|Year : 2018 | Volume
| Issue : 1 | Page : 87-95
Nasal colonization of methicillin-resistant Staphylococcus aureus among medical residents in Al-Azhar University Hospital, Damietta branch
Alaa Eldeen M Hashim1, Ali I Ali1, Khaled Elmola1, Mohammed A Ameen2, Hany Awdalla1, Ahmed A El hady1, Fathia M El raey1
1 Department of Tropical Medicine, Damietta, Cairo, Egypt
2 Department of Microbiology, Damietta, Cairo, Egypt
|Date of Submission||18-Nov-2016|
|Date of Acceptance||08-Dec-2016|
|Date of Web Publication||20-Nov-2018|
Ahmed A El hady
Department of Tropical Medicine, Damietta, Cairo
Source of Support: None, Conflict of Interest: None
Background Methicillin-resistant Staphylococcus aureus (MRSA) is a common nosocomial pathogen that causes infections among healthcare workers.
Objective The aim of this study was to detect the prevalence of MRSA among medical residents in different departments of Al-Azhar University Hospital, Damietta branch.
Patients and methods Eighty-four medical residents were subjected to a questionnaire that included questions on personal data, occupational experience, antimicrobial intake, infection-control training, and implementation of infection-control programs in the hospital, and a check list that indicated individual adherence to infection-control measures and bacteriological study for isolation and identification of MRSA. Nasal swabs were obtained from 84 residents. The isolates were identified as S. aureus on the basis of morphology, Gram stain, catalase test, coagulase test, mannitol salt agar fermentation, and cefoxitin disc diffusion.
Results The overall bacteria-carriage rate among residents was 41 (48.8%). The highest rate was found in ICU [seven (8.3%)], surgery [six (7.1%)], orthopedics [four (4.7%)], and gynecology [four (4.7%)] departments. Nineteen (22.6%) of all infections were S. aureus, 20 (23.8%) were coagulase-negative Staphylococcus, and two (2.4%) were Streptococcus; 15 (17.9%) S. aureus were MRSA strains, whereas four (4.7%) were methicillin-susceptible S. aureus strains. Thus, the nasal carriage rate of MRSA among the participating residents was 15 (17.2%). The overall MRSA carriage rate among residents was 15 (17.8%). The highest rate was found in neurosurgery [three (3.5%)], ICU [two (2.3%)], surgery [two (2.3%)], cardiothoracic [two (2.3%)], and gynecology [two (2.3%)] departments. There was an insignificant association between age, residence, frequency of antibiotic intake, duration of work, and carriage rate of MRSA among the participating healthcare workers.
Conclusion We concluded that it is important to detect the carriers of bacteria and ensure decolonization to reduce the transmission of S. aureus in the hospital.
Keywords: medical residents, methicillin-resistant Staphylococcus aureus, nasal carriers
|How to cite this article:|
Hashim AM, Ali AI, Elmola K, Ameen MA, Awdalla H, El hady AA, El raey FM. Nasal colonization of methicillin-resistant Staphylococcus aureus among medical residents in Al-Azhar University Hospital, Damietta branch. Al-Azhar Assiut Med J 2018;16:87-95
|How to cite this URL:|
Hashim AM, Ali AI, Elmola K, Ameen MA, Awdalla H, El hady AA, El raey FM. Nasal colonization of methicillin-resistant Staphylococcus aureus among medical residents in Al-Azhar University Hospital, Damietta branch. Al-Azhar Assiut Med J [serial online] 2018 [cited 2019 Aug 20];16:87-95. Available from: http://www.azmj.eg.net/text.asp?2018/16/1/87/244149
| Introduction|| |
Staphylococcus aureus, including methicillin-resistant S. aureus (MRSA) strains, are cluster-forming facultative anaerobes, Gram-positive cocci with the intrinsic ability to ferment carbohydrates, producing white to deep yellow pigmentation on solid culture media. They also ferment mannitol, turning mannitol salt agar (MSA) yellow .
MRSA isolates are strains of S. aureus that are resistant to methicillin (a potent bacterial cell wall inhibitor). MRSA is found in both hospital and community settings .
