7.2
CiteScore
3.7
Impact Factor
Generic selectors
Exact matches only
Search in title
Search in content
Post Type Selectors
Search in posts
Search in pages
Filter by Categories
ABUNDANCE ESTIMATION IN AN ARID ENVIRONMENT
Case Study
Correspondence
Corrigendum
Editorial
Full Length Article
Invited review
Letter to the Editor
Original Article
Retraction notice
REVIEW
Review Article
SHORT COMMUNICATION
Short review
7.2
CiteScore
3.7
Impact Factor
Generic selectors
Exact matches only
Search in title
Search in content
Post Type Selectors
Search in posts
Search in pages
Filter by Categories
ABUNDANCE ESTIMATION IN AN ARID ENVIRONMENT
Case Study
Correspondence
Corrigendum
Editorial
Full Length Article
Invited review
Letter to the Editor
Original Article
Retraction notice
REVIEW
Review Article
SHORT COMMUNICATION
Short review
View/Download PDF

Translate this page into:

Review
12 2021
:33;
101610
doi:
10.1016/j.jksus.2021.101610

Colistin-resistant Gram-negative bacteria in Saudi Arabia: A literature review

 Department of Clinical Laboratory Sciences, College of Applied Medical Sciences, King Saud University, PO Box 10219, Riyadh 11433, Saudi Arabia
Received: , Accepted: ,
© The Author(s) 2021
Disclaimer:
This article was originally published by Elsevier and was migrated to Scientific Scholar after the change of Publisher.

Peer review under responsibility of King Saud University.

Abstract

Gram-negative bacteria (GNB) represent a major source of morbidity worldwide. The antimicrobial resistance of GNB has recently increased worldwide, that led to using colistin to treat multidrug resistant (MDR) GNB infections. Annually, Saudi Arabia hosts mass religious occasions, where the risk of infectious disease transmission is very high. This review aimed to provide an update on the current prevalence and molecular epidemiology of colistin-resistant GNB locally. It also assessed the role of mass gatherings in triggering colistin resistance. Although colistin is still highly effective against GNB isolates locally, high colistin resistance has been identified among major GNB such as Acinetobacter baumannii and Klebsiella pneumoniae. Colistin resistance among certain MDR Escherichia coli clones, such as ST131, has recently emerged and this is alarming given the rapid global dissemination of this clone. Local data has shown the role of mass religious gatherings in triggering the acquisition of colistin resistance, which makes the screening of colistin resistance determinants very important to limit the spread of colistin resistant GNB between pilgrims.

Keywords

Antimicrobial resistance
Colistin
Gram-negative bacteria
Escherichia coli
Acinetobacter baumannii
1

1 Introduction

Gram-negative bacteria (GNB) cause a wide range of serious infections such as urinary tract and bloodstream infections (Hormozi et al., 2018). Over the past decades, the spectrum of resistance of GNB to many first-line agents, such as ciprofloxacin and cephalosporins, has increased substantially (Meier et al., 2011). More recently, GNB resistance to more powerful antibiotics, such as carbapenems, has also been increasingly reported (Hussein et al., 2013). This makes treatment options of infections due to GNB limited to last-line agents such as polymyxins (Alotaibi, 2019).

Colistin, a polymyxin E agent, was first introduced into clinical setting in 1959 and is considered a last line agent to treat multidrug resistant (MDR) infections caused by GNB. Although colistin has high nephrotoxicity and neurotoxicity that affected its use clinically, the use of this agent in the clinical practice has been resumed due to the increasingly reported resistance among GNB globally (Li et al., 2006). Over the past decade, however, the heavy use of colistin has driven the global emergence of colistin resistance among many bacterial species (Leangapichart et al., 2016).

Saudi Arabia is one of the largest countries in Asia that annually hosts millions of pilgrims during religious occasions such as Hajj (Memish et al., 2012). Given the proposed association between mass religious gatherings and the escalating risk of infectious disease transmission, and the increased levels of antibiotic resistance among major Gram-negative pathogens reported locally (Alqasim, 2020; Yezli et al., 2014) Saudi Arabia can be a center for the spread of drug resistance globally.

