Allele distribution and phenotypic resistance to ciprofloxacin and gentamicin among extended spectrum β-lactamases producing Escherichia coli from urine, stool, animals and environments of patients with presumptive urinary tract infection in Tanzania

Adam A. Mwakyoma; Benson R. Kidenya; Caroline A. Minja; Martha F. Mushi; Alison Fiona Sandeman; Wilber Sabiiti; Matthew Holden; Stephen E. Mshana

doi:10.3389/frabi.2023.1164016

Allele distribution and phenotypic resistance to ciprofloxacin and gentamicin among extended spectrum β-lactamases producing Escherichia coli from urine, stool, animals and environments of patients with presumptive urinary tract infection in Tanzania

Adam A. Mwakyoma, Benson R. Kidenya^*, Caroline A. Minja, Martha F. Mushi, Alison Fiona Sandeman, Wilber Sabiiti, Matthew Holden, Stephen E. Mshana

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Abstract

Background: Additional antimicrobial resistance to extended spectrum β-lactamases (ESBL)-producing E. coli exhausts treatment options. We investigated allele distribution and resistance to ciprofloxacin and gentamicin among ESBL-producing E. coli isolates from urine, stool, animals and environments of presumptive urinary tract infection (UTI) patients, in order to gain a crucial insight towards devising prevention and control measures, and treatment guidelines.

Methods: Archived ESBL-producing E. coli isolates from urine, stool, animals and surrounding environments of presumptive UTI patients were retrieved. Antimicrobial susceptibility profiles to ciprofloxacin and gentamicin were done followed by multi-plex PCR for bl_aCTX-M, bla_TEM and bla_SHV, to determine ESBL alleles distribution. Data were analysed using STATA version 17.

Results: A total of 472 confirmed ESBL-producing E. coli isolates from Mwanza 243 (51.5%), Kilimanjaro 143 (30.3%) and Mbeya 86 (18.2%) were analyzed. Of these, 75 (15.9%) were from urine, 199 (42.2%) from stool, 58 (12.3%) from rectal/cloaca swabs of animals and 140 (29.7%) from surrounding environments. Out of 472 ESBL producing E. coli, 98.9% (467) had at least one ESBL allele. The most frequent allele was bla_CTX-M detected in 88.1% (416/472) isolates, followed by bla_TEM allele detected in 51.5% (243/472) isolates. There were 40.7% (192/472) isolates harboring dual bla_CTX-M + bla_TEM alleles, and only 0.2% (1/472) isolate had dual bla_CTX-M+ bla_SHV alleles whereas 2.3% (11/472) isolates had a combination of all three alleles (bla_CTX-M + bla_TEM + bla_SHV). None of the isolates harbored a combination of bla_TEM + bla_SHV only. Resistance to ciprofloxacin and gentamicin was observed in 70.8% (334/472) and 46.0% (217/472) isolates, respectively. There was a significant difference in distribution of resistance to ciprofloxacin as well as to gentamicin among ESBL-producing E. coli isolated from various sources (p-value < 0.001 and 0.002, respectively.

Conclusion: Almost all ESBL-producing E. coli isolates carry bla_CTX-M, bla_TEM and bla_SHV either alone or in combination with the most common alleles being bla_CTX-M. The resistance to cipropfloxacin and gentamicin which are front-line antibiotics for UTIs among ESBL producing E. coli is high. This implies the need to continuously revise the local guidelines used for optimal empirical therapy for UTI and continual surveillance using one health approach.

Original language	English
Article number	1164016
Number of pages	11
Journal	Frontiers in Antibiotics
Volume	2
DOIs	https://doi.org/10.3389/frabi.2023.1164016
Publication status	Published - 5 Jun 2023

Keywords

ESBL-producing E. coli
ESBL allele
Non-beta lactam antiobiotic
Ciprofloxacin
Gentamicin

