Rats are rodents commonly found in Thailand that carry various zoonotic pathogens. Bacterial zoonosis can occur in a shared environment between humans and rats, especially in human communities and agricultural areas. Escherichia coli, particularly pathogenic and multidrug-resistant strains, is a significant public health concern that is transmitted by rats. This study aimed to investigate the antibiotic resistance (ABR) and biofilm formation of E. coli in caught rodents from Nakhon Si Thammarat province, Thailand. Captured rats were dissected to collect intestinal content for E. coli isolation. Two hundred and two confirmed E. coli were subjected for pathotype identification, antibiotic susceptibility testing, biofilm-forming ability (BFA), and the presence of related genes. Two E. coli isolates from intestinal content samples were atypical enteropathogenic (aEPEC). Predominantly, 52.97% of E. coli had azithromycin resistance, which was harbored by 35.64% of captured rats. Multidrug resistance (MDR) was found in 12.38% of E. coli isolates with 17 different MDR patterns. Remarkably, 96% of MDR isolates were resistant to azithromycin. Most E. coli harbored ereA (52%), followed by the blaTEM and aacC2 genes (6.44% each). Approximately 87% of isolated E. coli revealed moderate-to-high BFA. Predominantly, moderate-to-strong biofilm-forming E. coli harbored pgaA and pgaC genes. aEPEC, azithromycin resistance, MDR, and moderate-to-strong formation were the aspects of concern. Furthermore, the study of antibiotic-resistant E. coli in rats should be performed, particularly in terms of the transmission pathway, and the application of rats as bioindicators for ABR surveillance in Thailand should be established.
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References
1.
AslamB, KhurshidM, ArshadMI, et al.Antibiotic resistance: One health one world outlook. Front Cell Infect Microbiol, 2021; 11:771510; doi: 10.3389/fcimb.2021.771510
2.
AzimiT, AzimiL, FallahF, et al.Detection and characterization of Enterobacteriaceae family members carried by commensal Rattus norvegicus from Tehran, Iran. Arch Microbiol, 2021; 203(4):1321–1334; doi: 10.1007/s00203-020-02126-0
3.
BoripunR, SaengsawangP, IntongeadS, et al.Molecular characterization and nucleotide substitution of antibiotic resistance genes in multidrug-resistant Escherichia coli isolated from environmental swine farms. Emerg Contam, 2023; 9(4):100249; doi: 10.1016/j.emcon.2023.100249
4.
Clinical and Laboratory Standards Institute (CLSI). CLSI Supplement M100. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing. 2021.
5.
Desvars-LarriveA, RuppitschW, LepuschitzS, et al.Urban brown rats (Rattus norvegicus) as possible source of multidrug-resistant Enterobacteriaceae and meticillin-resistant Staphylococcus spp., Vienna, Austria, 2016 and 2017. Euro Surveill, 2019; 24(32); doi: 10.2807/1560-7917.ES.2019.24.32.1900149
6.
DominguezJE, RosarioL, JulianaS, et al.Rats as sources of multidrug-resistant Enterobacteriaceae in animal production environments. Zoonoses Public Health, 2023; 70(7):627–635; doi: 10.1111/zph.13071
7.
GomesC, Martínez-PucholS, PalmaN, et al.Macrolide resistance mechanisms in Enterobacteriaceae: Focus on azithromycin. Crit Rev Microbiol, 2017; 43(1):1–30; doi: 10.3109/1040841X.2015.1136261
8.
GwenziW, ChaukuraN, Muisa-ZikaliN, et al.Insects, rodents, and pets as reservoirs, vectors, and sentinels of antimicrobial resistance. Antibiot., 2021; 10(1):68; doi: 10.3390/antibiotics10010068
HernandesRT, EliasWP, VieiraMAM, et al.An overview of atypical enteropathogenic Escherichia coli. FEMS Microbiol Lett, 2009; 297(2):137–149; doi: 10.1111/j.1574-6968.2009.01664.x
11.
HimsworthCG, ZabekE, DesruisseauA, 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; doi: 10.7589/2014-09-242
12.
HuyH, Le KoizumiN, NuradjiH, et al.Antimicrobial resistance in Escherichia coli isolated from brown rats and house shrews in markets, Bogor, Indonesia. J Vet Med Sci, 2021; 83(3):531–534; doi: 10.1292/jvms.20-0558
13.
