Issue
Multidrug resistance, prevalence and phylogenetic analysis of genes encoding class II and III integrons in clinically isolated Escherichia coli
Corresponding Author(s) : Manal Mohamed Elhassan Taha
Cellular and Molecular Biology,
Vol. 64 No. 5: Issue 5
Abstract
The present study was conducted to evaluate the susceptibility, multidrug resistance and genetic characteristics of Escherichia coli (E. coli) strains, isolated from clinical samples from Jazan Hospital, Jazan, Saudi Arabia. A total of 95 samples were recruited from wound, urine, stool and blood. The isolates were assessed for their antibiotic susceptibilities and the presence of class II and III integrons was studied using PCR technique. Integron II-positive PCR products were further confirmed using partial sequencing. Ampicillin (84.2%) was found to be the most resistant antibiotic followed by ciprofloxacin (57.9%), gentamicin (56.8%), nalidixic acid (50.5%), cefotaxim (49.5%), ofloxacin (45.3%), amikacin (26.3%) and imipenem (16.8%), respectively. Seventy-six isolated strains were designated as multidrug resistant (MDR), while non-MDR was found in 19 strains (20.0%). Out of 76 MDR E. coli isolates, 41 (53.9%) were identified as positive for class II and 5 (6.5%) were positive for class III integron. Bioinformatics' analysis have shown that the sequences of our samples aligned along with many published sequences of integron II. Our findings further strengthen the significance of hospital-based and community E. coli strains on rising the burden of antimicrobial resistance.
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- W. H. DePas, A. K. Syed, M. Sifuentes, J. S. Lee, D. Warshaw, V. Saggar, G. Csankovszki, B. R. Boles and M. R. Chapman Biofilm formation protects Escherichia coli against killing by Caenorhabditis elegans and Myxococcus xanthus Applied and environmental microbiology 80 (2014) 7079-7087.
- A. Monteiro and S. C. Verde Bacterial Bioburden in Hospital Environment. in: Exposure to Microbiological Agents in Indoor and Occupational Environments (Ed.^, Eds.), Springer, 2017, 321-328.
- E. Scallan, R. Hoekstra, B. Mahon, T. Jones and P. Griffin An assessment of the human health impact of seven leading foodborne pathogens in the United States using disability adjusted life years Epidemiology & Infection 143 (2015) 2795-2804.
- E. Franz, P. Delaquis, S. Morabito, L. Beutin, K. Gobius, D. A. Rasko, J. Bono, N. French, J. Osek and B.-A. Lindstedt Exploiting the explosion of information associated with whole genome sequencing to tackle Shiga toxin-producing Escherichia coli (STEC) in global food production systems International journal of food microbiology 187 (2014) 57-72.
- R. Laxminarayan, A. Duse, C. Wattal, A. K. Zaidi, H. F. Wertheim, N. Sumpradit, E. Vlieghe, G. L. Hara, I. M. Gould and H. Goossens Antibiotic resistance”the need for global solutions The Lancet infectious diseases 13 (2013) 1057-1098.
- D. Venieri, I. Gounaki, M. Bikouvaraki, V. Binas, A. Zachopoulos, G. Kiriakidis and D. Mantzavinos Solar photocatalysis as disinfection technique: Inactivation of Klebsiella pneumoniae in sewage and investigation of changes in antibiotic resistance profile Journal of environmental management 195 (2017) 140-147.
- S. Abraham, H. S. Wong, J. Turnidge, J. R. Johnson and D. J. Trott Carbapenemase-producing bacteria in companion animals: a public health concern on the horizon Journal of Antimicrobial Chemotherapy 69 (2014) 1155-1157.
- M. M. Elseviers, Y. Van Camp, S. Nayaert, K. Duré, L. Annemans, A. Tanghe and S. Vermeersch Prevalence and management of antibiotic associated diarrhea in general hospitals BMC infectious diseases 15 (2015) 129.
- A. A. H. Abdalla Isolation and Antimicrobial Susceptibility Patterns of Escherichia Coli in Patients with Urinary Tract Infections in Al-Ribat University Hospital-Khartoum. (Ed.^, Eds.), Sudan University of Science & Technology, 2016.
- P. Harnvoravongchai, M. Pipatthana, S. Chankhamhaengdecha and T. Janvilisri Insights into drug resistance mechanisms in Clostridium difficile Essays In Biochemistry 61 (2017) 81-88.
