Prevalence of common microbes and pattern of their antibiotic

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EL-MINIA MED. BULL. VOL. 21, NO. 2, JUNE, 2010
Eldydamouny et al
PREVALENCE OF COMMON MICROBES AND PATTERN
OF THEIR ANTIBIOTIC SENSITIVITY AND RESISTANCE
IN TABUK, SAUDI ARABIA
By
Mohamad Aly Eldydamouny, *M.D., ** Kazmi Rashed Sayed, M.S.
*** Ghada Osman, M.D. and****Ashraf A. Ewis
*Consultant of Public Health, Infection Control Program, General Directorate of
Health Affairs in Tabuk Region, Tabuk, Kingdom of Saudi Arabia
**Microbiologist King Fahad Hospital, Tabuk, Kingdom of Saudi Arabia
***Specialist of Public Health, King Khalid Hospital, Tabuk, Kingdom of Saudi Arabia
and ****Dept. of Infection Control & Public Health,
Faculty of Medicine, El-Minia University, El-Minia, Egypt
ABSTRACT:
Objective: The study was aimed to identify common prevalent strains of microorganisms causing infection in Tabuk Region, Saudi Arabia, and to detect their
antimicrobial sensitivity and resistance pattern against locally available commonly
used antibiotics.
Materials and Methods: A total of 2423 culture positive laboratory samples from
four main hospitals in Tabuk province were included in this descriptive cross
sectional study. The samples were cultured in appropriate media using standard
microbiological procedures to identify the microbes. Antibiotic sensitivity and
resistance pattern were determined using the Kirby-Bauer disk diffusion method.
Sensitivity more than 70% for an antibiotic was regarded as ‘effective’ against the
particular microbe.
Results: Of 2423 culture positive sample-giver patients, Saudis (84.5%), females
(68.6%), and hospitalized patients (64.1%) were predominant. The age of the patients
ranged from 1 day to 100 years with a mean of 32.55 ± 27.12 years. Among the
samples, the most common variety was high vaginal swab (27.8%), followed by urine
(17.9%), wound swab (17%), throat swab (9.4%), sputum (5.2%), ear swab (5%),
blood (4.5%), umbilical swab (3.2%), and others. Klebsiella (22.3%) was found as the
most prevalent micro-organism, while other identified main microbes were
Escherichia coli (20.1%), Staphylococcus aureus (15.1%), Pseudomonas (13.7%),
Streptococci (5.7%), Proteus (5.3%), and MRSA (2.8%). Among 595
Staphylococcus-positive samples, Staphylococcus aurius (61.7%) was found as the
most prevalent one, followed by MRSA (11.6%), Staphylococcus epidermidis (7.4%),
Staphylococcus albus (7.2%), Coagulage negative Staphylococcus (7.1%), and others.
Staphylococcus aurius was also predominant among the gram positive samples
(n=717), and it was found more in high vaginal swab (79.3%), nasal swab (65%),
umbilical swab (61.9%), ear swab (55.2%), wound swab (53.5%), and urine (50.5%).
Among the gram negative samples (n=1683), Klebsiella was the most prevalent
organism, and it was found mainly in throat swab (70.3%), samples from axilla
(57.1%), and umbilical swab (52.6%). Amoxicillin was found as 100% sensitive for
Staphylocococcus aurius and E. coli infection, while Ceftriaxone had the same
sensitivity pattern against MRSA infection. Amikacin was found sensitive against E.
coli (93.9%), Klebsiella (88.9%), Pseudomonas (85.2%), Streptococcus (83.3%), and
MRSA (72.7%). Ciprofloxacin was also found sensitive against Klebsiella (89%),
Pseudomonas (78.1%), and E. coli (72.6%). Gentamycin was found effective against
Klebsiella (81.1%), E. coli (80.5%), Staphylococcus aurius (79.2%), MRSA (76.7%),
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Eldydamouny et al
and Pseudomonas (75.1%). Cefotaxime and Ceftriaxone both were found effective
against Streptococcus, E. coli, and Klebsiella. Ampicillin showed the highest
resistance pattern against all the top prevalent gram positive and gram negative
microbes indicating its general ineffectiveness. Moreover, Cotrimoxazole was found
as ineffective against all top three gram negative micro-organisms.
