Genotypic pattern of fluoroquinolone resistance among extended-spectrum beta-lactamase-producing <em>Escherichia coli</em>

Authors

  • Tati Febrianti Centre for Health Resilience and Resources Policy, Health Policy Agency, Ministry of Health of the Republic of Indonesia, Jakarta, Indonesia; Master’s Programme in Biomedical Science, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia
  • Nelly Puspandasari Centre for Health Resilience and Resources Policy, Health Policy Agency, Ministry of Health of the Republic of Indonesia, Jakarta, Indonesia
  • Dwi Febriyana Centre for Health Resilience and Resources Policy, Health Policy Agency, Ministry of Health of the Republic of Indonesia, Jakarta, Indonesia; Master’s Programme in Biomedical Science, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia
  • Tom Weaver DAI-Fleming Fund Country Grant to Indonesia
  • Anis Karuniawati Department of Microbiology, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia

DOI:

https://doi.org/10.13181/mji.oa.247544

Keywords:

Escherichia coli, fluoroquinolone, resistance
Abstract viewed: 0 times
PDF downloaded: 0 times
HTML downloaded: 0 times
EPUB downloaded: 0 times

Abstract

BACKGROUND Fluoroquinolone (FQ) is one of the therapeutic options for treating extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli (ESBL-Ec) infection, but its use could increase the resistance level of ESBL-Ec. This study aimed to analyze the resistant genes responsible for ESBL production and FQ resistance among the ESBL-Ec isolated from healthy humans and communal wastewater.

METHODS This was an observational study using stored isolates and laboratory data. Genome sequencing was done on 43 E. coli DNA isolates before resistance genes, mutations, and high-risk clones were examined through bioinformatic data analysis.

RESULTS The analysis of 39 ESBL-Ec isolates showed ESBL genes, including blaCTX-M-55 (56%), blaCTX-M-15 (31%), and blaCTX-M-27 (8%). ESBL-Ec isolates exhibited mutations in gyrA (54%), gyrB (0%), parC (28%), and parE (10%). Plasmid-mediated quinolone resistance genes detected included qnrS1 (54%), qnrS13 (13%), qnrB2 (3%), aac(6’)-Ib-cr5 (3%), qepA (0%), and oqxAB (0%). ESBL and FQ resistance genes were simultaneously detected in 33 ESBL-Ec isolates, with high-risk clones identified as ST155, ST10, ST23, ST38, ST131, and ST69 Cplx.

CONCLUSIONS ESBL and FQ resistance genes were simultaneously detected in ESBL-Ec isolated from healthy humans and communal wastewater.

Downloads

Download data is not yet available.

References

World Health Organization. WHO integrated global surveillance on ESBL-producing E. coli using a "One Health" approach: implementation and opportunities [Internet]. World Health Organization; 2021 [cited 2023 Jun 2]. Available from: https://www.who.int/publications/i/item/9789240021402.

World Health Organization. Antimicrobial resistance [Internet]. World Health Organization; 2021 [cited 2023 Jun 2]. Available from: https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance.

Sawatwong P, Sapchookul P, Whistler T, Gregory CJ, Sangwichian O, Makprasert S, et al. High burden of extendedspectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae bacteremia in older adults: a seven-year study in two rural Thai Provinces. Am J Trop Med Hyg. 2019;100(4):943−51. https://doi.org/10.4269/ajtmh.18-0394

Puspandari N, Sunarno S, Febrianti T, Febriyana D, Saraswati RD, Rooslamiati I, et al. Extended spectrum beta-lactamase-producing Escherichia coli surveillance in the human, food chain, and environment sectors: tricycle project (pilot) in Indonesia. One Health. 2021;13:100331. https://doi.org/10.1016/j.onehlt.2021.100331

Pathak A, Chandran SP, Mahadik K, Macaden R, Lundborg CS. Frequency and factors associated with carriage of multi-drug resistant commensal Escherichia coli among women attendingantenatal clinics in central India. BMC Infect Dis. 2013;13:199. https://doi.org/10.1186/1471-2334-13-199

Castanheira M, Simner PJ, Bradford PA. Extended-spectrum β-lactamases: an update on their characteristics, epidemiology and detection. JAC Antimicrob Resist. 2021;3(3):dlab092. https://doi.org/10.1093/jacamr/dlab092

