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Food handlers harbouring S. aureus on their noses or in hands are considered as the main source of food contamination. Antibiotic resistance in S. aureus is a serious issue. The study aimed to find out the prevalence of methicillin-resistant S. aureus among food handlers in restaurants of Duhok city. Nasal and hand swabs were taken from 200 food handlers. The collected swabs inoculated on mannitol salt agar and incubated at 37oC for 24-48h. Isolates identified as S. aureus underwent antimicrobial sensitivity testing to methicillin and vancomycin on Mueller Hinton agar. A total of 74 (37%) out of 200 cultures of food handlers were found to be colonized with S. aureus.53 (26.5%) isolated from the nose, compared with 8 (4.0%) from hands and 13 (6.5%) from both. 27% of the food handlers were found to be MRSA carrier, and none of the isolates were resistant to Vancomycin. The study revealed a high prevalence of MRSA among food handlers in Duhok city. Food handlers in public places are required to go through regular screening for both nasal and skin carriage of S. aureusfor the early detection and treatment of carriers. So as to protect the community from staphylococcal food poisoning and the spread of resistant S. aureus strains among the population.
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Vol. 6, No. 4, pp. 140145, Dec.-2018
p-ISSN: 2410-7549
e-ISSN: 2414-6943
140
PREVALENCE OF METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS
AMONG FOOD HANDLERS IN DUHOK CITY
Masood Abdulkareem Abdulrahman a,*, Arazoo Issa Taherb
a Community Health Department, Shekhan Technical College of Health, Duhok Polytechnic University -
Masood.Abdulkareem@dpu.edu.krd
b Bardarash Technical Institute, Duhok Polytechnic University- arezu.issa@gmail.com
Received: Sept. 2018 / Accepted: Nov., 2018 / Published: Dec., 2018 https://doi.org/10.25271/sjuoz.2018.6.4.540
ABSTRACT:
Food handlers harbouring S. aureus on their noses or in hands are considered as the main source of food contamination. Antibiotic
resistance in S. aureus is a serious issue. The study aimed to find out the prevalence of methicillin-resistant S. aureus among food
handlers in restaurants of Duhok city. Nasal and hand swabs were taken from 200 food handlers. The collected swabs inoculated
on mannitol salt agar and incubated at 37oC for 24-48h. Isolates identified as S. aureus underwent antimicrobial sensitivity testing
to methicillin and vancomycin on Mueller Hinton agar. A total of 74 (37%) out of 200 cultures of food handlers were found to be
colonized with S. aureus. 53 (26.5%) isolated from the nose, compared with 8 (4.0%) from hands and 13 (6.5%) from both. 27%
of the food handlers were found to be MRSA carrier, and none of the isolates were resistant to Vancomycin. The study revealed a
high prevalence of MRSA among food handlers in Duhok city. Food handlers in public places are required to go through regular
screening for both nasal and skin carriage of S. aureus for the early detection and treatment of carriers. This is to protect the
community from staphylococcal food poisoning and the spread of resistant S. aureus strains among the population. The
KEYWORDS: MRSA, Food handlers; Prevalence; Duhok.
1. INTRODUCTION
Staphylococcus aureus is a common commensal of the skin
and mucosal membranes of humans, with estimates of 20–
30% for persistent and 60% for intermittent asymptomatic
carriers. The presence of these bacteria in food occurs
frequently due to inappropriate manipulation of food by
carriers (Alhashimi et al., 2017). Globally, foodborne
diseases are one of the main health problems and the World
Health Organization (WHO) estimated that they caused 600
million foodborne illnesses and 420,000 deaths in 2010. The
global burden of foodborne diseases was 33 million disability
adjusted life years (WHO, 2015). Nasal carriage of S. aureus
in food handlers is the major risk of staphylococcal food
poisoning, but the skin is much less. Food handlers carrying
enterotoxin-producing S. aureus in their noses or on their
hands are concerned as the main source of food
contamination, by either manual contact or through
respiratory discharges (Ahmed and Mashat, 2014).