This review aimed to provide an update on the current local prevalence of colistin resistance of GNB in Saudi Arabia. It also determined the molecular epidemiology of colistin-resistant GNB circulating locally, and the role of mass religious gatherings in triggering this resistance. The PubMed was used to obtain research articles, published between 2003 and 2020, using these terms: colistin, antimicrobial resistance, Gram-negative bacteria, multidrug resistance, Escherichia coli, Pseudomonas aeruginosa, Acinetobacter baumannii, Klebsiella pneumoniae, molecular epidemiology of colistin resistant pathogens, Saudi Arabia.

2

2 Current prevalence of colistin resistance of major Gram-negative pathogens in Saudi Arabia

The local level of colistin resistance of major GNB, including Escherichia coli, Acinetobacter baumannii, Klebsiella pneumoniae and Pseudomonas aeruginosa, is demonstrated here.

2.1

2.1 Colistin resistance of Escherichia coli

Escherichia coli (E. coli) is the principal cause of urinary tract and bloodstream infections in humans (Russo and Johnson, 2003). Since 2000, the antimicrobial resistance of E. coli, particularly extraintestinal pathogenic E. coli (ExPEC), has increased markedly (Foxman, 2010). Additionally, the current global rise in antimicrobial resistance has been ascribed to the rapid dissemination of one ExPEC clone, known as E. coli sequence type 131 (E. coli ST131) (Alqasim, 2020). This clone is usually MDR and has high extended-spectrum β- lactamase (ESBL) carriage (Nicolas-Chanoine et al., 2014).

In Saudi Arabia, colistin resistance of E. coli was not reported until 2016, and many previous local studies showed entire colistin susceptibility among E. coli isolates (Al-Agamy et al., 2014; Ibrahim, 2018;Abdalhamid et al., 2014) (Table 1). Nonetheless, two recent reports have described the local emergence of colistin resistance among two ExPEC isolates (Sonnevend et al., 2016;Alghoribi et al., 2019).

Table 1 Colistin resistance rates among major GNB species in Saudi Arabia.
Bacterial species Year of sampling Total no. of isolates No. of colistin resistant isolates (%) Reference
A. baumannii 2006 506 0 (0%) Al-Obeid et al., 2015
2006–2008 253 8 (3%) Aly et al., 2014
2006–2014 503 8 (1.5%) Aly et al., 2016
2008–2012 83 0 (0%) Al-Sultan et al., 2015
2009 510 0 (0%) Al-Obeid et al., 2015
2010 27 8 (30%) Al-Agamy et al 2017
2010 84 0 (0%) Somily et al., 2012
2010–2012 141 0 (0%) Abdalhamid et al., 2014
2012 936 0 (0%) Al-Obeid et al., 2015
2012 64 2 (3.1%) Alsultan et al, 2014
2014 10 0 (0%) El-Mahdy et al., 2017
2014 47 0 (0%) Aljindan et al., 2015
2014–2015 105 0 (0%) Al Bshabshe et al., 2016
2016 9 1 (11%) Badger-Emeka et al., 2018
2016 6 2 (33%) Azim et al., 2019
2016–2018 75 3 (4%) Ibrahim, 2018
2017 50 0 (0%) Ramadan et al., 2018
K. pneumoniae 2003–2012 9 5 (55.6%) Garbati et al., 2013
2009 95 3 (3%) Saeed et al., 2010
2011–2012 98 0 (0%) Al-Al-Qahtani et al., 2014
2015 5 0 (0%) Abdalhamid et al., 2016
2016–2018 14 0 (0%) Ibrahim, 2018
P. aeruginosa 2009 123 10 (8%) Saeed et al., 2010
2010 33 2 (6%) Somily et al., 2012
2011 34 1 (2.9%) Al-Agamy et al., 2017
2014–2015 108 6 (5.5%) Ahmed, 2016
2014–2015 28 6 (21.6%) Ahmed and Asghar, 2017
2015 22 0 (0%) Abdalhamid et al., 2016
2016 25 0 (0%) Azim et al., 2019
2016–2018 10 3 (30%) Ibrahim, 2018
2017 43 0 (0%) Ramadan et al., 2018
2017–2018 174 29 (16.7%) Fatima et al., 2019
2019 17 3 (17.6%) Bandy and Almaeen 2020
E. coli 2009 39 0 (0%) Saeed et al., 2010
2010–2011 152 0 (0%) Al-Agamy et al., 2014
2015 3 0 (0%) Abdalhamid et al., 2016
2016–2018 4 0 (0%) Ibrahim, 2018
2019 4 0 (0%) Bandy and Almaeen 2020

