Analisa Jurnal

MIKROBIOLOGI dan PARASITOLOGI

Disusun untuk memenuhi tugas kuliah Patologi dalam Keperawatan

Dosen pembimbing Ns. Muhamad Zulfatul Ala, M.Kep

Oleh:

Kelompok 1

1. H.A.P. Desthalia C. NIM 162310101116

2. Mila Sari Lestia Devi NIM 162310101117
3. Siti Halimatus S NIM 162310101118
4. Maraytus Sissetyaningrul P. NIM 162310101119
5. Melasari Ika Safitri NIM 162310101121

PROGRAM STUDI ILMU KEPERAWATAN

UNIVERSITAS JEMBER

2017
 Konsep
Nama Analisis dengan mikrobiologi Implikasi
Penulis Judul Jurnal dan Tujuan Hasil dan Jurnal yang keperawa
Metodologi
Jurnal Jurnal Edisi dan Penelitian pembahasan Pembanding/Pen terdapat tan
Tahun guat pada jurnal

Elham Nasal American Menentukan Tempat 1. Dari penelitian ini 1. Pada penelitian 1. Staphyloco Tingginya
Jannati, colonizat Journal of prevalensi penelitian : didapatkan hasil jurnal penguat, ccus. S. prevalensi
Mohsen ion of Infection nasal Ardabil bahwasannya Perawat uji kepekaan aureus strain
Arzanlou mecA- Control 41 kolonisasi dan University of dan petugas lainnya antibiotik (MRSA) MRSA
, positive, (2013) resistensi Medical pada salah satu rumah mengungkapkan merupakan dapat
Shahram oxacilin- 1122-4 antibiotik Science sakit di Iran berisiko bahwa sebagian penyebab menjadi
Habibza susceptib profil MRSA tinggi terhadap besar S. aureus utama risiko
deh, le, pada staff Jumlah sampel penularan MRSA. isolat tetap infeksi penting di
Saeed methicili perawat di : 200 perawat Dalam penelitian ini, sensitif terhadap terkait rumah
Moham n- rumah sakit dari 173 subyek, 41 mayoritas perawatan sakit yang
madi, resistant pendidikan Kuesioner (23,7%) subyek adalah antibiotik, tetapi kesehatan. membutuh
Parisa Staphylo Ardabil yang pembawa S aureus, ada tingkat kan
Ahadi, coccus University of digunakan : dimana 8 (4,6%) adalah tinggi resistensi 2. Staphyloco perencana
Behnam aureus Medical Cross- pembawa MRSA. Dalam terhadap ccus. S. an untuk
Moham isolates Science Sectional meta-analisis 127 penisilin aureus pengendali
madi- among investigasi di seluruh (MRSA) an infeksi
Ghalehbi nursing dunia, rata-rata pembawa 2. Berdasarkan resisten yang
n, Hadi staff in MRSA di antara petugas hasil penelitian terhadap serius dan
Peeri an kesehatan adalah 4,6% pada jurnal antibiotik pengawasa
DDogah Iranian (kisaran, 1,6% -13,1%). penguat penisilin n untuk S.
eh, teaching Temuan penting dalam vankomisin, aureus
Solmaz hospital penelitian ini adalah rifampin, dalam
dibah, pembawa MRSA quinupristin dan pengatura
Ebrahim terutama para perawat linezolid adalah n
Kazemi yang bekerja di bangsal antibiotik yang masyaraka
memiliki infeksi paling efektif t. Dalam
nosokomial relatif tinggi. untuk kasus ini
Strain MRSA yang pengobatan S. perawat
diisolasi dalam aureus dan berperan
 penelitian ini infeksi MRSA. penting
menunjukkan 3 pola dalam
nilai MIC (minimum pengendali
inhibitori konsentration ) an
untuk oxacillin. Lima resistensi
isolat MRSA adalah gen bakteri
mecA positif dan terhadap
memiliki nilai MIC 512 antibiotik
mg / mL. Satu isolat dengan
MRSA adalah gen mecA cara cara
positif dan memiliki nilai mengontro
MIC 4 mg / mL untuk l
oxacillin. penggunaa
n
2. Strain ini rentan antibiotik
terhadap semua tersebut.
antibiotik diuji kecuali
penisilin dan amoxyclav

3. distribusi operator
MRSA di bangsal yang
menimbulkan risiko
tinggi untuk infeksi
nosokomial untuk pasien
rawat inap menekankan
menerapkan strategi
pengendalian infeksi
yang tepat untuk
mencegah penyebaran
organisme. Terjadinya
strain OS-MRSA
menunjukkan kebutuhan
untuk menggunakan
pendekatan yang tepat
untuk kedua nosis dan
pengobatan infeksi
MRSA
 DAFTAR PUSTAKA

Pourakbari B, Khodabandeh M, Mahmoudi S, Sabouni F, Aziz-Ahari A, Bahador

A, Valian S. K, Sadeghi R. H, Mamishi S. 2017. Molecular epidemiology
of Staphylococcus aureus nasal colonization among patients and their
parents /guardian in an Iranian referral hospital, Microbial Pathogenesis
107 (2017) 75e80. Dapat diakses pada
(http://www.sciencedirect.com/science/article/pii/S0882401016308737).
(Diakses pada tanggal 29 April 2017)
 American Journal of Infection Control 41 (2013) 1122-4

