Accessibility / Report Error

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

Abstract

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

INTRODUCTION

Staphylococcus aureus is a major cause of both nosocomial and community-acquired infections11. Castro A, Komora N, Ferreira V, Lira A, Mota M, Silva J, et al. Prevalence of Staphylococcus aureus from nares and hands on health care professionals in a Portuguese Hospital. J Appl Microbiol. 2016;121(3):831-9.. Over the past decades, the incidence of methicillin-resistant S. aureus (MRSA) in surgical site infections, bloodstream infections, and pneumonia has increased significantly22. Honda H, Krauss MJ, Coopersmith CM, Kollef MH, Richmond AM, Fraser VJ, et al. Staphylococcus aureus nasal colonization and subsequent infection in intensive care unit patients: does methicillin resistance matter? Infect Control Hosp Epidemiol. 2010;31(6):584-91.,33. Gurieva T, Bootsma MC, Bonten MJ. Cost and effects of different admission screening strategies to control the spread of methicillin-resistant Staphylococcus aureus. PLoS Comput Biol. 2013;9(2):e1002874.. MRSA strains are considered to be endemic in many hospitals throughout the world and are now responsible for approximately 40-60% of healthcare-associated infections44. Lu SY, Chang FY, Cheng CC, Lee KD, Huang YC. Methicillin-resistant Staphylococcus aureus nasal colonization among adult patients visiting emergency department in a medical center in Taiwan. PLoS One. 2011;6(6):e18620.. 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 costs55. Safdar N, Bradley EA. The risk of infection after nasal colonization with Staphylococcus aureus. Am J Med. 2008;121(4):310-5.

6. Cirkovic I, Stepanovic S, Skov R, Trajkovic J, Grgurevic A, Larsen AR. Carriage and genetic diversity of methicillin-resistant Staphylococcus aureus among patients and healthcare workers in a Serbian University Hospital. PLoS One . 2015;10(5):e0127347.
-77. Calfee DP, Salgado CD, Milstone AM, Harris AD, Kuhar DT, Moody J, et al. Strategies to prevent methicillin-resistant Staphylococcus aureus transmission and infection in acute care hospitals: 2014 update. Infect Control Hosp Epidemiol . 2014;35(7):772-96.. For example, the rate of death due to MRSA (11.8%) was considerably higher than that due to MSSA (5.1%)88. Melzer M, Eykyn SJ, Gransden WR, Chinn S. Is methicillin-resistant Staphylococcus aureus more virulent than methicillin-susceptible S. aureus? A comparative cohort study of British patients with nosocomial infection and bacteremia. Clin Infect Dis. 2003;37(11):1453-60.. The treatment of MRSA infections has become a global burden. Treatment options for MRSA infections have become more limited99. Shibabaw A, Abebe T, Mihret A. Nasal carriage rate of methicillin resistant Staphylococcus aureus among Dessie Referral Hospital Health Care Workers; Dessie, Northeast Ethiopia. Antimicrob Resist Infect Control. 2013;2(1):25.. S. aureus colonizes various niches of the human body, but the primary colonization site is the anterior nares66. Cirkovic I, Stepanovic S, Skov R, Trajkovic J, Grgurevic A, Larsen AR. Carriage and genetic diversity of methicillin-resistant Staphylococcus aureus among patients and healthcare workers in a Serbian University Hospital. PLoS One . 2015;10(5):e0127347.. It is estimated that 20-30% of individuals are persistent carriers of S. aureus, around 30% are intermittent carriers, and 40-50% are noncarriers1010. Espinosa-Gongora C, Dahl J, Elvstrom A, van Wamel WJ, Guardabassi L. Individual predisposition to Staphylococcus aureus colonization in pigs on the basis of quantification, carriage dynamics, and serological profiles. Appl Environ Microbiol. 2015;81(4):1251-6.. Nasal carriage among healthcare workers (HCWs) is the main source for the transmission of MRSA and most S. aureus among patients within and between wards1111. Ayliffe GA. The progressive intercontinental spread of methicillin-resistant Staphylococcus aureus. Clin Infect Dis . 1997;24(Suppl 1):S74-9.,1212. Khanal R, Sah P, Lamichhane P, Lamsal A, Upadhaya S, Pahwa VK. Nasal carriage of methicillin resistant Staphylococcus aureus among health care workers at a tertiary care hospital in Western Nepal. Antimicrob Resist Infect Control . 2015;4(1):39.. MRSA carriers create major problems for critically ill patients [e.g., intensive care unit (ICU) patients]1313. Vazquez-Guillamet C, Kollef MH. Treatment of Gram-positive infections in critically ill patients. BMC Infect Dis. 2014;14(1):92.. Screening of HCWs for early and rapid identification of MRSA carriage is recommended for reducing the spread of MRSA within hospitals66. Cirkovic I, Stepanovic S, Skov R, Trajkovic J, Grgurevic A, Larsen AR. Carriage and genetic diversity of methicillin-resistant Staphylococcus aureus among patients and healthcare workers in a Serbian University Hospital. PLoS One . 2015;10(5):e0127347.. In 2003, MRSA strains were first isolated from the nasal passages of HCWs in Milad Hospital in Tehran, Iran1414. Rahbar M, Karamiyar M, Gra-Agaji R. Nasal carriage of methicillin-resistant Staphylococcus aureus among healthcare workers of an Iranian hospital. Infect Control Hosp Epidemiol . 2003;24(4):236-7.. Currently, MRSA is considered a major cause of healthcare-associated infections1515. Fatholahzadeh B, Emaneini M, Gilbert G, Udo E, Aligholi M, Modarressi MH, et al. Staphylococcal cassette chromosome mec (SCCmec) analysis and antimicrobial susceptibility patterns of methicillin-resistant Staphylococcus aureus (MRSA) isolates in Tehran, Iran. Microb Drug Resist. 2008;14(3):217-20.. To date, the prevalence rates of MRSA among HCWs have been reported in several Iranian studies1616. 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(5):e241-7.,1717. Lari AR, Pourmand MR, Moghadam SO, Abdossamadi Z, Namvar AE, Asghari B. Prevalence of PVL-containing MRSA isolates among hospital staff nasal carriers. Lab Med 2011;42(5):283-6.. 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.

