Journal of Global Antimicrobial Resistance

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Review

Methicillin-resistant Staphylococcus aureus (MRSA) in Iran: A systematic review and meta-analysis

Masoud Dadashi

^a,

*, Mohammad Javad Nasiri

^a

, Fatemeh Fallah

^b

, Parviz Owlia

^c

, Bahareh Hajikhani

^a

, Mohammad Emaneini

^d

, Mirsasan Mirpour

^e

aDepartmentofMicrobiology,SchoolofMedicine,ShahidBeheshtiUniversityofMedicalSciences,Tehran,Iran

bPediatricInfectionsResearchCenter,MoﬁdHospital,ShahidBeheshtiUniversityofMedicalSciences,Tehran,Iran

cMolecularMicrobiologyResearchCenter,ShahedUniversity,Tehran,Iran

dDepartmentofMicrobiology,SchoolofMedicine,TehranUniversityofMedicalSciences,Tehran,Iran

eDepartmentofMicrobiology,FacultyofScience,IslamicAzadUniversityofLahijan,Gilan,Iran

ARTICLE INFO Articlehistory:

Received4April2017

Receivedinrevisedform15July2017 Accepted8September2017 Availableonline21September2017 Keywords:

MRSA

Systematicreview Meta-analysis Iran

ABSTRACT

Introduction:Methicillin-resistantStaphylococcusaureus(MRSA)isamongthemostprevalentpathogens causinghealthcare-associatedinfections.Accurateandupdateddatadescribingtheepidemiologyof MRSAarecrucialforthedevelopmentofnationalpoliciestocontrolMRSAinfectionineachcountry.This studyaimedtoestimatetheprevalenceofMRSAindifferentpartsofIran.

Methods:Severaldatabases,includingMEDLINE,Embase,WebofScienceandScientiﬁcInformation Database(http://www.sid.ir),weresearchedfrom1January2000to31March2016toidentifystudies addressingthefrequencyorprevalenceofMRSAinIran.ComprehensiveMeta-Analysissoftwarev.2.2 wasusedtoanalysethedata.

Results:Ofthe725recordsidentifiedfromthedatabases,31studiesfulfilledtheeligibilitycriteria.The analysesshowedthatthefrequencyofMRSAinfectionswas43.0%(95%confidenceinterval36.3–50.0%) amongconfirmedS.aureusisolates.FurtherstratifiedanalysesindicatedthattheprevalenceofMRSAwas higherinstudiesperformedaftertheyear2000.

Conclusions:Sinceahighrate ofMRSAinfectionswas seeninthis analysis,regularsurveillance of hospital-associatedinfections,monitoringofantibioticsensitivitypatterns,andformulationofdeﬁnite antibioticpolicymayfacilitatemoreaccurateactionforthepreventionandcontrolofMRSA.

Contents

1. Introduction ... 97

2. Methods ... 97

2.1. Literaturesearch ... 97

2.2. Inclusionandexclusioncriteria ... 97

2.3. Dataextractionanddeﬁnitions ... 97

2.4. Qualityassessment ... 97

2.5. Meta-analysis ... 97

3. Results ... 97

3.1. Characteristicsofincludedstudies ... 97

3.2. Riskofbiasassessment ... 97

3.3. Prevalenceofmethicillin-resistantStaphylococcusaureus(MRSA)strainsinclinicalsamples ... 98

4. Discussion ... 98

Funding ... 102

Competinginterests ... 102

*Correspondingauthor.

E-mailaddress:[email protected](M.Dadashi).

http://dx.doi.org/10.1016/j.jgar.2017.09.006

ContentslistsavailableatScienceDirect

j o u r n a l h o m ep a g e: w w w . el s e v i e r . c o m / l o c at e / j g a r

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Ethicalapproval ... 102 References... 102

1.Introduction

Methicillin-resistant

Staphylococcusaureus

(MRSA) is one of the most important pathogens causing healthcare-associated infections

[1,2].

