The emergence of colistin resistance in Escherichia coli is a global public health concern. Contaminated food can accelerate the spread of colistin-resistant E. coli to humans. This study aimed to detect and characterize colistin-resistant E. coli from broiler meat in Bangladesh. We analyzed 136 pooled broiler meat samples from 240 carcasses collected from 40 live bird markets in urban and rural areas and 8 metropolitan supermarkets. The mean count of E. coli in broiler meat samples collected from rural retail shops, metropolitan supermarkets, and urban retail shops was 5.3 ± 1.1, 4.1 ± 1.4, and 3.9 ± 0.8 log10 colony-forming unit per gram, respectively. Colistin-resistant E. coli (minimum inhibitory concentration >2 mg/L) was found in 78% (95% confidence interval 70.2–84.1%) of the samples. All colistin-resistant isolates harbored the mcr-1 gene, while the rest of the mcr genes (mcr-2 to mcr-9) were not detected. Most colistin-resistant E. coli isolates (98%) showed coresistance to tetracycline, sulfamethoxazole/trimethoprim followed by ciprofloxacin (95%). Alarmingly, all of the colistin-resistant isolates were found to be multidrug resistant. Phylogenetic analysis showed close similarities of the mcr-1 gene sequences of this study with many strains of Enterobacterales isolated from humans, animals, and the environment. This study detected colistin-resistant E. coli contamination in broiler meat, which can pose a serious public health threat.
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References
1.
ParvinMS, TalukderS, AliMY, et al.Antimicrobial resistance pattern of Escherichia coli isolated from frozen chicken meat in Bangladesh. Pathogens, 2020; 9(6):420.
2.
SkurnikD, RuimyR, AndremontA, et al.Effect of human vicinity on antimicrobial resistance and integrons in animal faecal Escherichia coli. J Antimicrob Chemother, 2006; 57(6):1215–1219.
3.
ImamT, GibsonJS, FoysalM, et al.A cross-sectional study of antimicrobial usage on commercial broiler and layer chicken farms in Bangladesh. Front Vet Sci, 2020; 7:576113.
4.
Islam KBMS, Shiraj-Um-MahmudaS, Hazzaz-Bin-KabirM. Antibiotic usage patterns in selected broiler farms of Bangladesh and their public health implications. J Public Heal Dev Ctries, 2016; 2(3):276–284.
5.
PoirelL, JayolA, NordmannaP. Polymyxins: Antibacterial activity, susceptibility testing, and resistance mechanisms encoded by plasmids or chromosomes. Clin Microbiol Rev, 2017; 30(2):557–596.
6.
LiuYY, WangY, WalshTR, 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):161–168.
BorowiakM, BaumannB, FischerJ, 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.
9.
WangC, FengY, LiuL, et al.Identification of novel mobile colistin resistance gene mcr-10. Emerg Microbes Infect, 2020; 9(1):508–516.
10.
HasmanH, HammerumAM, HansenF, et al.Detection of mcr-1 encoding plasmid-mediated colistin-resistant Escherichia coli isolates from human bloodstream infection and imported chicken meat, Denmark 2015. Euro Surveill, 2015; 20(49):1–5.
11.
IslamA, RahmanZ, MoniraS, et al.Colistin resistant Escherichia coli carrying mcr-1 in urban sludge samples: Dhaka, Bangladesh. Gut Pathog, 2017; 9(1):77.
12.
DuttaA, IslamMZ, BaruaH, et al.Acquisition of plasmid-mediated colistin resistance gene mcr-1 in Escherichia coli of livestock origin in Bangladesh. Microb Drug Resist, 2020; 26(9):1058–1062.
13.
AhmedS, DasT, IslamMZ, et al.High prevalence of mcr-1-encoded colistin resistance in commensal Escherichia coli from broiler chicken in Bangladesh. Sci Rep, 2020; 10(1):18637.
14.
JohuraFT, TasnimJ, BarmanI, et al.Colistin-resistant Escherichia coli carrying mcr-1 in food, water, hand rinse, and healthy human gut in Bangladesh. Gut Pathog, 2020; 12(1):1–8.
15.
DasT, IslamMZ, RanaEA, et al.Abundance of mobilized colistin resistance gene (mcr-1) in commensal Escherichia coli from diverse sources. Microb Drug Resist, 2021; 27(11):1585–1593.
16.
SoburMA, IevyS, HaqueZF, et al.Emergence of colistin-resistant Escherichia coli in poultry, house flies, and pond water in Mymensingh, Bangladesh. J Adv Vet Anim Res, 2019; 6(1):50–53.
17.
JalalMS, DuttaA, DasT, et al.First detection of plasmid-mediated colistin-resistance gene (mcr-1, mcr-2 and mcr-3) in Escherichia coli isolated from breeder poultry of Bangladesh. Int J Infect Dis, 2020; 101(Suppl 1):17.
18.
MonteDF, MemA, FernandesMR, et al.Chicken meat as a reservoir of colistin-resistant Escherichia coli strains carrying mcr-1 genes in South America. Antimicrob Agents Chemother, 2017; 61(5):e02718-16.
19.
MulveyMR, MatasejeLF, RobertsonJ, et al.Dissemination of the Mcr-1 colistin resistance gene. Lancet Infect Dis, 2016; 16(3):289–290.
20.
AliMW, UtshoKS, KarmakarS, et al.First report on the molecular characteristics of mcr-1 colistin resistant E. coli isolated from retail broiler meat in Bangladesh. Int J Food Microbiol, 2023; 388:110065.
21.
Masudur RahmanM, HusnaA, ElshabrawyHA, et al.Isolation and molecular characterization of multidrug-resistant Escherichia coli from chicken meat. Sci Rep, 2020; 10(1):21999.
22.