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Copyright © 2023 Mwakyoma, Kidenya, Minja, Mushi, Sandeman, Sabiti, Holden and Mshana. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
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Prof M Holden MRC: Holistic approach to unravel antibacterial resistance in East Africa (HATUA)
Holden, M. (PI), Gillespie, S. H. (CoI), Keenan, K. L. (CoI), Kesby, M. (CoI), Lynch, A. (CoI), Sabiiti, W. (CoI), Sloan, D. J. (CoI) & Smith, V. A. (CoI)
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Mwakyoma, A. A., Kidenya, B. R., Minja, C. A., Mushi, M. F., Sandeman, A. F., Sabiiti, W., Holden, M., & Mshana, S. E. (2023). Allele distribution and phenotypic resistance to ciprofloxacin and gentamicin among extended spectrum β-lactamases producing Escherichia coli from urine, stool, animals and environments of patients with presumptive urinary tract infection in Tanzania. Frontiers in Antibiotics, 2, Article 1164016. https://doi.org/10.3389/frabi.2023.1164016

@article{7e1833037d364470b6f2ccc5dd03e327,

title = "Allele distribution and phenotypic resistance to ciprofloxacin and gentamicin among extended spectrum β-lactamases producing Escherichia coli from urine, stool, animals and environments of patients with presumptive urinary tract infection in Tanzania",

abstract = "Background: Additional antimicrobial resistance to extended spectrum β-lactamases (ESBL)-producing E. coli exhausts treatment options. We investigated allele distribution and resistance to ciprofloxacin and gentamicin among ESBL-producing E. coli isolates from urine, stool, animals and environments of presumptive urinary tract infection (UTI) patients, in order to gain a crucial insight towards devising prevention and control measures, and treatment guidelines.Methods: Archived ESBL-producing E. coli isolates from urine, stool, animals and surrounding environments of presumptive UTI patients were retrieved. Antimicrobial susceptibility profiles to ciprofloxacin and gentamicin were done followed by multi-plex PCR for blaCTX-M, blaTEM and blaSHV, to determine ESBL alleles distribution. Data were analysed using STATA version 17.Results: A total of 472 confirmed ESBL-producing E. coli isolates from Mwanza 243 (51.5%), Kilimanjaro 143 (30.3%) and Mbeya 86 (18.2%) were analyzed. Of these, 75 (15.9%) were from urine, 199 (42.2%) from stool, 58 (12.3%) from rectal/cloaca swabs of animals and 140 (29.7%) from surrounding environments. Out of 472 ESBL producing E. coli, 98.9% (467) had at least one ESBL allele. The most frequent allele was blaCTX-M detected in 88.1% (416/472) isolates, followed by blaTEM allele detected in 51.5% (243/472) isolates. There were 40.7% (192/472) isolates harboring dual blaCTX-M + blaTEM alleles, and only 0.2% (1/472) isolate had dual blaCTX-M + blaSHV alleles whereas 2.3% (11/472) isolates had a combination of all three alleles (blaCTX-M + blaTEM + blaSHV). None of the isolates harbored a combination of blaTEM + blaSHV only. Resistance to ciprofloxacin and gentamicin was observed in 70.8% (334/472) and 46.0% (217/472) isolates, respectively. There was a significant difference in distribution of resistance to ciprofloxacin as well as to gentamicin among ESBL-producing E. coli isolated from various sources (p-value < 0.001 and 0.002, respectively. Conclusion: Almost all ESBL-producing E. coli isolates carry blaCTX-M, blaTEM and blaSHV either alone or in combination with the most common alleles being blaCTX-M. The resistance to cipropfloxacin and gentamicin which are front-line antibiotics for UTIs among ESBL producing E. coli is high. This implies the need to continuously revise the local guidelines used for optimal empirical therapy for UTI and continual surveillance using one health approach.",

keywords = "ESBL-producing E. coli, ESBL allele, Non-beta lactam antiobiotic, Ciprofloxacin, Gentamicin",

author = "Mwakyoma, {Adam A.} and Kidenya, {Benson R.} and Minja, {Caroline A.} and Mushi, {Martha F.} and Sandeman, {Alison Fiona} and Wilber Sabiiti and Matthew Holden and Mshana, {Stephen E.}",

note = "Funding: This study was funded by the Holistic Approach to Unravel Antibacterial Resistance in East Africa (HATUA) project funded by the National Institute for Health Research, Medical Research Council, and the Department of Health and Social Care, Award (MR/S004785/1).",