Conclusion: Our study found considerably higher occurrence of antibiotic resistance
in Tabuk province emphasizing the need for local and country-based surveillance to
characterize and monitor the infectious agents, and to develop strategies that would
improve the pattern of treatment and control of infection.
KEY WORDS:
Antibiotic Sensitivity
Micro organisms
Resistance
Infection control
expensive to treat. Antibiotic resistant
bacteria can cause harm for the
patients who suffer from common
infections that once could be cured by
antibiotics but now has become
difficult or impossible to treat.2,3 A
recently-discovered
strain
of
Staphylococcus bacteria does not
respond to antibiotic treatments at all,
leading medical analysts to worry that
certain 'super bugs' could emerge that
are resistant to even the most potent
drugs, rendering some infections
incurable.5
INTRODUCTION:
Now
a
days,
antibiotic
resistance has become a serious health
problem worldwide, and United States
Centre for Disease Control and
Prevention (CDC) calls antibiotic
resistance one of its 'top concerns'.1
This is because over the last decade,
almost every type of bacteria has
become stronger and less responsive to
antibiotic treatment when it is really
needed. Whenever an antibiotic is used
for treatment it promotes the
development of antibiotic resistant
bacteria. As a consequence when a
person takes antibiotics, sensitive
bacteria are killed, but resistant germs
may survive and continue to multiply
causing more harm.2,3
The number of infection caused
by resistant pathogens continues to
increase in Saudi Arabia like other
parts of the world. These infections
cause suffering, inability and death,
imposing an enormous financial
burden on both healthcare systems and
on the society in general, because of
direct costs due to prolongation of
illness and treatment in hospital,
indirect costs due to loss of
productivity, and societal costs due to
morbidity and mortality. This is likely
to lead to already-scarce healthcare
resources being diverted to infection
control efforts, and will have long-term
implications due to loss of confidence
in the medical profession and in the
public healthcare delivery system
provided
or
regulated
by
Factors contributing towards
antibiotic resistance include overuse of
broad-spectrum antibiotics, incorrect
diagnosis, unnecessary prescriptions,
improper use of antibiotics by patients,
the impregnation of household items
and children's toys with low levels of
antibiotics, and the use of antibiotics as
livestock food additives for growth
promotion.4
Antibiotic
resistant
bacteria can quickly spread among
family members, schoolmates and coworkers, providing opportunity to rise
emerging infectious diseases those are
more difficult to cure and more
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EL-MINIA MED. BULL. VOL. 21, NO. 2, JUNE, 2010
governments.6,7
Eldydamouny et al
The samples were collected in
aseptic condition and cultured in
incubator at 37o C for at least 72 hours.
The culture was performed in
appropriate media using standard
microbiological techniques in order to
identify the micro-organisms. Gramstaining for isolated microbes were
done when and where necessary before
proceeding to test for their antibiotic
sensitivity and resistance. Kirby-Bauer
disk diffusion method was used to
determine antibiotic sensitivity and
resistance pattern. Sensitivity more
than 70% for an antibiotic was
considered as ‘effective’ against the
respective microbe. Complete aseptic
environment was ensured in each
laboratory, and highly skilled and
experienced staffs performed the entire
procedure.
Surveillance
for
hospital
acquired infection and conducting
research on local antibiogram are
always the key strategies for hospital
infection control program. Several
studies8,9,10 have confirmed that the
way of this evidence based practice has
been
implemented
in
many
standardized hospitals in developed
world. We carried out this study to
identify prevalent strains of bacterial
pathogens causing infection in Tabuk
Region, Saudi Arabia, and to
determine
their
antimicrobial
sensitivity and resistance pattern
against locally available widely used
antibiotics.
