1887
  1. Home
  2. Eurosurveillance
  3. Volume 27, Issue 44, 03/Nov/2022
  4. Article
Research Open Access
Like 2
Download

Abstract

Background

The emergence of colistin resistance is a One Health antimicrobial resistance challenge worldwide. The close contact between companion animals and humans creates opportunities for transmission and dissemination of colistin-resistant bacteria.

Aim

To detect potential animal reservoirs of colistin-resistant and investigate the possible sharing of these bacteria between dogs, cats and their cohabiting humans in the community in Lisbon, Portugal.

Methods

A prospective longitudinal study was performed from 2018 to 2020. Faecal samples from dogs and cats either healthy or diagnosed with a skin and soft tissue or urinary tract infection, and their cohabiting humans were screened for the presence of colistin-resistant . All isolates were tested by broth microdilution against colistin and 12 other antimicrobials. Colistin-resistant isolates were screened for 30 resistance genes, including plasmid-mediated colistin resistance genes ( to ), and typed by multilocus sequence typing. Genetic relatedness between animal and human isolates was analysed by whole genome sequencing.

Results

Colistin-resistant strains harbouring the gene were recovered from faecal samples of companion animals (8/102; 7.8%) and humans (4/125; 3.2%). No difference between control and infection group was detected. Indistinguishable multidrug-resistant . ST744 strains harbouring the gene were found in humans and their dogs in two households.

Conclusions

The identification of identical . strains containing the plasmid-mediated gene in companion animals and humans in daily close contact is of concern. These results demonstrate the importance of the animal–human unit as possible disseminators of clinically important resistance genes in the community setting.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2022.27.44.2101144
2022-11-03
2024-11-21
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2022.27.44.2101144
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/27/44/eurosurv-27-44-4.html?itemId=/content/10.2807/1560-7917.ES.2022.27.44.2101144&mimeType=html&fmt=ahah

