Home » Volumes » Volume 50 September/October 2017 » Nasal carriage rate of methicillin resistant Staphylococcus aureus among Iranian healthcare workers: a systematic review and meta-analysis

Nasal carriage rate of methicillin resistant Staphylococcus aureus among Iranian healthcare workers: a systematic review and meta-analysis

Mohammad Emaneini1 Fereshteh Jabalameli1 Hosseinali Rahdar1 Willem B. van Leeuwen2 Reza Beigverdi1

1Department of Microbiology, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran. 2Department of Innovative Molecular Diagnostics, Faculty of Science & Technology, University of Applied Sciences. Leiden. Netherlands.

DOI: 10.1590/0037-8682-0534-2016

Staphylococcus aureus is a major cause of both nosocomial and community-acquired infections


Globally, methicillin-resistant Staphylococcus aureus (MRSA) remains a major cause of healthcare-associated infections. Healthcare workers (HCWs), patients and the environment may act as reservoirs for the spread of MRSA to patients and other HCWs. Screening and eradication of MRSA colonization is an effective method of reducing the MRSA infection rate. There are limited data on the prevalence of MRSA among Iranian HCWs. We performed a systematic search by using different electronic databases including Medline (via PubMed), Embase, Web of Science, and Iranian Databases (from January 2000 to July 2016). Meta-analysis was performed using the Comprehensive Meta-Analysis (Biostat V2.2) software. The meta-analyses showed that the prevalence of S. aureus and MRSA among HCWs were 22.7% [95% confidence interval (CI): 19.3-26.6] and 32.8% (95% CI: 26.0-40.4) respectively. The high rate of nasal MRSA carriage among Iranian HCWs has been attributed to poor compliance to hand hygiene, injudicious use of antibiotics, and ineffective infection control and prevention measures. The rational use of antibiotics plus strict infection control are the main pillars for controlling multidrug resistant microorganisms such as MRSA in the hospital setting. These measurements should be applied nationally.

Keywords: MRSA; Nasal carriage; Healthcare workers; Iran; Systematic review


Staphylococcus aureus is a major cause of both nosocomial and community-acquired infections1. Over the past decades, the incidence of methicillin-resistant S. aureus (MRSA) in surgical site infections, bloodstream infections, and pneumonia has increased significantly2,3. MRSA strains are considered to be endemic in many hospitals throughout the world and are now responsible for approximately 40-60% of healthcare-associated infections4. Compared to methicillin-susceptible S. aureus (MSSA), various studies have revealed that infection due to MRSA is associated with significant morbidity, mortality, length of hospital stay, and medical costs57. For example, the rate of death due to MRSA (11.8%) was considerably higher than that due to MSSA (5.1%)8. The treatment of MRSA infections has become a global burden. Treatment options for MRSA infections have become more limited9S. aureus colonizes various niches of the human body, but the primary colonization site is the anterior nares6. It is estimated that 20-30% of individuals are persistent carriers of S. aureus, around 30% are intermittent carriers, and 40-50% are noncarriers10. Nasal carriage among healthcare workers (HCWs) is the main source for the transmission of MRSA and most S. aureus among patients within and between wards11,12. MRSA carriers create major problems for critically ill patients [e.g., intensive care unit (ICU) patients]13. Screening of HCWs for early and rapid identification of MRSA carriage is recommended for reducing the spread of MRSA within hospitals6. In 2003, MRSA strains were first isolated from the nasal passages of HCWs in Milad Hospital in Tehran, Iran14. Currently, MRSA is considered a major cause of healthcare-associated infections15. To date, the prevalence rates of MRSA among HCWs have been reported in several Iranian studies16,17. Most of these studies presented local data, and no systematic study has been performed. The aim of this study was to identify the prevalence of nasal carriage of MRSA among HCWs in Iranian hospitals using a systematic review and meta-analysis according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses.



