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Research Article
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Antibiotic Resistance Pattern among Biofilm Producing and Non Producing Proteus Strains Isolated from Hospitalized Patients; Matter of Hospital Hygiene and Antimicrobial Stewardship |
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Houshang Shikh-Bardsiri
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Mohammad Reza Shakibaie
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ABSTRACT
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A retrospective study on antimicrobial susceptibility and
biofilm production were carried out for eighty eight strains of Proteus
strains isolated from UTI and other hospital samples during April 2011-April
2012. The antibiotic susceptibility was carried out by Kirby-Bauer disk diffusion
and MIC by E-test. Biofilm production was measured by microtiter method and
confirmed by Scanning electron microscopy. Plasmids from biofilm producing isolates
were detected by alkaline lysis technique. From 88 patients infected by proteus
species, 58% were female and 42% were mail. The most frequent age range was
20-29 (77.39%) and the least were 60-69 years old (3.4%) (p = 0.05). Eighty
one isolates were identified as P. mirabilis while, 7 identified as P.
vulgaris. 67.04% [n = 59] of the isolates showed MIC range (16-32±0.05
μg mL-1) to ceftriaxone, 46.59% [n = 41] exhibited least MIC
range to chloramphenicol (8-64±0.08 μg mL-1). 31% [n
= 28] of the isolates also exhibited MIC range 1-4 μg mL-1 to
ciprofloxacin. 17% [n = 15] of the isolates exhibited strong biofilm while,
6% [n = 6] did not show any biofilm (p≤0.05). Plasmid isolation from biofilm
producing isolates revealed that stains number 19, 24 and 87' that produced
strong biofilm carried similar high M. Wt. plasmid. From above results it can
be concluded that the majority of Proteus isolated from UTI patients were belong
to P. mirabilis. Ciprofloxacin was the most effective antibiotic for
treatment of the infected patients. Limited number of the isolates could produce
strong biofilm that were bearing plasmids. Majority of the biofilm producing
isolates were also resistance at least to 4 antibiotics routinely prescribed
in our hospital.
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How
to cite this article:
Houshang Shikh-Bardsiri and Mohammad Reza Shakibaie, 2013. Antibiotic Resistance Pattern among Biofilm Producing and Non Producing Proteus Strains Isolated from Hospitalized Patients; Matter of Hospital Hygiene and Antimicrobial Stewardship. Pakistan Journal of Biological Sciences, 16: 1496-1502. DOI: 10.3923/pjbs.2013.1496.1502 URL: https://scialert.net/abstract/?doi=pjbs.2013.1496.1502
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Received: January 22, 2013;
Accepted: March 03, 2013;
Published: May 08, 2013
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INTRODUCTION
Gram negative bacteria especially E. coli, Klebsiella, Serratia
and Proteus are important source of hospital associated infection in
many parts of the worlds. The important features of these bacteria are resistance
to different antibiotics which their genes usually carried on large molecular
weight plasmids (Lied, 2011; Khan
and Musharraf, 2004). Plasmids not only play important role in antibiotic
resistance phenomenon but also they probably can mediate the biofilm formation
using component of signal transduction system (Hola et
al., 2012; Tenke et al., 2006; Ghigo,
2001). Production of biofilm enables bacterium to attach to hospital devise
like catheter and withstand the antimicrobial activity of various antibiotics
(Saint and Chenoweth, 2003; Sharp
et al., 1974). Proteus mirabilis is main species that can
cause wide range of infections including urinary tract, blood and burn (Mozafari
Nia et al., 2011). This organism was often associated with Urinary
Tract Infections (UTI) in patients carried mechanical devices such as catheter
(Jacobsen and Shirtliff, 2011; Stickler,
2008). Urinary tract infections are very painful and can become lethal if
the infection spreads to other organ in the body (Warren
et al., 1987). Antibiotic resistant phenotypes of P. mirabilis
were reported by various authors (Coker et al.,
2000). In one study, Sabbuba et al. (2002)
examined the ability of organisms to stick to hospital devices. It was found
that, the swarmer cells of Proteus mirabilis migrated over all four types of
catheter such as hydrogel-coated latex, hydrogel/silver-coated latex, silicone-coated
latex and silicone.