Contents lists available at ScienceDirect

American Journal of Infection Control American Journal of

Infection Control

journal homepage: www.ajicjournal.org

Brief report

Nasal colonization of mecA-positive, oxacillin-susceptible, methicillin-resistant

Staphylococcus aureus isolates among nursing staff in an Iranian teaching hospital
Elham Jannati MSc a, Mohsen Arzanlou PhD b, *, Shahram Habibzadeh MD, MPH c, Saeed Mohammadi
BSc d, Parisa Ahadi MD e, Behnam Mohammadi-Ghalehbin PhD b, Hadi Peeri Dogaheh PhD b,
Solmaz Dibah MSc b, Ebrahim Kazemi MSc f
a
Young Researchers Club, Ardabil Branch, Islamic Azad University, Ardabil, Iran
b
Department of Microbiology and Parasitology, School of Medicine, Ardabil University of Medical Sciences, Ardabil, Iran
c
Department of Infectious Diseases, School of Medicine, Ardabil University of Medical Sciences, Ardabil, Iran
d
Ardabil Health Network, Ardabil University of Medical Sciences, Ardabil, Iran
e
Students of Medicine, School of Medicine, Ardabil University of Medical Sciences, Ardabil, Iran
f
Khoy Health Network, Urmia University of Medical Sciences, Urmia, Iran

Key Words: Methicillin-resistant Staphylococcus aureus (MRSA) is a major cause of health care-associated infections.
S aureaus In this study, a total of 173 nurses was screened for S aureus nasal colonization, of which 8 (4.6%) were
Antibiotic resistance MRSA carriers. Among the MRSA isolates, 6 were mecA positive and oxacillin resistant, and 2 were mecA-
Colonization surveillance
positive, oxacillin-susceptible (OS-MRSA) strains. Reports of the OS-MRSA strains are increasing
Health care workers
worldwide. To the best of our knowledge, this study is the rst report on the occurrence of OS-MRSA
Hospital infection control
strains in Iran.
Copyright 2013 by the Association for Professionals in Infection Control and Epidemiology, Inc.
Published by Elsevier Inc. All rights reserved.

Methicillin-resistant Staphylococcus aureus (MRSA) is endemic
in many hospitals worldwide.1 Nurses have a high frequency of
close contact with patients; hence, the risk for the acquisition and
carry of MRSA for this community is higher than for the other
health care workers (HCWs).2 Carriage of MRSA by HCWs is
important from 2 aspects: (1) Sometimes the source of staphylo-
coccal infections is endogenous, and carriage of MRSA may
predispose the carrier to subsequent staphylococcal infections.1 (2)
As carriers, HCWs can serve as reservoir for bacterium and transmit
it to their households and hospitalized patients.1 In this study, we
aimed to determine the prevalence of nasal colonization and
antibiotic resistance prole of MRSA strains in nursing staff in
a teaching hospital afliated to Ardabil University of Medical
Sciences in Iran.
METHODS
This cross-sectional study was performed in 2010 among
nursing staff in a major university-afliated teaching hospital. The
subjects were screened for nasal carriage of Staphylococcus aureus.
Antibiotic sensitivity of the isolates was tested by disk diffusion
method, except for vancomycin, which was determined using agar
dilution method. The minimum inhibitory concentration (MIC) of
pristinamycin for resistant strains (based on disk diffusion method)
was further determined using E-test strips. All tests were carried
out and interpreted according to Clinical and Laboratory Standards
Institute guidelines.3 Methicillin resistance was evaluated using 2
methods: polymerase chain reaction for the mecA gene (positive
indicated MRSA) and cefoxitin disk diffusion test (
21 mm indi-
cated MRSA). Additionally, oxacillin MICs (4 mg/mL indicated
MRSA) were determined using agar dilution method.3 In the liter-
ature, mecA-positive and oxacillin-susceptible Staphylococcus
aureus isolates are rare.
The protocol was approved by the local Ethical Committee of
Ardabil University of Medical Sciences, and informed consent was
obtained from each subjects. Data were analyzed using descriptive
statistics.

* Address correspondence to Mohsen Arzanlou, PhD, Department of Microbi-

RESULTS
ology and Parasitology, School of Medicine, Ardabil University of Medical Sciences,
Ardabil, Iran.
E-mail address: M.arzanlou@arums.ac.ir (M. Arzanlou). A total of 173 (86.5%) out of 200 nurses participated in the study.
Conicts of interest: None to report. The prevalence of nasal carriage of S aureus was 23.7% (41), of

0196-6553/$36.00 - Copyright 2013 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.ajic.2013.02.012
 E. Jannati et al. / American Journal of Infection Control 41 (2013) 1122-4 1123

Table 1
Prevalence of nasal carriage of MSSA and MRSA strains among nursing staff in relationship with hospital wards