METHODS

Design

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 Institute1818. The Clinical & Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fourth Informational Supplement (M100-S24). Wayne, PA: CLSI; 2014. 230p., 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 MRSA1818. The Clinical & Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fourth Informational Supplement (M100-S24). Wayne, PA: CLSI; 2014. 230p.,1919. Maes N, Magdalena J, Rottiers S, De Gheldre Y, Struelens MJ. Evaluation of a triplex PCR assay to discriminate Staphylococcus aureus from coagulase-negative Staphylococci and determine methicillin resistance from blood cultures. J Clin Microbiol. 2002;40(4):1514-7.. 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 Syntheses2020. Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(4): 264-9.. 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.

RESULTS

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

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 aureus; HCWs: healthcare workers.

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

DISCUSSION

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), respectively1414. Rahbar M, Karamiyar M, Gra-Agaji R. Nasal carriage of methicillin-resistant Staphylococcus aureus among healthcare workers of an Iranian hospital. Infect Control Hosp Epidemiol . 2003;24(4):236-7.,1616. 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(5):e241-7.,1717. Lari AR, Pourmand MR, Moghadam SO, Abdossamadi Z, Namvar AE, Asghari B. Prevalence of PVL-containing MRSA isolates among hospital staff nasal carriers. Lab Med 2011;42(5):283-6.,2121. Saderi H, Ôwlia P, Zafarghandi N, Jalali nadoshan MR. Evaluation of antibiotic resistance in Staphylococcus aureus isolated from nose of two teaching hospitals staff of shahed university. J Mazandaran Univ Med Sci. 2004;14(42):69-75.

22. Nikbakht M, Nahaei MR, Akhi MT, Asgharzadeh M, Nikvash S. Molecular fingerprinting of meticillin-resistant Staphylococcus aureus strains isolated from patients and staff of two Iranian hospitals. J Hosp Infect. 2008;69(1):46-55.

23. Armin S, Karimi A, Fahimzad A, Fallah F, Shamshiri A. Staphylococcal nasal colonization in Mofid children hospital staff; carrier state and antibiotic susceptibility. Arch Clin Infect Dis . 2007;2(2):57-60.

24. Nafisi MR, Kalhor H, Zamanzad B, Karimi A, FArokhi E, Validi M. Comparison of agar screen and duplex-PCR in determination of methicillin resistant Staphylococcus aureus (MRSA) strains isolated from nose of personnel in Hajar hospital of Shahre-kord, 2007. Arak Med Univ J. 2008;11(2):94-101.

25. Khalili MB, Sharifi-Yazdi MK, Dargahi H, Sadeghian HA.Nasal colonization rate of Staphylococcus aureus strains among health care service employee’s of Teaching University Hospitals in Yazd. Acta Med Iran. 2009;47(4):315-7.

26. Rahimi-Alang S, Asmar M, Cheraghali F, Yazarlou S, Amini A, Shakeri F, et al. Frequency of methicillin resistant Staphylococcus aureus in health care. Zahedan J Res Med Sci. 2011;13(1):17-22.

27. Moradi N, Mousavi A, Rouzrokh SH, Javadpour S. Frequency of nasal carriage for methicillin-resistant Staphylococcus aureus among the Hospital Staff-Bandar Abbas, Iran. Med J Hormozgan Univ. 2011;15(2):90-6.