MRSA emerged in the health sector and became a global public health problem in 1961, when the first strain of S. aureus that was methicillin resistant was reported in the UK, thus making it the first report of MRSA in the world .
Staphylococcal infections cause significant morbidity and mortality in both community and hospital settings. Treatment of infection caused by S. aureus has become more problematic since the development of antimicrobial-resistant S. aureus (MRSA). As the MRSA strains are resistant to all β-lactam antibiotics, the treatment options are limited significantly .
The incidence of nosocomial infections caused by MRSA continues to increase worldwide. Infections caused by MRSA strains are associated with longer hospital stay, prolonged antibiotic administration, and higher costs than infections caused by methicillin-susceptible S. aureus (MSSA) strains. The presence of S. aureus in the anterior nares of patients may serve as a source of infection to other patients and is known to be a significant risk factor. Within the hospital, healthcare workers (HCWs) harboring bacterial colonies act as reservoirs for the spread of MRSA to susceptible patients not harboring bacterial colonies .
The ecological niche of S. aureus strains is the anterior nares. Studies have shown that the nares are the area from which this organism can be isolated most consistently .
The prevalence of MRSA nasal carriage among hospital employees increases with the duration of work on a medical ward . The nasal carriage rate of coagulase-positive MRSA in HCWs was observed to be 15 (83.3%) among doctors and three (16.6%) among laboratory technicians in one study that was carried out in India .
In the USA, HCWs have been identified as the source of MRSA in numerous outbreak investigations and several studies have shown that about a half of nurses in a wards where epidemic of MRSA occurred, colonized with MRSA .
The potential for the acquisition and carriage of MRSA by HCWs is a cause of anxiety and concern among HCWs and public health. HCWs may be at a higher risk than the general population for chronic colonization with resistant bacteria. Accordingly, colonized HCWs may constitute a reservoir for the transmission of resistant organisms such as MRSA to patients .
| Aim|| |
The aim of this study was to detect the prevalence of MRSA among medical residents in different departments of Al-Azhar University Hospital, Damietta branch.
| Participants and methods|| |
This study was carried out in Al-Azhar University Hospital, Damietta branch, from March 2016 to June 2016.
This study was carried out on 84 medical residents who agreed to inclusion in the study; 14 medical residents refused participation. All residents were men; their age ranged from 27 to 30 years.
The residents were classified into three groups according to their duration of residency.
Group I: included medical residents in their first year of residency.
Group II: included medical residents in their second year of residency.
Group III: included medical residents in their third year of residency.
Residents were subjected to the following: (a) informed consent; (b) administration of a questionnaire that included personal data, work experience, antimicrobial intake, infection-control training, and application of infection-control programs in the hospital; (c) a check list that indicated individual adherence to infection-control measures; and (d) a bacteriological study for the isolation and identification of MRSA.
The specimens for culture were obtained from both the anterior nares of each resident using a sterile disposable cotton nasal swab.
Identification of S. aureus
The collected nasal swaps were subjected to the following:
- Gram-stained film.
- Chemical tests:
- Catalase test: 1 ml of a 3% hydrogen peroxide solution was poured over an overnight nutrient agar slope culture of the test organism; the tube was held in a slanting position and observed for the immediate production of gas bubbles.
- Coagulase test: it was used for the differentiation of coagulase-positive and coagulase-negative Staphylococci spp. A 1 : 6 dilution of human plasma in normal saline was prepared and 1 ml of the diluted plasma was placed in a small tube. A colony of staphylococci under test was emulsified in the tube containing the diluted plasma and another negative control tube of unseeded plasma was prepared to confirm that the plasma did not clot spontaneously. All tubes were incubated at 37°C in a water bath for up to 4 h and examined at 1, 2, and 4 h for clot formation by tilting the tube. The test was considered positive if there was any degree of clot formation and negative if plasma remained in the liquid or showed a flocculent or a ropy precipitate.
- MSA (Oxoid, Columbia base-CM331; Oxoid, Victoria, Australia), it is a selective and indicator medium for the isolation of pathogenic staphylococci. On MSA S. aureus colonies were identified as 1 mm yellow colonies surrounded by yellow medium.
- Nutrient agar (Oxoid): this was used for the preparation of blood agar.