MATERIALS AND METHODS:
This descriptive cross sectional
study was conducted during a period
between 1st January to 31st December,
2008 in Tabuk province which is
located along the North-Western part
of Saudi Arabia near the Red Sea.
Tabuk province possesses a surface
area of 108,000 sq km occupied by
573,691 populations according to the
KSA Census 2010 (Preliminary
results).
It
consists
of
five
'Governorates' (Umluj, Duba, Al-Wajh,
Haqel and Tayma'a) and one 'Cluster'
(Al-Bada).
Data were collected from
laboratory result sheets and registers
using a preformed unified checklist
applicable to all study-hospitals. The
collected data included information on
socio-demographic features of the
sample-givers, type and source of
tested samples, test results, sensitivity
and resistance pattern to commonly
used antibiotics. The collected data
were undergone several processes such
as data cleaning, check for missing
values, coding and recoding of
variables before they were entered into
SPSS (Statistical Package for Social
Sciences) version 12 for appropriate
statistical analysis.
A total of 2423 culture positive
laboratory samples from four main
hospitals in the province titled: Tabuk
Maternity and Children's Hospital, AlWajah hospital, King Khaled Hospital,
and King Fahad Hospital) were
included in the study. Among nine
general hospitals in the province,
above-mentioned four hospitals were
selected
because
workingmicrobiologists were available in the
laboratories of those hospitals during
the study.
RESULTS:
Table 1 shows the distribution
of culture positive laboratory samples
by hospital, sex, nationality and source
of collection. Of total 2423 culture
positive laboratory samples, the
highest proportion (41.2%) were from
Tabuk Maternity and Children’s
Hospital (MCH), followed by 24.2%
from Al-Wajh Hospital, 19.9% from
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King Fahad Hospital (KFH), and the
least (14.7%) from King Khaled
Hospital (KKH). Most of the culture
positive laboratory samples were
received from Saudis (84.5%) and
females (68.6%). The age of samplegiver patients ranged widely from 1
day to 100 years with a mean age of
32.55 ± 27.12 years. Maximum
(64.1%) samples were received from
hospitalized patients, while remaining
35.9% were collected from outpatient
departments. Figure 1 illustrates the
seasonal variation of culture positive
laboratory samples by months in the
year 2008. Of 2423 samples, 11.4%
were collected in the month of Rabi Al
Awwal which is quite higher than the
samples received in other months.
However, the lowest proportion (5.7%)
of the culture positive laboratory
samples was received in the month of
Ramadan.
Eldydamouny et al
total of nine varieties of Staphylococci
strains were isolated from the culture
positive laboratory samples [Figure 4].
Among the total 595 Staphylococcuspositive samples, Staphylococcus
aurius (61.7%) was found as the most
prevalent one, followed by MRSA
(11.6%), Staphylococcus epidermidis
(7.4%), Staphylococcus albus (7.2%),
Coagulage negative Staphylococcus
(7.1%), and others [Figure 4].
Of
the
culture
positive
laboratory samples, gram positive
organisms were found in 717 (29.9%)
samples,
while
gram
negative
organisms were isolated from 1683
(70.1%) samples. Among the samples
those showed gram positive microbes
(n=717), Staphylococcus aurius was
predominant and it was found highest
in high vaginal swab (79.3%),
followed by in nasal swab (65%),
umbilical swab (61.9%), ear swab
(55.2%), wound swab (53.5%), and
urine (50.5%) [Table 2]. Streptococci
were found higher in samples from
axilla (66.7%), sputum (60.3%), and
throat swab (50%), while MRSA were
found in samples from axilla (33.3%)
and nasal swab (25%) [Table 2].
Klebsiella, Escherichia coli and
Pseudomonas predominated among the
samples those showed gram negative
microbes (n=1683). Klebsiella was
found more in throat swab (70.3%),
samples from axilla (57.1%), and
umbilical wound swab (52.6%) [Table
3]. Escherichia coli was found highest
in urine (47%), whereas Pseudomonas
were plenty in rectal swab (72.7%),
eye swab (47.1%), and wound swab
(35%) [Table 3].