28. Hossein Zadegan H, Menati S, Tarahi Mj, Mohamadi F. Screening of Methicillin and Vancomycin resistant Staphylococcus aureus in the nasal of hospital personnel of Khorram Abad, Iran . Spring & Summer 2008;2(1): 26.

29. Afrough P, Pourmand MR, Sarajian AA, Saki M, Saremy S. Molecular investigation of Staphylococcus aureus, coa and spa genes in Ahvaz Hospitals, Staff Nose compared with patients clinical samples. Jundishapur J.Microbiol. 2013;6(4).e5377.

30. Talaie H, Kamalbeik S, Mahdavinejad A, Pajoumand A, Moghaddam SAB. Health care practice, Staphylococcus aureus in toxicological ICU, Loghman Hakim Hospital, Tehran, Iran. Iran J Clin Infect Dis. 2011;6(suppl):12-16.

31. Zaenaliniya N, Pourmand MR, Ghaneh M, Afrough P, Hossini M, Abdossamadi Z. Prevalence of Staphylococcus aureus among health care workers in hospitals of Tehran University of Medical Sciences. J Hosp Med. 2011;6(1):6-9.

32. Mamishi S, Mahmoudi S, Sadeghi RH, Movahedi Z, Hadipour R, Pourakbari B. Genotyping of Staphylococcus aureus strains among healthcare workers and patients in the tertiary referral Children’s Medical Hospital in Tehran, Iran. Br J Biomed Sci. 2012;69(4):173-7.

33. Khalili MB, Moshref M, Sharifi M, Sadeh M, Sazmand A. Prevalence of Staphylococcus aureus (SA) and methicillin resistant Staphylococcus aureus (MRSA) in personnel of operation room of Shahid Sadoughi Hospital, Yazd, Iran. J Pay Salamat. 2013;6(5):392-402.

34. Kalhor H, Validi M, Nafisi MR. Evaluation of the frequency of methicillin resistant Staphylococcus isolated from nose of nursing personnel of Hajar Hospital of Shahrekord. Qom Univ Med Sci J. 2013;7(1):42-9.

35. Jannati E, Arzanlou M, Habibzadeh S, Mohammadi S, Ahadi P, Mohammadi-Ghalehbin B, et al. Nasal colonization of mecA-positive, oxacillin-susceptible, methicillin-resistant Staphylococcus aureus isolates among nursing staff in an Iranian teaching hospital. Am J Infect Control. 2013;41(11):1122-4.

36. Saadat S, Solhjoo K, Kazemi A, Mradaneh J. Antibiotic resistance pattern of Staphylococcus aureus strains isolated from personnel of Jahrom Hospitals in 2012. Armaghane Danesh J. 2014;18(10):826-35.

37. Ahanjan M, Abdollahi S, Abdolian H. Prevalence of meticilin-resistant Staphylococcus aureus isolated from hand and nasal of hospital health worker. J Gorgan Uni Med Sci. 2014;16(4):131-6.

38. Navidinia M. Detection of inducible clindamycin resistance (MLSBi) among methicillin-resistant Staphylococcus aureus (MRSA) isolated from health care providers. J Paramed Sci. 2015;6(1):91-96.
-3939. Ohadian Moghadam S, Pourmand MR, Davoodabadi A. The detection of Mupirocin resistance and nasal carriage of methicillin resistant Staphylococcus aureus among healthcare workers at University Hospitals of Tehran, Iran. Iran J Public Health. 2015;44(3):361-8.. 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 MRSA4040. Hefzy EM, Hassan GM, Abd El Reheem F. Detection of Panton-Valentine leukocidin-positive methicillin-resistant Staphylococcus aureus nasal carriage among Egyptian health care workers. Surg Infect (Larchmt). 2016;17(3):369-75.. In Ethiopia, Shibabaw et al. reported that the prevalence of S. aureus among Ethiopian HCWs was 28.8% and among these 44.1% was MRSA99. Shibabaw A, Abebe T, Mihret A. Nasal carriage rate of methicillin resistant Staphylococcus aureus among Dessie Referral Hospital Health Care Workers; Dessie, Northeast Ethiopia. Antimicrob Resist Infect Control. 2013;2(1):25.. 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 MRSA4141. Chen B, Dai X, He B, Pan K, Li H, Liu X, et al. Differences in Staphylococcus aureus nasal carriage and molecular characteristics among community residents and healthcare workers at Sun Yat-Sen University, Guangzhou, Southern China. BMC Infect Dis . 2015;15:303.. 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 %, respectively4242. Albrich WC, Harbarth S. Health-care workers: source, vector, or victim of MRSA? Lancet Infect Dis. 2008;8(5):289-301.. However, nasal carriage of MRSA differs noticeably among countries99. Shibabaw A, Abebe T, Mihret A. Nasal carriage rate of methicillin resistant Staphylococcus aureus among Dessie Referral Hospital Health Care Workers; Dessie, Northeast Ethiopia. Antimicrob Resist Infect Control. 2013;2(1):25.,4040. Hefzy EM, Hassan GM, Abd El Reheem F. Detection of Panton-Valentine leukocidin-positive methicillin-resistant Staphylococcus aureus nasal carriage among Egyptian health care workers. Surg Infect (Larchmt). 2016;17(3):369-75.