Kawamura K, Nagano N, Suzuki M, Wachino JI, Kimura K, Arakawa Y. ESBL-producing Escherichia coli and its rapid rise among healthy people. Food Saf (Tokyo). 2017;5(4):122−50. https://doi.org/10.14252/foodsafetyfscj.2017011

Goldstein FW. Cephalosporinase induction and cephalosporin resistance: a longstanding misinterpretation. Clin Microbiol Infect. 2002;8(12):823−5. https://doi.org/10.1046/j.1469-0691.2002.00492.x

Tamma PD, Aitken SL, Bonomo RA, Mathers AJ, van Duin D, Clancy CJ. Infectious Diseases Society of America 2023 guidance on the treatment of antimicrobial resistant gram-negative infections. Clin Infect Dis. 2023:ciad428. https://doi.org/10.1093/cid/ciad428

Brar RK, Jyoti U, Patil RK, Patil HC. Fluoroquinolone antibiotics: an overview. Adesh Univ J Med Sci Res. 2020;2(1):26−30. https://doi.org/10.25259/AUJMSR_12_2020

Siahaan S, Herman MJ, Fitri N. Antimicrobial resistance situation in Indonesia: a challenge of multisector and global coordination. J Trop Med. 2022;2022:2783300. https://doi.org/10.1155/2022/2783300

Bitew A, Adane A, Abdeta A. Bacteriological spectrum, extended‑spectrum β‑lactamase production and antimicrobial resistance pattern among patients with bloodstream infection in Addis Ababa. Sci Rep. 2023;13(2071). https://doi.org/10.1038/s41598-023-29337-x

Kim B, Kim J, Jo HU, Kwon KT, Ryu SY, Wie SH, et al. Changes in the characteristics of community-onset fluoroquinolone-resistant Escherichia coli isolates causing community-acquired acute pyelonephritis in South Korea. J Microbiol Immunol Infect. 2022;55(4):678−85. https://doi.org/10.1016/j.jmii.2022.01.001

Zurfluh K, Abgottspon H, Hächler H, Nüesch-Inderbinen M, Stephan R. Quinolone resistance mechanisms among extended-spectrum beta-lactamase (ESBL) producing Escherichia coli isolated from rivers and lakes in Switzerland. PLoS One. 2014;9(4):e95864. https://doi.org/10.1371/journal.pone.0095864

Paltansing S, Kraakman ME, Ras JM, Wessels E, Bernards AT. Characterization of fluoroquinolone and cephalosporin resistance mechanisms in Enterobacteriaceae isolated in a Dutch teaching hospital reveals the presence of an Escherichia coli ST131 clone with a specific mutation in parE. J Antimicrob Chemother. 2013;68(1):40−5. https://doi.org/10.1093/jac/dks365

Yang JT, Zhang LJ, Lu Y, Zhang RM, Jiang HX. Genomic insights into global blaCTX-M-55-positive Escherichia coli epidemiology and transmission characteristics. Microbiol Spectr. 2023;11(4):e0108923. https://doi.org/10.1128/spectrum.01089-23

Bevan ER, Jones AM, Hawkey PM. Global epidemiology of CTX-M β-lactamases: temporal and geographical shifts in genotype. J Antimicrob Chemother. 2017;72(8):2145−55. https://doi.org/10.1093/jac/dkx146

Chotinantakul K, Chusri P, Okada S. Detection and characterization of ESBL-producing Escherichia coli and additional co-existence with mcr genes from river water in northern Thailand. PeerJ. 2022;10:e14408. https://doi.org/10.7717/peerj.14408

Robins-Browne RM, Holt KE, Ingle DJ, Hocking DM, Yang J, Tauschek M. Are Escherichia coli pathotypes still relevant in the era of whole-genome sequencing? Front Cell Infect Microbiol. 2016;6:141. https://doi.org/10.3389/fcimb.2016.00141

Negeri AA, Mamo H, Gahlot DK, Gurung JM, Seyoum ET, Francis MS. Characterization of plasmids carrying blaCTX-M genes among extra-intestinal Escherichia coli clinical isolates in Ethiopia. Sci Rep. 2023;13(8595). https://doi.org/10.1038/s41598-023-35402-2