Ability of P. mirabilis to attach in the hospital devices is mainly
due to biofilm production in this organism. It is reported that biofilms developed
by P. mirabilis is increasing source of catheter associated UTI infection
in the hospitals (Stickler et al., 1993). Majority
of patients also exhibited ascending urinary tract infection and pyelonephritis
(Hochreiter et al., 2003; Stickler
and Morgan, 2006).
It was known that treatment of catheter associated UTI was very difficult and
recurrent infection may occur in 62% of the patients (Absalon
et al., 2012).
P. mirabilis not only can produce infection in urinary tract but also
it can cause super infection in severely burn patients. Biofilm formation and
antibiotic resistance play important role in this phenomenon too (McManus
et al., 1982). Khan and Musharraf (2004)
studied drug resistance pattern and plasmid content of hospital isolates of
P. mirabilis. It was found that that this infection is more common in
young pregnant women. Catheter associated biofilm formation by P. mirabilis
found to be in both motile wild type and non motile mutant have same ability
to stick on the surface of catheter (Jones et al.,
2007).
Multiple antibiotic resistant P. mirabilis has created serious concern
in treatment of catheter associated UTI infections. The colonization of catheters
by biofilm producing strains of P. mirabilis and easy excess to urinary
tract caused treatment failure due to antibiotic resistance biofilm producing
strains.
The aim of this investigations were; to isolate Proteus species from
hospitalized patients, to study biofilm production and antibiotic sensitivity
of the isolates, finally to detect plasmid from those isolates that show strong
biofilm.
MATERIALS AND METHODS
Sampling and bacterial identification: Eighty eight strains of proteus
strains were collected from urinary tract and other sites patients hospitalized
in different hospitals in Kerman, Iran during April-2011 to April-2012. The
sample size was selected according to published paper (Mozafari
Nia et al., 2011). The sample from urinary tract catheter was obtained
by scraping of the biofilm with the help of sterile blade and inoculated in
to 2 mL sterile Stuart Transport (ST) medium while, the urine samples were obtained
from mid portion of urine and centrifuged. 0.1 mL of the lower part was then
inoculated into sterile ST medium. Both the samples were transferred to the
department of microbiology for further analysis within 1 to 2 h of sampling.
In case of burn and pulmonary infections, the samples were collected with the
help of sterile swabs and inoculated into 1 mL ST medium as previously suggested.
A loopful of the bacterial culture was suitably diluted (10-2) with
sterile 0.1 N normal saline and streaked onto MacConkey and sheep blood agar
medium (Merck, Germany), the plates incubated for 24 h at 37°C. Bacterial
identification were performed by routine microbiological tests such as gram
reaction, motility, ability to ferment lactose, H2S, Urease production,
Phenyl Alanine Deaminase (PAD), Lysine Decarboxylase (LDC), MR, VP and Indole
tests. The identified isolates were mixed with 40% glycerol in True NorthTM
Cryogenic Vials (TNC) containing 1mL sterile Trypticase Soy Broth (TSB) and
preserved at -70°C for further investigation.
Antibiotic sensitivity tests: Preliminarily antibiotic sensitivity of
the above isolates was determined by Kirby-Baur disk diffusion break point method
using following antibiotic disks; Ciprofloxacin (Cf) [5 μg/disk], Amikacin
(AK) [30 μg/disk], Kanamycin (K) [30 μg/disk], Gentamicin (Gm) [10
μg/disk], Cefotaxime (CE) [30 μg/disk], Ceftrixone (CI) [30 μg/disk],
Cefazoline (CZ) [30 μg/disk] and Chloramphenicol (C) [30 μg/disk].
