The spread of extended-spectrum beta-lactamase–producing Enterobacterales (ESBL-E) in communities has been facilitated by direct contact with humans or animal carriers and insects such as houseflies. Houseflies may have an increased risk of human exposure to antimicrobial-resistant pathogens, including ESBL-E. In this study, we determined the presence of ESBL-E in houseflies and ready-to-eat food samples from selected food vending sites in five health care facilities in Greater Accra, Ghana. Sixty (60) food vending sites were included in this study. Flies (10) were pooled, and food (5 g) was macerated and homogenized aseptically in brain-heart infusion agar. Suspensions were cultured on MacConkey agar supplemented with 4 µg/mL cefotaxime for ∼18 h. Phenotypic and molecular characterization of ESBL-E was performed using a combination disk diffusion method, multiplex polymerase chain reaction, and direct nucleotide sequencing. Of the 60 food vending sites, 62% (37) of the food vendors had flies within their premises that carried ESBL-E, and 15% (9) of the food samples collected from the vendors were contaminated with ESBL-E. The most predominant ESBL-producing Enterobacterales from housefly samples was Proteus vulgaris (54%) and that of food samples were P. vulgaris (22.5%) and Escherichia coli (22.5%). All Enterobacterales from flies and food samples harbored an ESBL gene with blaCTX-M, mostly blaCTX-M-15, being the predominant gene and gene type, respectively. Houseflies may be potential contributors to the spread of ESBL-producing Enterobacterales in Ghana.
BehrensW, KolteB, JunkerV, et al.Bacterial genome sequencing tracks the housefly-associated dispersal of fluoroquinolone- and cephalosporin-resistant Escherichia coli from a pig farm. Environ Microbiol, 2023; 25(6):1174–1185; doi: 10.1111/1462-2920.16352
3.
BevanER, JonesAM, HawkeyPM. Global epidemiology of CTX-M β-lactamases: Temporal and geographical shifts in genotype. J Antimicrob Chemother, 2017; 72(8):2145–2155; doi: 10.1093/jac/dkx146
4.
BonnetR. Growing group of extended-spectrum β-lactamases: The CTX-M enzymes. Antimicrob Agents Chemother, 2004; 48(1):1–14; doi: 10.1128/aac.48.1.1-14.2004
5.
BrowneLB, KerrRW. Influence of sex and prior protein feeding on preferences by the housefly, Musca domestica, between sucrose solutions and solutions of L-leucine or sodium phosphate buffer. Entomologia Exp Applicata, 1986; 41(2):135–138; doi: 10.1111/j.1570-7458.1986.tb00519.x
BushK, JacobyGA, MedeirosAA. A functional classification scheme for beta-lactamases and its correlation with molecular structure. Antimicrob Agents Chemother, 1995; 39(6):1211–1233; doi: 10.1128/AAC.39.6.1211
ChouchaniC, El SalabiA, MarrakchiR, et al.Characterization of IncA/C conjugative plasmid harboring blaTEM-52 and blaCTX-M-15 extended-spectrum β-Lactamases in clinical isolates of Escherichia coli in Tunisia. Eur J Clin Microbiol Infect Dis, 2012; 31(6):1081–1087; doi: 10.1007/s10096-011-1410-z
11.
DelaH, EgyirB, BeheneE, et al.Microbiological quality and antimicrobial resistance of bacteria species recovered from ready-to-eat food, water samples, and palm swabs of food vendors in Accra, Ghana. Int J Food Microbiol, 2023; 396:110195; doi: 10.1016/j.ijfoodmicro.2023.110195
12.
DelaH, EgyirB, MajekodunmiAO, et al.Diarrhoeagenic E. coli occurrence and antimicrobial resistance of extended spectrum beta-lactamases isolated from diarrhoea patients attending health facilities in Accra, Ghana. PLoS One, 2022; 17(5):e0268991; doi: 10.1371/journal.pone.0268991
13.