KhairunnesaM, JamanM, NoorunnaharM, et al.Evaluation of existing poultry processing and marketing in the wet market of Gazipur city in Bangladesh. Progress Agric, 2020; 31(3):205–217.
23.
MilesAA, MisraSS, IrwinJO. The estimation of the bactericidal power of the blood. J Hyg (Lond), 1938; 38(6):732–749.
24.
GodambeLP, BandekarJ, ShashidharR. Species specific PCR based detection of Escherichia coli from Indian foods. 3 Biotech, 2017; 7(2):130.
25.
BauerAW, KirbyWM, SherrisJC, et al.Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol, 1966; 45(4):493–496.
26.
EUCAST. European Committee on Antimicrobial Susceptibility Testing (EUCAST), Breakpoint Tables for Interpretation of MICs and Zone Diameters, vol. 8, EUCAST: Växjö, Sweden; 2020.
27.
MagiorakosAP, SrinivasanA, CareyRB, et al.Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect, 2012; 18(3):268–281.
28.
ISO. ISO—ISO 20776-2:2007—Clinical laboratory testing and in vitro diagnostic test systems—Susceptibility testing of infectious agents and evaluation of performance of antimicrobial susceptibility test devices—Part 2: Evaluation of performance of antimicrobial susceptibility test devices; 2007. Available from: https://www.iso.org/standard/41631.html [Last accessed: July14, 2021].
29.
RebeloAR, BortolaiaV, KjeldgaardJS, 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):17-00672.
30.
XavierBB, LammensC, RuhalR, et al.Identification of a novel plasmid-mediated colistin-resistance gene, mcr-2, in Escherichia coli, Belgium, June 2016. Euro Surveill, 2016; 21(27):30280.
31.
CarattoliA, VillaL, FeudiC, et al.Novel plasmid-mediated colistin resistance mcr-4 gene in Salmonella and Escherichia coli, Italy 2013, Spain and Belgium, 2015 to 2016. Euro Surveill, 2017; 22(31):30589.
32.
HuangX, MadanA. CAP3: A DNA sequence assembly program. Genome Res, 1999; 9(9):868–877.
33.
KatohK, MisawaK, KumaKI, MiyataT. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res, 2002; 30(14):3059–3066.
34.
GuindonS, DufayardJF, LefortV, et al.New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst Biol, 2010; 59(3):307–321.
35.
Core TeamR. R A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna; 2018.
36.
SinghaS, CecilianiF, RahmanM. et al. Factors influencing somatic cell counts and bacterial contamination in unpasteurized milk obtained from water buffalo in Bangladesh. Trop Anim Health Prod, 2023; 55:242.
37.
WestraE. Building Mapping Applications. Packt Publishing Ltd.: Olton, UK; 2014.
38.
UddinJ, HossainK, HossainS, et al.Bacteriological assessments of foodborne pathogens in poultry meat at different super shops in Dhaka, Bangladesh. Ital J Food Saf, 2019; 8(1):15–20.
39.
SenguptaR, DasR, GangulyS, et al.Original article survey on microbial quality of chicken meat in Kolkata, India. Int J Res Pure Appl Microbiol, 2011; 1(3):32–33.
40.
BhandariN, NepaliD, PaudyalS. Assessment of bacterial load in broiler chicken meat from the retail meat shops in Chitwan, Nepal. Int J Infect Microbiol, 2013; 2(3):99–104.
41.
AhmadMUD, SarwarA, NajeebMI, et al.Assessment of microbial load of raw meat at abattoirs and retail outlets. J Anim Plant Sci, 2013; 23(3):745–748.
42.
JoshiPR, ThummeepakR, LeungtongkamU, et al.The emergence of colistin-resistant Escherichia coli in chicken meats in Nepal. FEMS Microbiol Lett, 2019; 366(20):fnz237.
43.
HassanMM, KalamMA, AlimMA, et al.Knowledge, attitude, and practices on antimicrobial use and antimicrobial resistance among commercial poultry farmers in Bangladesh. Antibiotics (Basel), 2021; 10(7):784.
44.
NadimpalliML, MarksSJ, MontealegreMC, et al.Urban informal settlements as hotspots of antimicrobial resistance and the need to curb environmental transmission. Nat Microbiol, 2020; 5(6):787–795.
45.
BistaS, Thapa ShresthaU, DhungelB, et al.Detection of plasmid-mediated colistin resistant mcr-1 gene in Escherichia coli isolated from infected chicken livers in Nepal. Animals, 2020; 10(11):2060.
46.
Sweileh WM. Global research publications on irrational use of antimicrobials: Call for more research to contain antimicrobial resistance. Global Health, 2021; 17(1):1–12.
47.
BarlaamA, ParisiA, SpinelliE, et al.Global emergence of colistin-resistant Escherichia coli in food chains and associated food safety implications: A review. J Food Prot, 2019; 82(8):1440–1448.
48.
AminMB, SraboniAS, HossainMI, et al.Occurrence and genetic characteristics of mcr-1-positive colistin-resistant E. coli from poultry environments in Bangladesh. J Glob Antimicrob Resist, 2020; 22:546–552.
49.
IslamS, UrmiUL, RanaM, et al.High abundance of the colistin resistance gene mcr-1 in chicken gut-bacteria in Bangladesh. Sci Rep, 2020; 10(1):17292.
50.
KhanSA, ImtiazMA, SayeedMA, et al.Antimicrobial resistance pattern in domestic animal—Wildlife—Environmental niche via the food chain to humans with a Bangladesh perspective: A systematic review. BMC Vet Res, 2020; 16(1):302.
51.
AkliluE, RamanK. MCR-1 gene encoded colistin-resistant Escherichia coli in raw chicken meat and bean sprouts in Malaysia. Int J Microbiol, 2020; 2020:8853582.