All antibiotic disks were purchased from Padtan-Teb (Tehran, Iran). 0.1 mL of
each proteus isolate at 1x108 CFU mL-1 were inoculated
into Muller-Hinton agar (MHA) [Hi-media, India] and spread throughout medium
with the help of a sterile swab. The antibiotic disks (five disks in each plate)
were then kept on the surface of each plate and incubated at 37°C for 24
h. The zone of inhibition surrounding each disk was measured and labeled as
resistance, intermediate, sensitive according to CLS procedure (CLSI,
2009). Minimum Inhibitory Concentration (MIC) of above antibiotics against
the isolates was carried out by E-test. Inoculated plates were allowed to dry
before E-test strips were applied to the medium. E-test inoculum preparation
and plating, strip application and subsequent MIC determinations were carried
out in accordance with the manufacturers instructions and CLSI guidelines
(CLSI, 2009). P. mirabilis ATCC 29906 was included
as a control strain for susceptibility testing.
Biofilm production by microtiter plate method: The biofilm production
of the above Proteus isolates was determined by microtiter method as described
previously (Stepanovic et al., 2007). Briefly,
one loopful of colony from proteus isolates was inoculated into a 2 mL sterile
TSB medium containing 1% v/v glucose to optimize biofilm production. Optical
Density (OD) was adjusted to 650 nm (106 CFU mL-1) and
with final dilution (1:40). One hundred micro liter of the each bacterial growth
was added to two parallel Elisa-Reader wells (TeCan-Austria). Similarly, 100
μL of the medium was added to the two well without any bacterium (negative
control). The microtiter plate was kept under static condition. After 24 h at
37°C, no adherent cell suspensions were aseptically aspirated and replaced
with 10 μL 0.1 N sterile phosphate buffer (pH-7.5). One hundred and fifty
micro liter concentrated methanol was then added to each well and kept at room
temperature (24°C) for 10 min in order to fix the biofilm. The methanol
was slowly removed and replaced with 200 μL of 1% crystal violet dye. The
plates containing biofilm matrix then washed slowly with tape water and kept
at room temperature till dried. To this preparation, 160 μL glacial acetic
acid (33% v/v) was added and the optical density of each well was measured at
570 nm. Duplicate set was run at a time.
Biofilm detection by scanning electron microscope (SEM): SEM analysis
was done according the method described previously (Pour
et al., 2011). Briefly, One loopful growth of the biofilm producing
isolates from TSB medium on Elisa-Reader wells was transferred aseptically into
sterile petriplate containing 10 mL glutraldehyde (10% v/v) in double distilled
water at different time intervals (8, 16 and 24 h) and kept at 4°C overnight.
The samples were mounted on the standard specimen stubs and then placed on the
microscopic grids. The grids were coated with thin layer of gold. Samples were
observed with magnification of EHT 10.000 (11 WD) using Scanning Electron Microscope
(Philips-Holland). The experiment was repeated twice to check the genuinety
of the biofilm formation. The micrograph of the each sample at different time
interval was recorded by a camera attached to the high resolution recording
unit. A negative control consist of an isolate with no biofilm was taken along
the tests experiment.
Plasmid isolation from biofilm producing isolates: Plasmids from biofilm
producing Proteus strains were isolated by Birnboim and Doly alkaline
lysis technique (Birnboim and Doly, 1979) and observed
on 0.7% agarose gel. Electrophoresis was conducted for 4 h at 60 volt (35mA)
using 500 mL Tris-Borate-EDTA (TBE) buffer (pH-8.3) and plasmid bands were photographed
by a camera attached UV gel documentation system (UV Tech-Cambridge) after stained
with 0.5 μg mL-1 ethidium bromide.
Statistical analysis: The difference in susceptibility patterns was
analyzed by the Chi-square or two-tailed Fisher exact test. The significance
of the biofilm form by eighty eight isolates were analysed by using a one-way
analysis of variance (ANOVA). A p<0.05 was considered as statistically significant.