This was a systematic review and meta-analysis of the prevalence of nasal carriage of MRSA among Iranian HCWs

Search Strategies

We performed a computerized search of published studies in Medline (via PubMed), Embase, Web of Science, and an Iranian Database from January 2000 to July 2016 using the following terms: Staphylococcus aureus or S. aureus and methicillin resistant Staphylococcus aureus or MRSA and nasal carriage and HCWs in combination with Iran. Cross-sectional or cohort studies that reported the prevalence of MRSA in the nasal passages of HCWs were considered. The titles and abstracts were screened by two independent reviewers for possible inclusion in the review. The review was restricted to studies published in the English and Persian languages and assessed the prevalence or incidence of MRSA in the nasal passages of Iranian HCWs. Eligible articles were selected based on three stages: title, abstract, and full-text publication. Studies with the following characteristics were included: a standard method had to be used to detect MRSA, studies addressing the S. aureus nasal carriage in HCWs, reported data on the prevalence of MRSA. According to the guidelines of the Clinical and Laboratory Standards Institute18, the most reliable method for detecting MRSA strains is the measurement of minimum inhibitory concentration (MIC) by methods such as broth microdilution, agar dilution, and E-test as well as molecular methods [detection of the mecA gene, the most common gene that mediates methicillin resistance in staphylococci, by polymerase chain reaction (PCR)]. MIC and PCR tests are accurate and gold standard methods for detecting MRSA18,19. Studies that had one or more of the following characteristics were excluded: studies using nonstandard methods, duplicate and overlapping studies, studies published in languages other than English or Persian, studies that did not assess nasal carriage of S. aureus among HCWs, studies that did not report MRSA prevalence, nonhuman studies, review articles, congress abstracts, meta-analyses or systematic reviews, as well as articles available only in abstract form.

Data extraction and definitions

The following details were extracted from each study: the first author’s name, year of publication, year of study, study setting, number of cases investigated, methods of the studies, isolate source, sample size, and prevalence of nasal MRSA carriage among HCWs. Two reviewers independently extracted all data from the included studies, and the results were reviewed by a third reviewer. Inconsistencies between the reviewers were resolved by a general consensus.

Quality assessment of studies

The quality of the included studies was independently assessed by two reviewers, using the Joanna Briggs Institute Checklist for Systematic Reviews and Research Syntheses20. The checklist consists of 10 inquiries in which the reviewers responded to questions on the selected articles on an individual basis according to the evidence. The Yes answer for each question got a point; evidently, the scores ranged from zero to ten. Eventually, studies that attained greater than 6 points were included in this study.

Statistical analyses

Meta-analysis was performed using the Comprehensive Meta-Analysis (Biostat V2.2) software. We reported the amount of residual heterogeneity by using the I² statistic and Q statistic to test the heterogeneity among the studies. In order to assess any possible publication bias, the Begg rank correlation and Egger weighted regression methods in combination with a funnel plot were used. p <0.05 was considered indicative of statistically significant publication bias. We used the EndNote referencing software to collate the search results and remove duplicates.


Overall, 4,241 studies were identified. Of these, 2,527 articles remained after the duplicates were removed. By screening the titles and abstracts, 1,787 studies were excluded because they were not relevant. Of the remaining 740 articles, only 22 studies were included in this meta-analysis. The study selection process and reasons for exclusion are shown in Figure 1, and the main characteristics of the selected studies are described in Table 1. Based on the 22 selected articles, the pooled prevalence of S. aureus and MRSA was 22.7% [95% confidence interval (CI): 19.3-6.6] and 32.8% (95% CI: 26.0-40.4), respectively, as shown in Table 2. Heterogeneity between studies (I²=91, p <0.001 for S. aureus and I²=85, p <0.001 for MRSA) were found, so a random effects model was used for the meta-analysis. Figure 2 shows forest plots for the prevalence rate of MRSA among Iranian HCWs. As shown in Table 2, no evidence of publication bias was detected by Begg’s rank correlation test (p =0.2 for S. aureus and p =0.5 for MRSA) and Egger’s weighted regression (p =0.3 for S. aureus and p =0.7 for MRSA). However, the asymmetric shape of the funnel plot (Figure 3) shows some evidence of publication bias among the evaluated studies.

FIGURE 1: Summary of the literature search and study selection. MRSA: methicillin-resistant Staphylococcus aureus

TABLE 1: Characteristics of studies included in the meta-analysis. 

