We investigated the prevalence of carbapenemase-producing Enterobacteriaceae (CPE) in chicken meat in Western Algeria in 2017.
Results:
From February to July 2017, samples of chicken meat from three poultry farms in Western Algeria were screened for the presence of CPE. Strains were characterized with regard to antibiotic resistance, β-lactamase content, Plasmid-mediated quinolone resistance, sulfonamide resistance genes, clonality (repetitive sequence-based profiles and multilocus sequence typing) and virulence traits. Of 181 samples analyzed, 29 (16.0%) carbapenemase-producing Klebsiella pneumoniae were detected. Twenty-three OXA-48-producers (79.3%) and six (20.7%) New Delhi metallo (NDM)-1-producers were observed. Clonality analysis showed three distinct lineages and clonal expansions of the OXA-48-producing K. pneumoniae ST48 and the NDM-1-producing K. pneumoniae ST101. These isolates harbored fimH, ureA, mrkD, entB, uge, and wabG. Neither capsular serotype genes nor hypermucoviscous phenotype were detected. Plasmid analysis confirmed that all these isolates harbored the transferable IncL and IncFIIK plasmids.
Conclusions:
This study reports the spread of OXA-48 and NDM-1-producing K. pneumoniae ST48 and ST101 in chicken meat in Western Algeria and demonstrates that food represents a reservoir of the carbapenemases encoding genes.
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References
1.
NordmannP., DortetL., and PoirelL.. 2012. Carbapenem resistance in Enterobacteriaceae: here is the storm! Trends Mol. Med. 18:263–272.
2.
PoirelL., StephanR., PerretenV., and NordmannP.. 2014. The carbapenemase threat in the animal world: the wrong culprit. J. Antimicrob. Chemother. 69:2007–2008.
3.
KöckR., Daniels-HaardtI., BeckerK., MellmannA., FriedrichA.W, MeviusD., SchwarzS., and JurkeA.. 2018. Carbapenem-resistant Enterobacteriaceae in wildlife, food-producing, and companion animals: a systematic review. Clin. Microbiol. Infect. 24:1241–1250.
4.
MairiA., PantelA., SottoA., LavigneJ.-P, and TouatiA.. 2018. OXA-48-like carbapenemases producing Enterobacteriaceae in different niches. Eur. J. Clin. Microbiol. Infect. Dis. 37:587–604.
5.
Madec, J.Y. and HaenniM.. 2018. Antimicrobial resistance plasmid reservoir in food and food-producing animals. Plasmid, 99:72–81.
6.
FischerJ., RodriguezI., SchmogerS., FrieseA., RoeslerU., HelmithR., and GuerraB.. 2012. Escherichia coli producing VIM-1 carbapenemase isolated on a pig farm. J. Antimicrob. Chemother. 67:1793–1795.
7.
PoirelL., BerçotB., MillemannY., BonninR.A, PannauxG., and NordmannP.. 2012. Carbapenemase-producing Acinetobacter spp. in, cattle, France. Emerg. Infect. Dis. 18:523–525.
8.
KluytmansJ.2013. Ban resistant strains from food chain. Nature, 501:316.
9.
YousfiM., TouatiA., MuggeoA., MiraB., AsmaB., BrasmeL., GuillardT., and de ChampsC.. 2018. Clonal dissemination of OXA-48-producing Enterobacter cloacae isolates from companion animals in Algeria. J. Glob. Antimicrob. Resist. 12:187–191.
10.
YousfiM., TouatiA., MairiA., BrasmeL., Gharout-SaitA., GuillardT., and de ChampsC.. 2016. Emergence of carbapenemase-producing Escherichia coli isolated from companion animals in Algeria. Microb. Drug Resist. 22:342–346.
11.
MairiA., PantelA., OusalemF., SottoA., TouatiA., and LavigneJ.P.. 2019. OXA-48-producing Enterobacterales in different ecological niches in Algeria: clonal expansion, plasmid characteristics and virulence traits. J. Antimicrob. Chemother. 74:1848–1855.