year = "2023",

month = jun,

day = "5",

doi = "10.3389/frabi.2023.1164016",

language = "English",

volume = "2",

journal = "Frontiers in Antibiotics",

}

Mwakyoma, AA, Kidenya, BR, Minja, CA, Mushi, MF, Sandeman, AF , Sabiiti, W , Holden, M & Mshana, SE 2023, 'Allele distribution and phenotypic resistance to ciprofloxacin and gentamicin among extended spectrum β-lactamases producing Escherichia coli from urine, stool, animals and environments of patients with presumptive urinary tract infection in Tanzania', Frontiers in Antibiotics, vol. 2, 1164016. https://doi.org/10.3389/frabi.2023.1164016

Allele distribution and phenotypic resistance to ciprofloxacin and gentamicin among extended spectrum β-lactamases producing Escherichia coli from urine, stool, animals and environments of patients with presumptive urinary tract infection in Tanzania. / Mwakyoma, Adam A.; Kidenya, Benson R.; Minja, Caroline A. et al.
In: Frontiers in Antibiotics, Vol. 2, 1164016, 05.06.2023.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - Allele distribution and phenotypic resistance to ciprofloxacin and gentamicin among extended spectrum β-lactamases producing Escherichia coli from urine, stool, animals and environments of patients with presumptive urinary tract infection in Tanzania

AU - Mwakyoma, Adam A.

AU - Kidenya, Benson R.

AU - Minja, Caroline A.

AU - Mushi, Martha F.

AU - Sandeman, Alison Fiona

AU - Sabiiti, Wilber

AU - Holden, Matthew

AU - Mshana, Stephen E.

N1 - Funding: This study was funded by the Holistic Approach to Unravel Antibacterial Resistance in East Africa (HATUA) project funded by the National Institute for Health Research, Medical Research Council, and the Department of Health and Social Care, Award (MR/S004785/1).

PY - 2023/6/5

Y1 - 2023/6/5

N2 - Background: Additional antimicrobial resistance to extended spectrum β-lactamases (ESBL)-producing E. coli exhausts treatment options. We investigated allele distribution and resistance to ciprofloxacin and gentamicin among ESBL-producing E. coli isolates from urine, stool, animals and environments of presumptive urinary tract infection (UTI) patients, in order to gain a crucial insight towards devising prevention and control measures, and treatment guidelines.Methods: Archived ESBL-producing E. coli isolates from urine, stool, animals and surrounding environments of presumptive UTI patients were retrieved. Antimicrobial susceptibility profiles to ciprofloxacin and gentamicin were done followed by multi-plex PCR for blaCTX-M, blaTEM and blaSHV, to determine ESBL alleles distribution. Data were analysed using STATA version 17.Results: A total of 472 confirmed ESBL-producing E. coli isolates from Mwanza 243 (51.5%), Kilimanjaro 143 (30.3%) and Mbeya 86 (18.2%) were analyzed. Of these, 75 (15.9%) were from urine, 199 (42.2%) from stool, 58 (12.3%) from rectal/cloaca swabs of animals and 140 (29.7%) from surrounding environments. Out of 472 ESBL producing E. coli, 98.9% (467) had at least one ESBL allele. The most frequent allele was blaCTX-M detected in 88.1% (416/472) isolates, followed by blaTEM allele detected in 51.5% (243/472) isolates. There were 40.7% (192/472) isolates harboring dual blaCTX-M + blaTEM alleles, and only 0.2% (1/472) isolate had dual blaCTX-M + blaSHV alleles whereas 2.3% (11/472) isolates had a combination of all three alleles (blaCTX-M + blaTEM + blaSHV). None of the isolates harbored a combination of blaTEM + blaSHV only. Resistance to ciprofloxacin and gentamicin was observed in 70.8% (334/472) and 46.0% (217/472) isolates, respectively. There was a significant difference in distribution of resistance to ciprofloxacin as well as to gentamicin among ESBL-producing E. coli isolated from various sources (p-value < 0.001 and 0.002, respectively. Conclusion: Almost all ESBL-producing E. coli isolates carry blaCTX-M, blaTEM and blaSHV either alone or in combination with the most common alleles being blaCTX-M. The resistance to cipropfloxacin and gentamicin which are front-line antibiotics for UTIs among ESBL producing E. coli is high. This implies the need to continuously revise the local guidelines used for optimal empirical therapy for UTI and continual surveillance using one health approach.