- Blood agar: it is an enriched and indicator medium used to determine the hemolytic activity of S. aureus. On blood agar, they showed β-hemolytic colonies, and then colonies were identified by Gram-stained smears and by their metabolic activity by a catalase test and a coagulase (tube) test: coagulase-positive and catalase-positive colonies.
Screening for MRSA
Detection of susceptibility of isolates to methicillin was performed using the cefoxitin disc diffusion test. Direct colony suspension in saline was prepared and matched with the turbidity standard equivalent to 0.5 McFarland standard. A plate of Mueller Hinton agar was inoculated and cefoxitin disc 30 µg was applied to the plate. The plate was incubated at 37°c for 24 h.The results were interpreted according to clinical and laboratory standards institute guidelines for cefoxitin susceptibility testing: a zone size up to 19 mm was considered resistant and a zone size of at least 20 mm was considered susceptible .
The collected data were statistically analyzed using the statistical package for the social sciences (SPSS, version 16; SPSS Inc., Chicago, Illinois, USA). For qualitative data, frequency and percent distributions were calculated. For comparison between categorical groups, the χ2-test was used. For quantitative data, the mean±SD were calculated and for comparison between two groups, the independent-samples Student t-test was used for parametric values or the Mann–Whitney U-test for nonparametric values. Pearson’s correlation coefficient (r) was used to correlate different variables. For all statistical tests, a P value of up to 0.05 was considered significant.
| Results|| |
This study included 84 medical residents in different departments of Al-Azhar University Hospital. They were apparently healthy volunteers who had direct contact with patients: 12 (14%) ICU, nine (10%) surgery, five (6%) orthopedics, four (4.7%) urology, four (4.7%) neurosurgery, five (6%) cardiothoracic, two (2.3%) ophthalmology, two (2.3%) ENT, three (3.5%) radiology, six (7%) gynecology, five (6%) pediatrics, six (7%) internal medicine, three (3.5%) tropical, six (7%) cardio, four (4.7%) neurology, two (2.3%) chest, two (2.3%) rheumatology, three (3.5%) clinical pathology, one (1.1%) dermatology departments. Their ages ranged from 27 to 30 (mean: 28.1) years, as shown in [Table 1]. Duration of work ranged from 1 to 3 (mean: 2) years; 60 (71.4%) residents were from rural areas and 24 (28.5%) residents were from urban areas ([Table 2]).
The analysis of the questionnaire showed that none of the participating Residents had received infection-control training. In terms of antibiotic intake, only eight (9.5%) of the participating Residents took antibiotics and 76 (90.5%) did not take antibiotics.
The check revealed poor adherence to the infection-control program, owing to lack of training, work load, limited resources, and insufficient staff members.
Results of the bacteriological study
The overall bacteria-carriage rate among residents was 41 (48.8%). The highest rate was found in the ICU [seven (8.3%)], surgery [six (7.1%)], orthopedics [four (4.7%)], gynecology [four (4.7%)], urology [three (3.6%)], neurosurgery [three (3.6%)], cardiothoracics [three (3.6%)], ophthalmology [two (2.4%)], neurology [two (2.4%)], internal medicine [two (2.4%)], ENT [one (1.2%)], radiology [one (1.2%)], cardiology [one (1.2%)], chest [one (1.2%)], and rheumatology [one (1.2%)] departments as shown in [Table 3]; 19 (22.6%) infections were caused by S. aureus, 20 (23.8%) were caused by coagulase-negative Staphylococcus, and two (2.4%) were caused by Streptococcus spp. In 15 (17.9%) participants, S. aureus was the MRSA strain, whereas in four (4.7%) participants MSSA strains were present; thus, the nasal carriage rate of MRSA among the participating residents was 15 (17.2%) as shown in [Table 4].
|Table 3 Nasal carriage rate of bacteria among residents in different departments|
Click here to view
The overall MRSA carriage rate among residents was 15 (17.8%). The highest rate was found in neurosurgery [three (3.5%)], the ICU [two (2.3%)], surgery [two (2.3%)], cardiothoracics [two (2.3%)], gynecology [two (2.3%)], urology [one (1.2%)], ophthalmology [one (1.2%)], rheumatology [one (1.2%)], and cardiology [one (1.2%)] departments as shown in [Figure 1].