Ward Carriage, n (%) With MSSA, n (%) With MRSA, n (%) Total
Operating room 15 (46.9) 12 (80) 3 (20) 32
Emergency 7 (33.3) 5 (71.4) 2 (28.6) 21
Internal 4 (19.0) 4 (100) - 21
Surgery 3 (37.5) 2 (66.7) 1 (33.3) 8
Hematology 1 (6.2) 1 (100) - 16
Angiography 1 (16.7) 1 (100) - 6
Cardiology 1 (6.3) 1 (100) - 16
Cardiac care unit 2 (22.3) 2 (100) - 9
Infectious 1 (7.1) 1 (100) - 14
Dialysis - - - 5
Intensive care unit 5 (26.3) 3 (60) 2 (40) 19
Clinic 1 (16.7) 1 (100) - 6
Total 41 (23.7) 33 (19.1) 8 (4.6) 173

Table 2
Antibiotic susceptibility proles of S aureus strains isolated from nasal mucosa of nursing staff by disk diffusion method

MSSA (N 33), n (%) MRSA (N 8), n (%)*

Antibiotic Susceptible Intermediate Resistant Susceptible Intermediate Resistant

Cefoxitin 33 (100) - - 2 (25) - 6 (75)
Vancomyciny 33 (100) - - 8 (100) - -
Penicillin 3 (9.1) - 30 (90.9) - - 8 (100)
Amoxyclav 15 (45.4) - 18 (54.5) - - 8 (100)
Chloramphenicol 31 (93.9) 1 (3.0) 1 (3.0) 8 (100) - -
Tetracycline 16 (48.5) - 17 (51.6) 2 (25) 6 (75)
Ciprooxacin 33 (100) - - 6 (75) 2 (25) -
Ceftriaxone 32 (97.0) 1 (3.0) - 2 (25) 1 (12.5) 5 (62.5)
Cefazolin 29 (87.9) 4 (12.1) - 2 (25) 1 (12.5) 5 (62.5)
Clindamycin 33 (100) - - 2 (25) - 6 (75)
Imipenem 33 (100) - - 4 (50) - 4 (50)
Co-trimoxazole 33 (100) - - 6 (75) - 2 (25)
Rifampicin 33 (100) - - 4 (50) - 4 (50)
Pristinamycin 30 (91.0) - 3 (9.1) 2 (25) - 6 (75)
Linezolid 33 (100) - - 8 (100) - -
Mupirocin 33 (100) - - 8 (100) - -

* The oxacillin MIC to 1 out of 8 MRSA strains was 4 mg/mL. This strain was susceptible to all tested antibiotics except penicillin and amoxyclav. The oxacillin MIC to 2 of 8 MRSA
strains was 1 mg/mL. These strains were positive for mecA gene; both strains were susceptible to all tested antibiotics except penicillin and amoxyclav; and additionally 1 strain
was resistant to clindamycin.
y
Vancomycin susceptibility prole was determined using agar dilution method.