Studies indicate that the incidence of MRSA in the past few years has increased extensively worldwide

[3,4]

Infection due to MRSA imposes a high and increasing burden on healthcare resources as well as increased morbidity and mortality

[5].

MRSA infections kill ca. 20 000 hospitalised US patients annually; this is similar to the number of deaths due to acquired immune de

ﬁ

ciency syndrome (AIDS), tuberculosis and viral hepatitis combined

[6].

In Iran, the number of MRSA infections has dramatically increased and is a serious problem in the form of nosocomial infections

[7].

In the past 10 years, an alarming increase in the prevalence of MRSA has been observed

[8].

Thus, accurate and updated data describing the epidemiology of MRSA are crucial for the development of national policies to control MRSA infection in each country.

Although rates of MRSA have been reported in some studies in different parts of Iran, most of these reports have presented local information and a comprehensive analysis has not yet been performed

[9,10].

The present study aimed to estimate the true frequency of MRSA in Iran during the last 16 years (2000

–

2016) using a systematic review and meta-analysis according to the Preferred Reporting Items for Systematic reviews and Meta- Analyses (PRISMA) statement

[11].

2.Methods 2.1.Literaturesearch

Electronic medical databases, including MEDLINE (PubMed), Embase, Web of Science Core Collection and Scienti

ﬁ

c Information Database (http://www.sid.ir), were searched for studies published between 1 January 2000 and 31 March 2016 reporting the frequency or prevalence of MRSA in healthcare settings of Iran. The following keywords from Medical Subject Headings or titles or abstracts were used with the help of Boolean operators (and; or):

Staphylococcus aureus;

resistance;

MRSA; prevalence; frequency; proportion; incidence; and Iran.

The bibliographies of the retrieved articles were also searched for additional References

2.2.Inclusionandexclusioncriteria

Original articles were included if they met all of the following criteria: (i) observational study investigating the prevalence, frequency or proportion of MRSA in healthcare settings in Iran;

(ii) study population representative of the general population, i.e.

not a selected group with speci

ﬁ

c co-morbidities; (iii) study conducted in 2000 or after; (iv) study published in English or Persian language; and (v) used Clinical and Laboratory Standards Institute (CLSI) guidelines for diagnosis of MRSA, i.e. broth microdilution, Etest, disk diffusion for cefoxitin, and PCR.

Case reports, narrative reviews, studies with a high risk of bias (e.g. studies focused on speci

ﬁ

c groups of cases, i.e. immunocom- promised populations) and data overlap with other studies included in the analysis (studies with larger sample size or the longest study period were preferred) were excluded.

2.3.Dataextractionanddeﬁnitions

The following variables were extracted from included studies:

author name; study period; year of publication; study setting;

number of investigated cases; number of

S. aureus

and MRSA isolates; proportion or frequency of MRSA; source of isolates; and diagnostic methods. Two investigators extracted data from all of the included studies independently. Inconsistencies between reviewers were discussed to obtain consensus.

2.4.Qualityassessment

The quality of eligible studies was assessed using a quality assessment checklist designed by the Joanna Briggs Institute

[12].

Various methodological features of the studies were assessed using this checklist, including representativeness of the study population, sample size, study setting and statistical analysis. The tool has 10 items. Each study was given a score of 0 or 1 for each item. Studies with a total score of

>

7 were considered to have a low risk of bias. Every stage of critical appraisal was carried out by two reviewers independently, with discrepancies discussed with a third reviewer to reach consensus.

2.5.Meta-analysis

Analysis was performed using Comprehensive Meta-Analysis (CMA) software v.2.2 (Biostat Inc., Englewood, NJ). Random-effects models were used to combine the studies, taking into account the possibility of heterogeneity between studies, which was tested with the Cochrane

Q

test and

I²

test. To assess possible publication bias, Egger’s weighted regression methods were used. A

P-value

of

<

0.05 was considered indicative of statistically signi

ﬁ

cant publication bias.