Figure 2 shows the distribution
of culture positive laboratory samples
by their type and nature. Of total 2423
samples, the most common variety was
high vaginal swab (27.8%), while the
proportion of urine sample (17.9%)
and wound swab (17%) were nearly
equal. Throat swab (9.4%), sputum
(5.2%), ear swab (5%), blood (4.5%),
and umbilical wound swab (3.2%)
were also included in culture positive
samples. Moreover, samples from NG
tube tip, nasal swab, eye swab, samples
from axilla, and rectal swab played
important role to identify prevalent
organisms irrespective of their total
numbers.
Klebsiella (22.3%) was found
as the most prevalent micro-organism
among 2423 culture positive laboratory
samples, followed by Escherichia coli
(20.1%),
Staphylococcus
aureus
(15.1%),
Pseudomonas
(13.7%),
Streptococci (5.7%), Proteus (5.3%),
MRSA (2.8%), and so on [Figure 3]. A
Sensitivity
and
resistance
pattern of the locally available
antibiotics against top three prevalent
gram positive and gram negative
microbes has been shown in Table 2
and Table 3. Effectiveness of these
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antibiotics can be explained by their
sensitivity and resistance pattern.
Amoxicillin was found as 100%
effective for Staphylocococcus aurius
and E. coli infection, whereas
Ceftriaxone had the same effectiveness
against MRSA infection. Amikacin
was found effective against E. coli
(93.9%),
Klebsiella
(88.9%),
Pseudomonas (85.2%), Streptococcus
(83.3%),
and
MRSA
(72.7%).
Ciprofloxacin was also found effective
against
Klebsiella
(89%),
Pseudomonas (78.1%), and E. coli
(72.6%). Gentamycin was found
effective against Klebsiella (81.1%), E.
coli (80.5%), Staphylococcus aurius
Eldydamouny et al
(79.2%),
MRSA
(76.7%),
and
Pseudomonas (75.1%). Cefotaxime
and Ceftriaxone both were found
effective against Streptococcus, E. coli,
and Klebsiella. Ampicillin appeared as
the most ineffective antibiotic to fight
against all the top prevalent gram
positive and gram negative microbes
shown in Table 2 and Table 3.
Similarly, Cotrimoxazole was also
found as ineffective against all top
three gram negative micro-organisms
[Table 3]. Moreover, Salmonella was
found 100% resistant to Amikacin,
Ampicillin, Augmentin, Cephalothin,
Cotrimoxazole and Gentamycin [Data
not shown in the tables].
Table 1: Distribution of culture positive laboratory samples by hospital, sex,
nationality and source of collection, Tabuk, Saudi Arabia, 2008
Variable
Hospital (n=2423)
Sex (n=2215)a
Nationality (n=795)b
Source of sample
collection (n=2084)c
Category
Maternity and Children's Hospital
(MCH)
Al-Wajh Hospital
King Fahd Hospital (KFH)
King Khaled Hospital (KKH)
Male
Female
Saudi
Non-Saudi
Admitted patient at indoor
Non-admitted patient at outdoor
a
Frequency (%)
998 (41.2%)
586 (24.2%)
483 (19.9%)
356 (14.7%)
696 (31.4%)
1519 (68.6%)
672 (84.5%)
123 (15.5%)
1335 (64.1%)
749 (35.9%)
Sex was unknown for 208 (8.6%) samples due to unavailability of data
Nationality was unknown for 1628 (67.2%) samples due to unavailability of data
c
Source of sample collection was unknown for 339 (14%) samples due to
unavailability of data
b
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Eldydamouny et al
Figure 1: Seasonal variation of culture positive laboratory samples (n=2423) by
months, Tabuk, Saudi Arabia, 2008
Figure 2: Distribution of culture positive laboratory samples (n=2423) by their
type, Tabuk, Saudi Arabia, 2008
*
Others (3.3%) include stool, pus from abscess, pleural fluid, sample from skin,
sample from CVL tip, prostatic discharge, semen, swab from bed sore, urethral
discharge, breast nipple discharge, etc.