41. Chen B, Dai X, He B, Pan K, Li H, Liu X, et al. Differences in Staphylococcus aureus nasal carriage and molecular characteristics among community residents and healthcare workers at Sun Yat-Sen University, Guangzhou, Southern China. BMC Infect Dis . 2015;15:303.

42. Albrich WC, Harbarth S. Health-care workers: source, vector, or victim of MRSA? Lancet Infect Dis. 2008;8(5):289-301.

43. De Boeck H, Vandendriessche S, Hallin M, Batoko B, Alworonga JP, Mapendo B, et al. Staphylococcus aureus nasal carriage among healthcare workers in Kisangani, the Democratic Republic of the Congo. Eur J Clin Microbiol Infect Dis. 2015;34(8):1567-72.
-4444. Garcia C, Acuña-Villaorduña A, Dulanto A, Vandendriessche S, Hallin M, Jacobs J, et al. Dynamics of nasal carriage of methicillin-resistant Staphylococcus aureus among healthcare workers in a tertiary-care hospital in Peru. Eur J Clin Microbiol Infect Dis. 2016;35(1):89-93. which may reflect methodological differences (sampling technique, sample size, culture techniques, the sites chosen for sampling) and differences in infection control policies, among other factors1212. Khanal R, Sah P, Lamichhane P, Lamsal A, Upadhaya S, Pahwa VK. Nasal carriage of methicillin resistant Staphylococcus aureus among health care workers at a tertiary care hospital in Western Nepal. Antimicrob Resist Infect Control . 2015;4(1):39.,4343. De Boeck H, Vandendriessche S, Hallin M, Batoko B, Alworonga JP, Mapendo B, et al. Staphylococcus aureus nasal carriage among healthcare workers in Kisangani, the Democratic Republic of the Congo. Eur J Clin Microbiol Infect Dis. 2015;34(8):1567-72.. 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 Iran4545. Emaneini M, Hosseinkhani F, Jabalameli F, Nasiri MJ, Dadashi M, Pouriran R, et al. Prevalence of vancomycin-resistant Enterococcus in Iran: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2016;35(9):1387-92.. 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 enterococci4545. Emaneini M, Hosseinkhani F, Jabalameli F, Nasiri MJ, Dadashi M, Pouriran R, et al. Prevalence of vancomycin-resistant Enterococcus in Iran: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2016;35(9):1387-92.,4646. Clements A, Halton K, Graves N, Pettitt A, Morton A, Looke D, et al. Overcrowding and understaffing in modern health-care systems: key determinants in meticillin-resistant Staphylococcus aureus transmission. Lancet Infect Dis . 2008;8(7):427-34.. 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 compliance4545. Emaneini M, Hosseinkhani F, Jabalameli F, Nasiri MJ, Dadashi M, Pouriran R, et al. Prevalence of vancomycin-resistant Enterococcus in Iran: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2016;35(9):1387-92.