AB - Background: Additional antimicrobial resistance to extended spectrum β-lactamases (ESBL)-producing E. coli exhausts treatment options. We investigated allele distribution and resistance to ciprofloxacin and gentamicin among ESBL-producing E. coli isolates from urine, stool, animals and environments of presumptive urinary tract infection (UTI) patients, in order to gain a crucial insight towards devising prevention and control measures, and treatment guidelines.Methods: Archived ESBL-producing E. coli isolates from urine, stool, animals and surrounding environments of presumptive UTI patients were retrieved. Antimicrobial susceptibility profiles to ciprofloxacin and gentamicin were done followed by multi-plex PCR for blaCTX-M, blaTEM and blaSHV, to determine ESBL alleles distribution. Data were analysed using STATA version 17.Results: A total of 472 confirmed ESBL-producing E. coli isolates from Mwanza 243 (51.5%), Kilimanjaro 143 (30.3%) and Mbeya 86 (18.2%) were analyzed. Of these, 75 (15.9%) were from urine, 199 (42.2%) from stool, 58 (12.3%) from rectal/cloaca swabs of animals and 140 (29.7%) from surrounding environments. Out of 472 ESBL producing E. coli, 98.9% (467) had at least one ESBL allele. The most frequent allele was blaCTX-M detected in 88.1% (416/472) isolates, followed by blaTEM allele detected in 51.5% (243/472) isolates. There were 40.7% (192/472) isolates harboring dual blaCTX-M + blaTEM alleles, and only 0.2% (1/472) isolate had dual blaCTX-M + blaSHV alleles whereas 2.3% (11/472) isolates had a combination of all three alleles (blaCTX-M + blaTEM + blaSHV). None of the isolates harbored a combination of blaTEM + blaSHV only. Resistance to ciprofloxacin and gentamicin was observed in 70.8% (334/472) and 46.0% (217/472) isolates, respectively. There was a significant difference in distribution of resistance to ciprofloxacin as well as to gentamicin among ESBL-producing E. coli isolated from various sources (p-value < 0.001 and 0.002, respectively. Conclusion: Almost all ESBL-producing E. coli isolates carry blaCTX-M, blaTEM and blaSHV either alone or in combination with the most common alleles being blaCTX-M. The resistance to cipropfloxacin and gentamicin which are front-line antibiotics for UTIs among ESBL producing E. coli is high. This implies the need to continuously revise the local guidelines used for optimal empirical therapy for UTI and continual surveillance using one health approach.

KW - ESBL-producing E. coli

KW - ESBL allele

KW - Non-beta lactam antiobiotic

KW - Ciprofloxacin

KW - Gentamicin

U2 - 10.3389/frabi.2023.1164016

DO - 10.3389/frabi.2023.1164016

M3 - Article

VL - 2

JO - Frontiers in Antibiotics

JF - Frontiers in Antibiotics

M1 - 1164016

ER -

Mwakyoma AA, Kidenya BR, Minja CA, Mushi MF, Sandeman AF , Sabiiti W et al. Allele distribution and phenotypic resistance to ciprofloxacin and gentamicin among extended spectrum β-lactamases producing Escherichia coli from urine, stool, animals and environments of patients with presumptive urinary tract infection in Tanzania. Frontiers in Antibiotics. 2023 Jun 5;2:1164016. doi: 10.3389/frabi.2023.1164016

Allele distribution and phenotypic resistance to ciprofloxacin and gentamicin among extended spectrum β-lactamases producing Escherichia coli from urine, stool, animals and environments of patients with presumptive urinary tract infection in Tanzania

Abstract

Keywords

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Prof M Holden MRC: Holistic approach to unravel antibacterial resistance in East Africa (HATUA)

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