudintermedius (MRSP) among employees and in the environment of a small animal hospital.
      Our result showed that the prevalence of MRSA isolated from the nose and the cell phone was 31% (62) and 12%
      • Dibah S.
      • Arzanlou M.
      • Jannati E.
      • Shapouri R.
      Prevalence and antimicrobial resistance pattern of methicillin resistant Staphylococcus aureus (MRSA) strains isolated from clinical specimens in Ardabil, Iran.
      among the staff of the hospital, respectively.
      Rahimi et al. reported the rate of isolated MRSA from different hospitals in Tehran; it was 29.7%, which was almost consistent with our results.
      • Rahimi F.
      • Karimi S.
      Antibiotic resistance pattern and prophage typing of methicillin resistant Staphylococcus aureus strains isolated from chicken husbandries in tehran.
      The study by Kannan Sridhara et al., in 2014 reported 58.8% positive MRSA among nurses in a tertiary care hospital.
      • Sridharan K.
      • Mallik A.
      • Madan M.
      Prevalence of methicillin-resistant Staphylococcus aureus among hospital healthcare workers in a tertiary care hospital: a cross-sectional study.
      In the study by Nabil Abdullah et al. in Shifa hospital, MRSA carriage rate was highest among nurses.
      • El Aila N.A.
      • Al Laham N.A.
      • Ayesh B.M.
      Nasal carriage of methicillin resistant Staphylococcus aureus among health care workers at Al Shifa hospital in Gaza Strip.
      The Study by Jann-Tay Wang et al. among adults in Community Settings in Taiwan indicated that the MRSA colonization rate was 3.8%. Of course, it is necessary to mention this point that the samples were collected from the community, not healthcare personnel.
      • Saba C.K.S.
      • Amenyona J.K.
      • Kpordze S.W.
      Prevalence and pattern of antibiotic resistance of Staphylococcus aureus isolated from door handles and other points of contact in public hospitals in Ghana.
      In a study done by Schultz, 7.6% of the isolates from the nose of training soldiers were identified as MRSA; all of them were sensitive to vancomycin
      • Schultz M.
      Methicillin-resistant Staphylococcus aureus (MRSA) what the pharmacist should know.
      . Another study on the military population and their families in the United States by Kenner et al., in 2003 showed that 40% of the people had nasal staphylococci and 2%
      • Sobhani Poor M.H.
      • Mansouri S.
      • Saeidadeli N.
      Prevalence of methicillin-resistant Staphylococcus aureus (MRSA) and antibiotic resistance patterns of the isolates from the nose of training soldiers in kerman in 2012.
      carried MRSA in the nose.
      • Kenner J.
      • O'connor T.
      • Piantanida N.
      • et al.
      Rates of carriage of methicillin-resistant and methicillin-susceptible Staphylococcus aureus in an outpatient population.
      The study by Solmaz Dibah, which was done in Iran in 2014, found MRSA in 46.3% of isolates. Most of the MRSA strains (68.4%) were obtained from ICU hospitalized patients; all were susceptible to vancomycin
      • Dibah S.
      • Arzanlou M.
      • Jannati E.
      • Shapouri R.
      Prevalence and antimicrobial resistance pattern of methicillin resistant Staphylococcus aureus (MRSA) strains isolated from clinical specimens in Ardabil, Iran.
      . The study by Ramin Dibaj et al. in Esfahan Kindergartens demonstrated that 9.5% of children carried MRSA. All MRSA were susceptible to vancomycin
      • Dibaj R.
      • Shoaei P.
      • Shojaei H.
      Study of prevalence and characteristics of Staphylococcus aureus and CA-MRSA nasal colonization in 2-5 Years old children in isfahan.
      .
      In some studies, the prevalence of MRSA contamination in mobile phones was investigated. For example, a study done by Selim et al. in Egypt, for the identification of microbial contamination of mobile phones in a health care setting. The most prevalent bacterial contaminants were methicillin-resistant S. aureus (53%).
      • Selim H.S.
      • Abaza A.F.
      Tambe et al. reported 56.16% as the rate of contamination of cell phones among Health Care personnel.
      • Tambe N.N.
      • Pai C.
      A study of microbial flora and MRSA harboured by mobile phones of health care personnel.