12.
ChaalalW., ChaalalN., BakourS., KihalM., and RolainJ.M.. 2016. First occurrence of NDM-1 in Acinetobacter baumannii ST85 isolated from Algerian dairy farms. J. Glob. Antimicrob. Resist. 7:150–151.
13.
Gharout-SaitA., TouatiA., AhmimM., BrasmeL., GuillardT., AgsousA., and de ChampsC.. 2019. Occurrence of carbapenemase-producing Klebsiella pneumoniae in Bat Guano. Microb. Drug Resist. 25:1057–1062.
14.
BouazizA., LoucifL., AyachiA., GuehazK., BendjamaE., and RolainJ.M.. 2018. Migratory white stork (Ciconia ciconia): a potential vector of the OXA-48-producing Escherichia coli ST38 clone in Algeria. Microb. Drug Resist. 24:461–468.
15.
BachiriT., BakourS., LalaouiR., BelkeblaN., AllouacheM., RolainJ.M, and TouatiA.. 2018. Occurrence of carbapenemase-producing Enterobacteriaceae isolates in the wildlife: first report of OXA-48 in wild boars in Algeria. Microb. Drug Resist. 24:337–345.
16.
MorakchiH., LoucifL., Gacemi-KiraneD., and RolainJ.M.. 2017. Molecular characterisation of carbapenemases in urban pigeon droppings in France and Algeria. J. Glob. Antimicrob. Resist. 9:103–110.
17.
TafouktR., TouatiA., LeangapichartT., BakourS., and RolainJ.M.. 2017. Characterization of OXA-48-like-producing Enterobacteriaceae isolated from river water in Algeria. Water Res. 120:185–189.
18.
DjenadiK., ZhangL., MurrayA.K, and GazeW.H.. 2018. Carbapenem resistance in bacteria isolated from soil and water environments in Algeria. J. Glob. Antimicrob. Resist. 15:262–267.
19.
YaiciL., HaenniM., SarasE., BoudehoucheW., TouatiA., and MadecJ.Y.. 2016. blaNDM-5 -carrying IncX3 plasmid in Escherichia coli ST1284 isolated from raw milk collected in a dairy farm in Algeria. J. Antimicrob. Chemother. 71:2671–2672.
20.
PoirelL., PotronA., and NordmannP.. 2012. OXA-48-like carbapenemases: the phantom menace. J. Antimicrob. Chemother. 67:1597–1606.
21.
PantelA., SouzyD., SottoA., and LavigneJ.P.. 2015. Evaluation of the two phenotypic screening tests for carbapenemase-producing Enterobacteriaceae. J. Clin. Microbiol. 55:510–518.
22.
PitoutJ.D., HansonN.D, ChurchD.L, and LauplandK.B.. 2004. Population-based laboratory surveillance for Escherichia coli-producing extended-spectrum beta-lactamases: importance of community isolates with blaCTX-M genes. Clin. Infect. Dis., 38:1736–1741.
23.
RiceL.B., CariasL.L, HujerA.M, BonafedeM., HuttonR., HoyenC., and BonomoR.A.. 2000. High-level expression of chromosomally encoded SHV-1 beta-lactamase and an outer membrane protein change confer resistance to ceftazidime and piperacillin-tazobactam in a clinical isolate of Klebsiella pneumoniae. Antimicrob. Agents Chemother. 44:362–367.
24.
SáenzY., BriñasL., DominguezE., RuizJ., ZarazagaM., VilaJ., and TorresC.. 2004. Mechanisms of resistance in multiple-antibiotic-resistant Escherichia coli strains of human, animal, and food origins. Antimicrob. Agents Chemother. 48:3996–4001.
25.