Moreover, antibiotic resistance in S. aureus is a serious issue
and the resistance occurred in different media and on
different surfaces. Strains of methicillin-resistant
Staphylococcus aureus (MRSA) are of special concern as
they responsible for the substantial causes of morbidity and
mortality worldwide. Methicillin-resistant S. aureus is
resistant to all available penicillin and other lactam
antimicrobial drugs. Data collected from 28 countries during
2009-2012 showed a significant increase in the percentage of
MRSA isolates that reached up to 50% in some countries like
Portugal and Romania (Castro et al., 2015). The incidence of
community-acquired S. aureus infections has been rising
with the increasing emergence of MRSA, earlier MRSA
infections were limited to the hospitals, but it has been
steadily more reported in the community (Mainous et al.,
2006). Although, vancomycin is one of the first line
antibiotics that used to treat patients with MRSA but recently
cases of vancomycin resistance have been also recorded
(Shokouhi et al., 2017). Staphylococcal food poisoning
outbreaks (SFPOs) are ranked in the last years as the first
cause of food-borne illness outbreaks in many countries. S.
aureus has attributed to 23% of the food-borne disease outbreaks
in 2014 (Mossong et al., 2015).SFPOs are under-reported for
many reasons such as the short incubation period 30 minutes to 6
hours, only 10% of SFPOs patients visit a health facility, the
medical staff usually does not request a stool analysis and even if
a stool analysis is carried out, the routine procedures frequently
do not involve testing for the existence of enterotoxigenic S.
aureus unless particularly requested by the medical staff
(Mossong et al., 2015).
The main objective of this study is to evaluate the prevalence of
nasal and skin carriage of S. aureus and MRSA and to examine
the vancomycin sensitivity pattern amongst food handlers
working in different types of restaurants in Duhok city, Kurdistan
Region, Iraq.
A cross-sectional study was adopted to achieve our objectives.
The study was conducted from 1st November 2017 to 31st July
2018.
2. METHODS
2.1 Sampling
At the time of the study, there were (314) different restaurants in
Duhok city. The restaurants classified by Directorate of
Preventive Health Affairs in Duhok into three categories casual
dining (popular), fast foods and fine dining restaurants. The
classification depended on according to certain criteria like type
of services and total area (Directorate of Preventive Health
Affairs, 2017). The available restaurants are divided into three
types (strata), a stratified sampling procedure was used to enrol
40 restaurants from Duhok city through choosing proportionate
number of restuarants from each strata (restaurants lists) by
simple random sampling procedure (table1). These restaurants
are distributed throught all quarters, sectors and main malls in the
city. Two hunderd samples were taken from the selected
resturants.
M.A. Abdulrahman and A. I. Taherb/ Science Journal of University of Zakho 6(4), 140-145, December-2018
141
Table 1. Number & percentage of restaurants stratified by
types
Types of
Restaurants
Number of
selected
Restaurants
No.
%
Casual dining
(Popular)
219
69.7
27
Fine dining
41
13.1
6
Fast food
54
17.2
7
Total
314
100.0
40
2.2 Inclusion criteria
All persons who are serving in the enrolled restaurants and
involved in the process of food preparation and introducing
it like cooks, waiters and kitchen assistants are included in
the study.
2.3 Exclusion criteria
Other restaurants’ staffs such as administrative staff, owners
and others who do not have contact with food preparation or
serving are excluded from the study.
2.4 Isolation and identification of S. aureus
From each food handler two samples were taken one from
nasal cavities and the other from their hands, and two
different swabs were utilized for each of them. One sterile
swab was used for both anterior nares (left and right) of the
workers; the swab was inserted 1-2 cm inside the nasal cavity
with rotating 2-3 seconds around the insides of each nostril.
To inhibit any discomfort, the used swabs were moistened
with sterile distilled water. Moreover, another sterile swab
was used to swab both hands of the food handlers, involving
the rest of both hands and in between fingers about five
seconds for each hand. Then the swabs transferred into
transport media then cultured in Mannitol salt agar (Oxoid)
and incubated aerobically at 37oC for 24 to 48 hours. Then
isolates were considered S. aureus by using gram staining,
standard biochemical reactions (catalase and coagulase tests)
and fermentation on mannitol salt agar.
2.5 Antibiotic susceptibility testing of S. aureus
Antimicrobial susceptibility was performed on Mueller–
Hinton agar (LAB M, UK ) using Kirby-Bauer disk diffusion
method according to diameter interpretation standards charts.
The bacterial suspension prepared by emulsifying in 5 ml of
sterile normal saline until turbidity is approximately
equivalent to that of the McFarland No. 0.5 turbidity
standard. A sterile swab was dipped into the bacterial
mixture; removed excess inoculum by squeezing on the wall
of the test tube. Then, using this swab the surface of the agar
was then uniformly and lightly inoculated. Then by sterile
forceps two antibiotic disks (Methicillin 5µg and
Vancomycin 30µg) [ LAB M ™, A Neogen® company,
United Kingdom] were placed for each plate. The plates were
incubated at 35oC for 24 hours. After incubation time
finished, inhibition zones that observed on agar plate were
measured according to standard chart (Vandepitte et al.,
2013; CLSI, 2017).
