1887
  1. Home
  2. Eurosurveillance
  3. Volume 24, Issue 32, 08/Aug/2019
  4. Article
Research Open Access
Like 0
Download

Abstract

Background

Brown rats () are an important wildlife species in cities, where they live in close proximity to humans. However, few studies have investigated their role as reservoir of antimicrobial-resistant bacteria.

Aim

We intended to determine whether urban rats at two highly frequented sites in Vienna, Austria, carry extended-spectrum β-lactamase-producing Enterobacteriaceae fluoroquinolone-resistant Enterobacteriaceae and meticillin-resistant (MR) spp. (MRS).

Methods

We surveyed the presence of antimicrobial resistance in 62 urban brown rats captured in 2016 and 2017 in Vienna, Austria. Intestinal and nasopharyngeal samples were cultured on selective media. We characterised the isolates and their antimicrobial properties using microbiological and genetic methods including disk diffusion, microarray analysis, sequencing, and detection and characterisation of plasmids.

Results

Eight multidrug-resistant and two extensively drug-resistant New Delhi metallo-β-lactamases-1 (NDM-1)-producing ST114 ( complex) were isolated from nine of 62 rats. Nine Enterobacteriaceae isolates harboured the gene and one carried a plasmid-encoded gene (). Forty-four MRS were isolated from 37 rats; they belonged to seven different staphylococcal species: , , , , , (all -positive) and -positive .

Conclusion

Our findings suggest that brown rats in cities are a potential source of multidrug-resistant bacteria, including carbapenem-resistant . ST114. Considering the increasing worldwide urbanisation, rodent control remains an important priority for health in modern cities.

© 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.2019.24.32.1900149
2019-08-08
2024-12-22
/content/10.2807/1560-7917.ES.2019.24.32.1900149
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/24/32/eurosurv-24-32-3.html?itemId=/content/10.2807/1560-7917.ES.2019.24.32.1900149&mimeType=html&fmt=ahah