3.Results

3.1.Characteristicsofincludedstudies

Initially, a total of 725 articles were retrieved. In secondary screening, 671 of the articles were excluded on the basis of title and abstract evaluation (Fig.

1).

In the next step, 23 of the remaining 54 studies were excluded upon a full-text search. Thus, 31 eligible studies were selected for

ﬁ

nal analysis

[19–49].Fig.1

shows the reasons for study exclusion based on assessment of title/abstract and full-text articles. Characteristics of the included articles are summarised in

Table1.

All positive cultures were obtained inside hospital settings and appeared to be hospital-acquired. The geographic location of the studies covered east to west and north to south of Iran, with the majority of patients from central of Iran. All included studies used standard diagnostic methods for MRSA. MRSA were isolated from various clinical samples including nasal, wound, blood, urine, respiratory tract, sputum, bronchoalveolar, etc.

3.2.Riskofbiasassessment

Based on the quality assessment, all included studies for the meta-analysis were identi

ﬁ

ed as having a low risk of bias (quality assessment score

>

7).

M.Dadashietal./JournalofGlobalAntimicrobialResistance12(2018)96–103 97

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3.3.Prevalenceofmethicillin-resistant

Staphylococcus aureus

(MRSA)strainsinclinicalsamples

The pooled frequency of MRSA infections among con

ﬁ

rmed

S.

aureus

isolates was 43.0% [95% con

ﬁ

dence interval (CI) 36.3

–

50.0%]

(Table

2).

The MRSA infection rates in blood, wound and respiratory tract specimens are shown in

Table3.

The heterogene- ity test indicated that there were heterogeneities between studies (I

²

= 95.441;

P<

0.001).

Fig.2

shows the forest plot of meta-analysis of MRSA prevalence. As shown in

Table2

and

Fig.3,

no evidence of publication bias was observed (P

>

0.05 for Egger

’

s weighted regression analysis).

Table 4

shows the strati

ﬁ

ed analyses according to the geographic areas of included studies. The distribution of MRSA infections in different parts of Iran is shown in

Fig.4.

4.Discussion

This systematic review reports the frequency of MRSA infections in Iran. The analyses showed that the frequency of MRSA infections was 43.0% (95% CI 36.3

–

50.0%) among con

ﬁ

rmed

S.aureus

isolates in different parts of Iran (Table

2).

The frequency of MRSA in the current study was comparable with the results of studies from neighbouring countries

[13].

The epidemiology of MRSA is gradually changing since its emergence was

ﬁ

rst reported.

Initially there were occasional reports, but now it has become an

established hospital-acquired pathogen

[14].

Such a high preva-

lence of MRSA (43.0%) in healthcare settings in Iran may be due to

several factors. Along with indiscriminate use of antibiotics, the

insuf

ﬁ

cient implementation of prophylactic hygiene measures,

inadequate staff training and lack of hospital infection control

Fig.1.Flowchartofstudyselectionforinclusioninthesystematicreview.

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programmes are particular reasons for the signi

ﬁ

cant increase in MRSA prevalence. Insuf

ﬁ

cient MRSA management thus leads to the continued spread of MRSA in hospitals in Iran. Moreover, the association of multidrug resistance with MRSA has added to the problem

[15].

b -Lactam antibiotics such as penicillin and cefalexin

were not found to be effective against MRSA

[16].

Vancomycin appears to be the only antimicrobial agent for treating multidrug- resistant MRSA infections. Urgently needed measures in this case are the introduction of standard hygiene and adequate outbreak management as well as control of antibiotic use

[14,17].

MRSA may

Table2

Meta-analysisoftheprevalenceofmethicillin-resistantStaphylococcusaureus(MRSA)infectionsinIran.

Subgroup No.ofstudies PrevalenceofMRSA(%)(95%CI)^a n/N^b Heterogeneitytest Egger’stest

I²(%) P-value t P-value

Overalleffects 31 43.0(36.3–50.0) 2361/5689 95.441 <0.001 0.05 0.95

Researchbetween2000–2004 3 60.0(29.0–85.4) 179/321 96.167 <0.001 4.62 0.13

CI,conﬁdenceinterval.

aWeightedmeanofprevalence.

b n,numberofevents(MRSAisolates);N,totalnumberofS.aureus.