JahanNA, LindseyLL, LarsenPA. The role of peridomestic rodents as reservoirs for zoonotic foodborne pathogens. Vector Borne Zoonotic Dis, 2021; 21(3):133–148; doi: 10.1089/vbz.2020.2640
KrumpermanPH. Multiple Antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Appl Environ Microbiol, 1983; 46(1):165–170; doi: 10.1128/aem.46.1.165-170.1983
16.
KulnananP, ChupromJ, ThomrongsuwannakijT, et al.Antibacterial, antibiofilm, and anti- adhesion activities of Piper betle leaf extract against avian pathogenic Escherichia coli. Arch Microbiol, 2021; 204(1):49; doi: 10.1007/s00203-021-02701-z
17.
Le HuyH, KoizumiN, UngTTH, et al.Antibiotic-resistant Escherichia coli isolated from urban rodents in Hanoi, Vietnam. J Vet Med Sci, 2020; 82(5):653–660; doi: 10.1292/jvms.19-0697
18.
MalikK, MemonaH. Molecular and immunological studies of pathogenic Escherichia coli in meat samples collected from different localities of Lahore. Int J Cell Mol Biol, 2010; 1:218–224; doi: 10.1016/j.sjbs.2015.06.009
19.
MitsuwanW, IntongeadS, SaengsawangP, et al.Occurrence of multidrug resistance associated with extended-spectrum β–lactamase and the biofilm forming ability of Escherichia coli in environmental swine husbandry. Comp Immunol Microbiol Infect Dis, 2023; 103:102093; doi: 10.1016/j.cimid.2023.102093
20.
MoradpourN, BorjiH, DarvishJ, et al.Rodents helminth parasites in different region of Iran. Iran J Parasitol, 2018; 13(2):275–284.
21.
NhungNT, CuongNV, ThwaitesG, et al.Antimicrobial usage and antimicrobial resistance in animal production in Southeast Asia: A review. Antibiot., 2016; 5(4):37; doi: 10.3390/antibiotics5040037
22.
PakbinB, BrückWM, RossenJWA. Virulence factors of enteric pathogenic Escherichia coli: A review. Int J Mol Sci, 2021; 22(18):9922; doi: 10.3390/ijms22189922
23.
PaulD, ChawlaM, AhrodiaT, et al.Antibiotic potentiation as a promising strategy to combat macrolide resistance in bacterial pathogens. Antibiot., 2023; 12(12):1715; doi: 10.3390/antibiotics12121715
24.
PengX, YuK-Q, DengG-H, et al.Comparison of direct boiling method with commercial kits for extracting fecal microbiome DNA by Illumina sequencing of 16S rRNA tags. J Microbiol Methods, 2013; 95(3):455–462; doi: 10.1016/j.mimet.2013.07.015
25.
PormohammadA, NasiriMJ, AzimiT. Prevalence of antibiotic resistance in Escherichia coli strains simultaneously isolated from humans, animals, food, and the environment: A systematic review and meta-analysis. Infect Drug Resist, 2019; 12:1181–1197; doi: 10.2147/IDR.S201324
26.
R Core Team. R: A language and environment for statistical computing. 2020.
27.
RabieeMH, MahmoudiA, SiahsarvieR, et al.Rodent-borne diseases and their public health importance in Iran. PLoS Negl Trop Dis, 2018; 12(4):e0006256; doi: 10.1371/journal.pntd.0006256
28.
RatherMA, GuptaK, MandalM. Microbial biofilm: Formation, architecture, antibiotic resistance, and control strategies. Braz J Microbiol, 2021; 52(4):1701–1718; doi: 10.1007/s42770-021-00624-x
29.
RomyasamitC, SornseneeP, ChimpleeS, et al.Prevalence and characterization of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae isolated from raw vegetables retailed in Southern Thailand. PeerJ, 2021; 9:e11787; doi: 10.7717/peerj.11787
30.
RomyasamitC, SornseneeP, KawilaS, et al.Extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae: Insights from a tertiary hospital in Southern Thailand. Microbiol Spectr, 2024; 12(7):e0021324; doi: 10.1128/spectrum.00213-24
31.