2.2

2.2 Colistin resistance of Acinetobacter baumannii

Acinetobacter baumannii (A. baumannii) is a major etiological agent of many hospital-acquired infections such as nosocomial pneumonia, and is associated with a remarkable capability of acquiring resistance to nearly all available antibiotic families (Dijkshoorn et al., 2007). Colistin resistance of A. baumannii was first reported in 1999 (Hejnar et al., 1999), and since then the prevalence of this resistance of this pathogen has increased globally. For example, resistance to colistin was identified in 40.7% of A. baumannii isolates in Spain (Cai et al., 2012).

Locally, several previous studies, from different geographical regions, have concluded that A. baumannii isolates were entirely susceptible to colistin (Al-Obeid et al., 2015; Saeed et al., 2010) (Table 1). Others, however, have demonstrated variable resistance levels to colistin among A. baumannii isolates. For instance, Ibrahim et al have reported low colistin resistance rate, with 3 of 75 (4%) isolates showing insusceptibility to this agent (Ibrahim, 2018). Nonetheless, Al-Agamy and co-authors have found that colistin resistance was observed in 8 of 27 (30%) A. baumannii isolates (Al-Agamy et al., 2017) (Table 1).

2.3

2.3 Colistin resistance of Klebsiella pneumoniae

Klebsiella pneumoniae (K. pneumoniae) is associated with causing life-threatening infections such as pneumonia and bacteraemia (Paczosa and Mecsas, 2016). Recently, K. pneumoniae resistance to antibiotics has increased drastically, and the dissemination of carbapenem-resistant K. pneumoniae isolates has been reported globally (Pitout et al., 2015).

In Saudi Arabia, many reports have found full colistin susceptibility among K. pneumoniae isolates (Abdalhamid et al., 2016; Al-Qahtani et al., 2014). Others, however, have identified colistin resistance among K. pneumoniae isolates. For example, Saeed et al have concluded that 3 of 95 (3%) K. pneumoniae isolates were colistin-insusceptible (Saeed et al., 2010), while Gabarti and others have found that K. pneumoniae accounted for 5 of 9 (55.6%) colistin-resistant Enterobacteriaceae isolates (Garbati et al., 2013).

2.4

2.4 Colistin resistance of Pseudomonas aeruginosa

Pseudomonas aeruginosa (P. aeruginosa) causes a wide range of nosocomial illnesses such as urinary tract and bloodstream infections (Nathwani et al., 2014). P. aeruginosa is usually MDR, and carbapenem-resistant P. aeruginosa isolates have also been reported globally (Potron and Poirel, 2015). This highlights the threat posed by this pathogen to public health.

In Saudi Arabia, although full sensitivity to colistin among P. aeruginosa isolates has been reported (Azim et al., 2019; Ramadan et al., 2018), Saeed et al have demonstrated that 10 of 123 (8%) P. aeruginosa isolates were colistin-insusceptible (Saeed et al., 2010). Additionally, Ibrahim and others demonstrated colistin resistance in 3 of 10 (30%) P. aeruginosa isolates (Ibrahim, 2018).