2.6 Data analysis
All data pertaining to demographic information, and
laboratory results were entered and edited using Microsoft
Word 2010 for windows 10. Data analysis was conducted
with the Statistical Package for Social Science (SPSS)
software version 23. Descriptive statistics was provided for
the demographic data and questionnaire of the study. Chi-
square test was utilized to estimate the association of the
studied variables with MRSA. P-Values 0.05, was
considered statistically significant.
2.7 Ethical considerations
Before starting the study, it was approved first by the Scientific
Committee of Shekhan Technical College of Health in Duhok
Polytechnic University. At the same time, this study was
approved by the Research Ethical Committee of the Directorate
General of Health of Duhok governorate was obtained.
3. RESULTS
3.1 Demographic characteristics
There were 200 food handlers working in 40 different restaurants,
and all participants were males. The main age group of the
subjects was 20-29 years. About two thirds of the participants
were high school educated and illiterate, 37% and 35%,
respectively, and only 3.5% of the participants were graduates of
institute or university. Meanwhile about 36.5 % of food handlers
were involved in food preparation (chefs) followed by waiters
and kitchen assistants (including cleaners and dishwashers)
35.5% and 24%, respectively. These characteristics are presented
in table 2.
Table 2. Demographic characteristics of the food handlers.
Demographic Variables
Number (%)
Age
(years)
<20
20-29
30-39
40 and more
29(14.5)
80(40.0)
38 (19.0)
53 (26.5)
Education
level
Illiterate
Primary school
High school
Institute or university
70 (35)
49 (24.5)
74 (37)
7 (3.5)
Job title
Cook
Waiters
Kitchen assistants
Others
73(36.5)
71(35.5)
48(24)
8 (4)
3.2 Types of restaurants and number of food handlers
200 workers form 40 restaurants are included in the study. Casual
dining (popular) restaurants represent the bulk of included
restaurants 27 (67.5%) followed by fast food restaurants 7
(17.5%) and fine dining restaurants 6 (15%) respectively. Out of
200 food handlers included in the study, more than half of them
105 (52.5%) belonged to casual dining restaurants and 59
(29.5%) of them were from fine dining restaurants while the least
number 36 (18%) were from fast food restaurants, as shown in
table 3.
Table 3. Classification of restaurants and distribution of food
handlers
Types of restaurants
Food Handlers
No. (%)
No. (%)
Casual dining (popular)
27(67.5)
105 (52.5)
Fast food
7 (17.5)
36 (18.0)
Fine dining
6 (15)
59 (29.5)
Total
40 (100.0)
200 (100.0)
3.3 Staphylococcus aureus carriers and age groups
The prevalence of S. aureus carriers among food handlers was
37% (74 out of 200 food handlers). The distribution of S. aureus
carriers according to age groups are shown in table 4. There were
no significant association between age group and s. aureus
carriers.
M.A. Abdulrahman and A. I. Taherb/ Science Journal of University of Zakho 6(4), 140-145, December-2018
142
Table 4. Staphylococcus aureus carriers and age group
Age group in
years
Staphylococcus aureus carriers
Total (%)
Positive (%)
Negative (%)
<20
14 (18.9)
15 (11.9)
29 (14.5)
20-29
23 (31.1)
57 (45.2)
80 (40)
30-39
15 (20.3)
23 (18.3)
38 (19)
40 and above
22 (29.7)
31 (24.6)
53 (26.5)
Total
74 (100.0)
126 (100.0)
200 (100.0)
P-value=214
3.4 Prevalence of S. aureus carriers according to the
anatomical site
Table 5 shows that in 71.6 % of carriers, the S. aureus was
isolated from their noses only and in 10.8% was isolated from
the hands (skin) only, while in 17.6% the S. aureus was
isolated from both sites (nasal cavity and hand). There were
highly significant differences between the anatomical sites of
isolation (P- value< 0.001).
Table 5. Prevalence of S. aureus carriers according to the
anatomical site
S. aureus
carriers
All sample
size (n.200)
Carriers (no.74)
No. %
No. %
Nose
53 (26.5)
53 (71.6)
Hand
8 (4.0)
8 (10.8)
Nose and Hand
13 (6.5)
13 (17.6)
Total
74 (37)
74 (100.0)
P-Value< 0.001
3.5 Prevalence of S. aureus carriers and MRSA status
Table 6 shows that MRSA was detected among 54(73%) of
the S. aureus carriers and it represents 27% of the studied
population.