|Figure 1 Distribution of methicillin-resistant Staphylococcus aureus in nasal swabs of the 100 residents in different departments.|
Click here to view
There was an insignificant association between frequent antibiotic intake, duration of work, residence, age, and carriage rate of MRSA among the participating HCWs as shown in [Table 5],[Table 6],[Table 7],[Table 8], respectively.
|Table 5 Correlation between antibiotic intake and the carriage rate of methicillin-resistant Staphylococcus aureus among residents|
Click here to view
|Table 6 Correlation between duration of work and the carriage rate of methicillin-resistant Staphylococcus aureus among residents|
Click here to view
|Table 7 Correlation between residence and the carriage rate of methicillin-resistant Staphylococcus aureus among residents|
Click here to view
|Table 8 Correlation between age and the carriage rate of methicillin-resistant Staphylococcus aureus among residents|
Click here to view
| Discussion|| |
MRSA is a common hospital pathogen of major importance prevalent worldwide. The incidence of MRSA infections continues to increase since its discovery in 1961. MRSA infections are known to be associated with considerable morbidity and attributable mortality .
MRSA infections have increasingly been reported among groups of patients with no apparent exposure to hospitals. These strains are called community-acquired MRSA (CA-MRSA) strains. They are predominantly associated with skin and soft-tissue infections. Some strains of CA-MRSA are particularly virulent and capable of causing life-threatening diseases .
In contrast to hospital-acquired MRSA, CA-MRSA is characteristically susceptible to many antibiotics .
Healthcare-acquired MRSA is a potentially deadly strain of S. aureus that is resistant to several antibiotics. This superbug is becoming increasingly more prevalent in hospitals and other healthcare settings, representing a growing public health problem in the USA . Hospital-acquired MRSA infections occur frequently in hospitals and healthcare facilities, where patients undergo invasive medical procedures or have weakened immune systems .
MRSA infections are usually preceded by a period of carriage. Laboratory-based screening for MRSA colonization of patients and HCWs remains the cornerstone of infection-control measures to limit the spread of this organism .
Screening for carriage of MRSA is fundamental to modern-day nosocomial infection control both for epidemiologic investigation and for day-to-day decision on barrier isolation .
Accurate and rapid detection of MRSA is important not only to choose the appropriate antibiotic therapy for the individual patient but also to control the endemicity of MRSA .
Although many body sites such as the hands, rectum, perineum, axillae, vagina, pharynx, gastrointestinal tract, and intact or inflamed skin are frequently colonized for varying time periods, the main reservoir of MRSA is the anterior nares. Among nasal S. aureus carriers, approximately half also carry the organism on their skin .
The aims of this study were to assess the prevalence of MRSA nasal colonization among medical residents of Al-Azhar University Hospital, Damietta branch, as well as to identify the possible risk factors for this colonization.
The first step of MRSA identification in this study was detection of staphylococci from the clinical samples by Gram-stained films. This was followed by isolation of S. aureus on MSA as opaque yellow colonies surrounded by a yellow zone .
In this work, a total of 84 nasal swap samples were collected from medical residents in different departments of Al-Azhar University Hospital during the period from March 2016 to June 2016: 12 (14%) ICU, nine (10%) surgery, five (6%) orthopedics, four (4.7%) urology, four (4.7%) neurosurgery, five (6%) cardiothoracics, two (2.3%) ophthalmology, two (2.3%) ENT, three (3.5%) radiology, six (7%) gynecology, five (6%) pediatrics, six (7%) internal medicine, three (3.5%) tropical, six (7%) cardio, four (4.7%) neurology, two (2.3%) chest, two (2.3%) rheumatology, three (3.5%) clinical pathology, and one (1.1%) dermatology departments. All participating medical residents were men because this study was carried out in Al-Azhar University Hospital for men.
From 84 nasal swap samples collected, 39 (46.4%) staphylococcal strains and two (2.3%) streptococcal strains were isolated. Cormican and Jones  reported that staphylococci are prevalent in hospitals, accounting for almost 30% of all nosocomial infections and 50% of nosocomial septicemia. Staphylococci are also the most commonly isolated organisms in clinical laboratories.
