• NUHU TANKO Department of Pharmaceutics and Pharmaceutical Microbiology, Faculty of Pharmaceutical Sciences, Usmanu Danfodiyo University Sokoto
  • R. O. BOLAJI Department of Pharmaceutical Microbiology and Biotechnology, Faculty of Pharmaceutical Sciences, Ahmadu Bello University Zaria
  • B. O. OLAYINKA Department of Pharmaceutical Microbiology and Biotechnology, Faculty of Pharmaceutical Sciences, Ahmadu Bello University Zaria
  • O. B. B. EUGENE Institute for Research in Molecular Medicine, University Sains Malaysia


Objective: Infections of the urinary tract remains one of the most common bacterial infections with many implicated organisms being Gram-negative, which are increasingly resistant to antimicrobial agents. The aim of the study was to evaluate the resistance of ESBL producing Gram-negative enterobacteriaceae to commonly prescribed antibiotics and the prevalence of CTX-M genes from these isolates using polymerase chain reaction (PCR).

Methods: The isolates were collected from urine over a period of 4 mo and studied, and were identified using Microgen Identification Kit (GN-ID). Susceptibility testing was performed by the modified Kirby Bauer disc diffusion method, and results were interpreted according to Clinical and Laboratory Standard Institute (CLSI). Extended-Spectrum Beta-Lactamase (ESBL) production was detected by the double-disc synergy test (DDST). Molecular characterization was based on the isolates that were positive for the phenotypic detection of ESBL.

Results: Sixty one (61) isolates of Gram-negative uropathogens were identified. Of these, 19 (31.2%) were E. coli, 15 (24.6%) were Salmonella arizonae, Klebsiella pneumoniae were 7 (11.5%), Klebsiella oxytoca were 3 (4.9%), Enterobacter gergoviae were 6 (9.8%), 4 (6.6%) were Citrobacter freundii, 4 (6.6%) were Serratia marscence, and 1 (1.6%) were Enterobacter aerogenes, Proteus mirabilis, and Edwardsiella tarda each. Analysis of the bacterial susceptibility to antibiotics revealed most of them to be generally resistant to cotrimoxazole (73.3%), nalidixic acid (66.7%), norfloxacin (53.5%), ciprofloxacin (50.5%), gentamicin (48.6%), amoxicillin/clavulanate (45%), and the least resistant was displayed in nitrofurantoin (30%). Of the 15 ESBL producers, 11 (73.3%) were harbouring bla CTX-M genes.

Conclusion: The study revealed a high susceptibility to nitrofurantoin, whereas susceptibility to cotrimoxazole was lowest. It further portrays a high prevalence of enterobacteriaceae isolates harbouring bla CTX-M genes in Sokoto metropolis.

Keywords: Resistance, Prevalence, Gram-negative, Urinary Tract Infections, CTX-M


Download data is not yet available.