- V. Kasimanickam, K. Owen and R. Kasimanickam Detection of genes encoding multidrug resistance and biofilm virulence factor in uterine pathogenic bacteria in postpartum dairy cows Theriogenology 85 (2016) 173-179.
- B. Chen, K. Yuan, X. Chen, Y. Yang, T. Zhang, Y. Wang, T. Luan, S. Zou and X. Li Metagenomic analysis revealing antibiotic resistance genes (ARGs) and their genetic compartments in the Tibetan environment Environmental science & technology 50 (2016) 6670-6679.
- A. Fluit and F. J. Schmitz Resistance integrons and super-integrons Clinical Microbiology and Infection 10 (2004) 272-288.
- O. Fasugba, A. Gardner, B. G. Mitchell and G. Mnatzaganian Ciprofloxacin resistance in community-and hospital-acquired Escherichia coli urinary tract infections: a systematic review and meta-analysis of observational studies BMC infectious diseases 15 (2015) 545.
- C. Dureja, S. Mahajan and S. Raychaudhuri Phylogenetic distribution and prevalence of genes encoding class I integrons and CTX-M-15 extended-spectrum β-lactamases in Escherichia coli isolates from healthy humans in Chandigarh, India PloS one 9 (2014) e112551.
- A. Felten, B. Grandry, P. H. Lagrange and I. Casin Evaluation of three techniques for detection of low-level methicillin-resistant Staphylococcus aureus (MRSA): a disk diffusion method with cefoxitin and moxalactam, the Vitek 2 system, and the MRSA-screen latex agglutination test Journal of clinical microbiology 40 (2002) 2766-2771.
- A. P. Magiorakos, A. Srinivasan, R. Carey, Y. Carmeli, M. Falagas, C. Giske, S. Harbarth, J. Hindler, G. Kahlmeter and B. Olsson"Liljequist Multidrug"resistant, extensively drug"resistant and pandrug"resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance Clinical Microbiology and Infection 18 (2012) 268-281.
- A. D. Altalhi, Y. A. Gherbawy and S. A. Hassan Antibiotic resistance in Escherichia coli isolated from retail raw chicken meat in Taif, Saudi Arabia Foodborne pathogens and disease 7 (2010) 281-285.
- A. M. Hessain, A. A. Al-Arfaj, A. M. Zakri, J. K. El-Jakee, O. G. Al-Zogibi, H. A. Hemeg and I. M. Ibrahim Molecular characterization of Escherichia coli O157:H7 recovered from meat and meat products relevant to human health in Riyadh, Saudi Arabia Saudi Journal of Biological Sciences 22 (2015) 725-729. DOI: https://doi.org/10.1016/j.sjbs.2015.06.009.
- M. Bharathi, R. Ramakrishnan, V. Maneksha, C. Shivakumar, V. Nithya and S. Mittal Comparative bacteriology of acute and chronic dacryocystitis Eye 22 (2008) 953.
- D. Briscoe, A. Rubowitz and E. I. Assia Changing bacterial isolates and antibiotic sensitivities of purulent dacryocystitis Orbit 24 (2005) 29-32.
- P. Martinez-Freijo, A. Fluit, F. Schmitz, V. Grek, J. Verhoef and M. Jones Class I integrons in Gram-negative isolates from different European hospitals and association with decreased susceptibility to multiple antibiotic compounds The Journal of antimicrobial chemotherapy 42 (1998) 689-696.
- C.-Y. Chang, L.-L. Chang, Y.-H. Chang, T.-m. Lee and S.-f. Chang Characterisation of drug resistance gene cassettes associated with class 1 integrons in clinical isolates of Escherichia coli from Taiwan, ROC Journal of medical microbiology 49 (2000) 1097-1102.
- Z. Xu, L. Li, M. E. Shirtliff, B. M. Peters, Y. Peng, M. J. Alam, S. Yamasaki and L. Shi First report of class 2 integron in clinical Enterococcus faecalis and class 1 integron in Enterococcus faecium in South China Diagnostic microbiology and infectious disease 68 (2010) 315-317.
- F. Yao, Y. Qian, S. Chen, P. Wang and Y. Huang Incidence of Extended"Spectrum β"Lactamases and Characterization of Integrons in Extended"Spectrum β"Lactamase"producing Klebsiella pneumoniae Isolated in Shantou, China Acta biochimica et biophysica Sinica 39 (2007) 527-532.