DonkorES, HorlortuPZ, DayieNT, et al.Community acquired urinary tract infections among adults in Accra, Ghana. Infect Drug Resist, 2019; 12:2059–2067; doi: 10.2147/IDR.S204880
14.
EgbuleOS, IwerieborBC, OdumEI. Beta-lactamase-producing Escherichia coli isolates recovered from pig handlers in retail shops and abattoirs in selected localities in Southern Nigeria: Implications for public health. Antibiotics (Basel), 2020; 10(1):9; doi: 10.3390/antibiotics10010009
15.
EibachD, CamposCB, KrumkampR, et al.Extended spectrum beta-lactamase producing Enterobacteriaceae causing bloodstream infections in rural Ghana, 2007–2012. Int J Med Microbiol, 2016; 306(4):249–254; doi: 10.1016/j.ijmm.2016.05.006
16.
FisherML, FowlerFE, DenningSS, et al.Survival of the house fly (Diptera: Muscidae) on Truvia and other sweeteners. J Med Entomol, 2017; 54(4):999–1005; doi: 10.1093/jme/tjw241
17.
FortiniD, FashaeK, VillaL, et al.A novel plasmid carrying blaCTX-M-15 identified in commensal Escherichia coli from healthy pregnant women in Ibadan, Nigeria. J Glob Antimicrob Resist, 2015; 3(1):9–12; doi: 10.1016/j.jgar.2014.12.002
18.
GoulsonD, HughesWOH, ChapmanJW. Fly populations associated with landfill and composting sites used for household refuse disposal. Bull Entomol Res, 1999; 89(6):493–498; doi: 10.1017/S0007485399000644
19.
GuptaA, NayduchD, VermaP, et al.Phylogenetic characterization of bacteria in the gut of house flies (Musca Domestica L.). FEMS Microbiol Ecol, 2012; 79(3):581–593; doi: 10.1111/j.1574-6941.2011.01248.x
20.
JooE-J, KimSJ, BaekM, et al.Fecal carriage of antimicrobial-resistant Enterobacteriaceae in healthy Korean adults. J Microbiol Biotechnol, 2018; 28(7):1178–1184; doi: 10.4014/jmb.1801.12060
21.
MadecJ-Y, HaenniM, NordmannP, et al.Extended-spectrum β-lactamase/AmpC- and carbapenemase-producing Enterobacteriaceae in animals: A threat for humans? Clin Microbiol Infect, 2017; 23(11):826–833; doi: 10.1016/j.cmi.2017.01.013
22.
MarconJ, SchubertS, StiefCG, et al.In vitro efficacy of phytotherapeutics suggested for prevention and therapy of urinary tract infections. Infection, 2019; 47(6):937–944; doi: 10.1007/s15010-019-01315-4
23.
MoremiN, ClausH, VogelU, et al.Faecal carriage of CTX-M extended-spectrum beta-lactamase-producing Enterobacteriaceae among street children dwelling in Mwanza City, Tanzania. PLoS One, 2017; 12(9):e0184592; doi: 10.1371/journal.pone.0184592
24.
Obeng-NkrumahN, Tawiah-AbrokwaGD, OwusuE, et al.Role of CTX-M-15 gene in spread of extended-spectrum beta-lactamases among immunocompetent patients in Ghana. Afr J Lab Med, 2023; 12(1):2135; doi: 10.4102/ajlm.v12i1.2135
25.
Obeng-NkrumahN, Twum-DansoK, KrogfeltKA, et al.High levels of extended-spectrum beta-lactamases in a major teaching hospital in Ghana: The need for regular monitoring and evaluation of antibiotic resistance. Am J Trop Med Hyg, 2013; 89(5):960–964; doi: 10.4269/ajtmh.12-0642
26.
Oduro-MensahD, Obeng-NkrumahN, BonneyEY, et al.Genetic characterization of TEM-type ESBL-associated antibacterial resistance in Enterobacteriaceae in a tertiary hospital in Ghana. Ann Clin Microbiol Antimicrob, 2016; 15:29; doi: 10.1186/s12941-016-0144-2
27.
