Volume 10, Issue 3 (9-2022)                   JoMMID 2022, 10(3): 114-121 | Back to browse issues page

XML Print

Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:

Malaki A, Ferdosi-Shahandashti E, Maali A, Sabbagh P, Khademian A. Molecular Characterizations and Antimicrobial Susceptibility of Extended-Spectrum ß-lactamase (ESBL) Producing Proteus spp. Clinical Isolates in Babol, Northern Iran. JoMMID 2022; 10 (3) :114-121
URL: http://jommid.pasteur.ac.ir/article-1-437-en.html
Department of Medical Biotechnology, School of Medicine, Babol University of Medical Sciences, Babol, Iran; Infectious Diseases and Tropical Medicine Research Center, Babol University of Medical Sciences, Babol, Iran
Abstract:   (1132 Views)
Introduction: Proteus spp. are opportunistic members of Enterobacteriaceae, accounting for 10% of urinary tract infections and other primary clinical infections. They produce extended-spectrum beta-lactamases (ESBL) that can confer resistance to beta-lactam antibiotics. This study aimed to investigate the prevalence, antimicrobial susceptibility, molecular characteristics, and genetic relationship of ESBL-producing Proteus spp. clinical isolates in Babol, Northern Iran. Methods: In this cross-sectional study, out of 112 clinical samples, 30 Proteus spp. isolates were identified via specific biochemical assays. According to the Clinical and Laboratory Standards Institute (CLSI) guidelines, antibiotic susceptibility was evaluated using disc diffusion and agar dilution methods, and polymerase chain reaction (PCR) was used to detect blaTEM and blaSHV genes. Results: The resistance rate to tetracycline and sulfamethoxazole was highest by disk diffusion and agar dilution. Multiple drug-resistant (MDR) isolates were 86% and 60% in disk diffusion and agar dilution assays. Seven (23.3%) isolates had the blaTEM genes and 18 (60%) blaSHV. Conclusion:  ESBL-producing Proteus spp. was highly prevalent, and the blaSHV was the most common resistance contributing gene. These findings and relatively high resistance to ampicillin demand more care in prescribing antibiotics. Also, the high prevalence of MDR isolates in patients infected with ESBL-producing Proteus spp. requires continuous surveillance.
Full-Text [PDF 988 kb]   (351 Downloads)    
Type of Study: Original article | Subject: Anti-microbial agents, resistance and treatment protocols
Received: 2021/12/19 | Accepted: 2022/09/19 | Published: 2022/10/12