Sewunet T, Asrat D, Woldeamanuel Y, Ny S, Westerlund F, Aseffa A, et al. Polyclonal spread of blaCTX-M-15 through high-risk clones of Escherichia coli at a tertiary hospital in Ethiopia. J Glob Antimicrob Resist. 2022;29:405−12. https://doi.org/10.1016/j.jgar.2021.09.017

Chotinantakul K, Woottisin S, Okada S. The emergence of CTX-M-55 in extended-sectrum β-lactamase-producing Escherichia coli from vegetables sold in local markets of Northern Thailand. Jpn J Infect Dis. 2022;75(3):296−301. https://doi.org/10.7883/yoken.JJID.2021.139

Zhang Y, Peng S, Xu J, Li Y, Pu L, Han X, et al. Genetic context diversity of plasmid-borne blaCTX-M-55 in Escherichia coli isolated from waterfowl. J Glob Antimicrob Resist. 2022;28:185−94. https://doi.org/10.1016/j.jgar.2022.01.015

Gomi R, Yamamoto M, Tanaka M, Matsumura Y. Chromosomal integration of blaCTX-M genes in diverse Escherichia coli isolates recovered from river water in Japan. Curr Res Microb Sci. 2022;3:100144. https://doi.org/10.1016/j.crmicr.2022.100144

Barguigua A, El Otmani F, Talmi M, Zerouali K, Timinouni M. Prevalence and types of extended spectrum β-lactamases among urinary Escherichia coli isolates in Moroccan community. Microb Pathog. 2013;61−2:16−22. https://doi.org/10.1016/j.micpath.2013.04.010

Ridom GmbH. Ridom SeqSphere+ [Internet]. Germany: Ridom GmbH; 2023 [cited 2023 Jun 2]. Available from: https://www.ridom.de/seqsphere/.

Livermore DM, Day M, Cleary P, Hopkins KL, Toleman MA, Wareham DW, et al. OXA-1 β-lactamase and non-susceptibility to penicillin/β-lactamase inhibitor combinations among ESBL-producing Escherichia coli. J Antimicrob Chemother. 2019;74(2):326−33. https://doi.org/10.1093/jac/dky453

Deng H, Si HB, Zeng SY, Sun J, Fang LX, Yang RS, et al. Prevalence of extended-spectrum cephalosporin-resistant Escherichia coli in a farrowing farm: ST1121 clone harboring IncHI2 plasmid contributes to the dissemination of blaCMY-2. Front Microbiol. 2015;6:1210. https://doi.org/10.3389/fmicb.2015.01210

Johnning A, Kristiansson E, Fick J, Weijdegård B, Larsson DG. Resistance mutations in gyrA and parC are common in Escherichia communities of both fluoroquinolone-polluted and uncontaminated aquatic environments. Front Microbiol. 2015;6:1355. https://doi.org/10.3389/fmicb.2015.01355

Hamzah HA, Sirat R, A. Mustafa Mahmud MI, Baharudin R. Mutational analysis of quinolone-resistant determining region gyrA and parC genes in quinolone-resistant ESBL-producing E. coli. IIUM Med J Malaysia. 2021;20(3):101-9. https://doi.org/10.31436/imjm.v20i3.1825

Feng X, Zhang Z, Li X, Song Y, Kang J, Yin D, et al. Mutations in gyrB play an important role in ciprofloxacin-resistant Pseudomonas aeruginosa. Infect Drug Resist. 2019;12:261−72. https://doi.org/10.2147/IDR.S182272

Aworh MK, Abiodun-Adewusi O, Mba N, Helwigh B, Hendriksen RS. Prevalence and risk factors for faecal carriage of multidrug resistant Escherichia coli among slaughterhouse workers. Sci Rep. 2021;11(1):13362. https://doi.org/10.1038/s41598-021-92819-3

Kotb DN, Mahdy WK, Mahmoud MS, Khairy RM. Impact of co-existence of PMQR genes and QRDR mutations on fluoroquinolones resistance in Enterobacteriaceae strains isolated from community and hospital acquired UTIs. BMC Infect Dis. 2019;19(1):979. https://doi.org/10.1186/s12879-019-4606-y

Mustafa MS, Abdullah RM. Prevalence of quinolones resistance proteins encoding genes (qnr genes) and co-resistance with β-lactams among Klebsiella pneumoniae isolates from Iraqi patients. Baghdad Sci J. 2020;17(2):406−14. https://doi.org/10.21123/bsj.2020.17.2.0406