which 19.1% (33) and 4.6% (8) were methicillin-sensitive S aureus
(MSSA) and MRSA, respectively.
Polymerase chain reaction testing of 41 isolates identied
8 (19.5%) positive for the mecA gene, whereas the cefoxitin disk
diffusion and oxacillin MIC tests identied 6 (14.6%). The MICs for
oxacillin was between 1 to 512 mg/mL and
0.25 to 0.5 mg/mL for
MRSA and MSSA strains, respectively. The MICs for vancomycin
against both MRSA and MSSA strains were
0.25 to 1 mg/mL.
Table 1 shows the distribution of MSSA and MRSA carriage
among various wards. MRSA carriers have been working in oper-
ating room, surgical ward, intensive care unit, and the emergency
department. Table 2 represents the antibiotic resistance pattern of
S aureus isolates (MRSA and MSSA). The vancomycin, linezolid,
mupirocin, and chloramphenicol showed the lowest resistance rate
(0%) against MRSA isolates. Three (9.1%) of 33 MSSA and 6 (75%) of
8 MRSA isolates were resistant against pristinamycin. The MICs for
pristinamycin against resistant MRSA strains were >240 mg/mL
and for the resistant MSSA strains were >240 mg/mL for 1 of 3 and
30 mg/mL for 2 of 3 strains. The MICs of pristinamycin for susceptible
MRSA strains and representative MSSA strains were 0.01 mg/mL.
DISCUSSION
Nurses are at higher risk to the acquisition of MRSA among other
HCWs.2 In this study, out of 173, 41 (23.7%) of subjects were S aureus
carriers, of which 8 (4.6%) were MRSA carriers. In a meta-analysis of
127 investigations around the world, the average MRSA carriage
rate among HCWs was 4.6% (range, 1.6%-13.1%).1 The estimated
prevalence in our study locates in reported ranges.
In this study, the number of MRSA-positive subjects was too low
to attribute to work place. However, an important nding of this
study is that the MRSA carriers were mainly those who worked in
wards in which the risk for nosocomial infection is relatively high.
Similar ndings have been reported in other studies.2,4
MRSA strains isolated in the present study exhibited 3 patterns
of MIC values for oxacillin. Five MRSA isolates were mecA-gene
positive and had MIC values of  512 mg/mL. One MRSA isolate was
mecA-gene positive and had the MIC value of 4 mg/mL for oxacillin.
This strain was only resistant to b-lactam antibiotics.
Two isolates were mecA-gene-positive, oxacillin-susceptible (OS-
MRSA) (MIC: 1 mg/mL) S aureus strains. It has been reported in
a single study that OS-MRSA may be isolated twice as often as MRSA
from HCWs.5 Transmission of OS-MRSA is of concern because the
pathogen is not recognized as oxacillin resistant but may develop
phenotypic resistance during a course of antibiotic therapy.5,6
The high resistance rate for most commonly used antibiotics
was observed among MRSA isolates. None of the isolates tested
in our study were resistant to vancomycin, mupirocin, and line-
zolid. However, other studies have reported the vancomycin-
intermediate S aureus strains among HCWs.7
1124 E. Jannati et al. / American Journal of Infection Control 41 (2013) 1122-4
Unexpectedly, in this study, resistance to pristinamycin was
observed in both MSSA and MRSA isolates. This antibiotic is not
used for patient management in Iran. Emergence of pristinamycin-
resistant S aureus strains in the absence of antibiotic selective
pressure is surprising.
In conclusion, the distribution of MRSA carriers in wards that
pose high risks for nosocomial infection to hospitalized patients
emphasizes applying appropriate infection control strategies to
prevent the spread of organism. Occurrence of the OS-MRSA strains
shows the need for using appropriate approaches for both diag-
nosis and treatment of MRSA infections.
References
1. Albrich WC, Harbarth S. Healthcare workers: source, vector, or victim of MRSA?
Lancet Infect Dis 2008;8:289-301.
2. 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:e241-7.
3. Clinical and Laboratory Standards Institute. Performance standards for antimi-
crobial susceptibility testing. Twenty-rst informational supplement, M100e
MS21. Wayne [PA]: Clinical and Laboratory Standards Institute; 2011.
4. Cesur S, Cokca F. Nasal carriage of methicillin-resistant Staphylococcus aureus
among hospital staff and outpatients. Infect Control Hosp Epidemiol 2004;25:
169-71.
5. Kampf G, Adena S, Ruden H, Weist K. Inducibility and potential role of mecA-
gene positive oxacillin-susceptible Staphylococcus aureus from colonized
healthcare workers as a source for nosocomial infections. J Hosp Infect 2003;54:
124-9.
6. Hososaka Y, Hanaki H, Endo H, Suzuki Y, Nagasawa Z, Otsuka Y, et al. Charac-
terization of oxacillin-susceptible mecA-positive Staphylococcus aureus: a new
type of MRSA. J Infect Chemother 2007;13:79-86.
7. Banerjee T, Anupurba S. Colonization with vancomycin-intermediate Staphylo-
coccus aureus strains containing the vanA resistance gene in a tertiary-care
center in north India. J Clin Microbiol 2012;50:1730-2.
 Microbial Pathogenesis 107 (2017) 75e80

Contents lists available at ScienceDirect

Microbial Pathogenesis
journal homepage: www.elsevier.com/locate/micpath

Molecular epidemiology of Staphylococcus aureus nasal colonization

among patients and their parents /guardian in an Iranian referral
hospital
Babak Pourakbari a, Mahmoud Khodabandeh b, Shima Mahmoudi a, Farah Sabouni b,
Alireza Aziz-Ahari c, Abbas Bahador d, Sepideh Keshavarz Valian e,
Reihaneh Hosseinpour Sadeghi a, Setareh Mamishi a, b, *
a
Pediatric Infectious Disease Research Center, Tehran University of Medical Sciences, Tehran, Iran
b
Department of Infectious Diseases, Pediatrics Center of Excellence, Children's Medical Center, Tehran University of Medical Sciences, Tehran, Iran
c
Radiology Department, Rasool-e-Akram Hospital, Iran University of Medical Sciences, Tehran, Iran
d
Department of Microbiology, Tehran University of Medical Sciences, Tehran, Iran
e
School of Medicine, Tehran University of Medical Sciences, Tehran, Iran

a r t i c l e i n f o a b s t r a c t

Article history: Introduction: Carriage of Staphylococcus aureus in the nose appears to play a key role in the epidemiology
Received 13 December 2016 and pathogenesis of infection. It is important to investigate the genetic relatedness of S. aureus and MRSA
Received in revised form clones in different geographic regions. The aim of this study was to assess the nasal carriage rate of
8 March 2017
S. aureus, including MRSA strains in both hospitalized children and general adult population (parents/
Accepted 21 March 2017
Available online 22 March 2017
guardian). In addition, antibiotic susceptibility pattern and molecular diversity of S. aureus in both
population was evaluated in an Iranian referral pediatrics Hospital.
Material and methods: All samples were obtained through nasal screening of patients and general adult
Keywords:
Staphylococcus aureus
population at admission and discharge day. The prevalence, resistance, and molecular diversity of all
Genotyping S. aureus isolates were examined.
Antibiotic susceptibility patterns Results: In the current study, nasal carriage of S. aureus and Staphylococcus non aureus was identied in
384 (26%) and 1004 (68%) of the study population. The prevalence of MRSA nasal carriage in children and
adults was 6.6% (29 out of 438) and 2.8% (29 out of 1046), respectively.
Among S. aureus strains isolated obtained from patients and general adult population at admission day,
high sensitivity to most of the antibiotics such as vancomycin (100%), rifampin (95%), linezolid (94%),
quinupristin/dalfopristin (94%), minocycline (94%), chloramphenicol (89%), gentamycin (87%), amikacin
(87%), clindamycin (86%) and moxioxacin (83%) was seen. The most resistance antibiotics were peni-
cillin (96e98%) and methicillin (44e47%). The susceptibility patterns of nasal S. aureus strains isolated at
discharge day was not statistically different from S. aureus isolates obtained at admission day. Admission
S. aureus isolated strains of 77 patients (64%) were similar to the isolated S. aureus strains of discharge,
while S. aureus isolated strains of 43 patients (36%) was not similar to the strain of discharge (had
similarity of less than 70%).
Conclusion: High prevalence of nasal carriage of S. aureus and MRSA indicates the urgent need to
improve strategies for management of S. aureus infections.
Our ndings are useful for understanding of S. aureus nasal colonization dynamics within the patients
and general population. Surveillance for S. aureus in community settings can provide data on circulating
strains and might help developing control measures for reducing of infection spread in hospitals.
2017 Published by Elsevier Ltd.