References

  1. Centers for Disease Control and Prevention (CDC). Antibiotic resistance threats in the United States, 2013. Atlanta: CDC; 2013. Available from: https://www.cdc.gov/drugresistance/biggest_threats.html?CDC_AA_refVal=https%3A%2F%2Fwww.cdc.gov%2Fdrugresistance%2Fthreat-report-2013%2Findex.html
  2. European Centre for Disease Prevention and Control (ECDC). Antimicrobial resistance surveillance in Europe 2016. Annual Report of the European Antimicrobial Resistance Surveillance Network (EARS-Net). Stockholm: ECDC; 2017. Available from: https://ecdc.europa.eu/en/publications-data/antimicrobial-resistance-surveillance-europe-2016
  3. Walsh TR, Toleman MA. The new medical challenge: why NDM-1? Why Indian? Expert Rev Anti Infect Ther. 2011;9(2):137-41.  https://doi.org/10.1586/eri.10.159  PMID: 21342058 
  4. Wu J, Huang Y, Rao D, Zhang Y, Yang K. Evidence for environmental dissemination of antibiotic resistance mediated by wild birds. Front Microbiol. 2018;9:745.  https://doi.org/10.3389/fmicb.2018.00745  PMID: 29731740 
  5. Radhouani H, Poeta P, Gonçalves A, Pacheco R, Sargo R, Igrejas G. Wild birds as biological indicators of environmental pollution: antimicrobial resistance patterns of Escherichia coli and enterococci isolated from common buzzards (Buteo buteo). J Med Microbiol. 2012;61(Pt 6):837-43.  https://doi.org/10.1099/jmm.0.038364-0  PMID: 22403140 
  6. World Health Organization and UN-Habitat. Global report on urban health: equitable healthier cities for sustainable development. Geneva: World Health Organization; 2016. Available from: https://apps.who.int/iris/handle/10665/204715
  7. Hassell JM, Begon M, Ward MJ, Fèvre EM. Urbanization and disease emergence: dynamics at the wildlife-livestock-human interface. Trends Ecol Evol. 2017;32(1):55-67.  https://doi.org/10.1016/j.tree.2016.09.012  PMID: 28029378 
  8. Feng AYT, Himsworth CG. The secret life of the city rat: a review of the ecology of urban Norway and black rats (Rattus norvegicus and Rattus rattus). Urban Ecosyst. 2014;17(1):149-62.  https://doi.org/10.1007/s11252-013-0305-4 
  9. Guenther S, Bethe A, Fruth A, Semmler T, Ulrich RG, Wieler LH, et al. Frequent combination of antimicrobial multiresistance and extraintestinal pathogenicity in Escherichia coli isolates from urban rats (Rattus norvegicus) in Berlin, Germany. PLoS One. 2012;7(11):e50331.  https://doi.org/10.1371/journal.pone.0050331  PMID: 23189197 
  10. Hansen TA, Joshi T, Larsen AR, Andersen PS, Harms K, Mollerup S, et al. Vancomycin gene selection in the microbiome of urban Rattus norvegicus from hospital environment. Evol Med Public Health. 2016;2016(1):219-26.  https://doi.org/10.1093/emph/eow021  PMID: 27412864 
  11. Burriel AR, Kritas SK, Kontos V. Some microbiological aspects of rats captured alive at the port city of Piraeus, Greece. Int J Environ Health Res. 2008;18(2):159-64.  https://doi.org/10.1080/09603120701358432  PMID: 18365804 
  12. Ho P-L, Lo W-U, Lai EL, Law PY, Leung SM, Wang Y, et al. Clonal diversity of CTX-M-producing, multidrug-resistant Escherichia coli from rodents. J Med Microbiol. 2015;64(Pt 2):185-90.  https://doi.org/10.1099/jmm.0.000001  PMID: 25627207 
  13. Himsworth CG, Zabek E, Desruisseau A, Parmley EJ, Reid-Smith R, Jardine CM, et al. Prevalence and characteristics of Escherichia coli and Salmonella spp. in the feces of wild urban Norway and black rats (Rattus norvegicus and Rattus rattus) from an inner-city neighborhood of Vancouver, Canada. J Wildl Dis. 2015;51(3):589-600.  https://doi.org/10.7589/2014-09-242  PMID: 25932669 
  14. Kato Y, Matsunaga S, Misuna Y, Ushioda H, Yamamoto T, Kaneuchi C. Isolation and characterization of Staphylococcus aureus in rats trapped at restaurants in buildings in downtown Tokyo. J Vet Med Sci. 1995;57(3):499-502.  https://doi.org/10.1292/jvms.57.499  PMID: 7548405 
  15. Himsworth CG, Miller RR, Montoya V, Hoang L, Romney MG, Al-Rawahi GN, et al. Carriage of methicillin-resistant Staphylococcus aureus by wild urban Norway rats (Rattus norvegicus). PLoS One. 2014;9(2):e87983.  https://doi.org/10.1371/journal.pone.0087983  PMID: 24498421 
  16. Himsworth CG, Patrick DM, Parsons K, Feng A, Weese JS. Methicillin-resistant Staphylococcus pseudintermedius in rats. Emerg Infect Dis. 2013;19(1):169-70.  https://doi.org/10.3201/eid1901.120897  PMID: 23260061 
  17. Bradley CA, Altizer S. Urbanization and the ecology of wildlife diseases. Trends Ecol Evol. 2007;22(2):95-102.  https://doi.org/10.1016/j.tree.2006.11.001  PMID: 17113678 
  18. Nelson L, Clark FW. Correction for sprung traps in catch/effort calculations of trapping results. J Mammal. 1973;54(1):295-8.  https://doi.org/10.2307/1378903 
  19. Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing. 27th ed. Wayne: CLSI; 2017. Available from: https://clsi.org/standards/products/microbiology/documents/m100/