      In the study by Shekhar Pal et al. bacterial growth was shown in 81.8% of mobile phone swab samples. The most predominant isolates were Staphylococcus aureus which can transfer to the patients.
      • Pal S.
      • Juyal D.
      • Adekhandi S.
      • et al.
      Mobile phones: reservoirs for the transmission of nosocomial pathogens.
      In the study done by Almugadam BS et al., the prevalence of positive culture among mobile phone, ear, and hand swabs were 95% (57/60), 100% (30/30) and 96.7% (29/30), respectively; the frequency of MRSA was 98.6%.
      • Almugadam B.S.A.H.
      • Osman M.B.
      • Omer S.M.
      Frequency of MRSA isolates in mobile phones, ears and hands of healthcare workers.
      In a study for the determination of antibiotic resistance of S. aureus isolated from door handles and other points of contact in public hospitals in Ghana, 17% were putative MRSA isolates. Also, One MRSA isolate was resistant to all the used antibiotics (cefoxitin, oxacillin, ciprofloxacin, erythromycin, tetracycline, ampicillin, streptomycin, and sulfamethoxazole-trimethoprim.
      • Saba C.K.S.
      • Amenyona J.K.
      • Kpordze S.W.
      Prevalence and pattern of antibiotic resistance of Staphylococcus aureus isolated from door handles and other points of contact in public hospitals in Ghana.
      Investigation of Prevalence and antibiotic resistance pattern of methicillin-resistant Staphylococcus aureus in the Orthopaedic Hospital in Nigeria by Udobi et al. showed resistance pattern of: ampicillin 100%, pefloxacin 90.9%, ceftriaxone 69.7%, gentamicin 54.5%, and ciprofloxacin 51.5%.
      • Udobi C.
      • Obajuluwa A.
      • Onaolapo J.
      Prevalence and antibiotic resistance pattern of methicillin-resistant Staphylococcus aureus from an orthopaedic hospital in Nigeria.
      The study by Anupriya et al. revealed that microbial contamination of mobile phones in a tertiary care hospital was 87.3% and 56.4% among health care workers versus non-health care workers, but there was no MRSA.
      • Anupriya A.
      • Puhalenthi K.
      • Prethi R.
      • Hemasri V.
      Microbial contamination of mobile phones in a teritary care hospital.
      A Study by Nirmal et al. among health-care workers, explained that HA-MRSA carriage was seen in 47 individuals in their nasal vestibules; the colonization rate was 15.1%. HA-MRSA was also isolated from the cell phone surfaces.
      In this study, antibiotic susceptibility tests revealed that the HA-MRSA isolates are sensitive to most antibiotics, but there was a high rate of resistance against erythromycin (48%) and clindamycin (29%).
      • Pathare N.A.
      • Asogan H.
      • Tejani S.
      • et al.
      Prevalence of methicillin resistant Staphylococcus aureus [MRSA] colonization or carriage among health-care workers.
      In contrast, our current study shows a significantly higher percentage of nasal carriage of HA-MRSA. However, our results are similar to the Chinese study conducted in 2011.
      • Song J.-H.
      • Hsueh P.-R.
      • Chung D.R.
      • et al.
      Spread of methicillin-resistant Staphylococcus aureus between the community and the hospitals in Asian countries: an ANSORP study.
      The prevalence of MRSA indicates that the beta-lactamase positive staphylococci in non-hospital place are much lower in comparison to hospital, which can be a hazard to hospital staff.

      5. Conclusion

      Our result showed that the prevalence of MRSA is lower in non-hospital place in comparison to the hospital, and also since the cell phone is used in different places, can easily transmit the bacteria from the hospital environment to children, older people and who have a weakened immune system. Therefore, it is suggested to evaluate all people working in hospitals regarding the contamination to MRSA. Meanwhile, cell phone usage should be prohibited in the hospital sections. Disinfection of the mobile phone when leaving the hospital along with hand, face, and nose washing should be taken seriously.

      Declaration of competing interest

      The authors whose names are listed immediately below certify that they have NO affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript.

      References

        • Ramana K.V.
        • Mohanty S.K.
        • Wilson C.G.
        Staphylococcus aureus colonization of anterior nares of school going children.