OwusuFA, Obeng-NkrumahN, GyinaeE, et al.Occurrence of carbapenemases, extended-spectrum beta-lactamases and AmpCs among beta-lactamase-producing gram-negative bacteria from clinical sources in Accra, Ghana. Antibiotics (Basel), 2023; 12(6):1016; doi: 10.3390/antibiotics12061016
28.
PoudelA, HathcockT, ButayeP, et al.Multidrug-resistant Escherichia coli, Klebsiella pneumoniae and Staphylococcus spp. in houseflies and blowflies from farms and their environmental settings. Int J Environ Res Public Health, 2019; 16(19):3583; doi: 10.3390/ijerph16193583
29.
RybaríkováJ, DolejskáM, MaternaD, et al.Phenotypic and genotypic characteristics of antimicrobial resistant Escherichia coli isolated from symbovine flies, cattle and sympatric insectivorous house martins from a farm in the Czech Republic (2006–2007). Res Vet Sci, 2010; 89(2):179–183; doi: 10.1016/j.rvsc.2010.02.016
30.
SallemRB, SlamaKB, EstepaV, et al.Detection of CTX-M-15-producing Escherichia coli isolates of lineages ST410-A, ST617-A and ST354-D in faecal samples of hospitalized patients in a Mauritanian hospital. J Chemother, 2015; 27(2):114–116.
31.
SeetswaneE, LoetoD, MuzilaM, et al.Phenotypic and genotypic profiling reveals a high prevalence of methicillin-resistant Staphylococcus aureus isolated from hospitals, houseflies and adjacent informal food retailers in Botswana. Microbiology (Reading), 2022; 168(10):1213; doi: 10.1099/mic.0.001213
32.
SivakumarM, AbassG, VivekanandhanR, et al.Extended-spectrum beta-lactamase (ESBL) producing and multidrug-resistant Escherichia coli in street foods: A public health concern. J Food Sci Technol, 2021; 58(4):1247–1261; doi: 10.1007/s13197-020-04634-9
33.
Solà-GinésM, González-LópezJJ, Cameron-VeasK, et al.Houseflies (Musca domestica) as vectors for extended-spectrum β-lactamase-producing Escherichia coli on Spanish broiler farms. Appl Environ Microbiol, 2015; 81(11):3604–3611; doi: 10.1128/AEM.04252-14
34.
SongeMM, Hang’ombeBM, Knight-JonesTJD, et al.Antimicrobial resistant Enteropathogenic Escherichia coli and Salmonella spp. in houseflies infesting fish in food markets in Zambia. Int J Environ Res Public Health, 2017; 14(1):21; doi: 10.3390/ijerph14010021
35.
TufaTB, FuchsA, WienemannT, et al.Carriage of ESBL-producing gram-negative bacteria by flies captured in a hospital and its suburban surroundings in Ethiopia. Antimicrob Resist Infect Control, 2020; 9(1):175; doi: 10.1186/s13756-020-00836-0
36.
WangY-S, ShelomiM. Review of black soldier fly (Hermetia illucens) as animal feed and human food. Foods, 2017; 6(10):91; doi: 10.3390/foods6100091
37.
YamamotoRT, JensenE. Ingestion of feeding stimulants and protein by the female housefly, Musca domestica L. J Insect Physiol, 1967; 13(1):91–98; doi: 10.1016/0022-1910(67)90006-6
38.
Yeboah-ManD, KpeliG, AkyehM, et al.Bacteriological quality of ready-to-eat foods sold on and around university of Ghana Campus. Research J of Microbiology, 2010; 5(2):130–136.
39.
YeleliereE, CobbinaSJ, AbubakariZI. Review of microbial food contamination and food hygiene in selected capital cities of Ghana. Cogent Food Agric, 2017; 3(1):1395102; doi: 10.1080/23311932.2017.1395102
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