RESULTS
Bacterial distribution: Retrospective distribution of Proteus
strains among eighty eight hospitalized patients infected by this bacterium
according to age during showed that. Overall, 37 (42%) were male and 51 (58%)
were female (Table 1). The most frequently infected patients
by proteus species were in the range of 20-29±0.08 and least people infected
were in the range of 60-69±0.02 years old. 92.2% of the isolates were
collected from urinary tract and remaining 5.6% isolated from burn patients
and 2.2% from the other body sites (p = 0.05). In this study only seven isolates
were belong to P. vulgaris and remaining were all belong to P. mirabilis.
The colonies on MacConkey agar were circular, smooth, convex, translucent, mucoid,
nonpigmented and the lactose utilization test for all isolates was negative.
They were gram-negative short rod, highly motile and exhibited swarming on both
MacConkey and bloodagar medium.
Antibiotic sensitivity: The results of the antibiotic susceptibility
of the above isolates are shown in Table 2 and 3.
The results revealed that, 67% (n = 59) of the isolates were highly resistant
to ceftriaxone with MIC range 16-32 μg mL-1 while majority of
the isolates were sensitive or intermediate to ciprofloxacin with MIC range
1-4 μg mL-1.
Table 1: |
Distribution of Proteus strains isolated from patients
in Kerman hospitals according to ages |
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Table 2: |
Antibiotic susceptibility of eighty eight Proteus strains
isolated from patients to eight antibiotics routinely used in the hospital
for treatment of UTI patients |
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Muller-Hinton agar was used for susceptibility testing, Inoculum
diluted to obtain 1x108 CFU mL-1, Ciprofloxacin (Cf)
[5 μg/disk], Amikacin (AK) [30 μg/disk], Kanamycin (K) [30 μg/disk],
Gentamicin (Gm) [10 μg/disk], Cefotaxime (CE) [30 μg/disk], Ceftrixone
(CI) [30 μg/disk], Cefazoline (CZ) [30 μg/disk] and Chloramphenicol
(C) [30 μg/disk] |
29.54% of the isolate were resistant to kanamycin while, 46.59% were resistant
to amikacin with MIC range 4-64 μg mL-1 (Table
3). The isolates also exhibited high degree of resistance to cefotaxime
with MIC range 2-64 μg mL-1. The majority of P. mirabilis
isolates tolerated concentrations exceeding 64 μg mL-1 of antibiotics
from third generation of cephalosporins while, MIC to gentamycin did not exceed
16 μg mL-1 as shown in Table 3.
Biofilm production: Biofilm quantification of proteus isolates revealed
that 6.8% (n = 6) of the isolates did not show any biofilm while, 36% (n = 32)
exhibited weak, 39.7% (n = 35) showed intermediate biofilm and 17.4% (n = 15)
demonstrated strong biofilm activity.
Table 3: |
Minimum inhibitory concentration (MIC) of o eight antibiotics
against eighty eight strains of Proteus that isolated in this study |
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MIC was measured by E-test, The inoculum concentration was
adjusted to 1x108 CFU mL-1, The difference in susceptibility
patterns (MIC50 and MIC90 was analyzed by the Chi-square
and two-tailed Fisher exact test |
Quantification of biofilm production among proteus strains are shown in Fig.
1. The results were further confirmed by SEM technique as shown in Fig.
2a-c.
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Fig. 1: |
Percentage of biofilm production among Proteus strains
isolated in this study, OD: Was measured at 570 nm. NB: No biofilm |
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Fig. 2(a-c): |
Scanning electron micrograph of biofilm production among
strong biofilm producing Proteus isolates during (a) 8 h, (b) 16
h and (c) 24 h incubation in microtiter plate |
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Fig. 3: |
Agarose gel electrophoresis of plasmid isolated from strongly
producing Proteus strains isolated in this study. Electrophoresis
was conducted for 4 h at 60 volt (35 mA) using 500 mL Tris-Borate-EDTA (TBE)
buffer (pH-8.3), Lines 1 to 8 were plasmid bands from isolates No. 19, 29,
8, 31, 7, 87, 24 and 54 |
The result of SEM suggest that as time of incubation in microtiter increased,
the quantity of biofilm production was also increased and reached to a maximum
within 24 h.