46. Clements A, Halton K, Graves N, Pettitt A, Morton A, Looke D, et al. Overcrowding and understaffing in modern health-care systems: key determinants in meticillin-resistant Staphylococcus aureus transmission. Lancet Infect Dis . 2008;8(7):427-34.
-4747. Pittet D, Allegranzi B, Storr J, Bagheri Nejad S, Dziekan G, Leotsakos A, et al. Infection control as a major World Health Organization priority for developing countries. J Hosp Infect . 2008;68(4):285-92.. 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 compliance4545. Emaneini M, Hosseinkhani F, Jabalameli F, Nasiri MJ, Dadashi M, Pouriran R, et al. Prevalence of vancomycin-resistant Enterococcus in Iran: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2016;35(9):1387-92.,4848. Alp E, Damani N. Healthcare-associated infections in intensive care units: epidemiology and infection control in low-to-middle income countries. J Infect Dev Ctries. 2015;9(10):1040-5.. On the other hand, Iranian hospitals are poorly resourced with regard to personal protective equipment (PPE) (gowns, gloves, mask)4545. Emaneini M, Hosseinkhani F, Jabalameli F, Nasiri MJ, Dadashi M, Pouriran R, et al. Prevalence of vancomycin-resistant Enterococcus in Iran: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2016;35(9):1387-92.,4949. Alp E, Leblebicioglu H, Doganay M, Voss A. Infection control practice in countries with limited resources. Ann Clin Microbiol Antimicrob. 2011;10(1):36.. In contrast, in the Netherlands, all hospitals are equipped with appropriate PPEs4545. Emaneini M, Hosseinkhani F, Jabalameli F, Nasiri MJ, Dadashi M, Pouriran R, et al. Prevalence of vancomycin-resistant Enterococcus in Iran: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2016;35(9):1387-92.,4949. Alp E, Leblebicioglu H, Doganay M, Voss A. Infection control practice in countries with limited resources. Ann Clin Microbiol Antimicrob. 2011;10(1):36.. Second, it has been proven that treatment with intranasal mupirocin can reduce the rates of nosocomial MRSA infection5050. Septimus EJ, Schweizer ML. Decolonization in prevention of health care-associated infections . Clin Microbiol Rev. 2016;29(2):201-22.. 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 Iran5151. Shahsavan S, Emaneini M, Noorazar Khoshgnab B, Khoramian B, Asadollahi P, Aligholi M, et al. A high prevalence of mupirocin and macrolide resistance determinant among Staphylococcus aureus strains isolated from burnt patients. Burns. 2012;38(3):378-82.. Third, overprescribing or unregulated use of antibiotics in developing countries such as Iran is common4545. Emaneini M, Hosseinkhani F, Jabalameli F, Nasiri MJ, Dadashi M, Pouriran R, et al. Prevalence of vancomycin-resistant Enterococcus in Iran: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2016;35(9):1387-92.,4848. Alp E, Damani N. Healthcare-associated infections in intensive care units: epidemiology and infection control in low-to-middle income countries. J Infect Dev Ctries. 2015;9(10):1040-5.,5252. Damani N. Simple measures save lives: an approach to infection control in countries with limited resources. J Hosp Infect . 2007;65(Suppl 2):151-4.. For example, the use of cephalosporins and fluoroquinolones is prevalent, and their overuse may elicit the emergence of MRSA in hospitals5353. Cheng VC, Li IW, Wu AK, Tang BS, Ng KH, To KK, et al. Effect of antibiotics on the bacterial load of meticillin-resistant Staphylococcus aureus colonisation in anterior nares. J Hosp Infect . 2008;70(1):27-34.. 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 MRSA4545. Emaneini M, Hosseinkhani F, Jabalameli F, Nasiri MJ, Dadashi M, Pouriran R, et al. Prevalence of vancomycin-resistant Enterococcus in Iran: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2016;35(9):1387-92.,4848. Alp E, Damani N. Healthcare-associated infections in intensive care units: epidemiology and infection control in low-to-middle income countries. J Infect Dev Ctries. 2015;9(10):1040-5.. Fourth, hospitals do not have a sufficient number of isolation rooms; thus, MRSA-infected patients are admitted to the general wards together with uninfected patients4545. Emaneini M, Hosseinkhani F, Jabalameli F, Nasiri MJ, Dadashi M, Pouriran R, et al. Prevalence of vancomycin-resistant Enterococcus in Iran: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2016;35(9):1387-92.. As a result, there is an increased risk of transmission of MRSA from patients to both patients and HCWs4545. Emaneini M, Hosseinkhani F, Jabalameli F, Nasiri MJ, Dadashi M, Pouriran R, et al. Prevalence of vancomycin-resistant Enterococcus in Iran: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2016;35(9):1387-92.. Fifth, decontamination of the hospital environment is likely to be ineffective in Iran4545. Emaneini M, Hosseinkhani F, Jabalameli F, Nasiri MJ, Dadashi M, Pouriran R, et al. Prevalence of vancomycin-resistant Enterococcus in Iran: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2016;35(9):1387-92.; thus, MRSA can be spread by contact with contaminated surfaces4545. Emaneini M, Hosseinkhani F, Jabalameli F, Nasiri MJ, Dadashi M, Pouriran R, et al. Prevalence of vancomycin-resistant Enterococcus in Iran: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2016;35(9):1387-92.. In recent years, the incidence of MRSA infection has increased dramatically in Iranian hospitals1515. Fatholahzadeh B, Emaneini M, Gilbert G, Udo E, Aligholi M, Modarressi MH, et al. Staphylococcal cassette chromosome mec (SCCmec) analysis and antimicrobial susceptibility patterns of methicillin-resistant Staphylococcus aureus (MRSA) isolates in Tehran, Iran. Microb Drug Resist. 2008;14(3):217-20.. Finally, the hospital infection control teams are inexperienced, inadequate, not well trained, and worst of all, most of them do not include a clinical microbiologist4545. Emaneini M, Hosseinkhani F, Jabalameli F, Nasiri MJ, Dadashi M, Pouriran R, et al. Prevalence of vancomycin-resistant Enterococcus in Iran: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2016;35(9):1387-92.. 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.