Table1

Characteristicsofstudiesincludedinthemeta-analysis.

Study Studyperiod Province No.ofcases No.ofS.aureus No.ofMRSA Diagnosticmethod(s) Sourceofsamples

Alborzietal.[19] 1999–2000 Fars 106 106 40 BMD Burn

Vahdanietal.,[20] 2004 Tehran 100 100 90 BMD Skin,wounds,sputum

Japonietal.[21] 2003 Fars 115 115 49 AD/PCR Blood,urine

Saderietal.[22] 2007–2008 Tehran 222 222 122 DD/PCR Respiratorytract

Yadegaretal.[23] 2006–2007 Tehran 100 100 35 PCR Blood,sputum,wound

Shariﬁetal.[24] 2008 Qazvin 200 100 1 Oxacillinscreeningplate Nasal

Askarianetal.[25] 2006 Fars 600 186 32 Etest/PCR Nasal

Ekramietal.[26] 2006–2007 Khuzestan 185 185 112 Etest/PCR Wound

Rahimi-Alangetal.[27] 2009 Golestan 333 80 10 BMD Nasal

Japonietal.[28] 2006–2007 Fars 356 356 156 Etest Blood,sputum

HosainZadeganandMenati[29] 2010 Lorestan 300 64 16 AD Nasal

Davoodietal.[30] 2009–2010 Tehran 130 130 79 DD/PCR Wound,blood

Khosravietal.[31] 2010 Khuzestan 203 95 83 PCR Burn

Seiﬁetal.[32] 2011–2012 Khorasan-e- Razavi

211 211 88 Oxacillinscreeningplate Blood,wound

Havaeietal.[33] 2011 Khorasan-eRazavi 171 171 115 AD/PCR Blood,urine

Rahimietal.[34] 2007–2011 Tehran 726 726 216 Etest/PCR Wound

Japoni-Nejadetal.[35] 2011–2012 Markazi 700 154 7 DD/PCR/MLST Nasal

Bahmanietal.[36] 2012–2013 Kurdistan 138 44 35 DD/PCR Blood

Abbasi-Montazerietal.[37] 2007–2008 Khuzestan 116 96 77 DD/PCR Burns

Farhadian[38] 2006–2008 Tehran 250 250 108 Etest/PCR Wound,urine

Saffaretal.[39] 2011 Tehran 250 250 92 DD/PCR –

Moghadametal.[40] 2012–2013 Tehran 135 65 40 AD/PCR Wound

SadeghiandMansouri[41] 2011–2012 Kerman 162 162 92 Etest/PCR Wound,urine

Eramietal.[42] 2012–2013 Isfahan 350 92 33 Etest Nasal

Moghadametal.[43] 2013–2014 Tehran 135 67 45 DD/PCR Pus/wound

Nikfaretal.[44] 2010–2011 Khuzestan 846 240 11 DD/PCR Nasal

Arianpooretal.[45] 2011–2012 Khorasan-e- Razavi

238 238 107 DD Nasal

Taherikalanietal.[46] 2010–2011 Ilam 500 372 200 DD/PCR Urine,blood

Hassanzadehetal.[47] 2011–2012 Fars 180 180 23 AD Nasal

Ebrahim-Saraieetal.[48] 2012–2013 Fars 345 345 146 DD/PCR Wound,urine

Davoudietal.[49] 2012–2014 Mazandaran 187 187 101 AD Respiratorytractinfection

MRSA,methicillin-resistantStaphylococcusaureus;BMD,brothmicrodilution;AD,agardilution;DD,diskdiffusion;MLST,multilocussequencetyping.

Table3

Meta-analysisoftheprevalenceofmethicillin-resistantStaphylococcusaureus(MRSA)infectionsinblood,woundandrespiratorytractsamples.