- A. Bhattacharjee, M. Sen, P. Prakash, A. Gaur, S. Anupurba and G. Nath Observation on integron carriage among clinical isolates of Klebsiella pneumoniae producing extended-spectrum β-lactamases Indian journal of medical microbiology 28 (2010) 207.
- C. Baker-Austin, M. S. Wright, R. Stepanauskas and J. McArthur Co-selection of antibiotic and metal resistance Trends in microbiology 14 (2006) 176-182.
- C. Oliveira-Pinto, C. Diamantino, P. L. Oliveira, M. P. Reis, P. S. Costa, M. C. Paiva, R. M. Nardi, P. P. Magalhí£es, E. Chartone-Souza and A. M. Nascimento Occurrence and characterization of class 1 integrons in Escherichia coli from healthy individuals and those with urinary infection Journal of medical microbiology 66 (2017) 577-583.
References
W. H. DePas, A. K. Syed, M. Sifuentes, J. S. Lee, D. Warshaw, V. Saggar, G. Csankovszki, B. R. Boles and M. R. Chapman Biofilm formation protects Escherichia coli against killing by Caenorhabditis elegans and Myxococcus xanthus Applied and environmental microbiology 80 (2014) 7079-7087.
A. Monteiro and S. C. Verde Bacterial Bioburden in Hospital Environment. in: Exposure to Microbiological Agents in Indoor and Occupational Environments (Ed.^, Eds.), Springer, 2017, 321-328.
E. Scallan, R. Hoekstra, B. Mahon, T. Jones and P. Griffin An assessment of the human health impact of seven leading foodborne pathogens in the United States using disability adjusted life years Epidemiology & Infection 143 (2015) 2795-2804.
E. Franz, P. Delaquis, S. Morabito, L. Beutin, K. Gobius, D. A. Rasko, J. Bono, N. French, J. Osek and B.-A. Lindstedt Exploiting the explosion of information associated with whole genome sequencing to tackle Shiga toxin-producing Escherichia coli (STEC) in global food production systems International journal of food microbiology 187 (2014) 57-72.
R. Laxminarayan, A. Duse, C. Wattal, A. K. Zaidi, H. F. Wertheim, N. Sumpradit, E. Vlieghe, G. L. Hara, I. M. Gould and H. Goossens Antibiotic resistance”the need for global solutions The Lancet infectious diseases 13 (2013) 1057-1098.
D. Venieri, I. Gounaki, M. Bikouvaraki, V. Binas, A. Zachopoulos, G. Kiriakidis and D. Mantzavinos Solar photocatalysis as disinfection technique: Inactivation of Klebsiella pneumoniae in sewage and investigation of changes in antibiotic resistance profile Journal of environmental management 195 (2017) 140-147.
S. Abraham, H. S. Wong, J. Turnidge, J. R. Johnson and D. J. Trott Carbapenemase-producing bacteria in companion animals: a public health concern on the horizon Journal of Antimicrobial Chemotherapy 69 (2014) 1155-1157.
M. M. Elseviers, Y. Van Camp, S. Nayaert, K. Duré, L. Annemans, A. Tanghe and S. Vermeersch Prevalence and management of antibiotic associated diarrhea in general hospitals BMC infectious diseases 15 (2015) 129.
A. A. H. Abdalla Isolation and Antimicrobial Susceptibility Patterns of Escherichia Coli in Patients with Urinary Tract Infections in Al-Ribat University Hospital-Khartoum. (Ed.^, Eds.), Sudan University of Science & Technology, 2016.
P. Harnvoravongchai, M. Pipatthana, S. Chankhamhaengdecha and T. Janvilisri Insights into drug resistance mechanisms in Clostridium difficile Essays In Biochemistry 61 (2017) 81-88.
V. Kasimanickam, K. Owen and R. Kasimanickam Detection of genes encoding multidrug resistance and biofilm virulence factor in uterine pathogenic bacteria in postpartum dairy cows Theriogenology 85 (2016) 173-179.
B. Chen, K. Yuan, X. Chen, Y. Yang, T. Zhang, Y. Wang, T. Luan, S. Zou and X. Li Metagenomic analysis revealing antibiotic resistance genes (ARGs) and their genetic compartments in the Tibetan environment Environmental science & technology 50 (2016) 6670-6679.
A. Fluit and F. J. Schmitz Resistance integrons and super-integrons Clinical Microbiology and Infection 10 (2004) 272-288.
