ISSN: 2588-4115; Infection Epidemiology and Microbiology. 2023;9(2):99-106 10.52547/iem.9.2.

99

Molecular Typing of Multidrug-Resistant Pseudomonas

aeruginosa Isolates Obtained from Hospitalized Burn
Patients by Rep-PCR

ARTICLE INFO ABSTRACT

Backgrounds: Multidrug-resistant Pseudomonas aeruginosa is known as a major
Article Type opportunistic pathogen in burn patients with hospital-acquired infections. The aim of this
Original Article study was to investigate antibiotic resistance and the capability of (GTG) 5-PCR (polymerase
chain reaction) assay for molecular typing of P. aeruginosa strains isolated from clinical
Authors samples of hospitalized burn patients in southern Iran.
Nazanin Delroshan, MSc1
Fereshte Ghandehari, PhD1
Materials & Methods: This cross-sectional research was carried out on 70 P. aeruginosa
Rezvan Mirzaei, MSc1 isolates collected from hospitalized burn patients in southern Iran from June 2020 to January
Laleh Hoveida, PhD1* 2021. Antimicrobial susceptibility patterns of the isolates were determined using disk
diffusion method. Additionally, repetitive extragenic palindromic-PCR (rep-PCR) method
was used to examine the genetic similarities among the strains.
Findings: Antimicrobial susceptibility patterns revealed that the highest antibiotic resistance
was against gentamicin (95.8%), followed by imipenem (94.3%) and piperacillin–tazobactam
1
Department of Microbiology, (92.8%), while colistin was the most effective antimicrobial agent. Rep-PCR typing revealed
Falavarjan Branch, Islamic Azad
that 60 P. aeruginosa strains were classified into 49 GTG5 types (G1-G49), which were then
University, Isfahan, Iran
grouped into 12 clusters (A-L) and 10 isolates with unique banding patterns according to the
80% cut off point.
Conclusion: The present study data indicated a substantial resistance to the studied
antimicrobial agents, especially the last-resort antimicrobial agents. In addition, rep-PCR
analysis revealed that most of the evaluated strains had partial genetic diversity; therefore,
infection control activities should be carried out to decrease the colonization of MDR P.
aeruginosa isolates in the hospital setting.

Keywords: Pseudomonas aeruginosa, Drug-resistant, Molecular typing, Burns.

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CITATION LINKS
[1] Rossolini GM, Mantengoli E. Treatment and control of severe ... [2] Moradali MF,
Ghods S, Rehm BH. Pseudomonas aeruginosa lifest ... [3] Karlowsky JA, Jones ME,
Thornsberry C, Evangelista AT, Yee Y ... [4] Brzozowski M, Krukowska Ż� , Galant K, Jursa-
Kulesza J, Kosik- ... [5] Foumani AA, Kalurazi TY, Rostami FM, Ebrahim-Saraie HS, Naza
... [6] Strateva T, Yordanov D. Pseudomonas aeruginosa - a phenomeno ... [7] Parsa P,
* Correspondence Amirmozafari N, Nowruzi B, Bahar MA. Molecular char ... [8] Sorkh MA, Shokoohizadeh
Department of Microbiology, Fala- L, Rashidi N, Tajbakhsh E. Molecular ... [9] Heidari H, Halaji M, Taji A, Kazemian H, Abadi
varjan Branch, Islamic Azad Univer- MS, Taheripou ... [10] Faridi F, Javadpour S. REP-PCR typing, antibiogram pattern, ... [11]
sity, Isfahan, Iran Faghri J, Nouri S, Jalalifar S, Zalipoor M, Halaji M. Invest ... [12] Clinical and Laboratory
E-mail: La.Hoveida@iau.ac.ir Standards Institute. M100-S30: Perfo ... [13] Halaji M, Shahidi S, Atapour A, Ataei B,
Feizi A, Havaei SA. ... [14] Rashno Taee S, Khansarinejad B, Abtahi H, Najafimosleh M,
Gh ... [15] Raman G, Avendano EE, Chan J, Merchant S, Puzniak L. Risk fa ... [16] Nikbin
How to cite this article VS, Aslani MM, Sharafi Z, Hashemipour M, Shahcheraghi ... [17] Khan AA, Cerniglia CE.
Delroshan M., Ghandehari F., Detection of Pseudomonas aeruginosa f ... [18] Ranjbar R, Owlia P, Saderi H, Mansouri
Mirzaei R., Hoveida L. Molecular S, Jonaidi-Jafari N, ... [19] Khosravi AD, Motahar M, Abbasi Montazeri E. The frequency
Typing of Multidrug-Resistant of ... [20] Mobaraki S, Aghazadeh M, Barhaghi MH, Memar MY, Goli HR, Gho ... [21]
Pseudomonas aeruginosa Isolates Goli HR, Nahaei MR, Rezaee MA, Hasani A, Kafil HS, Aghazadeh ... [22] Fazeli H, Solgi
Obtained from Hospitalized Burn H, Havaei SA, Shokri D, Norouzi Barogh M, Za ... [23] Kashfi M, Hashemi A, Eslami G,
Patients by Rep-PCR. Infection
Sadredin Amin M, Tarashi S, T ... [24] Banar M, Emaneini M, Satarzadeh M, Abdellahi
Epidemiology and Microbiology.
2023;9(2): 99-106. N, Beigverdi R, ... [25] Zarei-Yazdeli M, Eslami G, Zandi H, Kiani M, Barzegar K, Ali ...
[26] Coetzee E, Rode H, Kahn D. Pseudomonas aeruginosa burn wound ... [27] Singh
[ DOI: 10.52547/iem.9.2.99 ]