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EL-MINIA MED. BULL. VOL. 21, NO. 2, JUNE, 2010
Eldydamouny et al
Figure 3: Micro-organisms isolated from culture positive laboratory samples
(n=2423), Tabuk, Saudi Arabia, 2008
25.0
22.3
20.1
Percent
20.0
15.1
15.0
13.7
10.0
5.7
5.3
5.0
2.8
2.5
4.1
1.8
1.8
1.7
1.5
1.5
0.0
*
Streptococci (5.7%) include Streptococcus Beta-haemolyticus, Streptococcus
pneumonae, Streptococcus viridance, etc.
**
Others (4.1%) include Staphylococcus haemolyticus, E. cloacae, E. fecalis,
Staphylococcus cohnii, Raoultella ornithinolytica, Yersina pestis, Salmonella, Citrobacter
fraundii, Micrococcus, Pantoea, Morganella morganii, Diplo viridance, etc.
Figure 4: Different strains of Staphylococci (n=595) isolated from culture
positive laboratory samples, Tabuk, Saudi Arabia, 2008
70.0
61.7
Percent
60.0
50.0
40.0
30.0
20.0
10.0
11.6
7.4
7.2
0.0
263
7.1
3.0
1.0
0.7
0.3
EL-MINIA MED. BULL. VOL. 21, NO. 2, JUNE, 2010
Eldydamouny et al
Table 2: Top three prevalent gram positive microbes by nature of laboratory sample,
antibiotic sensitivity and resistance pattern, Tabuk, Saudi Arabia, 2008
Gram positive
microbes
Nature of
laboratory
sample
High vaginal swab
Nasal swab
1.Staphylococcus Umbilical swab
aurius
Ear swab
Wound swab
Urine
Sample from axilla
Sputum
2. Streptococcus Throat swab
Eye swab
Urine
Ear swab
Sample from axilla
Nasal swab
3. MRSA
Sample from
ET/NGT tip
Wound swab
Sputum
Eye swab
Percentage* Antibiotic
sensitivity
Percentage* Antibiotic
resistance
Percentage*
79.3%
65.0%
61.9%
55.2%
53.5%
50.5%
66.7%
60.3%
50.0%
21.4%
15.5%
12.1%
33.3%
25.0%
21.4%
Amoxycillin
Vancomycin
Gentamycin
Ceftriaxone
Augmentin
Amikacin
Cefoxitin
Vancomycin
Ceftriaxone
Amikacin
Augmentin
Cefotaxime
Ceftriaxone
Vancomycin
Bacitracin
100%
82.7%
79.2%
69.7%
65.7%
64.8%
88.9%
85.9%
84.6%
83.3%
82.3%
75.0%
100.0%
97.1%
92.9%
Ampicillin
Cotrimoxazole
Cephalothin
Nalidixic Acid
Bacitracin
Aztreonam
Ampicillin
Polimixin B
Cotrimoxazole
Aztreonam
Ciprofloxacin
Cephalothin
Polimixin B
Ampicillin
Nalidixic Acid
74.5%
58.2%
54.3%
53.2%
53.1%
52.1%
68.9%
68.4%
65.5%
47.5%
46.9%
46.6%
80.0%
78.0%
54.5%
14.3%
9.5%
7.1%
Gentamycin
Ceftazidime
Amikacin
76.7%
75.0%
72.7%
Cotrimoxazole
Augmentin
Aztreonam
50.0%
50.0%
47.8%
*Percentage of total number of samples those showed gram positive microbes
(n=717) after laboratory test
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Eldydamouny et al
Table 3: Top three prevalent gram negative microbes by nature of laboratory sample,
antibiotic sensitivity and resistance pattern, Tabuk, Saudi Arabia, 2008
Gram
negative
microbes
Nature of
laboratory
sample
Throat swab
Sample from
1. Klebsiella axilla
Umbilical swab
Blood
High vaginal
swab
Ear swab
Urine
High vaginal
2.
swab
Escherichia
Sputum
coli
Nasal swab
Wound swab
Ear swab
Rectal swab
Eye swab
3.