  20. Loncaric I, Stalder GL, Mehinagic K, Rosengarten R, Hoelzl F, Knauer F, et al. Comparison of ESBL--and AmpC producing Enterobacteriaceae and methicillin-resistant Staphylococcus aureus (MRSA) isolated from migratory and resident population of rooks (Corvus frugilegus) in Austria. PLoS One. 2013;8(12):e84048.  https://doi.org/10.1371/journal.pone.0084048  PMID: 24391878 
  21. Nordmann P, Poirel L, Carrër A, Toleman MA, Walsh TR. How to detect NDM-1 producers. J Clin Microbiol. 2011;49(2):718-21.  https://doi.org/10.1128/JCM.01773-10  PMID: 21123531 
  22. Dolejska M, Frolkova P, Florek M, Jamborova I, Purgertova M, Kutilova I, et al. CTX-M-15-producing Escherichia coli clone B2-O25b-ST131 and Klebsiella spp. isolates in municipal wastewater treatment plant effluents. J Antimicrob Chemother. 2011;66(12):2784-90.  https://doi.org/10.1093/jac/dkr363  PMID: 21954457 
  23. Everett MJ, Jin YF, Ricci V, Piddock LJ. Contributions of individual mechanisms to fluoroquinolone resistance in 36 Escherichia coli strains isolated from humans and animals. Antimicrob Agents Chemother. 1996;40(10):2380-6.  https://doi.org/10.1128/AAC.40.10.2380  PMID: 8891148 
  24. Eckert C, Gautier V, Arlet G. DNA sequence analysis of the genetic environment of various blaCTX-M genes. J Antimicrob Chemother. 2006;57(1):14-23.  https://doi.org/10.1093/jac/dki398  PMID: 16291869 
  25. Clermont O, Christenson JK, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep. 2013;5(1):58-65.  https://doi.org/10.1111/1758-2229.12019  PMID: 23757131 
  26. 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 
  27. Miyoshi-Akiyama T, Hayakawa K, Ohmagari N, Shimojima M, Kirikae T. Multilocus sequence typing (MLST) for characterization of Enterobacter cloacae. PLoS One. 2013;8(6):e66358.  https://doi.org/10.1371/journal.pone.0066358  PMID: 23776664 
  28. Lepuschitz S, Huhulescu S, Hyden P, Springer B, Rattei T, Allerberger F, et al. Characterization of a community-acquired-MRSA USA300 isolate from a river sample in Austria and whole genome sequence based comparison to a diverse collection of USA300 isolates. Sci Rep. 2018;8(1):9467.  https://doi.org/10.1038/s41598-018-27781-8  PMID: 29930324 
  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. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics. 2016;32(6):929-31.  https://doi.org/10.1093/bioinformatics/btv681  PMID: 26576653 
  31. Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, Tsang KK, et al. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res. 2017;45(D1):D566-73.  https://doi.org/10.1093/nar/gkw1004  PMID: 27789705 
  32. Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O, Villa L, et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014;58(7):3895-903.  https://doi.org/10.1128/AAC.02412-14  PMID: 24777092 
  33. Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL, Threlfall EJ. Identification of plasmids by PCR-based replicon typing. J Microbiol Methods. 2005;63(3):219-28.  https://doi.org/10.1016/j.mimet.2005.03.018  PMID: 15935499 
  34. Senn L, Basset P, Nahimana I, Zanetti G, Blanc DS. Which anatomical sites should be sampled for screening of methicillin-resistant Staphylococcus aureus carriage by culture or by rapid PCR test? Clin Microbiol Infect. 2012;18(2):E31-3.  https://doi.org/10.1111/j.1469-0691.2011.03724.x  PMID: 22192160 
  35. Loncaric I, Kübber-Heiss A, Posautz A, Stalder GL, Hoffmann D, Rosengarten R, et al. Characterization of methicillin-resistant Staphylococcus spp. carrying the mecC gene, isolated from wildlife. J Antimicrob Chemother. 2013;68(10):2222-5.  https://doi.org/10.1093/jac/dkt186  PMID: 23674764 
  36. Mellmann A, Becker K, von Eiff C, Keckevoet U, Schumann P, Harmsen D. Sequencing and staphylococci identification. Emerg Infect Dis. 2006;12(2):333-6.  https://doi.org/10.3201/eid1202.050962  PMID: 16494767 
  37. Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, Borg M, et al. A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS One. 2011;6(4):e17936.  https://doi.org/10.1371/journal.pone.0017936  PMID: 21494333 
  38. Harmsen D, Claus H, Witte W, Rothgänger J, Claus H, Turnwald D, et al. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol. 2003;41(12):5442-8.  https://doi.org/10.1128/JCM.41.12.5442-5448.2003  PMID: 14662923 
  39. Monecke S, Slickers P, Gawlik D, Müller E, Reissig A, Ruppelt-Lorz A, et al. Molecular typing of ST239-MRSA-III from diverse geographic locations and the evolution of the SCCmec III element during its intercontinental spread. Front Microbiol. 2018;9:1436.  https://doi.org/10.3389/fmicb.2018.01436  PMID: 30087657 
  40. Sweeney MT, Lubbers BV, Schwarz S, Watts JL. Applying definitions for multidrug resistance, extensive drug resistance and pandrug resistance to clinically significant livestock and companion animal bacterial pathogens. J Antimicrob Chemother. 2018;73(6):1460-3.  https://doi.org/10.1093/jac/dky043  PMID: 29481657 