Plasmid isolation: Plasmid isolation from strongly producing biofilm
Proteus strains revealed that the isolate number 19, 8, 31, 7, 87, 24
and 54 carried similar high molecular weight plasmid. Those strains with no
biofilm or weak biofilm did not carry any plasmid. The experiment repeated twice
and similar observations were made. Isolate number 29 though exhibited strong
biofilm but did not carry any plasmid as shown in Fig. 3.
DISCUSSION
The urinary tract catheters are usually used to remove urine from patients
for any reason cannot do normal urination (Trautner and
Darouiche, 2004). The problem with catheter is that they are prone to contamination
and can easily cause UTI in hospitalized patients using them (Ramsay
et al., 1989; Adegbola et al., 1983;
Allison et al., 1992). The urinary tract infection
is not only important from treatment point of view but also increase considerably
the cost of therapy for those patients dependent on them. Majority of the bacteria
associated with catheters are resistance to many antibiotics. Previous studies
have identified an important association between the administration of inadequate
antimicrobial treatment of UTI infection due to biofilm and hospital mortality
(Stickler, 2008).
Tambyah et al. (1999) reported annually one
million of people are infected with contaminated catheter and Escherichia
coli remains the predominant uropathogen isolated in acute community-acquired
uncomplicated infections, followed by Staphylococcus saprophyticus Klebsiella,
Enterobacter and Proteus species (Johnson
et al., 1993). In one study in Argentina (Aiassa
et al., 2010), it was found that the biofilm producing Proteus
were resistant to ciprofloxacin. Proteus species are playing important role
in urinary stone formation by changing the pH of urine due to urease production
(Morris and Stickler, 1998).
In this study we found that the P. mirabilis were frequently infected
UTI people (92.2%) and women contributed the majority of patients (58%). This
may be due to close vicinity of urinary tract with vagina. Among biofilms producing
strains, only 17.4% could produce strong biofilm and all except one (isolate
number 29) carried similar high M.Wt. plasmid. In present study we found that
as the time passes the biofilms formation was also increased and it reaches
to a plateau after 24 h of incubation. This may be due to increase in production
of autoinducer like oxo-dodecaoyl-homoserine lactone (HSL) by this organism.
Cox and Hukins (1989) found that the shape of solid
substrate also play role in biofilm formation. it was also found that as the
length of cathetrization was increased the chance of catheter infection by Proteus
was also increased.
The susceptibility and antibiotic resistance pattern of Proteus strains isolated
from our hospitals revealed that, the majority of the isolates were simultaneously
resistance to at least four antibiotics (ceftriaxone, cefotaxime, amikacin and
gentamicin) routinely used in our hospitals for treatment of UTI and therefore
created problem in therapy of infection caused by this organism. Biofilm producing
strains of P. mirabilis found to be play Key role in multiple drug resistance
phenomenons in this study.
In Iran a few research were carried out in this subject, in one case, Dalal
et al. (2005) isolated 300 UTI samples isolated from ImamKhomini
hospital in Tehran. It was found that P. mirabilis was second position
among isolates. The results showed amikacin, ciprofloxacin and nalidixic acid
were most efficient antibiotics.
Further research must be performed regarding cloning and sequencing of biofilm
genes in this organism. Expression of the genes involved in biofilm production
among Proteus species and how to overcome the biofilm formation.
ACKNOWLEDGMENTS
The authors would like to thank the authority of Kerman University of Medical
Science for Research for financial support and Department of Microbiology School
of Medicine for providing facilities for this study. We also thank Kerman blood
transfusion center for providing help during this investigation.
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