3

3 Molecular epidemiology of colistin-resistant Gram-negative isolates

In Saudi Arabia, many studies have been conducted to uncover the mechanisms and molecular epidemiology of colistin resistance of major GNB.

For E. coli, Sonnevend and co-authors reported, for the first time, the emergence of colistin resistance among ExPEC isolates in 2016, and they identified a colistin-resistant ST68 blood isolate harbouring the plasmid mediated transferable colistin resistance gene, namely mcr-1, on IncHI2 plasmid (Sonnevend et al., 2016) (Table 2). Another multi-locus sequence typing (MLST)-based study has demonstrated a considerable clonal diversity among 10 mcr-1-producing colistin-resistant E. coli isolates that collected from rectal swabs of North African pilgrims during Hajj, and showed that colistin resistance was detected in E. coli isolates belonging to low antibiotic-resistant STs such as ST10, ST93 and ST155 (Leangapichart et al., 2016). More recently, a whole genome sequence (WGS)-based analysis has described one colistin-resistant E. coli ST131 isolate carrying the mcr-1 gene on IncHI2 plasmid (Alghoribi et al., 2019). This finding is important given the aforementioned high worldwide spread of E. coli ST131 and the role it plays in triggering drug resistance globally.

Table 2 Summery of molecular epidemiological findings obtained from studies on colistin resistant GNB in Saudi Arabia.
Bacterial species Year of sampling Colistin resistance mechanism(s) ST(s)/PFGE clone Reference
E. coli 2009–2013 mcr-1, on IncHI2 plasmid ST68 Sonnevend et al., 2016
K. pneumoniae 2011–2015 Mutation in PhoP gene ST974, ST37, ST709, ST348 Zaman et al., 2018
Mutation in mgrB gene ST14, ST15, ST16, ST22, ST48, ST101, ST152 & ST307
Mutations in PhoP & mgrB genes ST15
A. baumannii 2012 NA PFGE clone H Alsultan et al., 2014
E. coli 2013 mcr-1, on IncHI2 plasmid ST131 Alghoribi et al., 2019
K. pneumoniae 2013–2014 mcr-1 ST788 Leangapichart et al., 2016
E. coli 2013–2014 mcr-1 ST93, ST453, ST648, ST656, ST10, ST155, ST602 & ST1300 Leangapichart et al., 2016

For K. pneumoniae, Zaman and colleagues have characterized the mechanisms and molecular epidemiology of 23 colistin-resistant K. pneumoniae isolates using MLST, and demonstrated the presence of mutations in mgrB and phoP genes that mediate colistin resistance in these isolates. They also found great clonal diversity within this colistin-resistant K. pneumoniae population, with K. pneumoniae ST14 being the predominant ST type and it accounted for 26% of total colistin-resistant isolates (Zaman et al., 2018). Another study has identified one mcr-1-producing K. pneumoniae isolate belonging to ST788 (Leangapichart et al., 2016) (Table 2). Taken together, studying the factors the drive the success of locally circulated colistin resistant E. coli and K. pneumoniae STs is crucial to combat this issue.

With regard to A. baumannii, Alsultan and colleagues have explored the clonal diversity of 64 carbapenem-resistant A. baumannii (CRAB) isolates, obtained from 16 different regions in Saudi Arabian intensive care patients, using pulsed field gel electrophoresis (PFGE) (Alsultan et al., 2014). They found that 20 of 64 (31.3%) isolates belonging to clone H, and that the 2 colistin-resistant A. baumannii isolates were also members of this clone.