Acknowledgments

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

REFERENCES

  • 1
    Castro A, Komora N, Ferreira V, Lira A, Mota M, Silva J, et al. Prevalence of Staphylococcus aureus from nares and hands on health care professionals in a Portuguese Hospital. J Appl Microbiol. 2016;121(3):831-9.
  • 2
    Honda H, Krauss MJ, Coopersmith CM, Kollef MH, Richmond AM, Fraser VJ, et al. Staphylococcus aureus nasal colonization and subsequent infection in intensive care unit patients: does methicillin resistance matter? Infect Control Hosp Epidemiol. 2010;31(6):584-91.
  • 3
    Gurieva T, Bootsma MC, Bonten MJ. Cost and effects of different admission screening strategies to control the spread of methicillin-resistant Staphylococcus aureus PLoS Comput Biol. 2013;9(2):e1002874.
  • 4
    Lu SY, Chang FY, Cheng CC, Lee KD, Huang YC. Methicillin-resistant Staphylococcus aureus nasal colonization among adult patients visiting emergency department in a medical center in Taiwan. PLoS One. 2011;6(6):e18620.
  • 5
    Safdar N, Bradley EA. The risk of infection after nasal colonization with Staphylococcus aureus Am J Med. 2008;121(4):310-5.
  • 6
    Cirkovic I, Stepanovic S, Skov R, Trajkovic J, Grgurevic A, Larsen AR. Carriage and genetic diversity of methicillin-resistant Staphylococcus aureus among patients and healthcare workers in a Serbian University Hospital. PLoS One . 2015;10(5):e0127347.
  • 7
    Calfee DP, Salgado CD, Milstone AM, Harris AD, Kuhar DT, Moody J, et al. Strategies to prevent methicillin-resistant Staphylococcus aureus transmission and infection in acute care hospitals: 2014 update. Infect Control Hosp Epidemiol . 2014;35(7):772-96.
  • 8
    Melzer M, Eykyn SJ, Gransden WR, Chinn S. Is methicillin-resistant Staphylococcus aureus more virulent than methicillin-susceptible S. aureus? A comparative cohort study of British patients with nosocomial infection and bacteremia. Clin Infect Dis. 2003;37(11):1453-60.
  • 9
    Shibabaw A, Abebe T, Mihret A. Nasal carriage rate of methicillin resistant Staphylococcus aureus among Dessie Referral Hospital Health Care Workers; Dessie, Northeast Ethiopia. Antimicrob Resist Infect Control. 2013;2(1):25.
  • 10
    Espinosa-Gongora C, Dahl J, Elvstrom A, van Wamel WJ, Guardabassi L. Individual predisposition to Staphylococcus aureus colonization in pigs on the basis of quantification, carriage dynamics, and serological profiles. Appl Environ Microbiol. 2015;81(4):1251-6.
  • 11
    Ayliffe GA. The progressive intercontinental spread of methicillin-resistant Staphylococcus aureus Clin Infect Dis . 1997;24(Suppl 1):S74-9.
  • 12
    Khanal R, Sah P, Lamichhane P, Lamsal A, Upadhaya S, Pahwa VK. Nasal carriage of methicillin resistant Staphylococcus aureus among health care workers at a tertiary care hospital in Western Nepal. Antimicrob Resist Infect Control . 2015;4(1):39.
  • 13
    Vazquez-Guillamet C, Kollef MH. Treatment of Gram-positive infections in critically ill patients. BMC Infect Dis. 2014;14(1):92.
  • 14
    Rahbar M, Karamiyar M, Gra-Agaji R. Nasal carriage of methicillin-resistant Staphylococcus aureus among healthcare workers of an Iranian hospital. Infect Control Hosp Epidemiol . 2003;24(4):236-7.
  • 15
    Fatholahzadeh B, Emaneini M, Gilbert G, Udo E, Aligholi M, Modarressi MH, et al. Staphylococcal cassette chromosome mec (SCCmec) analysis and antimicrobial susceptibility patterns of methicillin-resistant Staphylococcus aureus (MRSA) isolates in Tehran, Iran. Microb Drug Resist. 2008;14(3):217-20.
  • 16
    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(5):e241-7.
  • 17
    Lari AR, Pourmand MR, Moghadam SO, Abdossamadi Z, Namvar AE, Asghari B. Prevalence of PVL-containing MRSA isolates among hospital staff nasal carriers. Lab Med 2011;42(5):283-6.
  • 18
    The Clinical & Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fourth Informational Supplement (M100-S24). Wayne, PA: CLSI; 2014. 230p.
  • 19