Table 6. Prevalence of S. aureus carriers and MRSA status
S. aureus
carriers
MRSA status
Total No. (%)
Positive
(%)
Negative
(%)
Yes
54 (73)
20 (27)
74 (37)
No
Not
applicable
126 (63)
126 (63)
Total No. (%)
54 (27)
146 (73)
200 (100.0)
3.6 Prevalence of S. aureus carriers and vancomycin
resistant S. aureus status
No cases of Vancomycin Resistant Staphylococcus aureus
(VRSA) were detected among all S. aureus food handlers'
carriers.
4. DISCUSSION
S aureus is involved in nearly all Staphylococcal food
poisoning. Food handlers are usually considered as one of the
primary sources of these organisms. However, it is difficult
to identify the source of the strains implicated in
Staphylococcal food poisoning outbreaks. The major source
of food contamination via direct contact or through
respiratory secretions is food handlers carrying enterotoxin-
producing S. aureus in their noses or on their hands.
Moreover, food handlers have been accepted to play an important
role in the transmission of foodborne diseases; imparting
important to the global incidence and burden of diseases
(Omololu-Aso et al., 2017).
4.1 Demographic Characteristics of Food Handlers
In the present study, all the food handlers were male and this
might be due to the reluctance of the female, the tradition and
customs of the region that may prevent female from working in
the restaurants or public places, and indeed, the owners of public
places in Duhok recruit foreigner workers. A similar result was
obtained by Simsek et al., (2009) who found that (299) food
handlers in Sanliurfa, in South-eastern Anatolia are males
because the majority of women in Southern Anatolia are
unemployed. Habiballah et al., (2017) found that majority of
workers (81.6%), who are working in tourist restaurants in Irbid,
Jordan were males; they found that females are not eager to work
in restaurants (Kasturwar and Shafee 2011). Other studies
revealed that their samples are mixed near to equal percentages
(Kasturwar and Shafee 2011; El-Shenawy et al., 2014; Castro et
al., 2016). Regarding the educational levels, the majority of food
handlers (96.5%) have high school or less educational levels,
because less educated people have little chances to work in high
ranking jobs. El-Shenawy et al., (2014) mentioned that all of their
study samples are either illiterate or high school educated, while
Kasturwar and Shafee, (2011) found that about only 20% of food
handlers having a degree above high school level. In this study,
the percentage of cooks (36.5%) is slightly more than waiters
(35.5%) in contrast to a study in Karimnagar, India, were the
majority of food handlers were serving food (waiters) 60.2% and
only 12% working in food preparations (cooks) (Kasturwar and
Shafee, 2011). Due to the financial crisis in Kurdistan region that
started in 2014, many companies and institutions reduced their
manpower including restaurants in Duhok city. They reduced the
number of waiters while kept their chefs and even many of the
owners and their family members worked as waiters to ease the
financial burden on them.
4.2 Prevalence of S. aureus carrier
The current study revealed that 37% of food handlers are carriers
of S. aureus, while Saeed, (2015) found about 29.24% (n=106)
of food handlers in restaurants and cafeterias of Duhok city are
carriers of S. aureus. Another study was done in Tikrit, Iraq by
Alsamarai et al., (2015) who found that 28% (n=100) of studied
food handlers were carrier for S. aureus. Alhashimi et al., (2017)
revealed that the prevalence of nasal carriage of S. aureus among
332 food handles in Karbala city, Iraq was 30.1%. A further study
was done in Turkey; in which S. aureus was lower than that of
the current study 20% (Vatansever et al., 2016). Mainous et al.,
(2006) estimated that about 32.40% of the total United States
population (86.9 million) was colonized with S. aureus.
Meanwhile, another study among 200 participants working in
three different food processing plants in Egypt that reported the
prevalence rate of S. aureus 38% that are in accordance with our
results (EL- Shenawy et al., 2014), and the prevalence of S.
aureus in Makkah city among food handlers working in city
kitchens was 40.3% (Ahmed and Mashat, 2014). In addition to
all of the previous studies, higher S. aureus carrier rates among
food handlers were recorded in many studies such as the study
done among 140 food handlers in public hospitals in Salvador
city, Brazil, were the carrier rates were 50% (Ferreira et al.,
2014), while higher rate 57.7% detected in Gaborone, Botswana.