4

4 The role of mass religious gatherings in the acquisition of colistin resistance

As mentioned earlier, Saudi Arabia hosts mass religious gatherings, such as Hajj, and these overcrowded occasions represent a major risk for propagation of antibiotic resistant bacteria between pilgrims. With respect to the association between mass religious gatherings and the acquisition of colistin resistant GNB, Leangapichart and others have evaluated the level of colistin resistance among pilgrims, before and after their pilgrimage, by testing the presence of the mcr-1 gene in 440 rectal swabs collected between 2013 and 2014 (Leangapichart et al., 2016). They found a significant high increase in the prevalence of mcr-1-producing isolates upon pilgrims return (i.e. in 2013, 1.55% before the pilgrimage compared to 8.53% after the pilgrimage; in 2014, 1.02% before the pilgrimage compared to 9.18% after the pilgrimage (Leangapichart et al., 2016). This highlights the high chance of acquiring colistin resistance determinants between millions of pilgrims during Hajj, and demonstrates that Saudi Arabia might be a center for the spread of antimicrobial resistance globally. Therefore, it is important to screen the mcr-1 carriage to prevent the risk of possible spread of colistin resistant bacteria among pilgrims.

5

5 Local colistin resistance trends of GNB

Few studies have assessed colistin resistance trends among GNB isolates, particularly A. baumannii, over time in many Saudi Arabian healthcare centers. For instance, Al-Obeid and co-authors have determined the antimicrobial susceptibility profiles of 506, 510 and 936 duplicate A. baumannii isolates collected during 2006, 2009 and 2012, respectively (Al-Obeid et al., 2015). They found similar colistin sensitivity rates for all A. baumannii isolates over the study period, with all isolates showing full susceptibility to colistin (Table 3). Likewise, AlMobarak et al have also demonstrated no change in colistin resistance pattern among 1176 A. baumannii isolates collected between 2010 and 2013, and they showed that all isolates were colistin-susceptible (Al Mobarak et al., 2014). Furthermore, Al-Mously and Hakawi have examined colistin resistance pattern, between 2006 and 2010, of A. baumannii blood isolates, and found similar full sensitivity to this agent over the surveillance period (Al-Mously and Hakawi, 2013). However, Baadani and colleagues have documented an increased pattern of colistin resistance among A. baumannii isolates over a 2-year period (2010–2011), and they demonstrated that the level of A. baumannii resistance to colistin increased from 2.6% in 2010 to 4.7% in 2011 (Baadani et al., 2013) (Table 3).

Table 3 Summery of colistin resistance patterns among GNB in Saudi Arabia.
Surveillance period Bacterial species Total no. of isolates Change in colistin resistance pattern Comments References
2006–2010 A. baumannii 191 No All isolates were colistin-susceptible over the study period Al-Mously and Hakawi, 2013
2006–2012 A. baumannii 1952 No All isolates were colistin-susceptible over the study period Al-Obeid et al., 2015
2010–2011 A. baumannii 1307 Yes Resistance to colistin increased from 2.6% in 2010 to 4.7% in 2011 Baadani et al., 2013
2010–2013 A. baumannii 1176 No All isolates were colistin-susceptible over the study period Al Mobarak et al., 2014

6

6 Concluding remarks and future perspective

This review has provided an update on the current local prevalence of colistin resistance of GNB. Although some reports have shown full susceptibility to colistin among major Gram-negative species, others have alarmingly documented the escalating levels of colistin resistance among A. baumannii, K. pneumoniae and P. aeruginosa isolates. This suggests the need to review the current guidelines used to treat MDR infections caused by these pathogens. Additionally, molecular epidemiological studies have recently demonstrated the emergence of colistin resistance among certain E. coli clones such as ST131. Given the rapid global dissemination of this MDR clone, it is crucial to identify the factors that drive the success of these clones. Finally, this review has shown the association between mass religious gathering and the acquisition of colistin resistance determinants during Hajj, and this implies the need to screen the presence of these determinants to prevent the risk of possible spread of colistin resistant bacteria among pilgrims. In the future, it is suggested that a nationwide antimicrobial resistance surveillance is required to accurately assess the level of colistin resistance locally, and that performing molecular-based studies on the factors that enhance this resistance in GNB is also crucial to combat this issue.