References

  1. European Medicines Agency (EMA). Updated advice on the use of colistin products in animals within the European Union: development of resistance and possible impact on human and animal health (EMA/CVMP/CHMP/231573/2016). London: EMA; 2016. Available from: https://www.ema.europa.eu/en/documents/scientific-guideline/updated-advice-use-colistin-products-animals-within-european-union-development-resistance-possible_en-0.pdf
  2. Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis. 2016;16(2):161-8.  https://doi.org/10.1016/S1473-3099(15)00424-7  PMID: 26603172 
  3. Skov RL, Monnet DL. Plasmid-mediated colistin resistance (mcr-1 gene): three months later, the story unfolds. Euro Surveill. 2016;21(9):30155.  https://doi.org/10.2807/1560-7917.ES.2016.21.9.30155  PMID: 26967914 
  4. Sulaiman AA, Kassem II. First report on the detection of the plasmid-borne colistin resistance gene mcr-1 in multi-drug resistant E. coli isolated from domestic and sewer waters in Syrian refugee camps in Lebanon. Travel Med Infect Dis. 2019;30:117-20.  https://doi.org/10.1016/j.tmaid.2019.06.014  PMID: 31260746 
  5. Ahlstrom CA, Ramey AM, Woksepp H, Bonnedahl J. Early emergence of mcr-1-positive Enterobacteriaceae in gulls from Spain and Portugal. Environ Microbiol Rep. 2019;11(5):669-71.  https://doi.org/10.1111/1758-2229.12779  PMID: 31216374 
  6. Hamame A, Davoust B, Cherak Z, Rolain JM, Diene SM. Mobile colistin resistance (mcr) genes in cats and dogs and their zoonotic transmission risks. Pathogens. 2022;11(6):698.  https://doi.org/10.3390/pathogens11060698  PMID: 35745552 
  7. Rebelo AR, Bortolaia V, Kjeldgaard JS, Pedersen SK, Leekitcharoenphon P, Hansen IM, et al. Multiplex PCR for detection of plasmid-mediated colistin resistance determinants, mcr-1, mcr-2, mcr-3, mcr-4 and mcr-5 for surveillance purposes. Euro Surveill. 2018;23(6):1-11.  https://doi.org/10.2807/1560-7917.ES.2018.23.6.17-00672  PMID: 29439754 
  8. Borowiak M, Baumann B, Fischer J, Thomas K, Deneke C, Hammerl JA, et al. Development of a Novel mcr-6 to mcr-9 Multiplex PCR and Assessment of mcr-1 to mcr-9 Occurrence in Colistin-Resistant Salmonella enterica Isolates From Environment, Feed, Animals and Food (2011-2018) in Germany. Front Microbiol. 2020;11:80.  https://doi.org/10.3389/fmicb.2020.00080  PMID: 32117115 
  9. Wang C, Feng Y, Liu L, Wei L, Kang M, Zong Z. Identification of novel mobile colistin resistance gene mcr-10. Emerg Microbes Infect. 2020;9(1):508-16.  https://doi.org/10.1080/22221751.2020.1732231  PMID: 32116151 
  10. Elbediwi M, Li Y, Paudyal N, Pan H, Li X, Xie S, et al. Global Burden of Colistin-Resistant Bacteria: Mobilized Colistin Resistance Genes Study (1980-2018). Microorganisms. 2019;7(10):E461.  https://doi.org/10.3390/microorganisms7100461  PMID: 31623244 
  11. Pomba C, Belas A, Menezes J, Marques C. The Public Health Risk of Companion Animal to Human Transmission of Antimicrobial Resistance During Different Types of Animal Infection. In: Freitas Duarte, A., Lopes da Costa, L. (eds) Advances in Animal Health, Medicine and Production. Springer, Cham. 2020. https://doi.org/10.1007/978-3-030-61981-7_14 
  12. Zhang XF, Doi Y, Huang X, Li HY, Zhong L-L, Zeng K-J, et al. Possible Transmission of mcr-1-Harboring Escherichia coli between Companion Animals and Human. Emerg Infect Dis. 2016;22(9):1679-81.  https://doi.org/10.3201/eid2209.160464  PMID: 27191649 
  13. Loayza-Villa F, Salinas L, Tijet N, Villavicencio F, Tamayo R, Salas S, et al. Diverse Escherichia coli lineages from domestic animals carrying colistin resistance gene mcr-1 in an Ecuadorian household. J Glob Antimicrob Resist. 2020;22:63-7.  https://doi.org/10.1016/j.jgar.2019.12.002  PMID: 31841712 
  14. European Centre for Disease Prevention and Control (ECDC)European Food Safety Authority (EFSA)European Medicines Agency (EMA). Third joint inter-agency report on integrated analysis of consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals in the EU/EEA: JIACRA III 2016-2018. EFSA J. 2021;19(6):e06712. PMID: 34221148 
  15. Lima T, Domingues S, Da Silva GJ. Plasmid-mediated colistin resistance in salmonella enterica: A review. Microorganisms. 2019;7(2):55.  https://doi.org/10.3390/microorganisms7020055  PMID: 30791454 