(n=200) (Loeto et al., 2017). The ability of S. aureus to colonize
or infect its host is related to its ability to express virulence
factors that facilitate their adherence to surfaces, cause damage
or its ability to evade host's immune system (Udo et al. , 2009).
M.A. Abdulrahman and A. I. Taherb/ Science Journal of University of Zakho 6(4), 140-145, December-2018
143
4.3 Prevalence of S. aureus carriers according to
anatomical sites
Staphylococcus aureus is part of the commensal flora of
human skin and mucosal surfaces. The main site for S. aureus
in human carriers is the nose, which may be colonized during
the first few days of life. Strains present in the nasal cavity
may contaminate the hands and nasal carriers can thus readily
become skin carriers (Hatakka et al., 2000). Approximately
20% (range, 12% to 30%) of healthy people are persistent S.
aureus nasal carriers, 30% (range, 16% to 70%) are
intermittent carriers, and 50% (range, 16% to 69%) are non-
carriers (Yan et al., 2015). Persistent carriers usually carry
the same strain for extended periods of time, whereas
intermittent carriers tend to host different strains over time.
The presence of S. aureus in the hands of the general
population range from 8-28%, according to independent
surveys (Hatakka et al., 2000).
The prevalence of S. aureus nasal carriage varies by
geographical location, age, gender, and ethnicity. The
carriage is highest amongst newborns (up to 70 %) but
steadily decreases with age (Aryee and Edgeworth, 2017).
Rates of carriage have also been found to be higher in patients
with certain diseases like diabetes mellitus, intravenous drug
addicts, haemodialysis patients, surgical patients and AIDS
patients. Despite the fact that S. aureus is found at multiple
body sites, most studies have only focused on nasal carriage
(Aryee and Edgeworth, 2017). The present study shows that
the distribution of carriers according to the anatomical sites
of swab collections was from the nasal cavity in 71.6 % of
(53 out of 74) of carriers, 10.8% from the hands (skin) and in
17.6% the S. aureus was isolated from both sites (nasal cavity
and hand). (Vatansever et al., 2016) investigated 282 food
workers in Kars city, Turkey. They took swabs from the nose,
mouth, and hands. S. aureus was isolated from 56 (20%) of
food workers which involving 32 (57 %) isolates from the
nasal nares, 13 (23%) isolates from the mouth and 11 (20 %)
isolates from the hands of food handlers respectively. In
Portugal, the prevalence of S. aureus among the studied
population was 24.7% (n=162), the distribution of carriers
according to the sites of swab taking was 32(19.8%), 18
(11.1%) and 10 (6.2%) from nose, hands and both sites
respectively (Castro et al., 2016).
In contrast, in (Ferreira et al., 2014) study S. aureus detected
from the skin in 50% of carriers and less detected from the
nasal cavity 29.3. In another study of the prevalence of S.
aureus carriage among food workers at the cafeteria of the
Federal University of Technology, Nigeria showed the S.
aureus was isolated from 28 (51.85%) of the 54 food handlers
examined, 21 (38.9%) harbour S. aureus in their nasal cavity,
11 (20.4%) in their throat and 6 (11.1%) in their both sites
(Emeakaroha et al., 2017). The distribution of the
microorganism varied according to sites on the body, with the
nasal cavity harbouring higher numbers of isolates (44.6%),
while the hand was (30.9%) and face was (24.5%) (Loeto et
al., 2017).
4.4 Prevalence of MRSA
In our study, the prevalence of MRSA among the study
population was 27%. This result was slightly different from
other studies done in Duhok province. (Habeeb et al., 2014)
conducted a big study in Duhok province and they found that
the MRSA rates had widely different between secondary
school students’ group (2 %) (10/489) and health care
workers (12%) (61/510). Three separate studies conducted in
Zakho city, the researchers found that the MRSA rates were
relatively low among University students (4.2%), and 4%
among primary school students, while higher rates 13.7%
detected among health care workers (Hussein et al., 2010;
Assafi et al., 2015). However, (Saeed, 2015) found that
22.5% of food handlers serving in restaurants and cafeterias in
Duhok city were positive for MRSA. Our results were in line with
two other studies (Al sa mar ai et al., 2015) study who
demonstrated the MRSA among 28% of food handlers in Tikrit,
and (Ferreira et al., 2014) study who demonstrated the MRSA
among 28.6% of food handlers.The higher prevalence rate of
MRSA was observed in a study done in Sweden among
household contacts was (36.8%) (42 /114) (Johansson et al.,
2007). Also, a higher MRSA rate detected by (Wolde et al.,
2016), they found that 92.5% of food handlers of Jigjiga
university student’s cafeteria were MRSA carrier. Lower MRSA
rate 9.8% was reported among food handlers working in Gondar
university in Ethiopia (Dagnew et al., 2012). (Shokouhi et al.,
2017) found that only 1.25% of the studied population in the
tertiary outpatient center in Iran had MRSA. In contrary to our
study, no cases of MRSA were detected by other studies (Castro
et al., 2016; Vatansever et al., 2016). Many different factors
contributed in the distribution of S. aureus and MRSA including
crowded housing, bad hygienic practices, sharing of personal
utensils, recurrent antibiotic usage, hospital admissions and
intravenous drug addicts (Braga et al., 2014; Assafi et al., 2017).