    Maes N, Magdalena J, Rottiers S, De Gheldre Y, Struelens MJ. Evaluation of a triplex PCR assay to discriminate Staphylococcus aureus from coagulase-negative Staphylococci and determine methicillin resistance from blood cultures. J Clin Microbiol. 2002;40(4):1514-7.
  • 20
    Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(4): 264-9.
  • 21
    Saderi H, Ôwlia P, Zafarghandi N, Jalali nadoshan MR. Evaluation of antibiotic resistance in Staphylococcus aureus isolated from nose of two teaching hospitals staff of shahed university. J Mazandaran Univ Med Sci. 2004;14(42):69-75.
  • 22
    Nikbakht M, Nahaei MR, Akhi MT, Asgharzadeh M, Nikvash S. Molecular fingerprinting of meticillin-resistant Staphylococcus aureus strains isolated from patients and staff of two Iranian hospitals. J Hosp Infect. 2008;69(1):46-55.
  • 23
    Armin S, Karimi A, Fahimzad A, Fallah F, Shamshiri A. Staphylococcal nasal colonization in Mofid children hospital staff; carrier state and antibiotic susceptibility. Arch Clin Infect Dis . 2007;2(2):57-60.
  • 24
    Nafisi MR, Kalhor H, Zamanzad B, Karimi A, FArokhi E, Validi M. Comparison of agar screen and duplex-PCR in determination of methicillin resistant Staphylococcus aureus (MRSA) strains isolated from nose of personnel in Hajar hospital of Shahre-kord, 2007. Arak Med Univ J. 2008;11(2):94-101.
  • 25
    Khalili MB, Sharifi-Yazdi MK, Dargahi H, Sadeghian HA.Nasal colonization rate of Staphylococcus aureus strains among health care service employee’s of Teaching University Hospitals in Yazd. Acta Med Iran. 2009;47(4):315-7.
  • 26
    Rahimi-Alang S, Asmar M, Cheraghali F, Yazarlou S, Amini A, Shakeri F, et al. Frequency of methicillin resistant Staphylococcus aureus in health care. Zahedan J Res Med Sci. 2011;13(1):17-22.
  • 27
    Moradi N, Mousavi A, Rouzrokh SH, Javadpour S. Frequency of nasal carriage for methicillin-resistant Staphylococcus aureus among the Hospital Staff-Bandar Abbas, Iran. Med J Hormozgan Univ. 2011;15(2):90-6.
  • 28
    Hossein Zadegan H, Menati S, Tarahi Mj, Mohamadi F. Screening of Methicillin and Vancomycin resistant Staphylococcus aureus in the nasal of hospital personnel of Khorram Abad, Iran . Spring & Summer 2008;2(1): 26.
  • 29
    Afrough P, Pourmand MR, Sarajian AA, Saki M, Saremy S. Molecular investigation of Staphylococcus aureus, coa and spa genes in Ahvaz Hospitals, Staff Nose compared with patients clinical samples. Jundishapur J.Microbiol. 2013;6(4).e5377.
  • 30
    Talaie H, Kamalbeik S, Mahdavinejad A, Pajoumand A, Moghaddam SAB. Health care practice, Staphylococcus aureus in toxicological ICU, Loghman Hakim Hospital, Tehran, Iran. Iran J Clin Infect Dis. 2011;6(suppl):12-16.
  • 31
    Zaenaliniya N, Pourmand MR, Ghaneh M, Afrough P, Hossini M, Abdossamadi Z. Prevalence of Staphylococcus aureus among health care workers in hospitals of Tehran University of Medical Sciences. J Hosp Med. 2011;6(1):6-9.
  • 32
    Mamishi S, Mahmoudi S, Sadeghi RH, Movahedi Z, Hadipour R, Pourakbari B. Genotyping of Staphylococcus aureus strains among healthcare workers and patients in the tertiary referral Children’s Medical Hospital in Tehran, Iran. Br J Biomed Sci. 2012;69(4):173-7.
  • 33
    Khalili MB, Moshref M, Sharifi M, Sadeh M, Sazmand A. Prevalence of Staphylococcus aureus (SA) and methicillin resistant Staphylococcus aureus (MRSA) in personnel of operation room of Shahid Sadoughi Hospital, Yazd, Iran. J Pay Salamat. 2013;6(5):392-402.
  • 34
    Kalhor H, Validi M, Nafisi MR. Evaluation of the frequency of methicillin resistant Staphylococcus isolated from nose of nursing personnel of Hajar Hospital of Shahrekord. Qom Univ Med Sci J. 2013;7(1):42-9.
  • 35
    Jannati E, Arzanlou M, Habibzadeh S, Mohammadi S, Ahadi P, Mohammadi-Ghalehbin B, et al. Nasal colonization of mecA-positive, oxacillin-susceptible, methicillin-resistant Staphylococcus aureus isolates among nursing staff in an Iranian teaching hospital. Am J Infect Control. 2013;41(11):1122-4.
  • 36
    Saadat S, Solhjoo K, Kazemi A, Mradaneh J. Antibiotic resistance pattern of Staphylococcus aureus strains isolated from personnel of Jahrom Hospitals in 2012. Armaghane Danesh J. 2014;18(10):826-35.