ParkC.H., RobicsekA., JacobyG.A, SahmD., and HooperD.C.. 2006. Prevalence in the United States of aac(6′)-Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob. Agents Chemother. 50:3953–3955.
26.
CattoirV., PoirelL., RotimiV., SoussyC.J, and NordmannP.. 2007. Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J. Antimicrob. Chemother. 60:394–397.
27.
KimH.B., WangM., ParkC.H, KimE.C, JacobyG.A, and HooperD.C.. 2009. oqxAB encoding a multidrug efflux pump in human clinical isolates of Enterobacteriaceae. Antimicrob. Agents Chemother. 53:3582–3584.
28.
YamaneK., WachinoJ.I, SuzukiS. and ArakawaY.. 2008. Plasmid-mediated QepA gene among Escherichia coli clinical isolates from Japan. Antimicrob. Agents Chemother. 52:1564–1566.
29.
CompainF., BabosanA., BrisseS., GenelN., AudoJ., AilloudF., Kassis-ChikhaniN., ArletG., and DecréD.. 2014. Multiplex PCR for detection of seven virulence factors and K1/K2 capsular serotypes of Klebsiella pneumoniae. J. Clin. Microbiol. 52:4377–4380.
30.
TurtonJ.F., PerryC., ElgohariS., and HamptonC.V.. 2010. PCR characterization and typing of Klebsiella pneumoniae using capsular type-specific, variable number tandem repeat and virulence gene targets. J. Med. Microbiol. 59:541–547.
31.
KadoC.I., and LiuS.T.. 1981. Rapid procedure for detection and isolation of large and small plasmids. J. Bacteriol. 145:1365–1373.
32.
SkalovaA., ChudejovaK., RotovaV., MedveckyM., StudentovaV., ChudackovaE., LavickaP., BergerovaT., JakubuV., ZemlickovaH., PapagiannitsisC.C, and HrabakJ.. 2017. Molecular characterization of OXA-48-like-producing Enterobacteriaceae in the Czech Republic and evidence for horizontal transfer of pOXA-48-like plasmids. Antimicrob. Agents Chemother. 61:pii: e01889-16.
33.
CompainF., PoissonA., Le HelloS., BrangerC., WeillF.X, ArletG., and DecréD.. 2014. Targeting relaxase genes for classification of the predominant plasmids in Enterobacteriaceae. Int. J. Med. Microbiol. 304:236–242.
34.
CarattoliA., SeiffertE.N, SchwendenerS., PerretenV., and EndimianiA.. 2015. Differentiation of IncL and IncM plasmids associated with the spread of clinically relevant anti-microbial resistance. PLoS One. 10:e0123063.
35.
AlonsoC.A., ZarazagaM., Ben SallemR., JouiniA., Ben SlamaK., and TorresC.. 2017. Antibiotic resistance in Escherichia coli in husbandry animals: the African perspective. Lett. Appl. Microbiol. 64:318–334.
36.
AbdallahH.M., ReulandE.A, WintermansB.B, Al NaiemiN., KoekA., AbdelwahabA.M, AmmarA.M, MohamedA.A, and Vandenbroucke-GraulsC.M.. 2015. Extended-spectrum β-lactamases and/or carbapenemases-producing Enterobacteriaceae isolated from retail chicken meat in Zagazig, Egypt. PLoS One, 10:e0136052.
37.
HamzaE., DorghamS.M, and HamzaD.A.. 2016. Carbapenemase-producing Klebsiella pneumoniae in broiler poultry farming in Egypt. J. Glob. Antimicrob. Resist. 7:8–10.
38.
ChabouS., LeulmiH., DavoustB., AouadiA., and RolainJ.M.. 2018. Prevalence of extended-spectrum β-lactamase- and carbapenemase-encoding genes in poultry faeces from Algeria and Marseille, France. J. Glob. Antimicrob. Resist. 13:28–32.
39.