Bodendoerfer E, Marchesi M, Imkamp F, Courvalin P, Böttger EC, Mancini S. Co-occurrence of aminoglycoside and β-lactam resistance mechanisms in aminoglycoside- non-susceptible Escherichia coli isolated in the Zurich area, Switzerland. Int J Antimicrob Agents. 2020;56(1):106019. https://doi.org/10.1016/j.ijantimicag.2020.106019

Kariuki K, Diakhate MM, Musembi S, Tornberg-Belanger SN, Rwigi D, Mutuma T, et al. Plasmid-mediated quinolone resistance genes detected in ciprofloxacin non-susceptible Escherichia coli and Klebsiella isolated from children under five years at hospital discharge, Kenya. BMC Microbiol. 2023;23(1):129. https://doi.org/10.1186/s12866-023-02849-2

Corona F, Martinez JL. Phenotypic resistance to antibiotics. Antibiotics (Basel). 2013;2(2):237−55. https://doi.org/10.3390/antibiotics2020237

Thomson KS, Cornish NE, Hong SG, Hemrick K, Herdt C, Moland ES. Comparison of Phoenix and VITEK 2 extended-spectrum-beta-lactamase detection tests for analysis of Escherichia coli and Klebsiella isolates with well-characterized beta-lactamases. J Clin Microbiol. 2007;45(8):2380−4. https://doi.org/10.1128/JCM.00776-07

Kocsis B, Gulyás D, Szabó D. Emergence and dissemination of extraintestinal pathogenic high-risk international clones of Escherichia coli. Life (Basel). 2022;12(12):2077. https://doi.org/10.3390/life12122077

Gasparrini AJ, Markley JL, Kumar H, Wang B, Fang L, Irum S, et al. Tetracycline-inactivating enzymes from environmental, human commensal, and pathogenic bacteria cause broad-spectrum tetracycline resistance. Commun Biol. 2020;3(1):241. https://doi.org/10.1038/s42003-020-0966-5

Liu X, Li X, Yang AW, Tang B, Jian ZJ, Zhong YM, et al. Community fecal carriage and molecular epidemiology of extended-spectrum β-lactamase- and carbapenemase-producing Escherichia coli from healthy children in the Central South China. Infect Drug Resist. 2022;15:1601−11. https://doi.org/10.2147/IDR.S357090

Kuntaman K, Lestari ES, Severin JA, Kershof IM, Mertaniasih NM, Purwanta M, et al. Fluoroquinolone-resistant Escherichia coli, Indonesia. Emerg Infect Dis. 2005;11(9):1363−9. https://doi.org/10.3201/eid1109.041207

European Committee on Antimicrobial Susceptibility Testing. EUCAST expert rules v3.2 January 2023. The European Comittee on Antimicrobial Susceptibility Testing; 2023.

Machuca J, Ortiz M, Recacha E, Díaz-De-Alba P, Docobo-Perez F, Rodríguez-Martínez JM, et al. Impact of AAC(6')-Ib-cr in combination with chromosomal-mediated mechanisms on clinical quinolone resistance in Escherichia coli. J Antimicrob Chemother. 2016;71(11):3066−71. https://doi.org/10.1093/jac/dkw258

Wong MH, Chan EW, Liu LZ, Chen S. PMQR genes oqxAB and aac(6')Ib-cr accelerate the development of fluoroquinolone resistance in Salmonella typhimurium. Front Microbiol. 2014;5:521. https://doi.org/10.3389/fmicb.2014.00521

Mandal SM, Paul D, editors. Bacterial adaptation to co-resistance. Gateway East, Singapore: Springer Nature Singapore Pte Ltd; 2019. https://doi.org/10.1007/978-981-13-8503-2

Manges AR, Geum HM, Guo A, Edens TJ, Fibke CD, Pitout JDD. Global extraintestinal pathogenic Escherichia coli (ExPEC) lineages. Clin Microbiol Rev. 2019;32(3):e00135−18. https://doi.org/10.1128/CMR.00135-18

Kudinha T, Kong F. Possible step-up in prevalence for Escherichia coli ST131 from fecal to clinical isolates: inferred virulence potential comparative studies within phylogenetic group B2. J Biomed Sci. 2022;29(1):78. https://doi.org/10.1186/s12929-022-00862-7