4.5 Prevalence of VRSA
Vancomycin is considered one of the last options of treatment for
S. aureus infections that are resistant to other antibiotics.
Analysis of different studies showed the emergence of VRSA
from different parts of the neighboring countries (Tiwari and Sen,
2006; Askari et al., 2012). Fortunately, no VRSA isolates were
found in this study. Similar results obtained in many studies done
in Duhok province (Hussein et al., 2010; Habeeb et al., 2014;
Saeed, 2015). This might be attributed to many reasons like
vancomycin which had been used rarely in Iraq during the United
Nation’s sanction period from 1990 to 2003; the drug was
expensive and was not available in many health facilities. Also,
our result was in accordance with the results of neighboring
countries (Udo et al., 2009; Dangnew et al., 2012; Shokouhi et
al., 2017).
In contrast, Alsamarai et al., (2015) revealed that the 18.6% of
studied food workers in Samara restaurants had vancomycin-
resistant S. aureus and Loeto et al., (2017) found that 27.3% of
food handlers with MRSA also were resistant to vancomycin; this
rate is near to that of the study done in Maharashtra among food
handlers working in medical college restaurant (26.5%)
(Kasturwar and Shafee, 2011). Moreover, Ferraria et al., (2014)
found a high percentage of VRSA 39.2% from the food handlers’
hands and less percentage 23.5% of VRSA from their anterior
nares.
5. CONCLUSION
The study revealed a high prevalence of MRSA among food
handlers in Duhok city. Food handlers in public places are
required to go through regular screening for both nasal and skin
carriage of S. aureus for the early detection and treatment of
carriers so as to protect the community from staphylococcal food
poisoning and the spread of resistant S. aureus strains among the
population.
COMPETING INTERESTS
The authors declare that they have no competing interests.
RECOMMENDATIONS
The current study recommends the demand for the regular
screening of food handlers in all public places for both nasal and
skin carriage of S. aureus in order to early detection and effective
treatment of carriers so as to protect the community from
staphylococcal food poisoning and the spread of resistant S.
M.A. Abdulrahman and A. I. Taherb/ Science Journal of University of Zakho 6(4), 140-145, December-2018
144
aureus strains among the population. As proven, many
staphylococcal foods borne disease is mostly caused by
incorrect food handling practices. It is recommended to give
proper training courses to food handlers so as to prevent the
contamination of food.
REFERENCES
Alhashimi H M, Ahmed M M, Mustafa J M (2017). Nasal carriage
of enterotoxig enic Staphylococcus aureus among food
handlers in Kerbala city. Karbala International Journal of
Modern Science,3: 69-
74.doi.org/10.1016/j.kijoms.2017.02.003.
Ahmed O B and Mashat B H (2014). Prevalence of classical
enterotoxin genes in Staphylococcus aureus isolated from
food handlers in Makkah city kitchens. Asian Journal of
Science and Technology. Umm Al-Qura University,
Makkah , Saudi Arabia., 5(11): 727-73.
Aryee A and Edgeworth J D (2017). Carriage, Clinical Microbiology
and transmission of Staphylococcus aureus. In: Bagnoli
F, Rappuoli R, Grandi G, editors. Staphyloc occus aureus:
Microbiol ogy, Path ology, I mmunology, Therapy and
Prophylaxis. Springe r International Publishing
Switzerland.pp .1-14. DOI 10.1007/82_2016_5.
Askari Z, Sadeghian A, Sadeghian H, Ghazvini K, Safdari H
(2012). Antibiotic Resistance Pattern of Hospital Isolates
of Staphylococcus aureus in Mashhad-Iran During 2009
2011. Archives of Clinical Infectious Diseases,7(3): 96-
8.DOI: 10.5812 /archcid.14468.