1. Malekjamshidi MR, Shahcheraghi F, Feizabadi MM. Detection and PFGE analysis of ESBL-producing isolates of Proteus species isolated from patients at Tehran hospitals. Med Sci Monit. 2010; 16 (10): BR327-BR32.
2. Peirano G, Pitout JD. Extended-spectrum β-lactamase-producing Enterobacteriaceae: update on molecular epidemiology and treatment options. Drugs. 2019: 79 (14): 1529-41. [DOI:10.1007/s40265-019-01180-3]
3. Ramadan AA, Abdelaziz NA, Amin MA, Aziz RK. Novel blaCTX-M variants and genotype-phenotype correlations among clinical isolates of extended spectrum beta lactamase-producing Escherichia coli. Sci Rep. 2019; 9 (1): 4224. [DOI:10.1038/s41598-019-39730-0]
4. Palmeira JD, Ferreira HMN. Extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in cattle production-a threat around the world. Heliyon. 2020; 6 (1): e03206. [DOI:10.1016/j.heliyon.2020.e03206]
5. Cullik A, Pfeifer Y, Prager R, Baum Hv, Witte W. A novel IS26 structure surrounds blaCTX-M genes in different plasmids from German clinical Escherichia coli isolates. J Med Microbiol. 2010; 59 (5): 580-7. [DOI:10.1099/jmm.0.016188-0]
6. Gröbner S, Linke D, Schütz W, Fladerer C, Madlung J, Autenrieth IB, et al. Emergence of carbapenem-non-susceptible extended-spectrum β-lactamase-producing Klebsiella pneumoniae isolates at the university hospital of Tübingen, Germany. J Med Microbiol. 2009; 58 (7): 912-22. [DOI:10.1099/jmm.0.005850-0]
7. Knudsen PK, Brandtzaeg P, Høiby EA, Bohlin J, Samuelsen Ø, Steinbakk M, et al. Impact of extensive antibiotic treatment on faecal carriage of antibiotic-resistant enterobacteria in children in a low resistance prevalence setting. PLoS One. 2017; 12 (11): e0187618. [DOI:10.1371/journal.pone.0187618]
8. Tumbarello M, Trecarichi EM, Fiori B, Losito AR, D'Inzeo T, Campana L, et al. Multidrug-resistant Proteus mirabilis bloodstream infections: risk factors and outcomes. Antimicrob Agents Chemother 2012; 56 (6): 3224-31. [DOI:10.1128/AAC.05966-11]
9. Vivas R, Barbosa AAT, Dolabela SS, Jain S. Multidrug-resistant bacteria and alternative methods to control them: An overview. Microb Drug Resist. 2019; 25 (6): 890-908. [DOI:10.1089/mdr.2018.0319]
10. Drzewiecka D. Significance and roles of Proteus spp. bacteria in natural environments. Microb Ecol. 2016; 72 (4): 741-58. [DOI:10.1007/s00248-015-0720-6]
11. Armbruster CE, Forsyth-DeOrnellas V, Johnson AO, Smith SN, Zhao L, Wu W, et al. Genome-wide transposon mutagenesis of Proteus mirabilis: Essential genes, fitness factors for catheter-associated urinary tract infection, and the impact of polymicrobial infection on fitness requirements. PLoS Pathog. 2017; 13 (6): e1006434. [DOI:10.1371/journal.ppat.1006434]
12. Schaffer JN, Pearson MMJ. Proteus mirabilis and urinary tract infections. Microbiol Spectr. 2015; 3 (5): 10. [DOI:10.1128/microbiolspec.UTI-0017-2013]
13. Chen C-Y, Chen Y-H, Lu P-L, Lin W-R, Chen T-C, Lin C-Y. Proteus mirabilis urinary tract infection and bacteremia: risk factors, clinical presentation, and outcomes. J Microbiol Immunol Infect. 2012; 45 (3): 228-36. [DOI:10.1016/j.jmii.2011.11.007]
14. Avlami A, Bekris S, Ganteris G, Kraniotaki E, Malamou-Lada E, Orfanidou M, et al. Detection of metallo-β-lactamase genes in clinical specimens by a commercial multiplex PCR system. J Microbiol Methods. 2010; 83 (2): 185-7. [DOI:10.1016/j.mimet.2010.08.014]
15. Japoni S, Japoni A, Farshad S, Ali AA, Jamalidoust M. Association between existence of integrons and multi-drug resistance in Acinetobacter isolated from patients in southern Iran. Pol J Microbiol. 2011; 60 (2): 163-8. [DOI:10.33073/pjm-2011-023]
16. Stalder T, Barraud O, Casellas M, Dagot C, Ploy M-C. Integron involvement in environmental spread of antibiotic resistance. Front Microbiol. 2012; 3: 119. [DOI:10.3389/fmicb.2012.00119]
17. Chen L, Al Laham N, Chavda KD, Mediavilla JR, Jacobs MR, Bonomo RA, et al. First report of an OXA-48-producing multidrug-resistant Proteus mirabilis strain from Gaza, Palestine. Antimicrob Agents Chemother. 2015; 59 (7): 4305-7. [DOI:10.1128/AAC.00565-15]
18. Uzunović S, Ibrahimagić A, Hodžić D, Bedenić B. Molecular epidemiology and antimicrobial susceptibility of AmpC-and/or extended-spectrum (ESBL) ß-lactamase-producing Proteus spp. clinical isolates in Zenica-Doboj Canton, Bosnia and Herzegovina. Med Glas (Zenica). 2016; 13 (2): 103-12. [DOI:10.1016/j.ijid.2016.11.114]