1. Introduction
* Corresponding author. Department of Pediatric Infectious Disease Children
Medical Center Hospital School of Medicine Tehran University of Medical Sciences
Among hospital-acquired infection in developing countries,
No.62, Gharib St., Keshavarz Blvd., Tehran, Iran.
E-mail address: smamishi@sina.tums.ac.ir (S. Mamishi). Staphylococcus aureus is the second most recognized causes after

http://dx.doi.org/10.1016/j.micpath.2017.03.023
0882-4010/ 2017 Published by Elsevier Ltd.
76 B. Pourakbari et al. / Microbial Pathogenesis 107 (2017) 75e80
the Enterobacteriaceae [1]. S. aureus is one of the most common
public health problem that increases the overall burden of infec-
tious disease in each setting [2]. Carriage of S. aureus in the nose
appears to play a key role in the epidemiology and pathogenesis of
infection [3]. Nosocomial infections caused by methicillin-resistant
S. aureus (MRSA) pose a serious problem in many countries; how-
ever, the exact burden of disease caused by MRSA remains largely
unknown [4].
One of the cardinal features of the rapid emergence of MRSA in
many parts of the world is the dissemination of specic clones
which has contributed to the accelerated increases in the incidence
of MRSA. Therefore, it is important to investigate the genotypic
characteristics and evolutionary pathway of MRSA clones as well as
the genetic relatedness of the strains isolated in different
geographic regions [5].
Early identication of patients colonized with MRSA and sub-
sequent prevention of its spread through infection control mea-
sures are believed to be essential [4]. It has been reported that
patients colonized with MRSA on admission were 15 times more
likely to develop MRSA Infection [6,7].
Identication of the epidemiology and infection patterns in local
hospital settings remains critical as it directly affects clinical
management plans and decision making about implementation of a
national universal screening program for MRSA. The aim of this
study was to evaluate the prevalence, resistance, and molecular
diversity of nasal S. aureus colonization/infection patients and
general adult population (parents/guardian) in an Iranian referral
pediatrics Hospital.
2. Material and methods
2.1. Sample collection and culture
This study was performed on patients and their parents/
guardian (general adult population) in an Iranian referral pediatric
Hospital. In our study parents/guardians represented as general
adults population; therefore, we asked them to participate in our
study if they had informed consent. In some cases, only the parents/
guardians were participated and their child was not taking part. All
patients and their parents/guardian were required to give written
informed consent to participate.
Sampling on admission and discharge consisted of swabbing of
anterior nares. Admission swabbing took place within the rst
hours after admission. Patients with missing swabs or swabs taken
outside the time criteria were excluded from analysis.
Discharge was dened as the patient leaving the hospital to
another hospital or care institution or to home. Discharge screening
took place up to 24 h before discharge.
The demographic information of all patients was recorded in
questioner's forms.
Nasal swabs were obtained by trained examiners from both
anterior nares using premoistened swab. Swabs were inserted into
the nasal vestibule, and the swab was rotated four times. Trypticase
soy broth (Merck, Germany) was used as the transport medium.
Nose swabs were transported at 4
C in a transportable compressor
cooler and processed immediately after sampling. Samples were
sent to the laboratory and were inoculated on mannitol salt agar
plates and incubated at 35
C for 48 h. For microbiological analysis,
one suspicious colony was chosen from the selective agar. S. aureus
was identied by colony morphology on mannitol salt agar plates,
Gram stain, catalase test and coagulase test.
2.2. Antimicrobial susceptibility testing
A standardized Kirby-Bauer disc-diffusion method was
performed on Mueller-Hinton agar according to the Clinical and
Laboratory Standards Institute (CLSI) criteria [8].
Isolates were tested for susceptibility to the following antibi-
otics: minocycline, trimethoprim-sulfamethoxazole, quinupristin/
dalfopristin, vancomycin, clindamycin, chloramphenicol, tetracy-
cline, amikacin, ciprooxacin, gentamycin, moxioxacin, linezolid,
rifampin, penicillin, cefoxitin, chloxacillin, azithromycin and cefa-
zolin. The diameters of incubation halos were interpreted after 24 h
of incubation at 37
C.
2.3. Molecular testing
DNA was extracted from S. aureus isolates using lysostaphin
digestion, as described previously [9]. Conrmation of MRSA was
achieved by polymerase chain reaction (PCR) targeting the mecA
gene [10].
2.4. ERIC-PCR reaction
S. aureus isolates were genotyped by enterobacterial repetitive
intergenic consensus PCR (ERIC-PCR), as described previously [10].
The primers used were ERIC-1R (50 - ATGTAAGCTCCTGGGGATTCAC-
30 ) and ERIC-2 (50 - AAGTAAGTGACTGGGGTGAGCG-30 ).
2.5. Data collection and analysis
All data were analyzed by SPSS version 13.5 (SPSS Inc., Chicago,
IL). Continuous data were presented as mean standard deviation
and/or median (25% quantile, 75% quantile). Categorical data were
presented as percentages. Student's t-test was used for statistical
analysis to compare the means between the two groups. A P value
of 0.05 was considered statistically signicant. Comparison of
ERIC-PCR banding patterns was performed using Gelcompar II,
version 6.5 (Applied Maths, Sint-Matens- Latem, Belgium). Isolates
producing ngerprints showing more than 80% relatedness (Dice
coefcient/unweighted pair-group method with arithmetic mean
[UPGMA]) were allocated to the one ERIC-PCR type.
3. Results
3.1. Sample sources and patient and their parents/guardians
demographics
A total of 1484 swabs were taken, 438 samples from children
and 1046 samples from adults. In the current study, overall carriage
rate nasal carriage of S. aureus and Staphylococcus non aureus from
both pediatric children and adults was 384 (26%) and 1004 (68%),
respectively. Of these, 146 children (33%) and 238 adults (23%) were
found to carry S. aureus (Fig. 1). The mean age of the children and
adults was 3.8 3.6 and 29.7 6.2 years, respectively.
Among 146 patients, nearly half of the patients were less than 1
year old (n 74, 51%), while 14 cases were between 1 and 2 years
(10%), 14 cases between 2 and 3 years and 44 patients were more
than 3 years old (30%). The mean interval day of admission to
discharge patients was 6.3 4.9.
The mean interval time of hospital stay among the patients that
had different admit/discharge strains was 6.8 6.1 day that was not
signicantly different from patients with similar admit/discharge
strains (5.4 1.5 day) (p value > 0.05).
The hospital location was not signicantly different between
patients with different or similar admit/discharge strains (64% and
60% of with patients with different admit/discharge strains had
been hospitalized in infectious ward and the rest of them were in
gastroenterology ward, while 60% of patients with similar admit/
discharge strains were hospitalized in infectious ward).
 B. Pourakbari et al. / Microbial Pathogenesis 107 (2017) 75e80 77