Assafi MS, Mohammed RQ, Hussein NR (2015). Nasal Carriage
Rates of Staphylococcus aureus and CA-Methicill in
Resistant S. aureus among University Students. Journal
of Microbiology Research ,5(4): 12327.DOI:
10.5923/j.icrobiology.20150504.01.
Assafi MS, Polse RF, Hussein NR, Haji AH, Issa AR (2017).The
prevalence of S. aureus nasal colonisation and its
antibiotic sensitivity pattern a mongst primary school
pupils .Science Journal of University of Zakho, 5(1):7-10.
Alsamarai A M, Abbas H M, Attia QM (2015). Nasal carriage of
methicillin-resistant Staph aureus in food provider in
restaurant at Samara city. International Journal of
Pharmacy and Pharmaceutical Sciences, 4 (06): 50-58.
Braga ED, Aguiar-Alves F, de Freitas Mde F, de e Silva MO, Correa
TV, Snyder RE et al, (2014). High prevalence of
Staphylococcus aureus and methicillin resistant S. aureus
colonization among Healthy children attending public
day care centers in informal settlements in a large urban
center in Brazil. BMC Infectious Diseases,6;14:538. doi:
10. 1186/ 1471-2334-14-538.
Castro A, Santos C, Meireles H, Silva J, Teixeira P (2015). Food
handlers as potential sources of dissemination of virulent
strains of Staphylococcus aureus in the community.
Journal of Infection and Public Health, 9: 153-160.
Clinical and Laboratory Standards Institute (2017). Performance
Standards for Antimicr obial Susceptibility Testing. 27th
ed. Wayne, Pennsylvania.
Dagnew M, Tiruneh M, Moges F, Tekeste Z (2012). Survey of nasal
carriage of Staphylococcus aureus and intestinal parasites
among food handlers working at Gondar University,
Northwest Ethiopia. BMC public Health, 12(1): 837.doi:
10.1186/1471 -2458-12-837.
Directorate of Preventive Health Affairs (2017). Department of
Health Inspection. DPHA, Duhok.
El-Shenawy M, Tawfeek M, El-Hosseiny L, El-Shenawy M, Farag
A, Baghdadi H, et al. (2014) Cross Sectional Study of
Skin Carriage and Enterotoxigen icity of Staphylococcus
aureus among Food Handlers. Open Journal of Medical
Microbiology,4(1): Article ID: 43014,
7pages.DOI:10.4236/ojmm.2014.41003.
Emeakaroha, Chioma M, Nkwocha, Gertrud e I, Adieze, Chibuzo N
et al, (2017). Antimicrobial susceptibility pattern of
Staphylococcus aureus, and their nasal and throat
carriage among food handlers at the Federal University of
Technology, Owerri Nigeria. International Journal of
Biomedical Science, 6(3): 1-7.
Ferreira J S, Costa W L, Cerqueira E S, Carvalho J S, Ol iveira L C
Almeida R C (2014). Food handler-associated
methicillin-resistant Staphylococcus aureus in public
hospitals in Salvador, Brazil. Food Control, 37: 395-400.
doi.org/ 10. 1016 /j. foodcont.2013.09.062.
Habeeb A, Hussein NR, Assai MS, Al-Dabbagh SA (2014). Methicillin
resistant Staphylococcus aureus nasal colonization among
secondary school students at Duhok City-Iraq. Journal of
Microbiology and Infectious Diseases, 4(2): 59-63. doi:
10.5799/ ahinjs. 02. 2014. 02.0128.
Habiballah M A, Al-Shakhsheer F, Al-Ababneh M M (2017). Restaurant
Employees’ Food Handling Practices in Irbid City, Jordan. J
Tourism and Hospitalit y Management ,5(1): 81-89. doi. org/
10.15640/jthm. v5n1a9.
Hatakka M, Björkroth K J, Asplund K, Mäki-Petäys N, K orkeala H J
(2000). Genotypes and enterotoxicity of Staphylococcus
aureus isolated from the hands and nasal cavities of flight-
catering employees. Journal of food protection, 63(11): 1487-
91.
Hussein N R, Assafi M S, Ijaz T (2010). Methicillin-resistant
Staphylococcus aureus nasal colonisation amongst healthcare
workers in Kurdistan Region, Iraq. Journal of Global
Antimicrobial Resistance, 9: 78-81. doi.org/ 10. 1016 / j.
jgar.2017.01.010.