NP, Goyal R, Manchanda V, Das S, Kaur I, Talwar V. Cha ... [28] Song W, Lee KM, Kang HJ,
Shin DH, Kim DK. Microbiologic aspe ... [29] Vaez H, Salehi-Abargouei A, Ghalehnoo ZR,
Khademi F. Multidr ... [30] Tarafdar F, Jafari B, Azimi T. Evaluating the antimicrobial
Article History ... [31] Khan F, Khan A, Kazmi SU. Prevalence and susceptibility patt ... [32] Mirzaei
Received: December 13, 2022 B, Bazgir ZN, Goli HR, Iranpour F, Mohammadi F, Baba ... [33] Doléans-Jordheim A,
Accepted: June 03, 2023 Cournoyer B, Bergeron E, Croizé J, Salor ...
Published: August 19, 2023

Copyright@ 2023, TMU Press. This open-access article is published under the terms of the Creative Commons Attribution-NonCommercial 4.0
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 Molecular typing of P. aeruginosa 100

Introduction 2021, a total of 70 P. aeruginosa isolates were

Pseudomonas aeruginosa is one of the most collected from the specimens of hospitalized
widespread opportunistic bacteria, which burn patients in a teaching hospital in Ahvaz,
often lives in moist environments and causes southern Iran. P. aeruginosa strains were
serious infections in patients and rarely isolated from a variety of clinical samples,
infects healthy hosts [1-5]. Empirical therapies including biopsy, wound, blood, and sputum
including monotherapy (e.g., carbapenem, specimens.
ceftazidime, cefepime, piperacillin, or The specimens were cultured on MacConkey
piperacillin-tazobactam) and combination agar and blood agar (Merck, Germany) and
therapy (an antipseudomonal b-lactam with incubated at 37 °C for 24 hrs. P. aeruginosa
an aminoglycoside or a fluoroquinolone) are isolates were identified based on standard
used to treat P. aeruginosa infected cases [1, 3, 6]. microbiological tests and the presence of the
However, treatment of P. aeruginosa infections tox-A gene (genotypic method) [11].
in burn patients could be a major challenge as All P. aeruginosa isolates were investigated for
this organism is intrinsically resistant to many susceptibility against six antibiotics by Kirby-
available antibiotics and rapidly develops Bauer disk diffusion susceptibility method
resistance to all effective antimicrobial according to Clinical and Laboratory Standards
medicines during treatment [1]. Institute (CLSI, 2020) guidelines [12].
Understanding the local molecular The tested antibiotics (Mast Group Ltd.,
epidemiology of P. aeruginosa is necessary UK.) were imipenem (10 μg), gentamicin
to control the spread of this bacterium in (30 μg), ciprofloxacin (5 μg), ceftazidime
hospital settings [7]. Among PCR (polymerase (30 μg), piperacillin– tazobactam (100/10
chain reaction) based genotyping methods, μg), and colistin (10 μg). P. aeruginosa ATCC
repetitive extragenic palindromic-PCR (rep- 27853 was also tested as the quality control.
PCR) as a straightforward, reliable, and E-test was used to evaluate the antimicrobial
reproducible typing technique is appropriate susceptibility of P. aeruginosa isolates against
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for local typing of Gram-negative enteric colistin. Non-susceptibility to at least one agent
bacteria [8, 9]. It is an extragenic typing in three or more antibiotic chemical classes
technique that targets bacterial genomic was defined as multidrug resistance (MDR).
areas of repetitive non-coding sequences Genomic DNA was extracted by a simple
[10]
. Given the significance of P. aeruginosa boiling method according to the method
infections in patients with burn injuries, previously described [13]. PCR was performed
little information is available about the to detect the toxA gene using specific
molecular characteristics of these isolates in primers [14]. PCR amplification included an
nosocomial infections. initial denaturation step at 95 °C for 5 min,
Objectives: The purpose of this study was followed by 35 cycles of denaturation at
to determine genotypic relationships and 95 °C for 60 s, annealing at 68 °C for 45 s,
distribution of antibiotic resistance among and extension at 72 °C for 1 min. The final
P. aeruginosa isolates obtained from burn extension step was performed at 72 °C for 5
patients in a teaching burn hospital in Ahvaz, min. After electrophoresis of amplification
southern Iran. products on 1% agarose gel (with safe stain
dye (CinnaGen Co. Iran)), the presence of
[ DOI: 10.52547/iem.9.2.99 ]