Fig. 1. Flowchart of the result of the total swabs taken and the numbers of S. aureus and non S. aureus isolated in patient and parent/guardian.

Table 1
Antibiotic susceptibility proles of S. aureus strains isolated from patients and their parents/guardian on admission and discharge.

Antibiotic Isolates of admission Isolates of discharge

S I R S I R

N (%) N (%) N (%) N (%) N (%) N (%)

Minocycline 116 (94) 2 (2) 5 (4) 115 (93) 2 (2) 6 (5)

Trimethoprim-sulfamethoxazole 87 (70) 0 (0) 36 (30) 86 (70) 0 (0) 37 (30)
Quinupristin/dalfopristin 116 (94) 3 (2) 4 (3) 117 (95) 4 (3) 2 (2)
Vancomycin 123 (100) 0 (0) 0 (0) 123 (100) 0 (0) 0 (0)
Clindamycin 106 (86) 5 (4) 15 (10) 103 (84) 9 (7) 11 (9)
Chloramphenicol 110 (89) 6 (5) 7 (6) 105 (85) 13 (10) 5 (4)
Tetracycline 80 (65) 1 (1) 42 (34) 78 (63) 0 (0) 45 (37)
Amikacin 107 (87) 0 (0) 16 (13) 107 (87) 2 (2) 14 (11)
Ciprooxacin 90 (73) 12 (10) 21 (17) 89 (72) 16 (13) 18 (15)
Gentamycin 107 (87) 2 (2) 14 (11) 110 (89) 0 (0) 13 (11)
Moxioxacin 102 (83) 3 (2) 18 (15) 101 (82) 5 (4) 17 (14)
Linezolid 116 (94) 0 (0) 7 (6) 115 (93) 0 (0) 8 (7)
Rifampin 117 (95) 3 (2) 3 (2) 116 (94) 2 (2) 5 (4)
Penicillin 5 (4) 0 (0) 118 (96) 2 (2) 0 (0) 121 (98)
Methicillin 69 (56) 0 (0) 54 (44) 65 (53) 0 (0) 58 (47)
Chloxacillin 76 (72) 1 (1) 28 (27) 75 (80) 0 (0) 18 (20)
Azithromycin 68 (61) 1 (1) 42 (38) 71 (69) 0 (0) 32 (31)
Cefazolin 92 (75) 5 (4) 26 (21) 91 (74) 8 (7) 24 (19)

S Sensitive I Intermediate R Resistant.

