The Surveillance of Antimicrobial Susceptibility Pattern and blaCTX-M Gene Encoding in Escherichia coli Isolated from Healthy Goat Farms in Sai Yok District, Kanchanaburi Province, Thailand
Keywords:Escherichia coli, goat, Antimicrobial susceptibility, blaCTX-M, Kanchanaburi
This observation study aimed to investigate the antimicrobial susceptibility pattern and blaCTX-M gene encoding in Escherichia coli isolates collected from healthy goat farms in Sai Yok District, Kanchanaburi Province, Thailand. By collecting 92 samples from rectal swabs from goats in 7 subdistricts in Sai Yok District, the bacterial identification, antimicrobial susceptibility test, and detection of the presence of blaCTX-M genes by conventional polymerase chain reaction (PCR) techniques were performed. Based on the results of the study, E. coli prevalence was found in 72.8% of the samples (n = 67). The prevalence rate of E. coli isolated from the samples from 6 subdistricts (85.7%) was higher than or equal to 50%. One influencing factor of the high E. coli detection was the person administering antimicrobial agents to goats (p < 0.001). The number of E. coli isolated from goats drinking water from natural sources was higher than that isolated from goats drinking from the tap water system (p < 0.038). The antimicrobial susceptibility of amoxicillin/clavulanic acid, imipenem, fluoroquinolones, piperacillin/tazobactam, and trimethoprim/sulfamethoxazole completely covered entire isolations. E. coli showed the highest resistance rate to cefotaxime (19.4%). The antimicrobial resistance (AMR) patterns were categorized by the number of antimicrobial agents into three patterns: one, two, and at least three AMRs (63%, 27%, and 10%, respectively). Every drug resistance pattern contained cefotaxime in all groups. The blaCTX-M gene was not found from all E. coli isolates. The study suggested the slightly high prevalence with the welling trend of AMR characteristics among the E. coli isolates collected from healthy goat farms in Sai Yok District, Kanchanaburi Province. Some influencing factors may be important for farm management to prevent the occurrence and spread of antimicrobial-resistant characteristics in goat farms.
Abdalhamed AM, Ghazy AA, Ibrahim ES, Arafa AA, Zeedan GSG. Therapeutic effect of biosynthetic gold nanoparticles on multidrug-resistant Escherichia coli and Salmonella species isolated from ruminants. Vet World. 2021;14(12):3200-10.
Al-Ajmi D, Rahman S, Banu S. Occurrence, virulence genes, and antimicrobial profiles of Escherichia coli O157 isolated from ruminants slaughtered in Al Ain, United Arab Emirates. BMC Microbiol. 2020;20(1):210.
Álvarez-Suárez ME, Otero A, García-López ML, Dahbi G, Blanco M, Mora A, Blanco J, Santos JA. Genetic characterization of Shiga toxin-producing Escherichia coli (STEC) and atypical enteropathogenic Escherichia coli (EPEC) isolates from goat's milk and goat farm environment. Int J Food Microbiol. 2016;236:148-54.
Atlaw NA, Keelara S, Correa M, Foster D, Gebreyes W, Aidara-Kane A, et al. Identification of CTX-M Type ESBL E. coli from sheep and their abattoir environment using whole-genome sequencing. Pathogens. 2021;10(11):1480.
Bai J, Shi X, Nagaraja TG. A multiplex PCR procedure for the detection of six major virulence genes in Escherichia coli O157:H7. J Microbiol Methods. 2010;82(1):85-9.
Balázs B, Nagy JB, Tóth Z, Nagy F, Károlyi S, Turcsányi I, et al. Occurrence of Escherichia coli producing extended spectrum β-lactamases in food-producing animals. Acta Vet Hung. 2021;69(3):211-15.
Bessalah S, Fairbrother JM, Salhi I, Vanier G, Khorchani T, Seddik M-M, et al. Characterization and antimicrobial susceptibility of Escherichia coli isolated from healthy farm animals in Tunisia. Anim Biotechnol. 2021;32(6):748-57.
Blount ZD. The unexhausted potential of E. coli. eLife. 2015;4:e05826.
Bosilevac JM, Gassem MA, Al Sheddy IA, Almaiman SA, Al-Mohizea IS, Alowaimer A, et al. Prevalence of Escherichia coli O157:H7 and Salmonella in camels, cattle, goats, and sheep harvested for meat in Riyadh. J Food Prot. 2015;78(1):89-96.
Brinkmeyer R, Amon RM, Schwarz JR, Saxton T, Roberts D, Harrison S, et al. Distribution and persistence of Escherichia coli and Enterococci in stream bed and bank sediments from two urban streams in Houston, TX. Sci Total Environ. 2015;502:650-8.