Materials and Methods expected fragments was analyzed.

In this cross-sectional study conducted All P. aeruginosa isolates were analyzed by
during 7 months from June 2020 to January rep-PCR, and the primer sequence was 5'–

Infection Epidemiology and Microbiology Spring 2023, Volume 9, Issue 2

 101 Delroshan M. et al.

GTG GTG GTG GTG GTG-3'. For molecular to all antibiotics, except colistin, and only
typing of P. aeruginosa isolates, rep-PCR one out of 70 isolates was susceptible to all
was done as described previously [14]. tested antibiotics. The susceptibility rates
Genetic relationships among P. aeruginosa of the isolates to the studied antibiotics are
isolates were analyzed using GelJ software presented in Table 1.
Version 2.0, and isolates with a similarity Dendrogram and gel electrophoresis images
coefficient equal to or above 80% were of rep-PCR products are showed in Figure 1.
classified into the same genotypes. The number of fragments varied from 3 to
10 per strain, and the size of rep-PCR bands
Findings ranged from 100 to 1.5 kb. In this study, out
During the 7-month study period, 70 P. of 70 P. aeruginosa isolates, 10 isolates did
aeruginosa isolates were obtained. Overall, not show any product in the reactions and
out of 70 confirmed P. aeruginosa isolates thereby were non-typeable. Rep-PCR typing
from various clinical specimens, 51.5 revealed that 60 P. aeruginosa strains were
and 48.5% were obtained from male and classified into 49 GTG5 types (G1-G49).
female patients, respectively. Most of the According to the 80% cut off point, these
isolates were obtained from burn-wound types were grouped into 12 clusters (A-L)
biopsy samples (63%), followed by blood and 10 isolates with unique banding patterns
culture (27%), wound swab (5.7%), and and distinct genotypes not belonging to any
sputum (4.3%) specimens. According to the cluster. Some P. aeruginosa strains were
findings, 51.4% of the strains were isolated 100% similar in terms of electrophoretic
from patients in the intensive care unit band pattern, and as a result, these strains
(ICU). were classified in a GTG, such as G24, G34,
Among 70 P. aeruginosa isolates, resistance and G40. Cluster A was the most common
to gentamicin was the most prevalent rep-type, including 11 (18.3%) isolates,
(95.8%), followed by imipenem (94.3%) followed by cluster B (eight isolates, 13.3%)
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and piperacillin– tazobactam (92.8%). None and C (seven isolates, 11.6%). However,
of the isolates were found to be resistant the rep-PCR analysis results showed
to colistin. According to MDR definition, high genetic diversity among most of the
66 (94%) isolates were identified as MDR, examined strains. The distribution of rep-
most of which belonged to the ICU ward. types in different hospital wards is shown in
Moreover, 52 (74%) isolates were resistant Table 2.

Table 1) Antibiotic susceptibility pattern of P. aeruginosa isolates obtained from burn patients in this study

Sensitive Intermediate Resistant

Antimicrobial Agent
No (%) No (%) No (%)

Gentamicin 2 (2.8) 1 (1.4) 67 (95.8)

Imipenem 4 (5.7) - 66 (94.3)

Piperacillin-tazobactam 5 (7.2) - 65 (92.8)

Ceftazidime 9 (12.8) - 61 (87.2)

[ DOI: 10.52547/iem.9.2.99 ]

Ciprofloxacin 11 (15.7) 2 (2.8) 57 (81.5)

Colistin 70 (100) - -

Infection Epidemiology and Microbiology Spring 2023, Volume 9, Issue 2

 Molecular typing of P. aeruginosa 102

Table 2) Frequency of rep types of Pseudomonas aeruginosa isolates in different hospital wards