19. Fattah Hamid S, Bahadeen Taha A, Jamel Abdulwahid M. Distribution of blaTEM, blaSHV, blaCTX-M, blaOXA, and blaDHA in Proteus mirabilis Isolated from Diabetic Foot Infections in Erbil, Iraq. Cell Mol Biol (Noisy-le-grand). 2020; 66 (1): 88-94. [DOI:10.14715/cmb/2019.66.1.15]
20. Li Z, Peng C, Zhang G, Shen Y, Zhang Y, Liu C, et al. Prevalence and characteristics of multidrug-resistant Proteus mirabilis from broiler farms in Shandong Province, China. Poult Sci. 2022; 101 (4): 101710. [DOI:10.1016/j.psj.2022.101710]
21. Di Conza JA, Badaracco A, Ayala J, Rodríguez C, Famiglietti A, Gutkind GO. β-lactamases produced by amoxicillin-clavulanate-resistant enterobacteria isolated in Buenos Aires, Argentina: a new blaTEM gene. Rev Argent Microbiol. 2014; 46 (3): 210-7. [DOI:10.1016/S0325-7541(14)70075-6]
22. Chinnam BK, Nelapati S, Tumati SR, Bobbadi S, Chaitanya Peddada V, Bodempudi B. Detection of β-Lactamase-Producing Proteus mirabilis Strains of Animal Origin in Andhra Pradesh, India and Their Genetic Diversity. J Food Prot. 2021; 84 (8): 1374-9. [DOI:10.4315/JFP-20-399]
23. Algammal AM, Hashem HR, Alfifi KJ, Hetta HF, Sheraba NS, Ramadan H, et al. atpD gene sequencing, multi-drug resistance traits, virulence-determinants, and antimicrobial resistance genes of emerging XDR and MDR-Proteus mirabilis. Sci Rep. 2021; 11 (1): 9476. [DOI:10.1038/s41598-021-88861-w]
24. Malekjamshidi MR, Shahcheraghi F, Feizabadi MM. Detection and PFGE analysis of ESBL-producing isolates of Proteus species isolated from patients at Tehran hospitals. Med Sci Monit. 2010; 16 (10): Br327-32.
25. Fouch S, Mitchell J, Lwaleed B, Zinkevich VJ. Evaluation of the shift in antimicrobial resistance due to extended spectrum beta lactamase and AmpC producing enterobacteriaceae in Hampshire England. Ann Adv Biomed Sci. 2018; 1 (2): 000109. [DOI:10.23880/aabsc-16000109]
26. Liakopoulos A, Mevius D, Ceccarelli DJ. A review of SHV extended-spectrum β-lactamases: neglected yet ubiquitous. Front Microbiol. 2016; 7: 1374. [DOI:10.3389/fmicb.2016.01374]
27. Fattahi K, Rostamzad AJ. Distribution of blaCTX-M, blaTEM genes among ESBL producing Proteus species isolated from urinary tract infections (UTI) in Ilam. J Res Med Sci. 2015; 39 (1): 41-7.
28. Uyanga FZ, Ekundayo EO, Nwankwo EOJ. bla TEM, bla SHV and bla CTX-M-15 Extended Spectrum Beta-lactamase Produced by Acinetobacter baumanii, Enterobacter clocae and Proteus mirabilis from Pregnant Women in Three Secondary Health Care Facilities in South-south, Nigeria. J Adv Microbiol. 2019: 1-9. [DOI:10.9734/jamb/2019/v18i130154]
29. Lev AI, Astashkin EI, Kislichkina AA, Solovieva EV, Kombarova TI, Korobova OV, et al. Comparative analysis of Klebsiella pneumoniae strains isolated in 2012-2016 that differ by antibiotic resistance genes and virulence genes profiles. Pathog Glob Health. 2018; 112 (3): 142-51. [DOI:10.1080/20477724.2018.1460949]
30. Musa HA, Osman MA, Abdelaziz YH, Mohamed S, Ibrahim-Saeed MJ. Distribution of extended-spectrum beta-lactamase TEM and CTX-M resistance genes among Proteus species isolated in Sudan. VacciMonitor. 2019; 28 (2): 80-4.
31. Kurihara Y, Hitomi S, Oishi T, Kondo T, Ebihara T, Funayama Y, et al. Characteristics of bacteremia caused by extended-spectrum beta-lactamase-producing Proteus mirabilis. J Infect Chemother. 2013; 19 (5): 799-805. [DOI:10.1007/s10156-013-0563-3]
32. Schmiedel J, Falgenhauer L, Domann E, Bauerfeind R, Prenger-Berninghoff E, Imirzalioglu C, et al. Multiresistant extended-spectrum β-lactamase-producing Enterobacteriaceae from humans, companion animals and horses in central Hesse, Germany. BMC Microbiol. 2014; 14 (1): 187. [DOI:10.1186/1471-2180-14-187]
33. Hujer AM, Page MG, Helfand MS, Yeiser B, Bonomo RA. Development of a sensitive and specific enzyme-linked immunosorbent assay for detecting and quantifying CMY-2 and SHV β-lactamases. J Clin Microbiol. 2002; 40 (6): 1947-57. [DOI:10.1128/JCM.40.6.1947-1957.2002]

Add your comments about this article : Your username or Email:

Send email to the article author

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.