  41. Annavajhala MK, Gomez-Simmonds A, Uhlemann A-C. Multidrug-resistant Enterobacter cloacae complex emerging as a global, diversifying threat. Front Microbiol. 2019;10(44):44.  https://doi.org/10.3389/fmicb.2019.00044  PMID: 30766518 
  42. Rozwandowicz M, Brouwer MSM, Fischer J, Wagenaar JA, Gonzalez-Zorn B, Guerra B, et al. Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae. J Antimicrob Chemother. 2018;73(5):1121-37.  https://doi.org/10.1093/jac/dkx488  PMID: 29370371 
  43. Zarfel G, Hoenigl M, Würstl B, Leitner E, Salzer HJF, Valentin T, et al. Emergence of carbapenem-resistant Enterobacteriaceae in Austria, 2001-2010. Clin Microbiol Infect. 2011;17(11):E5-8.  https://doi.org/10.1111/j.1469-0691.2011.03659.x  PMID: 21939472 
  44. Izdebski R, Baraniak A, Herda M, Fiett J, Bonten MJM, Carmeli Y, et al. MLST reveals potentially high-risk international clones of Enterobacter cloacae. J Antimicrob Chemother. 2015;70(1):48-56.  https://doi.org/10.1093/jac/dku359  PMID: 25216820 
  45. Loncaric I, Künzel F, Licka T, Simhofer H, Spergser J, Rosengarten R. Identification and characterization of methicillin-resistant Staphylococcus aureus (MRSA) from Austrian companion animals and horses. Vet Microbiol. 2014;168(2-4):381-7.  https://doi.org/10.1016/j.vetmic.2013.11.022  PMID: 24332703 
  46. Krziwanek K, Metz-Gercek S, Mittermayer H. Methicillin-resistant Staphylococcus aureus ST398 from human patients, upper Austria. Emerg Infect Dis. 2009;15(5):766-9.  https://doi.org/10.1111/j.1469-0691.2007.01896.x  PMID: 18070133 
  47. Loncaric I, Kübber-Heiss A, Posautz A, Ruppitsch W, Lepuschitz S, Schauer B, et al. Characterization of mecC gene-carrying coagulase-negative Staphylococcus spp. isolated from various animals. Vet Microbiol. 2019;230:138-44.  https://doi.org/10.1016/j.vetmic.2019.02.014  PMID: 30827379 
  48. Leibler JH, Zakhour CM, Gadhoke P, Gaeta JM. Zoonotic and vector-borne infections among urban homeless and marginalized people in the United States and Europe, 1990-2014. Vector Borne Zoonotic Dis. 2016;16(7):435-44.  https://doi.org/10.1089/vbz.2015.1863  PMID: 27159039 
  49. Lood R, Ertürk G, Mattiasson B. Revisiting antibiotic resistance spreading in wastewater treatment plants - Bacteriophages as a much neglected potential transmission vehicle. Front Microbiol. 2017;8:2298.  https://doi.org/10.3389/fmicb.2017.02298  PMID: 29209304 
  50. Furness LE, Campbell A, Zhang L, Gaze WH, McDonald RA. Wild small mammals as sentinels for the environmental transmission of antimicrobial resistance. Environ Res. 2017;154(Supplement C):28-34.  https://doi.org/10.1016/j.envres.2016.12.014  PMID: 28013185 
Urban brown rats (Rattus norvegicus) as possible source of multidrug-resistant Enterobacteriaceae and meticillin-resistant Staphylococcus spp., Vienna, Austria, 2016 and 2017
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Am%C3%A9lie+Desvars-Larrive&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Desvars-Larrive Amélie</a>, <a href="/search?value1=Werner+Ruppitsch&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ruppitsch Werner</a>, <a href="/search?value1=Sarah+Lepuschitz&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lepuschitz Sarah</a>, <a href="/search?value1=Michael+P+Szostak&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Szostak Michael P</a>, <a href="/search?value1=Joachim+Spergser&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Spergser Joachim</a>, <a href="/search?value1=Andrea+T+Fe%C3%9Fler&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Feßler Andrea T</a>, <a href="/search?value1=Stefan+Schwarz&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Schwarz Stefan</a>, <a href="/search?value1=Stefan+Monecke&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Monecke Stefan</a>, <a href="/search?value1=Ralf+Ehricht&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ehricht Ralf</a>, <a href="/search?value1=Chris+Walzer&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Walzer Chris</a>, <a href="/search?value1=Igor+Loncaric&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Loncaric Igor</a></span>. Urban brown rats (Rattus norvegicus) as possible source of multidrug-resistant Enterobacteriaceae and meticillin-resistant Staphylococcus spp., Vienna, Austria, 2016 and 2017. <a href="/content/ecdc">Euro Surveill.</a> 2019;24(32):pii=1900149. <a href="https://doi.org/10.2807/1560-7917.ES.2019.24.32.1900149" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2019.24.32.1900149</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 25 Feb 2019;&nbsp;&nbsp; <span class="generated">Accepted</span>: 03 Jun 2019 </span> </p>
/content/10.2807/1560-7917.ES.2019.24.32.1900149
/content/10.2807/1560-7917.ES.2019.24.32.1900149
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