First author of the study Time of study Year of Publication Province Nasal swab Staphylococcus aureus (no) MRSA (no) Detection Method
Rahbar et al.14 2002 2003 Tehran 230 92 35 Agar dilution method
Saderi et al.21 2002-2003 2004 Tehran 348 87 10 Agar dilution method
Nikbakht et al.22 2004-2005 2007 Tabriz 220 72 22 Agar dilution method
Armin et al.23 2006 2007 Tehran 237 50 17 Micro-dilution method
Nafisi et al.24 2007 2008 Shahrekord 204 52 27 Agar dilution method, PCR
Askarian et al.16 2006 2009 Shiraz 600 186 32 E-test, PCR
Khalili et al.25 2007-2008 2009 Yazd 742 94 57 Agar dilution method
Rahimialang et al.26 2009 2010 Gorgan 333 69 9 Micro-dilution method
Moradi et al.27 2007 2011 Bandar abbas 85 24 4 Agar dilution method
Rastegarlari et al.17 2010 2011 Tehran 270 72 23 Agar dilution method
HosainZadegan et al.28 2010 2011 khorramabad 300 64 16 Agar dilution method
Afrough et al.29 2010-2011 2013 Tehran 157 70 29 Agar dilution method
Talaei et al.30 2011 2012 Tehran 70 17 6 Agar dilution method
Zeinalineia et al.31 2011 2011 Tehran 261 70 29 PCR
Mamishi et al.32 2010 2012 Tehran 190 47 7 Agar dilution method, PCR
Khalili et al.33 2010-2011 2012 Yazd 151 29 8 Agar dilution method
Kalhour et al.34 2006 2013 Shahrekord 204 52 23 Agar dilution method
Janaati et al.35 2010 2013 Ardabi 173 41 8 Agar dilution method, PCR
Saadat et al.36 2012 2013 Jahrom 397 47 9 E-test
Ahanjan et al.37 2012 2014 Sari 148 14 10 Micro-dilution method
Navidinia et al.38 2012-2013 2015 Tehran 229 27 21 PCR
Ohadian Moghadam et al.39 2013 2015 Tehran 270 39 17 E-test, PCR

MRSA: methicillin-resistant Staphylococcus aureusPCR: polymerase chain reaction.

TABLE 2: Meta-analysis of prevalence of Staphylococcus aureus and MRSA among Iranian HCWs. 

Subgroups Studies (no) Prevalence n/N Heterogeneity test, I2 Heterogeneity test, p value Begg’s test Egger’s test
S. aureus 22 22.7 (19.3-26.6) 1,315/5,819 91 <.001 0.2 0.3
MRSA 22 32.8 (26.0-40.4) 419/1,315 85 <.001 0.5 0.7

MRSA: methicillin-resistant Staphylococcus aureusHCWs: healthcare workers; n: number of events (S. aureus and MRSA); N: total number of HCWs and S. aureus S: Staphylococcus .

FIGURE 2: Forest plot of prevalence of MRSA among HCWs. (The squares represent the point estimates of individual studies with their 95% confidence intervals and the size of the square represents the weight given to each study in the meta-analysis. The diamond represents the overall result and 95% confidence interval of the random effect meta-analysis. Vertical line: null value). 95% CI: 95% confidence interval; MRSA: methicillin-resistant Staphylococcus aureusHCWs: healthcare workers. 

FIGURE 3: Funnel plot of prevalence of MRSA among HCWs. (Funnel asymmetry suggests bias in the meta-analysis). MRSA:methicillin-resistant Staphylococcus aureusHCWs: healthcare workers. 