Johansson PJ, Gustafsson EB, Ringberg H (2007). High prevalence of
MRSA in household contacts. Scand Journal of Infectious
Diseases, 39(9):764-8.
Kasturwar N B and Shafee M (2011). Knowledge, Practices and
Prevalence of MRSA among Food Handlers. International
Journal of Biological Medical Research, 2(4): 889 -894.
Loeto D, Matsheka M I , Gashe B A (2017). Enterotoxigenic and
antibiotic resistance determination of Staphylococcus aureus
strains isolated from food handlers in Gaborone, B otswana.
Journal of Food Protection,70(12): 2764-8.
Mainous A G, Hueston WJ, Everett C J, Diaz V A (2006). Nasal Carriage
of Staphylococcus aureus and Methicillin-Resistant S. aureus
in the United States, 2001-2002. Annals of Family
Medicine,4: 132-7. DOI: 10.1370/afm.526.
Mossong J, Decruyenaere F, Moris G, Ragimbeau C, Olinger C, Johler
S et al (2015). Investigation of a staphylococcal food
poisoning outbreak combining case-control, traditional typing
and whole genome sequencing methods, Luxembourg, June
2014. Euro Sur veil, 20(45): pp.30059. DOI: Http://
dx.doi.org/10.2807/1560-7917. ES. 2015.20.45.30059
Omololu-Aso J, Omololu-Aso O O, Otusanya O O, Ochada H C, Shesha
A (2017). Nasal Colonization of Methicillin Resistance
Staphylococcus aureus among Food Handlers in the Ea teries
Obafemi Awolowo University Ile Ife, Nigeria. Journal of
Clinical Nutrition and Dietetics, 3(1:9): 1-4. DOI:
10.4172/2472-1921.100043.
Saeed AY (2015). Enterotoxigenicity and antibiogram pr ofile of
Staphylococcus aureus isolated from food handlers in
restaurants and cafeterias in Duhok city, Iraq. Journal of
American science, 11(3s) : 21 -24.
Shokouhi S, Darazam I, Zamanian M H (201 7). Community-acquired
methicillin-resistant Staphylococcus aureus carriage rate and
antimicrobial susceptibility in a tertiary center, Iran. Journal
of Research in Medical Sciences, 22(1): 71. DOI: 10.4103/
jrms. JRMS_833_16.
Simsek Z, Koruk I, C opur A C, Gürses G (2009). Prevalence of
Staphylococcus aureus and intestinal parasites among food
handlers in Sanliurfa, Southeastern Anatolia. Journal of
public health management and Practice, 15(6): 518-23.
Tiwari HK and Sen MR (2006). Emergence of vancomycin resistant
Staphylococcus aureus (VRSA) from a tertiary care hospital
from northern part of India. BMC Infectious Diseases, 6:156.
Udo E E, Al-Mufti S, Albert M J (2009). The prevalence of antimicrobial
resistance and carriage of virulence genes in Staphylococcus
aureus isolated from food handlers in Kuwait City
restaurants. BMC research notes,2(1 ): 108. doi: 10.
1186/1756-0500-2-108.
Vandepitte J, Verhaegen K, Engbaek P, Rohner P, Piot C (2003).
Basic Laboratory Procedures in Clinical Bacteriology. 2th ed.
Geneva: WHO. pp. 111-7.
Vatansever L, Sezer Ç, Bilge N (2016). Carriage rate and methicillin
resistance of Staphylococcus aureus in food handlers in Kars
City, Turkey . Springer Plus, 5(1): 608. DOI 10.1186/s40064-
016-2278-2.
Wolde T, Abate M, Mehari L (2016) . Prevalence and Antibiotics
Resistance Pattern of Staphylococcus aureus among Food
Handlers of Jigjiga University Student’s Cafeteria. IJSRET,
2(1): 476-8.
M.A. Abdulrahman and A. I. Taherb/ Science Journal of University of Zakho 6(4), 140-145, December-2018
145
World Health Organization (2015). WHO Estimates of The Global
Burden of Foodborne Diseases: Foodborne Disease
Burden Epidemiology Reference Group 2007-2015.
Geneva: WHO.
Yan X, Song Y, Yu X, Tao X, Yan J, Luo F et al, (2015). Factors
associated with Staphylococcus aureus nasal carriage
among healthy people in Northern China. Clincal
Microbiology Infection, 21: 157 162. http://dx.doi.org/10.
1016/j. cmi. 2014.08.023.
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