Declaration of Competing Interest

The author declares that there is no competing interests or personal relationships that could have appeared to influence the work reported in this paper.

References

  1. , , , , . Characterization of carbapenem-resistant Acinetobacter baumannii clinical isolates in a tertiary care hospital in Saudi Arabia. New Microbiol. 2014;37(1):65-73.
    [Google Scholar]
  2. , , , , , . Rates of gastrointestinal tract colonization of carbapenem-resistant Enterobacteriaceae and Pseudomonas aeruginosa in hospitals in Saudi Arabia. New Microbes New Infect. 2016;10:77-83.
    [Google Scholar]
  3. , . Incidence and antibiotic susceptibility pattern of Pseudomonas aeruginosa Isolated from Inpatients in Two Tertiary Hospitals. Clin Microbiol. 2016;5:1-4.
    [Google Scholar]
  4. , , . Antibiotic susceptibility pattern of Pseudomonas aeruginosa expressing blaGES and blaPER genes in two different hospitals. Afr J Biotechnol. 2017;16(21):1197-1202.
    [Google Scholar]
  5. , , , , , , . Characterization of extended-spectrum beta-lactamase-producing Klebsiella pneumoniae from Riyadh. Saudi Arabia. J Chemother. 2014;26(3):139-145.
    [Google Scholar]
  6. , . Carbapenem-resistant Enterobacteriaceae: an update narrative review from Saudi Arabia. J Infect Public Health. 2019;12(4):465-471.
    [Google Scholar]
  7. , . Extraintestinal pathogenic Escherichia coli in Saudi Arabia: A review of antimicrobial resistance and molecular epidemiology. Trop J Pharm Res. 2020;19(2):447-453.
    [Google Scholar]
  8. , , , , , , . Molecular characteristics of extended-spectrum β-lactamase-producing Escherichia coli in Riyadh: emergence of CTX-M-15-producing E. coli ST131. Ann Clin Microbiol Antimicrob.. 2014;13(1):1-7.
    [Google Scholar]
  9. , , , , , , . Complete Genome Sequence of a Colistin-Resistant Uropathogenic Escherichia coli Sequence Type 131 fimH22 Strain Harboring mcr-1 on an IncHI2 Plasmid, Isolated in Riyadh. Saudi Arabia. Microbiol Resour Announc. 2019;8(18):1-3.
    [Google Scholar]
  10. , , , , , . Epidemiology of extensive drug resistant Acinetobacter baumannii (XDRAB) at Security Forces Hospital (SFH) in Kingdom of Saudi Arabia (KSA) J Chemother. 2015;27(3):156-162.
    [Google Scholar]
  11. , , , , , , , . First detection of GES-5 carbapenemase-producing Acinetobacter baumannii isolate. Microb Drug Resist. 2017;23(5):556-562.
    [Google Scholar]
  12. , , , , , . Prevalence and Antibiotic Susceptibility Among Gram Negative Bacteria Isolated from Intensive Care Units at a Tertiary Care Hospital in Riyadh. Saudi Arabia. J Pure Appl Microbiol. 2019;13(1):201-208.
    [Google Scholar]
  13. , , , , . Clonal diversity of Acinetobacter baumannii from diabetic patients in Saudi Arabian hospitals. J Med Microbiol. 2014;63(11):1460-1466.
    [Google Scholar]
  14. , , , , , , , . Antimicrobial resistance patterns among Acinetobacter baumannii isolated from King Abdulaziz Hospital, Jeddah, Saudi Arabia, four-year surveillance study (2010–2013) Egypt J Med Microbiol. 2014;23:53-60.
    [Google Scholar]
  15. , , . Acinetobacter baumannii bloodstream infections in a tertiary hospital: Antimicrobial resistance surveillance. Int J Infect Control. 2013;9(2):1-8.
    [Google Scholar]
  16. , , , , , , , . Genetic diversity of OXA-51-like genes among multidrug-resistant Acinetobacter baumannii in Riyadh, Saudi Arabia. Eur J Clin Microbiol Infect Dis. 2014;33(7):1223-1228.