        Indian J Pediatr. 2009; 76 (813–6)
        • Klein E.
        • Smith D.L.
        • Laxminarayan R.
        Community-associated methicillin-resistant Staphylococcus aureus in outpatients, United States, 1999–2006.
        Emerg Infect Dis. 2009; 15: 1925
        • Rahimi F.
        • Karimi S.
        Antibiotic resistance pattern and prophage typing of methicillin resistant Staphylococcus aureus strains isolated from chicken husbandries in tehran.
        Iran. J. Clin. Infect. Dis. Trop. Med. 2014; 18: 17-22
        • Plata K.
        • Rosato A.E.
        • Wegrzyn G.
        Staphylococcus aureus as an infectious agent: overview of biochemistry and molecular genetics of its pathogenicity.
        Acta Biochim Pol. 2009; 56: 597
        • Havaei S.A.
        • Vidovic S.
        • Tahmineh N.
        • et al.
        Epidemic methicillin-susceptible Staphylococcus aureus lineages are the main cause of infections at an Iranian university hospital.
        J Clin Microbiol. 2011; 49: 3990-3993
        • Havaei S.A.
        • Halaji M.
        • Vidovic S.
        • et al.
        Prevalence and genotyping of methicillin-resistant and-susceptible Staphylococcus aureus strains isolated from patients in a university hospital, Isfahan, Iran.
        Jundishapur J Microbiol. 2017; 10
        • Rezazadeh M.
        • Yousefi M.R.
        • Sarmadian H.
        • Ghaznavirad E.
        Antibiotic Profile of Methicillin-Resistant Staphylococcus aureus with Multiple-Drug Resistances Isolated from Nosocomial Infections in Vali-Asr Hospital of Arak.
        2013
        • Sobhani Poor M.H.
        • Mansouri S.
        • Saeidadeli N.
        Prevalence of methicillin-resistant Staphylococcus aureus (MRSA) and antibiotic resistance patterns of the isolates from the nose of training soldiers in kerman in 2012.
        Iran J Med Microbiol. 2014; 8: 15-21
        • Otter J.A.
        • French G.L.
        Molecular epidemiology of community-associated meticillin-resistant Staphylococcus aureus in Europe.
        Lancet Infect Dis. 2010; 10: 227-239
        • Feßler A.T.
        • Schünemann R.
        • Kadlec K.
        • et al.
        Methicillin-resistant Staphylococcus aureus (MRSA) and methicillin-resistant Staphylococcus pseudintermedius (MRSP) among employees and in the environment of a small animal hospital.
        Vet Microbiol. 2018; 221: 153-158
        • Safdari H.
        • Neshani A.
        • Sadeghian A.
        • Ebrahimi M.
        • Iranshahi M.
        • Sadeghian H.
        Potent and selective inhibitors of class A β-lactamase: 7-prenyloxy coumarins.
        J Antibiot. 2014; 67: 373
        • Hudzicki J.
        Kirby-Bauer Disk Diffusion Susceptibility Test Protocol.
        2009
        • Appelbaum P.C.
        Microbiology of antibiotic resistance in Staphylococcus aureus.
        Clin Infect Dis. 2007; 45: S165-S170
        • Khaledi A.
        • Esmaeili D.
        • Jamehdar S.A.
        • Esmaeili S.-A.
        • Neshani A.
        • Bahador A.
        Expression of MFS efflux pumps among multidrug resistant Acinetobacter baumannii clinical isolates.
        Der Pharm Lett. 2016; 8: 262-267
        • Esmaeili D.
        • Daymad S.F.
        • Neshani A.
        • Rashki S.
        • Marzhoseyni Z.
        • Khaledi A.
        Alerting prevalence of MBLs producing Pseudomonas aeruginosa isolates.
        Gene Reports. 2019; 16100460
        • Kholoujini M.
        • Karami P.
        • Khaledi A.
        • Neshani A.
        • Matin P.
        • Alikhani M.Y.
        Identification of Pathogenic Bacteria in Blood Cultures and Susceptibility Testing of Isolates with Various Antibiotics.
        2016
        • Neshani A.
        • Zare H.
        • Eidgahi M.R.A.
        • Khaledi A.
        • Ghazvini K.