3.2. Antibiotic resistance/susceptibility patterns
The prevalence of MRSA nasal carriage in children and adults
was 6.6% (29 out of 438) and 2.8% (29 out of 1046), respectively.
Table 1 represents the resistance pattern of S. aureus isolates to
the tested antibiotics. Among S. aureus strains isolated obtained
from patients and general adult population at admission day, high
sensitivity to most of the antibiotics such as vancomycin (100%),
rifampin (95%), linezolid (94%), quinupristin/dalfopristin (94%),
minocycline (94%), chloramphenicol (89%), gentamycin (87%),
amikacin (87%), clindamycin (86%) and moxioxacin (83%) was
seen (Table 1). The most resistance antibiotics were penicillin
(96e98%) and methicillin (44e47%). The frequency of MRSA in
patients on admission and discharge was 46% and 52%, while this
78 B. Pourakbari et al. / Microbial Pathogenesis 107 (2017) 75e80

typing typing frequency in parents/guardians on admission and discharge was

42% and 43%, respectively. The susceptibility patterns of nasal

100
S. aureus strains isolated at discharge day was not statistically
55

60

65

70

75

80

85

90

95
191D
different from S. aureus isolates obtained at admission day (Table 1).
41D
378D Admission S. aureus isolated strains of 77 patients (64%) were
50D similar to the isolated S. aureus strains of discharge, while S. aureus
79D
isolated strains of 43 patients (36%) was not similar to the strain of
65D
168D discharge (had similarity of less than 70%) (Fig. 2). Among these 43
410D S. aureus isolates, 27 of them (63%) had more than 80% genetic
194D
135D
similarity to each other and were included in one cluster (Fig. 3).
365D Among these 27 S. aureus isolates the most effective antibiotics
419D were vancomycin (100%), rifampin (93%), quinupristin/dalfopristin
399D
417D
(93%), linezolid (92%), minocycline (89%) and gentamycin (89%).
182D The most resistant antibiotics among these isolates were penicillin
192D
(96%), methicillin (48%) and trimethoprim-sulfamethoxazole (44%)
384D
137D
(Table 2).
359D
69D
4. Discussion
288D
88D
58D To our knowledge, this is the rst study to provide insight into
38D
415D
the prevalence of nasal carriage, antimicrobial susceptibility, and
175D clonal structure of S. aureus in patients and the general population
127D (parents/guardians) in Iran. While extensive data on the burden of
391D
49D
disease due to S. aureus are available from many industrialized
25D countries, there are few data from developing countries [1]. It is
366D
important to know differences in carriage rates in different age
260D
421D
groups because carriage rates in one group may act as a reservoir
189D for infection of others [11]. In our study, the prevalence of coloni-
67D
zation with S. aureus in children and adults was 33% and 23%,
113D
296D respectively. Higher prevalence of MRSA nasal carriage was found
155D in children (patients) compare to the adults (general population)
80D
205D
(6.6% vs. 2.8%).
258D In our study, overall nasal carriage of S. aureus was identied in
68D 26% of the study population that was similar to the previous reports
149D
183D
in China and Taiwan [12,13]. In the United Kingdom, the prevalence
129D of colonization with S. aureus in the general population was 28%
385D [11]. The overall prevalence of S. aureus in general population in
364D
429D
Germany was 41% [14]. Community-acquired MRSA has emerged
117D globally as an important pathogen; however, its epidemiology in
19D
general population has been investigated to some extent [15].
17D
108D
Although the prevalence of colonization with S. aureus in both
61D developed and underdeveloped countries is usually consistent, the
160D
prevalence of MRSA nasal colonization in these countries varies
362D
435D [16,17].
18D Nasal carriers of S. aureus in Pakistan was 15% and 19.5% of
394D
35D
isolates were MRSA [16].
329D The prevalence of MRSA carriage in the community outpatient
94D populations in Dutch-German was low (<1%) [18]. Community
239D
397D
MRSA nasal carriage rate in Italy was <1% [19]. In the United States
116D study 9.2% MRSA carriage rate was found [20], while MRSA carriage
405D
was very low the general population in Hong Kong and Australia
355D
89D
(<1%) [17,21]. In the Gamblin et al. study, in a community popula-
420D tion in the UK, prevalence of MRSA was 1.9% [11].
166D
Antibiotic resistance pattern of S. aureus strains isolated from
7D
395D patients and general adult population on admission and discharge
171D showed no signicant difference.
235D
28D
In this study, antibiotic susceptibility tests revealed that most of
243D the S. aureus isolates remained sensitive to the majority of antibi-
251D otics, but there was a high rate of resistance against penicillin that
287D
229D
was similar to the report of Chen et al. in China [13].
3D High frequency of MRSA is disquieting and has important im-
247D
plications for future antibiotic prescribing guidelines in our coun-
361D.
try. The notable point in the present study was the high frequency
Fig. 2. Dendrogram of genotyping analysis derived from all S. aureus isolates. The scale of MRSA among both patients and general population that was
represents the genetic distance between isolates. more than other reports [22e27]. However, there are some reports
 B. Pourakbari et al. / Microbial Pathogenesis 107 (2017) 75e80 79

typing typing Table 2

Antibiotic susceptibility proles of 27 S. aureus isolated strains that were not similar
to the strain of discharge and had more than 80% similarity with each other.