Wound swab
Pseudomonas Sputum
Sample from
ET/NGT tip
Ear swab
Percentage*
Antibiotic
sensitivity
Percentage* Antibiotic
resistance
Percentage*
70.3%
57.1%
Ciprofloxacin
Amikacin
89.0%
88.9%
Ampicillin
Cotrimoxazole
80.2%
64.4%
52.6%
44.6%
35.0%
Amoxycillin
Gentamycin
Cefotaxime
85.7%
81.1%
72.4%
Cephalothin
Vancomycin
Aztreonam
58.3%
55.2%
52.8%
33.8%
47.0%
33.2%
Ceftriaxone
Amoxycillin
Amikacin
71.1%
100%
93.9%
Bacitracin
Ampicillin
Cotrimoxazole
52.5%
76.0%
69.9%
26.6%
23.5%
22.8%
20.0%
72.7%
47.1%
35.0%
34.4%
33.3%
Gentamycin
Cefotaxime
Ceftriaxone
Ciprofloxacin
Amikacin
Ciprofloxacin
Gentamycin
Bacitracin
80.5%
77.6%
76.7%
72.6%
85.2%
78.1%
75.1%
69.6%
Cephalothin
Polimixin B
Nalidixic Acid
Aztreonam
Ampicillin
Cotrimoxazole
Cephalothin
Vancomycin
Augmentin
59.4%
57.1%
45.3%
42.8%
83.3%
75.5%
69.1%
64.4%
52.8%
Polimixin B
50.0%
29.2%
*Percentage of total number of samples those showed gram negative microbes
(n=1683) after laboratory test
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Eldydamouny et al
Antibiotics are considered as
the essential drugs prescribed by the
physicians to treat infections, although
existing antibiotics are losing their
effect at an alarming pace, day by day.
In one study, fluoroquinolones were
clearly associated with Clostridium
difficile infection, which is a leading
cause of nosocomial diarrhoea and a
major cause of death, worldwide.11
Modern medicine could be seriously
threatened if antibiotic resistance is not
tackled urgently.
DISCUSSION:
In our study, maximum
(64.1%) samples were received from
hospitalized patients, while remaining
35.9% were collected from the
outpatients. Source of the sample can
give an idea about whether the
infection is community acquired or
associated with staying in hospital,
although confirmation depends upon
other clinical and laboratory findings
of patient. Our study revealed that the
lowest proportion (5.7%) of the total
culture positive laboratory samples
was received in the holy month of
Ramadan, indicating the usual
declining number of treatment seeking
patients in the study hospitals for being
‘day time fasting’ during this month.
Rational use of antibiotics may
reduce the chance of development of
opportunistic infections by antibioticresistant bacteria. Moreover, selection
of the appropriate antibiotic that would
target the particular causative pathogen, avoiding antibiotic for a viral
infection such as common cold or flu,
taking antibiotics only according to the
physician’s prescription, not by the
patients themselves, might be the ways
to prevent antibiotic resistance.2,4
Our study findings showed a
similarity with several previous
studies11,12,13,14,
where
increased
presence of gram negative bacilli were
found in respiratory, urinary tract, and
gastro-urinary infections. In our study,
Klebsiella, Escherichia coli, and
Pseudomonas were found respectively
more in throat swab, urine, and rectal
swab [Table 3]. This study also
revealed similar results in relation to
sensitivity and resistance pattern of the
antibiotics against different gram
positive and gram negative microbes as
mentioned in several studies15,16,17,18
conducted previously. Ampicillin
appeared as the most out of date
antibiotic in this study, which is
analogous to the results shown in a
number of earlier studies11,12,13,14. The
rate of Cotrimoxazole resistance
against E. coli was found more than
20% in a study conducted in 19964,
which was found almost 70% in our
study. However, Cotrimoxazole was
found least effective against nearly all
strains of Staphylococcus and Streptococcus in our study.