  16. Tacão M, Tavares RDS, Teixeira P, Roxo I, Ramalheira E, Ferreira S, et al. mcr-1 and blaKPC-3 in Escherichia coli Sequence Type 744 after Meropenem and Colistin Therapy, Portugal. Emerg Infect Dis. 2017;23(8):1419-21.  https://doi.org/10.3201/eid2308.170162  PMID: 28726622 
  17. Weese JS, Blondeau J, Boothe D, Guardabassi LG, Gumley N, Papich M, et al. International Society for Companion Animal Infectious Diseases (ISCAID) guidelines for the diagnosis and management of bacterial urinary tract infections in dogs and cats. Vet J. 2019;247:8-25.  https://doi.org/10.1016/j.tvjl.2019.02.008  PMID: 30971357 
  18. European Commission. Commission Notice: Guidelines for the prudent use of antimicrobials in veterinary medicine. 2015/C 299/04. Luxembourg: Official Journal of the European Union. 11 Sep 2015. Available from: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:52015XC0911(01)
  19. Nordmann P, Jayol A, Poirel L. A universal culture medium for screening polymyxin-resistant gram-negative isolates. J Clin Microbiol. 2016;54(5):1395-9.  https://doi.org/10.1128/JCM.00446-16  PMID: 26984971 
  20. The European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters. Version 11.0. Växjö: EUCAST. [Accessed: 30 March 2021]. Available from: http://www.eucast.org/clinical_breakpoints
  21. Féria C, Ferreira E, Correia JD, Gonçalves J, Caniça M. Patterns and mechanisms of resistance to β-lactams and β-lactamase inhibitors in uropathogenic Escherichia coli isolated from dogs in Portugal. J Antimicrob Chemother. 2002;49(1):77-85.  https://doi.org/10.1093/jac/49.1.77  PMID: 11751770 
  22. Doumith M, Day MJ, Hope R, Wain J, Woodford N. Improved multiplex PCR strategy for rapid assignment of the four major Escherichia coli phylogenetic groups. J Clin Microbiol. 2012;50(9):3108-10.  https://doi.org/10.1128/JCM.01468-12  PMID: 22785193 
  23. Marques C, Menezes J, Belas A, Aboim C, Cavaco-Silva P, Trigueiro G, et al. Klebsiella pneumoniae causing urinary tract infections in companion animals and humans: population structure, antimicrobial resistance and virulence genes. J Antimicrob Chemother. 2019;74(3):594-602.  https://doi.org/10.1093/jac/dky499  PMID: 30535393 
  24. Poirel L, Walsh TR, Cuvillier V, Nordmann P. Multiplex PCR for detection of acquired carbapenemase genes. Diagn Microbiol Infect Dis. 2011;70(1):119-23.  https://doi.org/10.1016/j.diagmicrobio.2010.12.002  PMID: 21398074 
  25. Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, et al. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol. 2006;60(5):1136-51.  https://doi.org/10.1111/j.1365-2958.2006.05172.x  PMID: 16689791 
  26. Babraham Bioinformatics group. FastQC. A quality control tool for high throughput sequence data. Cambridge: Babraham Institute. [Accessed: 10 Jan 2021]. Available from: https://www.bioinformatics.babraham.ac.uk/projects/fastqc
  27. Gordon A. The FASTX-Toolkit. San Francisco: GitHub. [Accessed: 15 Jan 2021]. Available from: https://github.com/agordon/fastx_toolkit
  28. Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics. 2011;27(6):863-4.  https://doi.org/10.1093/bioinformatics/btr026  PMID: 21278185 
  29. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455-77.  https://doi.org/10.1089/cmb.2012.0021  PMID: 22506599 
  30. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 2014;9(11):e112963.  https://doi.org/10.1371/journal.pone.0112963  PMID: 25409509 
  31. Treangen TJ, Ondov BD, Koren S, Phillippy AM. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol. 2014;15(11):524.  https://doi.org/10.1186/s13059-014-0524-x  PMID: 25410596 
  32. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA, Bentley SD, et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 2015;43(3):e15.  https://doi.org/10.1093/nar/gku1196  PMID: 25414349 
  33. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics. 2019;35(21):4453-5.  https://doi.org/10.1093/bioinformatics/btz305  PMID: 31070718 
  34. Argimón S, Abudahab K, Goater RJE, Fedosejev A, Bhai J, Glasner C, et al. Microreact: visualizing and sharing data for genomic epidemiology and phylogeography. Microb Genom. 2016;2(11):e000093.  https://doi.org/10.1099/mgen.0.000093  PMID: 28348833 
  35. The Research Group for Genomic Epidemiology. Center for Genomic Epidemiology. Lyngby: Technical University of Denmark (DTU). [Accessed: 30 Jan 2021]. Available from: http://www.genomicepidemiology.org