Out of 39 isolated staphylococcal strains, 22.6% (19/84) of S. aureus strains and 23.8% (20/84) of coagulase-negative Staphylococcus were isolated.
Our result for the nasal carriage rate of S. aureus is markedly lower than that reported in Yemen by Abdelmonem et al. , and Nigeria by Fadeyi et al. . These authors reported an overall nasal carriage of S. aureus among HCWs of 85% (60/70) and 52.5% (104/198), respectively. However, the carriage rate of S. aureus in the present study is quite high compared with others, such as Vinodhkumaradithyaa et al. , who carried out a study in India and found a carriage rate of nasal S. aureus among HCWs of 13% (13/100).
However, a similar study by Rongpharpi et al.  carried out in India on 315 HCWs reported results similar to ours in terms of the nasal carriage rate of S. aureus; S. aureus was detected in 70 (20.2%) HCWs. The discrepancies between our results and these studies may be attributed to the newly applicable infection-control program in our hospital, and abuse of rational antibiotic policy.
This proves that S. aureus remains one of the most frequently encountered nosocomial pathogens. Human carriers are predominantly colonized by S. aureus in their nares and may contaminate their hands .
Phenotype identification of MRSA in our study was carried out using cefoxitin disc diffusion.
Methicillin resistance in S. aureus strains is routinely determined using the oxacillin disc diffusion method, but it was reported that the results of cefoxitin disc diffusion tests correlate better with the presence of the mecA gene than the results of disc diffusion tests using oxacillin .
It was found that out of 19 isolated strains of S. aureus, the cefoxitin disc diffusion method yielded 15 (17.8%) resistant (MRSA) and four (4.7%) sensitive (MSSA) strains.
These results are in agreement with Wang et al. , who found that MRSA accounts for as much as 80% of all S. aureus isolates causing nosocomial infections.
In terms of the prevalence of MRSA, the result was in agreement with Shakya et al. , who reported that the international range of MRSA carriage is ∼6–18% among the HCWs in the hospital setting, and closer to the result reported by Abdel Rahman et al.  at Ain Shams University Hospital, Egypt, of a nasal MRSA carriage of 20%.
However, the overall carriage rate of MRSA in the present study is high compared with other studies such as the study at Nazami Hospital in Iran by Askarian et al. . They found that the prevalence of nasal carriage of MRSA in HCWs was 5.3%, Bertin et al. , and Seybold et al.  reported a mean nasal MRSA carriage in HCWs of 4.1%, and in an Italian Hospital, MRSA carriage was found in only 1.5% of HCWs .
The carriage rate of MRSA in our study can be attributed to several factors for example, prevalence of MRSA among patients; this increases the potential for exposure among the participating HCWs. Suboptimal infection-control practices have a strong influence on the possibility of transmission between patients and HCWs.
Also, this study showed that the MRSA carriage rate among residents was 15 (17.8%). The highest rate was found in the departments of neurosurgery [three (3.5%)], the ICU [two (2.3%)], general surgery [two (2.3%)], cardiothoracic surgery [two (2.3%)], gynecology [two (2.3%)], urology [one (1.2%)], ophthalmology [one (1.2%)], rheumatology [one (1.2%)], and cardiology [one (1.2%)].
Similar studies have been carried out to determine the prevalence of MRSA in different hospital departments by Pan et al. ; they found the highest rate among the staff members in the ICU, followed by surgery in an Italian Hospital. Apisarthanarak et al.  found the highest rate among the staff in the orthopedics department, followed by HCWs in surgery in an Iranian Hospital.
This may be attributed to the fact that several modes of transmission exist, including transient colonization of hospital staff and contact with heavily contaminated fomites and environmental surfaces around infected patients in these departments .In the present study, none of the participating residents had received training on infection control. Initial educational programs need to be followed by reinforcement, and infection-control staff should evaluate intrahospital compliance and identify lapses for further measures and education. Many acute care facilities in resource-poor countries have no effective infection-control measures in place. There are still limitations in resources and expertise in infection-control measures .
In terms of antibiotic intake, 25% of residents who used to take antibiotics frequently were MRSA positive and 75% were MRSA negative, whereas 17% of residents who did not take antibiotics frequently were MRSA positive and 83% were MRSA negative; there was no statistically significant difference between those who received antibiotics frequently and those who did not.