    [Google Scholar]
  17. , , , , , . High prevalence of the PER-1 gene among carbapenem-resistant Acinetobacter baumannii in Riyadh, Saudi Arabia. Eur J Clin Microbiol Infect Dis. 2016;35(11):1759-1766.
    [Google Scholar]
  18. , , , , , , . Dissemination of multiple carbapenem-resistant clones of Acinetobacter baumannii in the Eastern District of Saudi Arabia. Front Microbiol. 2015;6:1-7.
    [Google Scholar]
  19. , , , , . Prevalence of digestive tract colonization of carbapenem-resistant Acinetobacter baumannii in hospitals in Saudi Arabia. J Med Microbiol. 2015;64(4):400-406.
    [Google Scholar]
  20. , , , , , . Multidrug resistance Acinetobacter species at the intensive care unit, Aseer Central Hospital, Saudi Arabia: a one year analysis. Asian Pac J Trop Med.. 2016;9(9):903-908.
    [Google Scholar]
  21. , , , , . Prevalence of colistin and tigecycline resistance in Acinetobacter baumannii clinical isolates from 2 hospitals in Riyadh Region over a 2-year period. Saudi Med J. 2013;34(3):248-253.
    [Google Scholar]
  22. , , . Pathogenic spectrum of blood stream infections and resistance pattern in Gram-negative bacteria from Aljouf region of Saudi Arabia. Plos One. 2020;15(6):1-14.
    [Google Scholar]
  23. , , , , , . Antimicrobial susceptibility pattern of Gram negative bacteria isolated from intensive care units in Al-Ahsa, Kingdom of Saudi Arabia. Afr J Microbiol Res. 2018;12(31):747-753.
    [Google Scholar]
  24. , , , , , . Colistin resistance of Acinetobacter baumannii: clinical reports, mechanisms and antimicrobial strategies. J Antimicrob Chemother. 2012;67(7):1607-1615.
    [Google Scholar]
  25. , , , . An increasing threat in hospitals: multidrug-resistant Acinetobacter baumannii. Nat Rev Microbiol. 2007;5(12):939-951.
    [Google Scholar]
  26. , , , , . Detection of bla OXA-23-like and bla NDM-1 in Acinetobacter baumannii from the Eastern Region. Saudi Arabia. Microb Drug Resist. 2017;23(1):115-121.
    [Google Scholar]
  27. , , , , , , . Effect of Combined Therapy on Colistin Resistant Pseudomonas aeruginosa: An in Vitro Study. Adv Microbiol. 2019;9(10):877-892.
    [Google Scholar]
  28. , . The epidemiology of urinary tract infection. Nat Rev Urol. 2010;7(12):653-660.
    [Google Scholar]
  29. , , , , . Infection due to colistin-resistant Enterobacteriacae in critically-ill patients. J Infect Dev Ctries. 2013;7(10):713-719.
    [Google Scholar]
  30. , , , . Characteristics of Acinetobacter strains (phenotype classification, antibiotic susceptibility and production of ss-lactamases) isolated from haemocultures from patients at the Teaching Hospital in Olomouc. Acta Univ Palacki Olomuc Fac Med. 1999;142:73-77.
    [Google Scholar]
  31. , , , , , . Antibiotic resistance in patients suffering from nosocomial infections in Besat Hospital. Eur J Transl Myol. 2018;28(3):304-308.
    [Google Scholar]
  32. , , , , , , , . Impact of carbapenem resistance on the outcome of patients' hospital-acquired bacteraemia caused by Klebsiella pneumoniae. J Hosp Infect. 2013;83(4):307-313.
    [Google Scholar]
  33. , . High antimicrobial resistant rates among Gram-negative pathogens in intensive care units: A retrospective study at a tertiary care hospital in Southwest Saudi Arabia. Saudi Med J. 2018;39(10):1035-1043.