  36. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res. 2006;34:D32-6.  https://doi.org/10.1093/nar/gkj014  PMID: 16381877 
  37. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics. 2011;12(1):402.  https://doi.org/10.1186/1471-2164-12-402  PMID: 21824423 
  38. Flament-Simon SC, de Toro M, Mora A, García V, García-Meniño I, Díaz-Jiménez D, et al. Whole genome sequencing and characteristics of mcr-1-harboring plasmids of porcine Escherichia coli isolates belonging to the high-risk clone O25b:H4-ST131 Clade B. Front Microbiol. 2020;11:387.  https://doi.org/10.3389/fmicb.2020.00387  PMID: 32265859 
  39. Lei L, Wang Y, Schwarz S, Walsh TR, Ou Y, Wu Y, et al. mcr-1 in Enterobacteriaceae from companion animals, Beijing, China, 2012-2016. Emerg Infect Dis. 2017;23(4):710-1.  https://doi.org/10.3201/eid2304.161732  PMID: 28322714 
  40. Guenther S, Falgenhauer L, Semmler T, Imirzalioglu C, Chakraborty T, Roesler U, et al. Environmental emission of multiresistant Escherichia coli carrying the colistin resistance gene mcr-1 from German swine farms. J Antimicrob Chemother. 2017;72(5):1289-92. PMID: 28122910 
  41. Matamoros S, van Hattem JM, Arcilla MS, Willemse N, Melles DC, Penders J, et al. Global phylogenetic analysis of Escherichia coli and plasmids carrying the mcr-1 gene indicates bacterial diversity but plasmid restriction. Sci Rep. 2017;7(1):15364.  https://doi.org/10.1038/s41598-017-15539-7  PMID: 29127343 
  42. Fuentes-Castillo D, Esposito F, Cardoso B, Dalazen G, Moura Q, Fuga B, et al. Genomic data reveal international lineages of critical priority Escherichia coli harbouring wide resistome in Andean condors (Vultur gryphus Linnaeus, 1758). Mol Ecol. 2020;29(10):1919-35.  https://doi.org/10.1111/mec.15455  PMID: 32335957 
  43. Maciuca IE, Cummins ML, Cozma AP, Rimbu CM, Guguianu E, Panzaru C, et al. Genetic features of mcr-1 mediated colistin resistance in CMY-2-producing Escherichia coli from Romanian poultry. Front Microbiol. 2019;10:2267.  https://doi.org/10.3389/fmicb.2019.02267  PMID: 31681191 
  44. Wang R, van Dorp L, Shaw LP, Bradley P, Wang Q, Wang X, et al. The global distribution and spread of the mobilized colistin resistance gene mcr-1. Nat Commun. 2018;9(1):1179.  https://doi.org/10.1038/s41467-018-03205-z  PMID: 29563494 
mcr-1 colistin resistance gene sharing between Escherichia coli from cohabiting dogs and humans, Lisbon, Portugal, 2018 to 2020
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Juliana+Menezes&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Menezes Juliana</a>, <a href="/search?value1=Joana+Moreira+da+Silva&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Moreira da Silva Joana</a>, <a href="/search?value1=Sian-Marie+Frosini&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Frosini Sian-Marie</a>, <a href="/search?value1=Anette+Loeffler&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Loeffler Anette</a>, <a href="/search?value1=Scott+Weese&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Weese Scott</a>, <a href="/search?value1=Vincent+Perreten&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Perreten Vincent</a>, <a href="/search?value1=Stefan+Schwarz&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Schwarz Stefan</a>, <a href="/search?value1=Lu%C3%ADs+Telo+da+Gama&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Telo da Gama Luís</a>, <a href="/search?value1=Andreia+Jesus+Amaral&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Amaral Andreia Jesus</a>, <a href="/search?value1=Constan%C3%A7a+Pomba&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pomba Constança</a></span>. mcr-1 colistin resistance gene sharing between Escherichia coli from cohabiting dogs and humans, Lisbon, Portugal, 2018 to 2020. <a href="/content/ecdc">Euro Surveill.</a> 2022;27(44):pii=2101144. <a href="https://doi.org/10.2807/1560-7917.ES.2022.27.44.2101144" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2022.27.44.2101144</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 09 Dec 2021;&nbsp;&nbsp; <span class="generated">Accepted</span>: 25 Apr 2022 </span> </p>
/content/10.2807/1560-7917.ES.2022.27.44.2101144
/content/10.2807/1560-7917.ES.2022.27.44.2101144
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error