In contrast to our study, Sadoyama and Gontijo-Filho , reported a significant relation between MRSA infection and the use of three or more antimicrobials.
This discrepancy may be attributed to the fact that antimicrobials will kill the susceptible strains, leaving resistant ones to flourish.
Also, there was no statistically significant difference between ages, duration of work, residence, and nasal carriage rate of MRSA, which can be explained by the small sample size, the same age range of 27–30 years (mean: 28±0.9). Similarly, Rahbar et al.  found no association between ages or years of service and the nasal carriage rate of MRSA.
In contrast, Eveillard et al. , found a higher prevalence of MRSA carriage for HCWs when their duration of work exceeded 5 years. This observation could reflect longer exposure to patients with MRSA colonization or infection .
To conclude, the present study found that HCWs who have contact with patients are at risk of acquisition and colonization with antimicrobial-resistant bacteria, especially MRSA.
Transient hand colonization is the primary means of transmission of MRSA. Simple education of HCWs on hygienic measures, especially proper hand hygiene, is the key to overcome MRSA infections.
Methods to detect MRSA in clinical samples should ideally have high sensitivity and specificity .
In conclusion, the frequency of the MRSA carriage rate among residents was 15 (17.8%). The highest rate was found in the departments of neurosurgery [three (3.5%)], the ICU [two (2.3%)], general surgery [two (2.3%)], cardiothoracic surgery [two (2.3%)], gynecology [two (2.3%)], urology [one (1.2%)], ophthalmology [one (1.2%)], rheumatology [one (1.2%)], and cardiology [one (1.2%)].
There was an insignificant association between frequency of antibiotic intake, duration of work, residence, and carriage rate of MRSA among the participating HCWs.
Suboptimal infection-control practices have a strong influence on the possibility of transmission between patients and HCWs.
The single most important factor for preventing nosocomial infections is compliance of the health professionals with the sanitary and antibacterial guidelines. Simple preventive measures such as hand hygiene before and after examination of patients, the use of sterile aprons and masks in the postoperative wards, awareness during the examination of immunocompromised patients, and avoiding touching one’s nose during work can reduce the disease transmission rate considerably.
Screening should be an essential protocol to assess the carrier-transmitted drug-resistant strains of Staphylococci from the community to the hospital settings and from the hospital settings to the community.
The health professionals should be informed about the potential outcomes of the nosocomial infections, both inside and outside the hospital, and their cooperation should be sought to decrease the carriage of S. aureus.
| Conclusion|| |
The present study showed that medical residents who have contact with patients are at risk of acquisition and colonization with antimicrobial-resistant bacteria, especially MRSA.
Transient hand colonization is the primary means of transmission of MRSA. Simple education of HCWs on hygienic measures, especially proper hand hygiene, is the key to overcoming MRSA infections.
The single most important factor for preventing nosocomial infections is compliance of the health professionals with the sanitary and antibacterial guidelines.
The health professionals should be informed about the potential consequences of the nosocomial infections, both inside and outside the hospital, and their cooperation should be sought to decrease the carriage of S. aureus.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Bannerman TI, Murray PR, Baron EI, Jorgensen IH, Landry ML, Pfaller MA. Staphylococcus
, micrococcus and other catalase − positive cocci that grow aerobically. In: Manual of clinical microbiology. 8th ed. Washington DC: ASM Press; 2006. pp. 384–404.
Alli OT, Ogbolu DO, Akorede E, Onemu OM, Okanlawon BM. Distribution of mecA gene amongst Staphylococcus aureus
isolates from Southwestern Nigeria. Afr J Biomed Res 2011; 14:9–16.
Michael ZD, Robert SD. Community associated methicillin resistant Staphylococcus aureus
: epidemiology and clinical consequences of emerging epidemic. Clin Microbiol Rev 2010; 23:616–687.
Carmeli Y, Venkataraman L, Samore MH. Stool colonization of health care workers with selected resistant bacteria. Infect Control Hosp Epidemiol 1998; 19:38–40.