Finn TJ, Scriver L, Lam L, Duong M, Peirano G, Lynch T, et al. A comprehensive account of Escherichia coli sequence type 131 in wastewater reveals an abundance of fluoroquinolone-resistant clade a strains. Appl Environ Microbiol. 2020;86(4):e01913−19. https://doi.org/10.1128/AEM.01913-19

Liss MA, Peterson EM, Johnston B, Osann K, Johnson JR. Prevalence of ST131 among fluoroquinolone-resistant Escherichia coli obtained from rectal swabs before transrectal prostate biopsy. Urology. 2013;81(3):548−55. https://doi.org/10.1016/j.urology.2012.10.056

Veilleux S, Holt N, Schultz BD, Dubreuil JD. Escherichia coli EAST1 toxin toxicity of variants 17-2 and O 42. Comp Immunol Microbiol Infect Dis. 2008;31(6):567−78. https://doi.org/10.1016/j.cimid.2007.10.003

Ciesielczuk H, Doumith M, Hope R, Woodford N, Wareham DW. Characterization of the extra-intestinal pathogenic Escherichia coli ST131 clone among isolates recovered from urinary and bloodstream infections in the United Kingdom. J Med Microbiol. 2015;64(12):1496−503. https://doi.org/10.1099/jmm.0.000179

Kromann S, Baig S, Olsen RH, Edslev SM, Thøfner I, Bojesen AM, et al. Dramatic increase in slaughter condemnations due to Escherichia coli ST23 and ST101 within the Danish broiler production. Vet Microbiol. 2023;280:109696. https://doi.org/10.1016/j.vetmic.2023.109696

Neumann B, Rackwitz W, Hunfeld KP, Fuchs S, Werner G, Pfeifer Y. Genome sequences of two clinical Escherichia coli isolates harboring the novel colistin-resistance gene variants mcr-1.26 and mcr-1.27. Gut Pathog. 2020;12:40. https://doi.org/10.1186/s13099-020-00375-4

Ballén V, Gabasa Y, Ratia C, Sánchez M, Soto S. Correlation between antimicrobial resistance, virulence determinants and biofilm formation ability among extraintestinal pathogenic Escherichia coli strains isolated in Catalonia, Spain. Front Microbiol. 2022;12:803862. https://doi.org/10.3389/fmicb.2021.803862

Laconi A, Tolosi R, Apostolakos I, Piccirillo A. Biofilm formation ability of ESBL/pAmpC-producing Escherichia coli isolated from the broiler production Pyramid. Antibiotics (Basel). 2023;12(1):155. https://doi.org/10.3390/antibiotics12010155

Schwan WR. Regulation of fim genes in uropathogenic Escherichia coli. World J Clin Infect Dis. 2011;1(1):17−25. https://doi.org/10.5495/wjcid.v1.i1.17

Fuga B, Sellera FP, Cerdeira L, Esposito F, Cardoso B, Fontana H, et al. WHO critical priority Escherichia coli as one health challenge for a post-pandemic scenario: genomic surveillance and analysis of current trends in Brazil. Microbiol Spectr. 2022;10(2):e0125621. https://doi.org/10.1128/spectrum.01256-21

Salim A, Babu P, Mohan K, Moorthy M, Raj D, Kallampillil Thirumeni S, et al. Draft genome sequence of an Escherichia coli sequence type 155 strain isolated from Sewage in Kerala, India. Microbiol Resour Announc. 2019;8(27):e01707−18. https://doi.org/10.1128/MRA.01707-18

Published

2025-02-10

How to Cite

1.
Febrianti T, Puspandasari N, Febriyana D, Weaver T, Karuniawati A. Genotypic pattern of fluoroquinolone resistance among extended-spectrum beta-lactamase-producing &lt;em&gt;Escherichia coli&lt;/em&gt;. Med J Indones [Internet]. 2025Feb.10 [cited 2025Feb.20];33(4):213-24. Available from: https://mji.ui.ac.id/journal/index.php/mji/article/view/7544

Issue

Section

Basic Medical Research
Abstract viewed = 0 times
PDF downloaded = 0 times HTML downloaded = 0 times EPUB downloaded = 0 times