  • 37
    Ahanjan M, Abdollahi S, Abdolian H. Prevalence of meticilin-resistant Staphylococcus aureus isolated from hand and nasal of hospital health worker. J Gorgan Uni Med Sci. 2014;16(4):131-6.
  • 38
    Navidinia M. Detection of inducible clindamycin resistance (MLSBi) among methicillin-resistant Staphylococcus aureus (MRSA) isolated from health care providers. J Paramed Sci. 2015;6(1):91-96.
  • 39
    Ohadian Moghadam S, Pourmand MR, Davoodabadi A. The detection of Mupirocin resistance and nasal carriage of methicillin resistant Staphylococcus aureus among healthcare workers at University Hospitals of Tehran, Iran. Iran J Public Health. 2015;44(3):361-8.
  • 40
    Hefzy EM, Hassan GM, Abd El Reheem F. Detection of Panton-Valentine leukocidin-positive methicillin-resistant Staphylococcus aureus nasal carriage among Egyptian health care workers. Surg Infect (Larchmt). 2016;17(3):369-75.
  • 41
    Chen B, Dai X, He B, Pan K, Li H, Liu X, et al. Differences in Staphylococcus aureus nasal carriage and molecular characteristics among community residents and healthcare workers at Sun Yat-Sen University, Guangzhou, Southern China. BMC Infect Dis . 2015;15:303.
  • 42
    Albrich WC, Harbarth S. Health-care workers: source, vector, or victim of MRSA? Lancet Infect Dis. 2008;8(5):289-301.
  • 43
    De Boeck H, Vandendriessche S, Hallin M, Batoko B, Alworonga JP, Mapendo B, et al. Staphylococcus aureus nasal carriage among healthcare workers in Kisangani, the Democratic Republic of the Congo. Eur J Clin Microbiol Infect Dis. 2015;34(8):1567-72.
  • 44
    Garcia C, Acuña-Villaorduña A, Dulanto A, Vandendriessche S, Hallin M, Jacobs J, et al. Dynamics of nasal carriage of methicillin-resistant Staphylococcus aureus among healthcare workers in a tertiary-care hospital in Peru. Eur J Clin Microbiol Infect Dis. 2016;35(1):89-93.
  • 45
    Emaneini M, Hosseinkhani F, Jabalameli F, Nasiri MJ, Dadashi M, Pouriran R, et al. Prevalence of vancomycin-resistant Enterococcus in Iran: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2016;35(9):1387-92.
  • 46
    Clements A, Halton K, Graves N, Pettitt A, Morton A, Looke D, et al. Overcrowding and understaffing in modern health-care systems: key determinants in meticillin-resistant Staphylococcus aureus transmission. Lancet Infect Dis . 2008;8(7):427-34.
  • 47
    Pittet D, Allegranzi B, Storr J, Bagheri Nejad S, Dziekan G, Leotsakos A, et al. Infection control as a major World Health Organization priority for developing countries. J Hosp Infect . 2008;68(4):285-92.
  • 48
    Alp E, Damani N. Healthcare-associated infections in intensive care units: epidemiology and infection control in low-to-middle income countries. J Infect Dev Ctries. 2015;9(10):1040-5.
  • 49
    Alp E, Leblebicioglu H, Doganay M, Voss A. Infection control practice in countries with limited resources. Ann Clin Microbiol Antimicrob. 2011;10(1):36.
  • 50
    Septimus EJ, Schweizer ML. Decolonization in prevention of health care-associated infections . Clin Microbiol Rev. 2016;29(2):201-22.
  • 51
    Shahsavan S, Emaneini M, Noorazar Khoshgnab B, Khoramian B, Asadollahi P, Aligholi M, et al. A high prevalence of mupirocin and macrolide resistance determinant among Staphylococcus aureus strains isolated from burnt patients. Burns. 2012;38(3):378-82.
  • 52
    Damani N. Simple measures save lives: an approach to infection control in countries with limited resources. J Hosp Infect . 2007;65(Suppl 2):151-4.
  • 53
    Cheng VC, Li IW, Wu AK, Tang BS, Ng KH, To KK, et al. Effect of antibiotics on the bacterial load of meticillin-resistant Staphylococcus aureus colonisation in anterior nares. J Hosp Infect . 2008;70(1):27-34.

Publication Dates

  • Publication in this collection
    Sep-Oct 2017

History

  • Received
    05 Apr 2017
  • Accepted
    05 June 2017
Sociedade Brasileira de Medicina Tropical - SBMT Caixa Postal 118, 38001-970 Uberaba MG Brazil, Tel.: +55 34 3318-5255 / +55 34 3318-5636/ +55 34 3318-5287, http://rsbmt.org.br/ - Uberaba - MG - Brazil
E-mail: rsbmt@uftm.edu.br