1. Manikandan S, Ganesapandian S, Manoj S, Kumaraguru AK. Antimicrobial susceptibility pattern of urinary tract infection causing human pathogenic bacteria. Asian J Med Sci 2011;3:56-60.
2. Angima BK, Usha R. Modification of urinary catheters using antimicrobials from Streptomyces sp. ABK 07 for urinary tract infection resistance. Asian J Clin Res 2018;11:158-62.
3. Khalifa AAF, Harb AO, Alkout AM. Urinary tract infection in sobrata, algmel cities in libya 2013. J Clin Microbiol 2014;3:1000163.
4. Wagenlehner FME, Naber KG. Treatment of bacterial urinary tract infections: present and future. J Euro Assoc Urol 2006;49:235-44.
5. Chom Tompkins NH. Multidrug-resistant gram-negative infections bringing back the old. J Crit Care Nurs 2011;34:87-100.
6. Dominika O, Pawel S, Piotr W, Slawomir C, Anna M, Jadwiga J, et al. The occurrence of blaCTX-M, blaSHV, and blaTEM genes in extended-spectrum beta-lactamase positive strains of Klebsiella pneumoniae, Escherichia coli, and Proteus mirabilis in poland. Int J Antibiotics 2014:1-7. 935842.
7. Song S, Lee EY, Koh EM, Ha HS, Jeong HJ, Bae IK, et al. Antibiotic resistance mechanisms of Escherichia coli isolates from urinary specimens. Korean J Lab Med 2009;29:17-24.
8. Dhillon RH, Clark J. ESBLs: a clear and present danger? Crit Care Res Pract 2012:625170. Doi:10.1155/2012/625170
9. Sridhar Rao PN. Extended-spectrum beta-lactamases-a comprehensive review. Available from: [Last accessed on 15 Feb 2017].
10. Mathur P, Kapil A, Das B, Dhawan B. Prevalence of extended-spectrum beta-lactamase-producing gram-negative bacteria in tertiary care hospital. Indian J Med Res 2002;115:153-7.
11. David ML, Canton R, Gniakowski M, Nordmann P, Rossolini GM, Ayala J, et al. CTX-M: changing the face of ESBLs in Europe. J Antmicr Chem 2007;59:165-74.
12. Ogbolu DO, Terry Alli OA, Webber MA, Oluremi AS, Oloyede OM. CTX-M-15 is established in most multidrug-resistant uropathogenic enterobacteriaceae and Pseudomonaceae from Hospitals in Nigeria. Euro J Microbiol Immun 2018;8:20–4.
13. Aibinu I, Odugbemi T, Koenig W, Ghebremedhin B. Sequence type ST131 and ST10 complex (ST617) predominant among CTX-M-15-producing Escherichia coli isolates from Nigeria. J Clin Microbiol Infect 2012;18:E49-E51.
14. Bajpai T, Pandey M, Varma M, Bhatambare GS. Prevalence of TEM, SHV, and CTX-M beta lactamase genes in the urinary isolates of a tertiary care hospital. Avicenna J Med 2017;7:12-6.
15. Naseer U, Sundsfjord A. The CTX-M conundrum: dissemination of plasmids and Escherichia coli clones. J Microbiol Drug Resist 2011;17:83-97.
16. Canton R, Gonzalez Alba JM, Galan JC. CTX-M enzymes: origin and diffusion. Front Microbiol 2012;3:110.
17. Clinical Laboratory Standard Institute (CLSI). Perfomance standards of antimicrobial disc and dilution susceptibility tests for bacteria isolated from animal, approved standard. 3rd edition; 2012.
18. Agamy GT, Tharwat RE, Maggie AI, Adel EA. Detection of extended-spectrum beta-lactamases produced by E. coli urinary pathogens at Assiut University Hospital. Bull Pharm Sci Assiut University 2011;34:93-103.
19. Colodner R. Extended-spectrum beta lactamses: a challenge for clinical microbiologists and infection control specialists. Am J Infect Control 2005;33:104-7.
20. El-Kersh TA, Marie MA. Al-Sheikh YA, Al-Kahtani SA. Prevalence and risk factors of community-acquired urinary tract infections due to ESBL-producing Gram negative bacteria in an armed forces hospital in Southern Saudi Arabia. Glo Adv Res J Med Med Sci 2015;4:321-30.
21. Hawkey PM. Prevalence and clonality of extended spectrum beta lactamases in Asia. J Clin Microbiol Infect 2008;14(Suppl 1):159-63.
22. Fernandes R, Amador P, Oliveira C, Prudencio C. Molecular characterization of ESBL-producing Enterobacteriaceae in Northern Portugal. Sci World J 2014. Doi:10.1155/2014/ 782897.
23. Bali EB, Accedil L, Sultan N. Phenotypic and molecular characterization of SHV, TEM CTX-M and extended spectrum beta-lactamase produced by E. coli, Acinetobacter baumanii and Klebsiella isolates in a Turkish hospital. Afr J Microbiol Res 2010;4:650-4.
24. Nisha KV, Veena SA, Rathika SD, Vijaya SM, Avinash SK. Antimicrobial susceptibility; risk factors and prevalence of bla cefotaximase, temoneira, and sulfhydryl variable genes among E. coli in community-acquired pediatric urinary tract infection. J Lab Phys 2017;9:156-62.
25. Rezai MS, Salehifar E, Rafiei A, Langee T, Rafati M, Shafahi K, et al. Characterization of multidrug-resistant extended-spectrum beta-lactamase-producing E. coli among uropathogens of pediatrics on North of Iran. Biomed Res Int 2015.
26. Shahid M, Singh A, Sobia F, Rashid M, Malik A, Shukla I, et al. Bla (CTX-M), bla (TEM), and bla (SHV) in enterobacteriaceae from North-Indian tertiary hospital: High occurrence of combination genes. Asian Pac J Trop Med 2011;4:101-5.
27. Sima SS, Mehdi G, Fattaneh S. Relation between blaTEM, blaSHV and blaCTX-M genes and acute urinary tract infections. J Acute Dis 2016;5:71-6.
28. Muhammad NU, Bature M, Nuhu T, Nafiu A. Antibiotic susceptibility testing for Escherichia coli causing urinary tract infections in sokoto metropolis. Asian J Pharm Clin Res 2018;11:373-6.
161 Views | 211 Downloads
How to Cite
TANKO, N., R. O. BOLAJI, B. O. OLAYINKA, and O. B. B. EUGENE. “PREVALENCE OF CTX-M-PRODUCING GRAM-NEGATIVE UROPATHOGENS IN SOKOTO, NORTH-WESTERN NIGERIA”. International Journal of Pharmacy and Pharmaceutical Sciences, Vol. 12, no. 1, Jan. 2020, pp. 21-25, doi:10.22159/ijpps.2020v12i1.35863.
Original Article(s)