Rep-Types
(No. of Isolates)
Wards (No.)
A B C D E F G H I J K L Unique

ICU (29) 7 4 4 1 2 3 2 2 2 2

Pediatric (10) 1 1 1 2 1 4

Men (10) 1 1 2 1 1 4

Surgery (6) 1 2 1 1 1

Women (5) 1 2 1 1

Total (60) 11 8 7 4 3 3 2 2 2 2 2 4 10

Discussion obtained from wound infection [18]. In this

Due to the intrinsic and acquired regard, Faghri et al. (2018) reported that P.
antimicrobial resistance of P. aeruginosa aeruginosa strains were typically isolated
strains and the emergence of MDR isolates from the ICU ward (50%) and different
in clinical settings, it is difficult to identify clinical samples [11].
an antibiotic that could effectively treat In the present research, colistin was the
infections caused by these bacteria [15]. most effective antibacterial agent with
This study investigated the antibiotic a sensitivity rate of 100% based on the
susceptibility and (GTG) 5-PCR fingerprinting antibiotic susceptibility pattern, while the
of P. aeruginosa strains isolated from majority of P. aeruginosa isolates showed high
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hospitalized burn patients in a burn center antibiotic resistance to other antimicrobials.

in Ahvaz, Iran. In this study, in addition In accordance with these findings, Goli et
to phenotypic methods, PCR was used to al. (2017) and Mobaraki et al. (2018) in the
identify the toxA gene, which is specific to P. northwest of Iran and Khosravi et al. (2017)
aeruginosa, and only the strains that harbored in Ahvaz have also reported colistin as the
this gene were included in the study. Exotoxin most effective antibiotic in the treatment
A is regulated by the toxA gene, leading to and management of nosocomial infections
inhibition of protein biosynthesis and tissue [19-21]
. In another study performed by Fazeli
damage in the host. Therefore, the exotoxin et al. (2014) [22] in Isfahan, a lower resistance
A gene was used to detect and confirm P. rate was reported against cephems and
aeruginosa isolates. Identification of the toxA quinolones. In their study, 63 and 63.1% of
gene as a genotypic method has previously the isolates were resistant to ciprofloxacin
been shown in other studies [16, 17]. and ceftazidime, respectively, while in the
In this study, P. aeruginosa strains were present study, resistance to ciprofloxacin
mostly isolated from burn-wound biopsy and ceftazidime was higher, which shows
(63%) and blood culture (27%) samples, and the increasing trend of antibiotic resistance
more than half of them were obtained from in hospitalized patients. This may also be
[ DOI: 10.52547/iem.9.2.99 ]

the ICU ward. This finding is in agreement related to the type of infection; for example,
with the finding of another study by Ranjbar in a study performed by Kashfi et al. (2017)
et al. (2011), where most of the isolates were on patients with burn infection, antibiotic