PitoutJ.D., NordmannP., and PoirelL.. 2015. Carbapenemase-producing Klebsiella pneumoniae, a key pathogen set for global nosocomial dominance. Antimicrob. Agents Chemother. 59:5873–5884.
40.
KhanA.U., MaryamL., and ZarrilliR.. 2017. Structure, genetics and worldwide spread of New Delhi Metallo-β-lactamase (NDM): a threat to public health. BMC Microbiol. 17:101.
41.
AbderrahimA., DjahmiN., PujolC., NedjaiS., BentakoukM.C, Kirane-GacemiD., DekhilM., SottoA., LavigneJ.P, and PantelA.. 2017. First case of NDM-1-producing Klebsiella pneumoniae in Annaba University Hospital, Algeria. Microb. Drug Resist. 23:895–900.
42.
PoirelL., DortetL., BernabeuS., and NordmannP.. 2011. Genetic features of blaNDM-1-positive Enterobacteriaceae. Antimicrob. Agents Chemother. 55:5403–5407.
43.
ZhengZ., LiR., YeL., ChanE.W, and ChenS.. 2018. Identification and characterization of IncA/C conjugative, blaNDM-1-bearing plasmid in Vibrio alginolyticus of food origin. Antimicrob. Agents Chemother. 62:pii:e01897-18.
44.
BonninR.A., PoirelL., CarattoliA., and NordmannP.. 2012. Characterization of an IncFII plasmid encoding NDM-1 from Escherichia coli ST131. PLoS One, 7:e34752.
45.
AlouacheS., EstepaV., MessaiY., RuizE., TorresC., and BakourR.. 2014. Characterization of ESBLs and associated quinolone resistance in Escherichia coli and Klebsiella pneumoniae isolates from an urban wastewater treatment plant in Algeria. Microb. Drug Resist. 20:30–38.
46.
BourafaN., ChaalalW., BakourS., LalaouiR., BoutefnouchetN., DieneS.M, and RolainJ.M.. 2018. Molecular characterization of carbapenem-resistant Gram-negative bacilli clinical isolates in Algeria. Infect. Drug Resist. 11:735–742.
47.
YousfiH., HadjadjL., DandachiI., LalaouiR., MerahA., AmouraK., DahiA., DekhilM., MessalhiN., DieneS.M, BaronS., and RolainJ.M.. 2019. Colistin- and carbapenem-resistant Klebsiella pneumoniae clinical isolates: Algeria. Microb. Drug Resist. 25:258–263.
48.
LoucifL., Kassah-LaouarA., SaidiM., MessalaA., ChelaghmaW., and RolainJ.M.. 2016. Outbreak of OXA-48-producing Klebsiella pneumoniae involving a sequence type 101 clone in Batna University Hospital, Algeria. Antimicrob. Agents Chemother. 60:7494–7497.
49.
MansourW., HaenniM., SarasE., GramiR., ManiY., Ben Haj KhalifaA., El AtroussS., KhederM., Fekih HassenM., BoujâafarN., BouallegueO., and MadecJ.Y.. 2017. Outbreak of colistin-resistant carbapenemase-producing Klebsiella pneumoniae in Tunisia. J. Glob. Antimicrob. Resist. 10:88–94.
50.
GonaF., BongiornoD., AprileA., CorazzaE., PasquaB., ScuderiM.G, ChiacchiarettaM., CirilloD.M, StefaniS., and MezzatestaM.L. 2019. Emergence of two novel sequence types (3366 and 3367) NDM-1- and OXA-48-co-producing K. pneumoniae in Italy. Eur. J. Clin. Microbiol. Infect. Dis. 38:1687–1691.
51.
QamarM.U., WalshT.R, TolemanM.A, TyrellJ.M, SaleemS., AboklaishA., and JahanS.. 2019. Dissemination of genetically diverse NDM-1, -5, -7 producing Gram-negative pathogens isolated from paediatric patients in Pakistan. Future Microbiol. 14:691–704.
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