Carlos C, Pires MM, Stoppe NC, Hachich EM, Sato MI, Gomes TA, et al. Escherichia coli phylogenetic group determination and its application in the identification of the major animal source of fecal contamination. BMC Microbiol. 2010;10:161.
Castanheira M, Simner PJ, Bradford PA. Extended-spectrum β-lactamases: an update on their characteristics, epidemiology and detection. JAC-Antimicrobial Resistance. 2021;3(3):dlab092.
CLSI. M100 Performance Standards for antimicrobial susceptibility testing. 28th ed. Wayne, PA: Clinical and laboratory standards institute;2018.
Dulo F, Feleke A, Szonyi B, Fries R, Baumann MPO, Grace D. Isolation of multidrug-resistant Escherichia coli O157 from goats in the Somali region of Ethiopia: A cross-sectional, abattoir-based study. PLoS One. 2015;10(11):e0142905.
Elzhraa F, Al-Ashmawy M, El-Sherbini M, Abdelkhalek A. Critical occurrence of verotoxgenic E.coli and non-typhoidal salmonella in some heat treated dairy products. Ital J Food Saf. 2021;10(2):9318.
Gonzalez AGM, Cerqueira AMF. Shiga toxin-producing Escherichia coli in the animal reservoir and food in Brazil. J Appl Microbiol. 2020;128(6):1568-82.
Google. Map (Sai Yok) [Internet]. Google 2022 [cited 2022 Mach 22]. Available from: http://maps.google.co.th/.
Göttling J, Heckel J-O, Hotzel H, Fruth A, Pfeifer Y, Henning K, et al. Zoonotic bacteria in clinically healthy goats in petting zoo settings of zoological gardens in Germany. Zoonoses Public Health. 2022;69(4):333-43.
Gutta VR, Kannan G, Lee JH, Kouakou B, Getz WR. Influences of short-term pre-slaughter dietary manipulation in sheep and goats on pH and microbial loads of gastrointestinal tract. ScienceDirect. 2009;81(1):21-28.
Hanlon KE, Miller MF, Guillen LM, Echeverry A, Dormedy E, Cemo B, et al. Presence of Salmonella and Escherichia coli O157 on the hide, and presence of Salmonella, Escherichia coli O157 and Campylobacter in feces from small-ruminant (goat and lamb) samples collected in the United States, Bahamas and Mexico. Meat Sci. 2018;135:1-5.
Hawkey PM, Jones AM. The changing epidemiology of resistance. J Antimicrob Chemother. 2009;64 (Suppl 1):i3-10.
Ioanna F, Quaglia NC, Storelli MM, Castiglia D, Goffredo E, Storelli A, et al. Survival of Escherichia coli O157:H7 during the manufacture and ripening of Cacioricotta goat cheese. Food Microbiol. 2018;70:200-5.
Kaur J, Chopra S, Sheevani, Mahajan G. Modified double-disc synergy test to detect ESBL production in urinary isolates of Escherichia coli and Klebsiella pneumonia. J Clin Diagn Res. 2013;7(2):227-31.
Kannan G, Mahapatra AK, Degala HL. Preharvest management and postharvest intervention strategies to reduce Escherichia coli contamination in goat meat: A Review. Animals (Basel). 2021;11(10):2943.
Lambrecht NJ, Wilson ML, Bridges D, Eisenberg JNS, Adu B, Baylin A, et al. Ruminant-related risk factors are associated with shiga toxin-producing Escherichia coli infection in children in Southern Ghana. Am J Trop Med Hyg. 2021;106(2):513-22.
La Ragione RM, Best A, Woodward MJ, Wales AD. Escherichia coli O157:H7 colonization in small domestic ruminants. FEMS Microbiol Rev. 2009;33(2):394-410.
Leekitcharoenphon P, Johansson MHK, Munk P, Malorny B, Skarżyńska M, Wadepohl K, et al. Genomic evolution of antimicrobial resistance in Escherichia coli. Sci Rep. 2021;11(1):15108.
Liao CY, Balasubramanian B, Peng JJ, Tao SR, Liu WC, Ma Y. Antimicrobial resistance of Escherichia coli from aquaculture farms and their environment in Zhanjiang, China. Front Vet Sci. 2021;8:806653.
Lihan S, Lee SY, Toh SC, Leong SS. Plasmid-mediated antibiotic resistant Escherichia coli in sarawak rivers and aquaculture farms, Northwest of Borneo. Antibiotics (Basel). 2021;10(7):776.