Subgroup No.ofstudies PrevalenceofMRSA(%)(95%CI)^a n/N^b Heterogeneitytest Egger’stest

Overalleffects 23 19.6(14.8–25.5) 655/3003 86.990 <0.001 2.96 0.00

Blood 6 21.3(18.4–24.5) 156/885 87.783 <0.001 3.89 0.17

Wound 9 26.8(18.5–37.4) 318/1141 84.882 <0.001 1.49 0.17

Respiratorytract 8 13.8(7.2–24.8) 181/977 88.536 <0.001 2.88 0.03

CI,conﬁdenceinterval.

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be nosocomial or community-acquired. From an epidemiological standpoint, MRSA can be de

ﬁ

ned as community-acquired if the positive culture was obtained outside the hospital setting or

<

2 days after hospital admission

[18]

and if the subject had no prior history of hospitalisation within the preceding 2 years. In the current analysis, all positive culture was obtained inside hospital settings. Based on the low incidence of community-acquired MRSA and given the fact that MRSA colonisation may persist for months

to years in the hospital, we suggest that MRSA isolated in this analysis were acquired from the hospital. However, owing to the lack of information, we do not know exactly whether the MRSA were from community or hospital sources.

Some limitations of this study should be discussed. First, as with any systematic review, the existence of potential publication bias should be considered. Second, heterogeneity was detected among the included studies. Although the random-effects model allows

Fig.2.Forestplotofthemeta-analysisontheprevalenceofmethicillin-resistantStaphylococcusaureus(MRSA)infections.CI,conﬁdenceinterval.

Fig.3.Funnelplotofthemeta-analysisontheprevalenceofmethicillin-resistantStaphylococcusaureus(MRSA)infections.

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for the presence of heterogeneity, there may still be some controversy about combining included studies. Third, it cannot fully represent the frequency of MRSA in Iran because the extent of MRSA has not yet been examined in many regions of the country.

In conclusion, the increase in the number of MRSA infections is a major public health problem in Iran and merits further attention by health authorities, physicians and microbiologists. Regular surveillance of hospital-associated infections, monitoring of

Table4

Meta-analysisoftheprevalenceofmethicillin-resistantStaphylococcusaureus(MRSA)infectionsindifferentpartsofIran.

Province No.ofstudies PrevalenceofMRSA(%)(95%CI)^a n/N^b Heterogeneitytest Egger’stest

Overalleffects 31 43.0(36.3–50.0) 2361/5689 95.441 <0.001 0.05 0.95

Fars 6 31.2(21.6–42.8) 446/1288 93.75 <0.001 2.1 0.09

Tehran 9 53.7(42.1–64.8) 827/1910 95.126 <0.001 4.0 0.005

Khuzestan 4 54.6(17.1–87.6) 283/616 98.167 <0.001 0.2 0.8

Ilam,Kurdistan,Qazvin,Lorestan(westofIran) 3 52.8(27.9–76.4) 251/480 93.57 <0.001 0.04 0.97

Khorasan-e-Razavi 3 51.4(36.6–65.9) 310/620 92.763 <0.001 2.0 0.28

Mazandaran,Isfahan,Markazi,GolestanKerman 6 20.5(9.0–40.0) 244/775 95.722 <0.001 4.4 0.01 CI,conﬁdenceinterval.

Fig.4.Distributionofmethicillin-resistantStaphylococcusaureus(MRSA)infectionsindifferentpartsofIran.

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antibiotic sensitivity patterns, and formulation of de

ﬁ

nite antibiotic policy may facilitate more accurate action for the prevention and control of MRSA infections in Iran. In particular, the introduction of MRSA screening based on rapid and reliable diagnosis during inpatient admission of patients is indispensable.

Funding

None.

Competinginterests

None declared.

Ethicalapproval

Not required.

AppendixA.Supplementarydata

Supplementary data associated with this article can be found, in the online version, at

http://dx.doi.org/10.1016/j.jgar.2017.09.006.

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