Our study finding in relation to
the antibiotic resistance warns us to
take immediate steps to tackle the
situation for microbial resistance. The
inevitable fact is that effective antibiotics may not be available to treat
seriously ill patients in the near future,
if the situation continues like this.15
Acknowledgement
The authors acknowledge the
remarkable contribution of Dr. Naela
Ali Diab, (Microbiologist, Maternity
and Child Hospital, Tabuk, KSA). She
initiated this study and without her
great effort it was not possible to be
completed. We would like to thank
Mr. Bander Ghabban (Alwajh
Hospital, KSA) for his tremendous
help and cordial cooperation in data
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EL-MINIA MED. BULL. VOL. 21, NO. 2, JUNE, 2010
collection. We also acknowledge the
significant contribution made by Dr.
M. Al Mamun (Public Health
Specialist Physician, Department of
Primary Health Care and Preventive
Medicine, General Directorate of
Health Affairs in Tabuk Region,
Tabuk, KSA), who thoroughly revised
and edited the full manuscript.
Eldydamouny et al
patient outcomes: Mortality, length of
hospital stay, and health care costs.
Clin Infect Dis ‘06; 42: 82-89.
8. French, GL. Closing the loop:
audit in infection control. J Hosp
Infect. 1993;24:301–308. doi: 10.1016/
0195-6701(93)90062-5.
9. Pellowe, CM; Pratt, RJ; Harper, P;
et al; Guideline Development Group.
Prevention of healthcare-associated
infections in primary and community
care. J Hosp Infect. 2003;55:S5–S127.
10. Hay, A. Audit in infection
control. J Hosp Infect. 2006;62:270–
277. doi: 10.1016/j.jhin.2005.09.008.
11. McCusker ME, Harris AD,
Perencevich E, Roghmann MC (2003).
Fluoroquinolone use and Clostridium
difficile-associated diarrhea. Emerging
Infect. Dis. 9 (6): 730–3.
12. Frost F, Craun GF, Calderon
RL (1998). Increasing hospitalization
and death possibly due to Clostridium
difficile diarrheal disease. Emerging
Infect. Dis. 4 (4): 619–25.
13. Centers for Disease Control
and
Prevention;
retrieved
from
http://www.cdc.gov/ncidod/eid/vol4no4/
frost.htm
14. Kahler J, Acute Infectious
Diarrhea. Department of Emergency
Medicine, University of Michigan
Health System, Ann Arbor, MI.
15. Scheetz, marc h.; hurt, kristin
m. et al. Applying antimicrobial
pharmacodynamics to resistant gramnegative pathogens. American Journal
of Health-System Pharmacy. 63(14):
1346-1360, July 15, 2006.
REFERENCES:
1. West L; Antibiotic Resistance is
Becoming a Serious Health Issue;
retrieved from http://environment.
about.com/od/healthenvironment/a/sup
erbugs.htm
2. Gupta R. Antibiotic Resistant
Bacteria; retrieved from http:// www.
buzzle.com/articles/antibiotic-resistantbacteria.html
3. Ranji SR, Steinman MA, Shojania
KG, Gonzales R. Interventions to
Reduce
Unnecessary
Antibiotic
Prescribing. A Systematic Review and
Quantitative Analysis. Med Care
2008;46:847-862.
4. Antibiotic resistance; retrieved
from http://www.sciencedaily.com/
articles/a/antibiotic_resistance.htm
5. Mestres H. Why do modern
bacteria "resist" antibiotics, confounding medical treatment? Seattle, WA.
Retrieved from www. Keepantibioticsworking.com
6. Cosgrove S, Carmeli Y. The
impact of antimicrobial resistance on
health and economic outcomes. Clin
Infect Dis 2003; 36: 1433-1437.
7. Cosgrove S. The relationship
between antimicrobial resistance and
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