Lugsomya K, Chatsuwan T, Niyomtham W, Tummaruk P, Hampson DJ, Prapasarakul N. Routine prophylactic antimicrobial use Is associated with increased phenotypic and genotypic resistance in commensal Escherichia coli isolates recovered from healthy fattening pigs on farms in Thailand. Microb Drud Resist. 2018;24(2):213-23.
Ma CY, Sugie Y, Yu Z, Okuno Y, Tanaka H, Ihara M. Occurrence of E. coli and antibiotic-resistant E. coli in the southern watershed of Lake Biwa, including in wastewater treatment plant effluent and inflow rivers. Chemosphere. 2022;301:134372.
Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, 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):268-81.
Magnusson U, Moodley A, Osbjer K. Antimicrobial resistance at the livestock-human interface: implications for veterinary services. Rev Sci Tech. 2021;40(2):511-21.
Magouras I, Carmo LP, Stärk KDC, Schüpbach-Regula G. Antimicrobial usage and -resistance in livestock: where should we focus?. Front Vet Sci. 2017;4:148.
Magray MS, Kumar A, Rawat AK, Srivastava S. Identification of Escherichia coli through analysis of 16S rRNA and 16S-23S rRNA internal transcribed spacer region sequences. Bio information. 2011;6(10):370-1.
Malahlela MN, Cenci-Goga BT, Marufu MC, Fonkui TY, Grispoldi L, Etter E, et al. Occurrence, aerotypes and virulence characteristics of shiga-toxin-producing Escherichia coli isolates from goats on communal rangeland in South Africa. Toxins (Basel). 2022;14(5):353.
Manishimwe R, Moncada PM, Musanayire V, Shyaka A, Scott HM, Loneragan GH. Antibiotic-Resistant Escherichia coli and Salmonella from the feces of food animals in the east province of rwanda. Animals (Basel). 2021;11(4):1013.
Meijs AP, Gijsbers EF, Hengeveld PD, Dierikx CM, de Greeff SC, van Duijkeren E. ESBL/pAmpC-producing Escherichia coli and Klebsiella pneumoniae carriage among veterinary healthcare workers in the Netherlands. Antimicrob Resist Infect Control. 2021;10(1):147.
Miltgen G, Martak D, Valot B, Kamus L, Garrigos T, Verchere G, et al. One Health compartmental analysis of ESBL-producing Escherichia coli on Reunion Island reveals partitioning between humans and livestock. J Antimicrob Chemother. 2022;77(5):1254-62.
Mora A, Herrrera A, Lopez C, Dahbi G, Mamani R, Pita JM, et al. Characteristics of the Shiga-toxin-producing enteroaggregative Escherichia coli O104:H4 German outbreak strain and of STEC strains isolated in Spain. Int Microbiol. 2011;14(3):121-41.
Murphy CP, Carson C, Smith BA, Chapman B, Marrotte J, McCann M, et al. Factors potentially linked with the occurrence of antimicrobial resistance in selected bacteria from cattle, chickens and pigs: A scoping review of publications for use in modelling of antimicrobial resistance (IAM.AMR Project). Zoonoses Public Health. 2018;65(8):957-71.
Mwanyika G, Call DR, Rugumisa B, Luanda C, Murutu R, Subbiah M, et al. Prevalence of antimicrobial-resistant Escherichia coli from fresh goat meat in Arusha, Tanzania. J Food Prot. 2016;79(9):1635-41.
Ndegwa E, Almehmadi H, Chyer K, Kaseloo P, Ako AA. Longitudinal shedding patterns and characterization of antibiotic resistant E. coli in pastured goats using a cohort study. Antibiotics. 2019;8(3):136.
Nichols MC, Gacek P, Phan Q, Gambino-Shirley KJ, Gollarza LM, Schroeder MN, et al. Agritourism and kidding season: A large outbreak of human shiga toxin-producing Escherichia coli O157 (STEC O157) infections linked to a goat dairy farm-connecticut, 2016. Front Vet Sci. 2021;8:744055.
Novotna R, Alexa P, Hamrik J, Madanat A, Smola J, Cizek A. Isolation and characterization shiga toxin-producing Escherichia coli from sheep and goats in Jordan with evidence of multiresistant serotype O157:H7. Veterinarni Medicina. 2005;50(3):111-18.
Nüesch-Inderbinen M, Hänni C, Zurfluh K, Hartnack S, Stephan R. Antimicrobial resistance profiles of Escherichia coli and prevalence of extended-spectrum beta-lactamase-producing Enterobacteriaceae in calves from organic and conventional dairy farms in Switzerland. Microbiologyopen. 2022;11(2):e1269.