Ahmad S. The prevalence of Staphylococcus aureus
colonization among health care workers at a specialist hospital in Saudi Arabia. J Clin Diagn Res 2010; 4:2438–2441.
Eveillard M, Martin Y, Hidri N, Boussougant Y, Joly-Guillou ML. Carriage of methicillin-resistant Staphylococcus aureus
among hospital employees: Prevalence, duration, and transmission to households. Infect Control Hosp Epidemiol 2004; 25:114–120.
Kumar P, Shukla I, Varshney S. Nasal screening of healthcare workers for nasal carriage of coagulase positive MRSA and prevalence of nasal colonization with Staphylococcus aureus
. Biol Med 2011; 3:182–186.
Sherertz RJ, Bassetti S, Bassetti-Wyss B. ‘Cloud’ health-care workers. Emerg Infect Dis 2001; 7:241–244.
Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing CLSI approved standard M100-S15. Wayne, PA: 2005.
Engemann JJ, Carmeli Y, Cosgrove SE, Fowler VG, Bronstein MZ, Trivette SL et al.
Adverse clinical and economic outcomes attributable to methicillin resistance among patients with Staphylococcus aureus
surgical site infection. Clin Infect Dis 2003; 36:592–598.
Uhlemann AC, Dordel J, Knox JR, Raven KE, Parkhill J, Holden MT et al.
Molecular tracing of the emergence, diversification, and transmission of S. aureus
sequence type 8 in a New York community. Proc Natl Acad Sci USA 2014; 111:6738–6743.
Suggs AH, Maranan MC, Boyle-Vavra A, Daum RS. Methicillin-resistant and borderline methicillin-resistant asymptomatic Staphylococcus aureus
colonization in children without identifiable risk factors. Pediatr Infect Dis J 1999; 18:410–414.
Bano S, Tunio S, Mal S, Jatt A. Frequency of methicillin resistant Staphylococcus aureus among isolates of wound infections from Hyderabad. Sindh Univ Res J 2015; 44.
Sydnor ER, Perl TM. Hospital epidemiology and infection control in acute-care settings. Clin Microbiol Rev 2011; 24:141–173.
Wolk DM, Picton E, Johnson D, Davis T, Pancholi P, Ginocchio CC et al.
Multicenter evaluation of the Cepheid Xpert methicillin-resistant Staphylococcus aureus
(MRSA) test as a rapid screening method for detection of MRSA in nares. J Clin Microbiol 2009; 47:758–764.
Daef EA, Elsherbiny NM, Ibrahim MA, Ahmed EH. Decolonization of methicillin resistant Staphylococcus aureus
nasal carriage among health care workers. Life Sci J 2012; 9:4496–4501.
Skov R, Smyth R, Kahlmeter G. Evaluation of a cefoxitin 30 µg disc on Iso-Sensitest agar for detection of MRSA. J Antimicrob Chemother 2003; 52:204–207.
Wertheim HF, Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A et al.
The role of nasal carriage in Staphylococcus aureus
infections. Lancet Infect Dis 2005; 5:751–756.
Baird D. Staphylococcus
: cluster-forming Gram-positive cocci. In: Collee JG, Fraser AG, Marmion BP, Simmons A, editors. Mackie & McCartney practical medical microbiology. New York: Churchill Livingstone; 1996. pp. 245–261.
Cormican MG, Jones RN. Emerging resistance to antimicrobial agents in gram-positive bacteria. Enterococci, staphylococci and nonpneumococcal streptococci. Drugs 1996; 51(Suppl 1):6–12.
Abdelmonem MO. Nasal Carriage of Staphylococcus aureus
among healthcare workers in Althawra Hospital, Taiz City, Republic of Yemen. Aust J Basic Appl Sci 2012; 6:417–424.
Fadeyi A, Bolaji BO, Oyedepo OO. Methicillin resistant Staphylococcus aureus
carriage amongst healthcare workers of the critical care units in a Nigerian Hospital. Am J Infect Dis 2010; 6:18–23.
Vinodhkumaradithyaa A, Uma A, Srinivasan M, Ananthalakshmi I. Nasal carriage of methicillin resistant Staphylococcus aureus
among surgical unit staff. Jpn J Infect Dis 2009; 62:228–229.