        Epinecidin-1, a highly potent marine antimicrobial peptide with anticancer and immunomodulatory activities.
        BMC Pharmacol. Toxicol. 2019; 20: 33
        • Mansury D.
        • Khaledi A.
        • Ghazvini K.
        • et al.
        Study of bacterial infections among patients receiving kidney transplant in Mashhad, Iran.
        Exp. Clin. Transplant. 2018; 16: 282-286
        • Sridharan K.
        • Mallik A.
        • Madan M.
        Prevalence of methicillin-resistant Staphylococcus aureus among hospital healthcare workers in a tertiary care hospital: a cross-sectional study.
        Int. J. Health. Allied Sci. 2016; 5: 169
        • El Aila N.A.
        • Al Laham N.A.
        • Ayesh B.M.
        Nasal carriage of methicillin resistant Staphylococcus aureus among health care workers at Al Shifa hospital in Gaza Strip.
        BMC Infect Dis. 2017; 17: 28
        • Saba C.K.S.
        • Amenyona J.K.
        • Kpordze S.W.
        Prevalence and pattern of antibiotic resistance of Staphylococcus aureus isolated from door handles and other points of contact in public hospitals in Ghana.
        Antimicrob Resist Infect Contr. 2017; 6: 44
        • Schultz M.
        Methicillin-resistant Staphylococcus aureus (MRSA) what the pharmacist should know.
        SA Pharm J. 2009; 76: 28-30
        • Kenner J.
        • O'connor T.
        • Piantanida N.
        • et al.
        Rates of carriage of methicillin-resistant and methicillin-susceptible Staphylococcus aureus in an outpatient population.
        Infect Contr Hosp Epidemiol. 2003; 24: 439-444
        • Dibah S.
        • Arzanlou M.
        • Jannati E.
        • Shapouri R.
        Prevalence and antimicrobial resistance pattern of methicillin resistant Staphylococcus aureus (MRSA) strains isolated from clinical specimens in Ardabil, Iran.
        Iran J Microbiol. 2014; 6: 163
        • Dibaj R.
        • Shoaei P.
        • Shojaei H.
        Study of prevalence and characteristics of Staphylococcus aureus and CA-MRSA nasal colonization in 2-5 Years old children in isfahan.
        Iran J Med Microbiol. 2014; 8: 22-30
        • Selim H.S.
        • Abaza A.F.
        Microbial Contamination of Mobile Phones in a Health Care Setting in Alexandria, Egypt. vol. 10. GMS hygiene and infection control, 2015
        • Tambe N.N.
        • Pai C.
        A study of microbial flora and MRSA harboured by mobile phones of health care personnel.
        Int J Recent Trends Sci Technol. 2012; 4: 14-18
        • Pal S.
        • Juyal D.
        • Adekhandi S.
        • et al.
        Mobile phones: reservoirs for the transmission of nosocomial pathogens.
        Adv Biomed Res. 2015; 4
        • Almugadam B.S.A.H.
        • Osman M.B.
        • Omer S.M.
        Frequency of MRSA isolates in mobile phones, ears and hands of healthcare workers.
        Antimicrob Agents. 2018; 4: 161
        • Udobi C.
        • Obajuluwa A.
        • Onaolapo J.
        Prevalence and antibiotic resistance pattern of methicillin-resistant Staphylococcus aureus from an orthopaedic hospital in Nigeria.
        BioMed Res Int. 2013; 2013
        • Anupriya A.
        • Puhalenthi K.
        • Prethi R.
        • Hemasri V.
        Microbial contamination of mobile phones in a teritary care hospital.
        Int. J. Community Med. Public Health. 2018; 5: 2313-2316
        • Pathare N.A.
        • Asogan H.
        • Tejani S.
        • et al.
        Prevalence of methicillin resistant Staphylococcus aureus [MRSA] colonization or carriage among health-care workers.
        J. Infect. Public Health. 2016; 9: 571-576
        • Song J.-H.
        • Hsueh P.-R.
        • Chung D.R.
        • et al.
        Spread of methicillin-resistant Staphylococcus aureus between the community and the hospitals in Asian countries: an ANSORP study.
        J Antimicrob Chemother. 2011; 66: 1061-1069