Infection Epidemiology and Microbiology Spring 2023, Volume 9, Issue 2

 103 Delroshan M. et al.

resistance to ciprofloxacin and ceftazidime determine the genotype and investigate the
was reported to be 94 and 75%, respectively genetic features and genetic relatedness
[23]
. In the present study, the highest antibiotic of P. aeruginosa strains isolated from
resistance was observed against gentamicin the studied specimens [7, 33]. The rep-PCR
(95.7%), which is consistent with the results analysis results indicated high genetic
of the studies conducted by Banar et al. diversity among most of the examined
(2016) and Zarei-Yazdeli et al. (2018) [24, strains. In this study, 49 GTG5 types were
25]
. Different gentamicin resistance rates found among 60 P. aeruginosa strains typed
have been reported in different studies; for by rep-PCR, although some of GTG5 types
example, in the studies performed by Song et such as G24, G34, and G40 were common
al. (2001) and Singh et al. (2003), resistance in several isolates. Also, in present study,
to gentamicin was observed in 20 and 31% according to the 80% cut off point, these
of the isolates, respectively, while in the types were grouped into 12 clusters (A-
study conducted by Coetzee and colleagues L) and 10 isolates with unique banding
(2013), gentamicin resistance rate was 92% patterns. This study results also showed
[26-28]
. This difference in gentamicin resistance that the highest genetic diversity and
rates in different studies is probably due distribution of rep types was related
to variation in the type of infection, sample to the ICU; on the other hand, most of
examined, or geographical area. the isolates that showed the lowest and
In this study, 66 (94%) isolates were resistant highest antibiotic resistance (diversity in
to at least three classes of antibiotics, and antibiotic susceptibility) were obtained
they actually exhibited an MDR pattern; from the ICU ward, which is consistent
also, 52 (74%) strains were resistant to all with the rep-PCR results. The greater the
antibiotics, except colistin. In a meta-analysis number and size of clusters in a hospital,
study conducted by Vaez et al. (2018) in the more contamination and circulation of
Iran, the frequency of MDR P. aeruginosa genetically diverse bacteria in the hospital.
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in different parts of Iran was 58%, and the In the current study, clusters A, B, and C had
highest (100%) and lowest (16%) frequency the highest number of strains, indicating
of MDR P. aeruginosa was observed in that the strains related to these clusters are
Tehran and Zahedan, respectively [29]. In a more circulating in the hospital. Similarly,
study performed by Tarafdar and colleagues Ghaleh Sorkh et al. (2017) found that P.
in 2018-2019, similar proportions of MDR aeruginosa strains isolated from this burn
P. aeruginosa were observed in patients center had a significant level of genotypic
admitted to a teaching hospital in Tehran, variability (20 common types of A-T and 20
and 100% of all isolates were MDR [30]. unique types among 75 strains) according
In contrast to the current study results, Khan to rep-PCR analysis [8]. In contrast to the
and colleagues (2014) reported a lower present study results, Faridi and Javadpour
incidence rate of MDR P. aeruginosa isolates (2015) in Bandar Abbas reported only seven
in hospitals in Karachi, Pakistan, where genotypic clusters among 67 P. aeruginosa
30% of isolates were MDR [31]. Additionally, isolates, indicating less genetic diversity
a research performed in the northeast of among the isolates [10]. However, the genetic
Iran found that the prevalence of MDR P. diversity and antibiotic resistance of P.
[ DOI: 10.52547/iem.9.2.99 ]

aeruginosa was 16.5% [32], which is lower aeruginosa strains might help these strains
than the present study finding. survive in the environment.
An essential matter in infection control is to

Infection Epidemiology and Microbiology Spring 2023, Volume 9, Issue 2

 Molecular typing of P. aeruginosa 104
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[ DOI: 10.52547/iem.9.2.99 ]

Figure 1) Dendrogram showing relatedness between rep-PCR patterns of 60 Pseudomonas aeruginosa strains
isolated in this study

Infection Epidemiology and Microbiology Spring 2023, Volume 9, Issue 2

 105 Delroshan M. et al.

Conclusion 3. Karlowsky JA, Jones ME, Thornsberry C,

In summary, the high rate of antibiotic Evangelista AT, Yee YC, Sahm DF. Stable
antimicrobial susceptibility rates for clinical
resistance of P. aeruginosa strains in the isolates of Pseudomonas aeruginosa from the
current study is a serious concern in 2001-2003 tracking resistance in the United
hospital wards because it is difficult to States today surveillance studies. Clin Infect Dis.
prevent infections caused by such drug- 2005;40(Suppl 2):S89-98.
4. Brzozowski M, Krukowska Ż� , Galant K,
resistant strains. The rep-PCR analysis Jursa-Kulesza J, Kosik-Bogacka D. Genotypic
results demonstrated high genetic diversity characterisation and antimicrobial resistance of
among P. aeruginosa strains, and this might Pseudomonas aeruginosa strains isolated from
complicate the treatment of illnesses caused patients of different hospitals and medical centres
in Poland. BMC Infect Dis. 2020;20(1):1-9.
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Saraie HS, Nazari-Alam A, Halaji M. Epidemiology
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Not applicable. patients in Iran: A systematic review and meta-
analysis. Infez Med. 2020;28(3):314-21.
Ethical permissions: The present study 6. Strateva T, Yordanov D. Pseudomonas aeruginosa
was conducted in accordance with the - a phenomenon of bacterial resistance. J Med
declaration of Helsinki and evaluated and Microbiol. 2009;58(9):1133-48.
approved by the Ethics Committee of Islamic 7. Parsa P, Amirmozafari N, Nowruzi B, Bahar MA.
Molecular characterization of polymorphisms
Azad University, Falavarjan Branch, Isfahan, among Pseudomonas aeruginosa strains
Iran (IR.IAU.FALA.REC.1398.061). However, isolated from burn patients' wounds. Heliyon.
the ethics committee waived the need for 2020;6(12):e05041.
informed consent since only medical records 8. Sorkh MA, Shokoohizadeh L, Rashidi N, Tajbakhsh
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[ DOI: 10.52547/iem.9.2.99 ]

aeruginosa strains isolated from burn patients.

Arch Clin Infect Dis. 2017;12(1):e40896.

Infection Epidemiology and Microbiology Spring 2023, Volume 9, Issue 2

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