SanoE, EspositoF, FontanaH, et al.One Health clones of multidrug-resistant Escherichia coli carried by synanthropic animals in Brazil. One Health, 2023; 16:100476; doi: 10.1016/j.onehlt.2022.100476
32.
SiriY, BumyutA, PrechaN, et al.Multidrug antibiotic resistance in hospital wastewater as a reflection of antibiotic prescription and infection cases. Sci Total Environ, 2024; 908:168453; doi: 10.1016/j.scitotenv.2023.168453
33.
SornseneeP, ChimpleeS, ArbubakerA, et al.Occurrence, antimicrobial resistance profile, and characterization of extended-spectrum β-lactamase-producing Escherichia coli isolates from minced meat at local markets in Thailand. Foodborne Pathog Dis, 2022; 19(3):232–240; doi: 10.1089/fpd.2021.0059
34.
TanthanathipchaiN, MitsuwanW, ChaisiriK, et al.Trypanosoma lewisi in blood of Rattus rattus complex residing in human settlements, Nakhon Si Thammarat, Thailand: Microscopic and molecular investigations. Comp Immunol Microbiol Infect Dis, 2023; 98:102010; doi: 10.1016/j.cimid.2023.102010
35.
ThaikoedS, MitsuwanW, ChaisiriK, et al.The infection of Cysticercus fasciolaris in natural rats (Rattus species) residing in human residence areas, Nakhon Si Thammarat, Thailand. Comp Immunol Microbiol Infect Dis, 2024; 107:102152; doi: 10.1016/j.cimid.2024.102152
36.
ThomrongsuwannakijT, NarinthornR, MahawanT, et al.Molecular and phenotypic characterization of avian pathogenic Escherichia coli isolated from commercial broilers and native chickens. Poult Sci, 2022; 101(1):101527; doi: 10.1016/j.psj.2021.101527
37.
Uea-AnuwongT, BiggelM, CernelaN, et al.Antimicrobial resistance and phylogenetic relatedness of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli in peridomestic rats (Rattus norvegicus and Rattus tanezumi) linked to city areas and animal farms in Hong Kong. Environ Res, 2024; 251(Pt 1):118623; doi: 10.1016/j.envres.2024.118623
38.
Urban-ChmielR, MarekA, Stępień-PyśniakD, et al.Antibiotic resistance in bacteria-a review. Antibiot. 2022; 11(8):1079; doi: 10.3390/antibiotics11081079
39.
Van DuinD, PatersonDL. Multidrug-resistant bacteria in the community: An update. Infect Dis Clin North Am, 2020; 34(4):709–722; doi: 10.1016/j.idc.2020.08.002
40.
VarelaMF, StephenJ, LekshmiM, et al.Bacterial resistance to antimicrobial agents. Antibiot, 2021; 10(5):593; doi: 10.3390/antibiotics10050593
41.
WirthT, FalushD, LanR, et al.Sex and virulence in Escherichia coli: An evolutionary perspective. Mol Microbiol, 2006; 60(5):1136–1151; doi: 10.1111/j.1365-2958.2006.05172.x
42.
WongtawanT, NarinthornR, SontigunN, et al.Characterizing the antimicrobial resistance profile of Escherichia coli found in sport animals (figihting cocks, figihting bulls, and sport horses) and soils from their environment. Vet World, 2022; 15(11):2673–2680; doi: 10.1420/2/vetworld
43.
Xing-WeiL, Peng-LiangL, Ya-JunZ, et al.Upregulation of outer membrane porin gene OmpC contributed to enhancement of azithromycin susceptibility in multidrug-resistant Escherichia coli. Microbiol Spectr, 2024; 12(4):e03918-23; doi: 10.1128/spectrum.03918-23
44.
YamaniLZ, ElhadiN. Virulence characteristics, antibiotic resistance patterns and molecular yyping of enteropathogenic producing Escherichia coli (EPEC) isolates in eastern province of Saudi Arabia: 2013-2014. Infect Drug Resist, 2022; 15:6763–6772; doi: 10.2147/IDR.S388956
45.
ZielińskiM, ParkJ, SlenoB, et al.Structural and functional insights into esterase-mediated macrolide resistance. Nat Commun, 2021; 12(1):1732; doi: 10.1038/s41467-021-22016-3
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