Rongpharpi SR, Hazarika NK, Kalita H. The prevalence of nasal carriage of Staphylococcus aureus
among healthcare workers at a tertiary care hospital in Assam with special reference to MRSA. J Clin Diagn Res 2013; 7:257–260.
Weese JS, van Duijkeren E. Methicillin-resistant Staphylococcus aureus
and Staphylococcus pseudintermedius
in veterinary medicine. Vet Microbiol 2010; 140:418–429.
Swenson JM, Tenover FC. Results of disc diffusion testing with cefoxitin correlate with presence of mecA in Staphylococcus
spp. J Clin Microbiol 2005; 43:3818–3823.
Wang JT, Fang CT, Chen YC, Wu CL, Chen ML, Chang SC. Staphylococcal cassette chromosome mec in MRSA, Taiwan. Emerg Infect Dis 2007; 13:494–497.
Shakya B, Shrestha S, Mitra T. Nasal carriage rate of methicillin resistant Staphylococcus aureus
at the National Medical College Teaching Hospital, Birgunj, Nepal. Nepal Med Coll J 2010; 12:26–29.
Abdel Rahman AT, Hafez SF, Abdelhakam SM, Ali-Eldin ZA, Esmat IM, Elsayed MS, Aboul-Fotouh A. Antimicrobial resistant bacteria among health care workers in intensive care units at Ain Shams University Hospitals. J Egypt Soc Parasitol 2010; 40:71–83.
Askarian M, Zeinalzadeh A, Japoni A, Alborzi A, Memish ZA. Prevalence of nasal carriage of methicillin resistant Staphylococcus aureus
and its antibiotic susceptibility pattern in healthcare workers at Namazi Hospital, Shiraz, Iran. Int J Infect Dis 2009; 13:241–247.
Bertin ML, Vinski J, Schmitt S, Sabella C, Danziger-Isakov L, McHugh M et al.
Outbreak of methicillin resistant Staphylococcus aureus
colonization and infection in a neonatal intensive care unit epidemiologically linked to a healthcare worker with chronic otitis. Infect Control Hosp Epidemiol 2006; 27:581–585.
Seybold U, Kourbatova EV, Johnson JG, Halvosa SJ, Wang YF, King MD et al.
Emergence of community-associated methicillin-resistant Staphylococcus aureus
USA300 genotype as a major cause of health care-associated blood stream infections. Clin Infect Dis 2006; 42:647–656.
Orsi GB, Marrone R, Ferraro F, Tavella F, Colosi A. Low colonization with MRSA among health-care workers in an Italian hospital. Ann Ig 2008; 20:503–508.
Pan A, Lorenzotti S, Ferrari L, Granata L, Signorini L, Carnevale G. Low rates of nasal colonization with methicillin-resistant Staphylococcus aureus
among staff members of an Italian hospital. Infect Control Hosp Epidemiol 2006; 27:218–220.
Apisarnthanarak A, Rahbar M, Yaghoobi M. Prevalence of nasal carriage of Staphylococcus aureus
and susceptibility of isolates to methicillin and mupirocin among healthcare workers in an Iranian Hospital. Infect Control Hospital Epidemiol 2006; 27:323–325.
Khan F, Shukla I, Rizvi M, Sultan A, Kumar P, Mansoor T, Sharma SC. Screening for detection of MRSA in patients and hospital staff of a tertiary institutional hospital. Int J Curr Microbiol App Sci 2013; 2:569–574.
World Health Organization. Infection control programmes to contain antimicrobial resistance (WHO/CDC/CSR/2001). WHO; 2001.
Sadoyama G, Gontijo-Filho PP. Risk factors for methicillin-resistant and sensitive Staphylococcus aureus
infection in Brazilian University Hospital. Braz J Infect Dis 2000; 4:135–143.
Rahbar M, Karamiyar M, Agazi R. Nasal carriage of MRSA among HCWs of an Iranign hospital. Infect Control Hosp Epidemiol 2003; 24:236–237.
Caliendo AM, Gilbert DN, Ginocchio CC, Hanson KE, May L, Quinn TC et al.
Better tests, better care: improved diagnostics for infectious diseases. Clin Infect Dis 2013; 57(Suppl 3):S139–S170.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8]