Obaidat MM, Bani Salman AE, Davis MA, Roess AA. Major diseases, extensive misuse, and high antimicrobial resistance of Escherichia coli in large- and small-scale dairy cattle farms in Jordan. J Dairy Sci. 2018;101(3):2324-34.
Peng JJ, Balasubramanian B, Ming YY, Niu JL, Yi CM, Ma Y, et al. Identification of antimicrobial resistance genes and drug resistance analysis of Escherichia coli in the animal farm environment. J Infect Public Health. 2021;14(12):1788-95.
Prapasawat W, Intarapuk A. Prevalence of antimicrobial resistance and integrons in Escherichia coli isolated from feces of dairy goats in Nong Chok, Bangkok, Thailand. Vet Integr Sci. 2021;19(2): 223-36.
Ragione RML, Best A, Woodward MJ, Wales AD. Escherichia coli O157:H7 colonization in small domestic ruminants, FEMS Microbiology Rev. 2009;33(2):394–410.
Ramadan AA, Abdelaziz NA, Amin MA, Aziz RK. Novel blaCTX-M variants and genotype-phenotype correlations among clinical isolates of extended spectrum beta lactamase-producing Escherichia coli. Sci Rep. 2019;9(1):4224.
Riley LW. Distinguishing Pathovars from Nonpathovars: Escherichia coli. Microbiol Spectr. 2020;8(4).
Salam S, McDaniel R, Bleakley B, Amegbletor L, Mardani S. Variability of E. coli in streambed sediment and its implication for sediment sampling. J Contam Hydrol. 2021;242:103859.
Saladin M, Cao VT, Lambert T, Donay JL, Herrmann JL, Ould-Hocine Z, et al. Diversity of CTX-M beta-lactamases and their promoter regions from Enterobacteriaceae isolated in three Parisian hospitals. FEMS Microbiol Lett. 2002;209(2):161-8.
Samreen, Ahmad I, Malak HA, Abulreesh HH. Environmental antimicrobial resistance and its drivers: a potential threat to public health. J Glob Antimicrob Resist. 2021;27:101-11.
Schrijver R, Stijntjes M, Rodríguez-Baño J, Tacconelli E, Babu Rajendran N, Voss A. Review of antimicrobial resistance surveillance programmes in livestock and meat in EU with focus on humans. Clin Microbiol Infect. 2018;24(6):577-90.
Shafiq M, Rahman SU, Bilal H, Ullah A, Noman SM, Zeng M, et al. Incidence and molecular characterization of ESBL-producing and colistin-resistant Escherichia coli isolates recovered from healthy food-producing animals in Pakistan. J Appl Microbiol. 2022;133(3):1169-82.
Shabana II, Al-Enazi AT. Investigation of plasmid-mediated resistance in E. coli isolated from healthy and diarrheic sheep and goats. Saudi J Biol Sci. 2020;27(3):788-96.
Smolders A, Rolls RJ, Ryder D, Watkinson A, Mackenzie M. Cattle-derived microbial input to source water catchments: An experimental assessment of stream crossing modification. J Environ Manage. 2015;156:143-9.
Tropea E, Hynds P, McDermott K, Brown RS, Majury A. Environmental adaptation of E. coli within private groundwater sources in southeastern Ontario: Implications for groundwater quality monitoring and human health. Environ Pollut. 2021;285:117263.
Tsilipounidaki K, Florou Z, Lianou DT, Michael CK, Katsarou EI, Skoulakis A, et al. Detection of zoonotic gastrointestinal pathogens in dairy sheep and goats by using FilmArray® multiplex-PCR technology. Microorganisms. 2022;10(4):714.
van Hoek AHAM, Veenman C, Florijn A, Huijbers PMC, Graat EAM, de Greeff S, et al. Longitudinal study of ESBL Escherichia coli carriage on an organic broiler farm. J Antimicrob Chemother. 2018;73(12):3298-304.
Vu-Khac H, Cornick NA. Prevalence and genetic profiles of Shiga toxin-producing Escherichia coli strains isolated from buffaloes, cattle, and goats in central Vietnam. Vet Microbiol. 2008;126(4):356-63.
Waade J, Seibt U, Honscha W, Rachidi F, Starke A, Speck S, et al. Multidrug-resistant enterobacteria in newborn dairy calves in Germany. PLoS One. 2021;16(3):e0248291.
Yadav V, Prakash S, Srivastava S, Verma PC, Gupta V, Basu V, et al. Identification of Comamonas species using 16S rRNA gene sequence. Bioinformation. 2009;3(9):381-3.
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