100
60

80
Antibiotic Sensitive Resistant
296E N (%) N (%)

389E Minocycline 24 (89) 3 (11)

Trimethoprim-sulfamethoxazole 15 (56) 12 (44)
175E Quinupristin/dalfopristin 25 (93) 2 (7)
Vancomycin 27 (100) 0 (0)
235D Clindamycin 21 (78) 6 (22)
Chloramphenicol 21 (78) 6 (22)
7D Tetracycline 17 (63) 10 (37)
Amikacin 21 (78) 6 (22)
287D Ciprooxacin 20 (74) 7 (26)
Gentamycin 24 (89) 3 (11)
355E Moxioxacin 20 (74) 7 (26)
Linezolid 25 (92) 2 (8)
362E Rifampin 25 (92) 2 (8)
Penicillin 1 (4) 26 (96)
296D Methicillin 14 (52) 13 (48)
Chloxacillin 15 (75) 5 (25)
412E Azithromycin 15 (62) 9 (38)
Cefazolin 19 (70) 8 (30)
69D
56E
Since healthcare workers can be considered as one of the sources of
421E the dissemination of infection, active surveillance such as preva-
415D lence or incidence studies of infection, interpretation, feedback of
interventions for preventive action, and evaluation of their effect is
79D highly recommended [29]. The frequency of MRSA in both patients
and general population in this study was similar at admission and
127D
discharge and was similar to our previous MRSA report in S. aureus
410E isolates were obtained from patients in our hospital [8]. Methicillin
resistance against S. aureus in our country expresses alarm that the
352E indiscriminate use of antibiotics. The high prevalence of MRSA
25D strains can be an important risk in hospital which requires planning
for serious infection control and surveillance for S. aureus in com-
420E munity settings is highly recommended and it can provide data on
circulating strains.
413E
Based on the results of the present study vancomycin, rifampin,
205D quinupristin and linezolid are the most effective antibiotic for
treatment of S. aureus and MRSA infections.
121E The genotyping analysis of S. aureus isolates showed that 77
385D (64%) patients had similar strain at admission and discharge. This
nding reveals that 36% of cases acquire S. aureus strains in hospital
23E through their hospitalization. In Kao et al. study, molecular genetics
studies revealed that most MRSA isolates were healthcare-
233E
associated clones and that nasal and clinical isolates exhibited up
65D to 75% shared identity [30]. In our previous study in this center, the
ERIC-PCR proles did not reveal any genetic similarity among the
19D S. aureus strains from HCWs and the clinical samples [10]. In Chen
364D et al. report, 49% of S. aureus strains isolated from community
residents and healthcare workers at Southern China belonged to
180E one PFGE pattern [13].
This study has some limitations. First of all, the sampling was
185E
limited to the anterior nares. However, this site is considered as the
35D primary colonization site for S. aureus, other sites such as the throat,
groin, axilla, and perianal areas might be colonized. Only consid-
435D ering the nasal reservoir clearly underestimates the frequency of
S. aureus carriage/infection and clonal diversity. Moreover, since the
Fig. 3. Dendrogram of genotyping analysis derived from S. aureus isolates that were frequency of S. aureus carriage/infection is different among pop-
not similar to the strain of discharge. The scale represents the genetic distance be-
tween isolates.
ulations from geographic location, it raises questions about the
generalizability of these data in to other populations.
We screened all participants for S. aureus carriage using selec-
that reported higher frequency of MRSA [28]. tive methods, but we picked only one colony (unless phenotypic
In our previous report in this center, 24.7% of S. aureus strains colonial differences were observed) and subjected it to molecular
obtained from nasal swab of healthcare workers were MRSA [10]. analysis. This might have hampered redetection of persistently
80 B. Pourakbari et al. / Microbial Pathogenesis 107 (2017) 75e80
colonizing strains. Despite of thses limitations, this study can still
provide an epidemiologic feature of S. aureus carriage in the study
population and thus implement better infection control measures.
5. Conclusion
High prevalence of nasal carriage of S. aureus and MRSA in-
dicates the urgent need to improve strategies for management of
S. aureus infections.
In our study admission prevalence and acquisition of nasal
carriage of MRSA among patients and general adult population was
not different. It should be stated that the low level of S. aureus
carriage may have been missed with the direct culture method and
the accurate rate might actually be higher if the molecular detec-
tion of S. aureus had been used.
However, the ERIC-PCR used in this study have less discrimi-
natory power than the gold standard method (PFGE), our ndings
are useful for understanding of S. aureus nasal colonization dy-
namics within the patients and general population, and for
designing strategies to prevent S. aureus infection and its dissem-
ination. Further evaluation of nasal colonization of hospital
personnel and their genotyping in all parts of the hospital are
highly recommended.
Conict of interest
The authors declare no conict of interest.
Acknowledgments
This study was Dr. Mahmoud Khodabandeh postgraduate thesis.
This study was supported by a grant (grant number: 92-02-88-
22170) from Tehran University of Medical Sciences and Health
Services to Dr. Setareh Mamishi.
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