    [Google Scholar]
  34. , , , , , , , . Colistin: the re-emerging antibiotic for multidrug-resistant Gram-negative bacterial infections. Lancet Infect Dis. 2006;6(9):589-601.
    [Google Scholar]
  35. , , , , , , . Acquisition of mcr-1 plasmid-mediated colistin resistance in Escherichia coli and Klebsiella pneumoniae during Hajj 2013 and 2014. Antimicrob Agents Chemothe. 2016;60(11):6998-6999.
    [Google Scholar]
  36. , , , , , . Extended-spectrum β-lactamase-producing Gram-negative pathogens in community-acquired urinary tract infections: an increasing challenge for antimicrobial therapy. Infection. 2011;39(4):333-340.
    [Google Scholar]
  37. , , , , . Emergence of medicine for mass gatherings: lessons from the Hajj. Lancet Infect Dis. 2012;12(1):56-65.
    [Google Scholar]
  38. , , , , , . Clinical and economic consequences of hospital-acquired resistant and multidrug-resistant Pseudomonas aeruginosa infections: a systematic review and meta-analysis. Antimicrob Resist Infect Control. 2014;3(1):1-16.
    [Google Scholar]
  39. , , , . Escherichia coli ST131, an intriguing clonal group. Clin Microbiol Rev. 2014;27(3):543-574.
    [Google Scholar]
  40. , , . Klebsiella pneumoniae: going on the offense with a strong defense. MICROBIOL MOL BIOL R. 2016;80(3):629-661.
    [Google Scholar]
  41. , , , . Carbapenemase-producing Klebsiella pneumoniae, a key pathogen set for global nosocomial dominance. Antimicrob Agents Chemother. 2015;59(10):5873-5884.
    [Google Scholar]
  42. , , . Nordmann Emerging broad-spectrum resistance in Pseudomonas aeruginosa and Acinetobacter baumannii: mechanisms and epidemiology. Int J Antimicrob Agents. 2015;45(6):568-585.
    [Google Scholar]
  43. , , , , . Carbapenem-resistant Acinetobacter baumannii and Pseudomonas aeruginosa: characterization of carbapenemase genes and E-test evaluation of colistin-based combinations. Infect Drug Resist. 2018;11:1261.
    [Google Scholar]
  44. , , . Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes Infect. 2003;5(5):449-456.
    [Google Scholar]
  45. , , , , , , , . Plasmid-mediated colistin resistance in Escherichia coli from the Arabian Peninsula. Int J Infect Dis. 2016;50:85-90.
    [Google Scholar]
  46. , , , . Antimicrobial-resistant bacteria in a general intensive care unit in Saudi Arabia. Saudi Med J. 2010;31(12):1341-1349.
    [Google Scholar]
  47. , , , , , , . Antimicrobial susceptibility patterns of multidrug-resistant Pseudomonas aeruginosa and Acinetobacter baumannii against carbapenems, colistin, and tigecycline. Saudi Med J. 2012;33(7):750-755.
    [Google Scholar]
  48. , , , , . Prevalence and antimicrobial resistance among Gram-negative pathogens in Saudi Arabia. Journal of Chemotherapy. 2014;26(5):257-272.
    [Google Scholar]
  49. , , , , , . Insertion element mediated mgrB disruption and presence of ISKpn28 in colistin-resistant Klebsiella pneumoniae isolates from Saudi Arabia. Infect Drug resist. 2018;11:1183-1187.
    [Google Scholar]

Fulltext Views
26

PDF downloads
24
View/Download PDF
Download Citations
BibTeX
RIS
Show Sections

Suggested read for related articles:

© Copyright 2025 – Journal of King Saud University – Science.

Published by Scientific Scholar on behalf of King Saud University.

ISSN (Print): 1018-3647
ISSN (Online): 2213-686X

Scientific Scholar CrossRef Creative Commons Open Acess Portico