O. Fasugba, A. Gardner, B. G. Mitchell and G. Mnatzaganian Ciprofloxacin resistance in community-and hospital-acquired Escherichia coli urinary tract infections: a systematic review and meta-analysis of observational studies BMC infectious diseases 15 (2015) 545.
C. Dureja, S. Mahajan and S. Raychaudhuri Phylogenetic distribution and prevalence of genes encoding class I integrons and CTX-M-15 extended-spectrum β-lactamases in Escherichia coli isolates from healthy humans in Chandigarh, India PloS one 9 (2014) e112551.
A. Felten, B. Grandry, P. H. Lagrange and I. Casin Evaluation of three techniques for detection of low-level methicillin-resistant Staphylococcus aureus (MRSA): a disk diffusion method with cefoxitin and moxalactam, the Vitek 2 system, and the MRSA-screen latex agglutination test Journal of clinical microbiology 40 (2002) 2766-2771.
A. P. Magiorakos, A. Srinivasan, R. Carey, Y. Carmeli, M. Falagas, C. Giske, S. Harbarth, J. Hindler, G. Kahlmeter and B. Olsson"Liljequist Multidrug"resistant, extensively drug"resistant and pandrug"resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance Clinical Microbiology and Infection 18 (2012) 268-281.
A. D. Altalhi, Y. A. Gherbawy and S. A. Hassan Antibiotic resistance in Escherichia coli isolated from retail raw chicken meat in Taif, Saudi Arabia Foodborne pathogens and disease 7 (2010) 281-285.
A. M. Hessain, A. A. Al-Arfaj, A. M. Zakri, J. K. El-Jakee, O. G. Al-Zogibi, H. A. Hemeg and I. M. Ibrahim Molecular characterization of Escherichia coli O157:H7 recovered from meat and meat products relevant to human health in Riyadh, Saudi Arabia Saudi Journal of Biological Sciences 22 (2015) 725-729. DOI: https://doi.org/10.1016/j.sjbs.2015.06.009.
M. Bharathi, R. Ramakrishnan, V. Maneksha, C. Shivakumar, V. Nithya and S. Mittal Comparative bacteriology of acute and chronic dacryocystitis Eye 22 (2008) 953.
D. Briscoe, A. Rubowitz and E. I. Assia Changing bacterial isolates and antibiotic sensitivities of purulent dacryocystitis Orbit 24 (2005) 29-32.
P. Martinez-Freijo, A. Fluit, F. Schmitz, V. Grek, J. Verhoef and M. Jones Class I integrons in Gram-negative isolates from different European hospitals and association with decreased susceptibility to multiple antibiotic compounds The Journal of antimicrobial chemotherapy 42 (1998) 689-696.
C.-Y. Chang, L.-L. Chang, Y.-H. Chang, T.-m. Lee and S.-f. Chang Characterisation of drug resistance gene cassettes associated with class 1 integrons in clinical isolates of Escherichia coli from Taiwan, ROC Journal of medical microbiology 49 (2000) 1097-1102.
Z. Xu, L. Li, M. E. Shirtliff, B. M. Peters, Y. Peng, M. J. Alam, S. Yamasaki and L. Shi First report of class 2 integron in clinical Enterococcus faecalis and class 1 integron in Enterococcus faecium in South China Diagnostic microbiology and infectious disease 68 (2010) 315-317.
F. Yao, Y. Qian, S. Chen, P. Wang and Y. Huang Incidence of Extended"Spectrum β"Lactamases and Characterization of Integrons in Extended"Spectrum β"Lactamase"producing Klebsiella pneumoniae Isolated in Shantou, China Acta biochimica et biophysica Sinica 39 (2007) 527-532.
A. Bhattacharjee, M. Sen, P. Prakash, A. Gaur, S. Anupurba and G. Nath Observation on integron carriage among clinical isolates of Klebsiella pneumoniae producing extended-spectrum β-lactamases Indian journal of medical microbiology 28 (2010) 207.
C. Baker-Austin, M. S. Wright, R. Stepanauskas and J. McArthur Co-selection of antibiotic and metal resistance Trends in microbiology 14 (2006) 176-182.
C. Oliveira-Pinto, C. Diamantino, P. L. Oliveira, M. P. Reis, P. S. Costa, M. C. Paiva, R. M. Nardi, P. P. Magalhí£es, E. Chartone-Souza and A. M. Nascimento Occurrence and characterization of class 1 integrons in Escherichia coli from healthy individuals and those with urinary infection Journal of medical microbiology 66 (2017) 577-583.