To the best of our knowledge, the current study is the first comprehensive systematic review regarding the prevalence of S. aureus and MRSA among Iranian HCWs. Based on the meta-analysis results, the pooled prevalence of S. aureus and MRSA were 22.7% (95% CI: 19.3-26.6) and 32.8% (95% CI: 26.0-40.4), respectively14,16,17,2139. In Egypt, Hefzy et al. showed that the prevalence of nasal carriage of S. aureus among Egyptian HCWs was 22.9% and among these 58.8% was MRSA40. In Ethiopia, Shibabaw et al. reported that the prevalence of S. aureus among Ethiopian HCWs was 28.8% and among these 44.1% was MRSA9. In China, Chen et al. reported that that the prevalence of S. aureus among Chinese HCWs was 21.6 % and among these 4.7% was MRSA41. In a meta-analysis study conducted by Albrich et al. the average S. aureus and MRSA prevalence among HCWs were 23.7 and 4.6 %, respectively42. However, nasal carriage of MRSA differs noticeably among countries9,4044 which may reflect methodological differences (sampling technique, sample size, culture techniques, the sites chosen for sampling) and differences in infection control policies, among other factors12,43. Several factors may explain the high incidence rate of S. aureus and MRSA among HCWs observed in this study. First, infection control policies are likely to be ineffective in Iran45. For instance, hand hygiene (effective handwashing) is widely regarded as the most important way of reducing the spread of MRSA and other nosocomial pathogens such as vancomycin-resistant enterococci45,46. Hand hygiene compliance among Iranian HCWs is generally low. Heavy workload, understaffing, limited infrastructure (lack of sinks, unavailability of hygiene products), behavioral aspects, and skin irritation by hand hygiene products are important barriers to appropriate compliance4547. Lack of knowledge about the modes of transmission (direct skin-to-skin contact, indirect contact via contaminated hands, surfaces, and medical devices), lack of knowledge regarding the importance of hand hygiene in reducing the spread of MRSA and on how hands become contaminated, lack of knowledge regarding correct hand hygiene techniques, patient overcrowding, and lack of national guidelines on hand hygiene are additional barriers to hand hygiene compliance45,48. On the other hand, Iranian hospitals are poorly resourced with regard to personal protective equipment (PPE) (gowns, gloves, mask)45,49. In contrast, in the Netherlands, all hospitals are equipped with appropriate PPEs45,49. Second, it has been proven that treatment with intranasal mupirocin can reduce the rates of nosocomial MRSA infection50. It seems that the identification and treatment of nasal carriers (patients and HCWs) with mupirocin were not performed in Iran, or if performed, the existing MRSA strains had become resistant to this agent. High-level mupirocin resistance in clinically-acquired MRSA infections has been reported in Iran51. Third, overprescribing or unregulated use of antibiotics in developing countries such as Iran is common45,48,52. For example, the use of cephalosporins and fluoroquinolones is prevalent, and their overuse may elicit the emergence of MRSA in hospitals53. On the other hand, clinicians face serious problems in choosing effective antimicrobial agents due to lack of good microbiological laboratory capacity; therefore, the overuse or misuse of antibiotics has led to the emergence and spread of MRSA45,48. Fourth, hospitals do not have a sufficient number of isolation rooms; thus, MRSA-infected patients are admitted to the general wards together with uninfected patients45. As a result, there is an increased risk of transmission of MRSA from patients to both patients and HCWs45. Fifth, decontamination of the hospital environment is likely to be ineffective in Iran45; thus, MRSA can be spread by contact with contaminated surfaces45. In recent years, the incidence of MRSA infection has increased dramatically in Iranian hospitals15. Finally, the hospital infection control teams are inexperienced, inadequate, not well trained, and worst of all, most of them do not include a clinical microbiologist45. As a result, there is failure in controlling or reducing the transmission of MRSA. The present review has several limitations. First, the study could not fully assess the prevalence of MRSA among HCWs in Iran since the magnitude of MRSA among HCWs has not been identified in different regions of the country. Second, we only considered published articles in the current meta-analysis; just like any other meta-analysis, the potential for publication bias should be considered as well. Third, heterogeneity was observed among the included studies which may be due to differences in sample size, different methods for the detection of MRSA and geographical diversity.

In conclusion, poor hand hygiene compliance, non-judicious use of antibiotics and ineffective infection control measures may explain the relatively high nasal carriage of S. aureus and MRSA among Iranian HCWs. Therefore, reducing antibiotic overuse, adherence to hand hygiene, screening and decolonization of carriers, education and training in antibiotic prescribing, environmental cleaning, routine environmental cultures, contact precautions, and active surveillance are recommended strategies for the prevention and control of MRSA transmission in our healthcare setting.


This research has been supported by the Tehran University of Medical Sciences and Health Services (study grant no: 93-03-30-26234).


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Received: April 05, 2017; Accepted: June 05, 2017

Corresponding author: Dr. Reza Beigverdi e-mailr-beigverdi@tums.ac.ir

Conflicts of interest : The authors declare that there is no conflict of interest.