Restricted accessResearch articleFirst published online 2025-02
Antimicrobial Resistance Characteristics of Fecal Escherichia coli and Enterococcus Species in U.S. Goats: 2019 National Animal Health Monitoring System Enteric Study
Escherichia coli and Enterococcus species are normal bacteria of the gastrointestinal tract and serve as indicator organisms for the epidemiology and emergence of antimicrobial resistance in their hosts and the environment. Some E. coli serovars, including E. coli O157:H7, are important human pathogens, although reservoir species such as goats remain asymptomatic. We describe the prevalence and antimicrobial resistance of generic E. coli, E. coli O157:H7, and Enterococcus species collected from a national surveillance study of goat feces as part of the National Animal Health Monitoring System (NAHMS) Goat 2019 study. Fecal samples were collected from 4918 goats on 332 operations across the United States. Expectedly, a high prevalence of E. coli (98.7%, 4850/4915) and Enterococcus species (94.8%, 4662/4918) was found. E. coli O157:H7 prevalence was low (0.2%; 10/4918). E. coli isolates, up to three per operation, were evaluated for antimicrobial susceptibility and 84.7% (571/674) were pansusceptible. Multidrug resistance (MDR; ≥3 classes) was uncommon among E. coli, occurring in 8.2% of isolates (55/674). Resistance toward seven antimicrobial classes was observed in a single isolate. Resistance to tetracycline alone (13.6%, 92/674) or to tetracycline, streptomycin, and sulfisoxazole (7.0% 47/674) was the most common pattern. All E. coli O157:H7 isolates were pansusceptible. Enterococcus isolates, up to four per operation, were prioritized by public health importance, including Enterococcus faecium and Enterococcus faecalis and evaluated. Resistance to lincomycin (93.8%, 1232/1313) was most common, with MDR detected in 29.5% (388/1313) of isolates. The combination of ciprofloxacin, lincomycin, and quinupristin resistance (27.1%, 105/388) was the most common pattern detected. Distribution and characteristics of antimicrobial resistance in E. coli and Enterococcus in the U.S. goat population from this study can inform stewardship considerations and public health efforts surrounding goats and their products.
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References
1.
AasmäeB, HäkkinenL, KaartT, et al.Antimicrobial resistance of Escherichia coli and Enterococcus spp. isolated from estonian cattle and swine from 2010 to 2015. Acta Vet Scand, 2019; 61(1):5; doi: 10.1186/s13028-019-0441-9
2.
AmpeF, SirventA, ZakhiaN. Dynamics of the microbial community responsible for traditional sour cassava starch fermentation studied by denaturing gradient gel electrophoresis and quantitative RRNA hybridization. Int J Food Microbiol, 2001; 65(1–2):45–54; doi: 10.1016/s0168-1605(00)00502-x
3.
AunE, KisandV, LahtM, et al.Molecular characterization of Enterococcus isolates from different sources in Estonia reveals potential transmission of resistance genes among different reservoirs. Front Microbiol, 2021; 12:601490.
4.
AwosileBB, HeiderLC, SaabME, et al.Antimicrobial resistance in mastitis, respiratory and enteric bacteria isolated from ruminant animals from the Atlantic Provinces of Canada from 1994–2013. Can Vet J, 2018; 59(10):1099–1104.
5.
BachSJ, McAllisterTA, VeiraDM, et al.Transmission and control of Escherichia coli O157:H7—A review. Can J Anim Sci, 2002; 82(4):475–490; doi: 10.4141/A02-021
6.
BaiJ, ShiX, NagarajaTG. A multiplex PCR procedure for the detection of six major virulence genes in Escherichia coli O157:H7. J Microbiol Methods, 2010; 82(1):85–89; doi: 10.1016/j.mimet.2010.05.003
7.
BarlowRS, McMillanKE, DuffyLL, et al.Antimicrobial resistance status of Enterococcus from Australian cattle populations at slaughter. PLoS One, 2017; 12(5):e0177728; doi: 10.1371/journal.pone.0177728
8.
BennaniH, CornelsenL, StärkKDC, et al.Evaluating integrated surveillance for antimicrobial use and resistance in England: A qualitative study. Front Vet Sci, 2021; 8:743857.
9.
BeukersAG, ZaheerR, GojiN, et al.Comparative genomics of Enterococcus spp. isolated from bovine feces. BMC Microbiol, 2017; 17:52; doi: 10.1186/s12866-017-0962-1
10.
BowenJS. Common health challenges for small-scale sheep and goat herds. Am Assoc Bov Pract Conf Proc, 2013; 2013:116–120; doi: 10.2142/3/aabppro20133797
11.
BurakoffA, BrownK, KnutsenJ, et al.Outbreak of fluoroquinolone-resistant Campylobacter jejuni infections associated with raw milk consumption from a Herdshare dairy—Colorado, 2016. MMWR Morb Mortal Wkly Rep, 2018; 67(5):146–148; doi: 10.1558/5/mmwr.mm6705a2
Center for Veterinary Medicine (CVM). Recommendations for Sponsors of Medically Important Antimicrobial Drugs Approved for Use in Animals to Voluntarily Bring Under Veterinary Oversight All Products That Continue to Be Available Over-the-Counter Guidance for Industry; 2021. Available from: https://www.fda.gov/media/130610/download?attachment [Last accessed: August17, 2023].
CortésC, De la FuenteR, ContrerasA, et al.Occurrence and preliminary study of antimicrobial resistance of Enterococci isolated from dairy goats in Spain. Int J Food Microbiol, 2006; 110(1):100–103; doi: 10.1016/j.ijfoodmicro.2006.01.033
20.
CuiP, FengL, ZhangL, et al.Antimicrobial resistance, virulence genes, and biofilm formation capacity among Enterococcus species from Yaks in Aba Tibetan Autonomous Prefecture, China. Front Microbiol, 2020;11:1250.
21.
DanmallamFA, PimenovNV. Study on prevalence, clinical presentation, and associated bacterial pathogens of goat mastitis in Bauchi, Plateau, and Edo States, Nigeria. Vet World, 2019; 12(5):638–645; doi: 10.1420/2/vetworld.2019.638-645
22.
de JongA, SimjeeS, GarchFE, et al.Antimicrobial susceptibility of Enterococci recovered from healthy cattle, pigs and chickens in nine EU Countries (EASSA study) to critically important antibiotics. Vet Microbiol, 2018; 216:168–175; doi: 10.1016/j.vetmic.2018.02.010
23.
El-ZamkanMA, MohamedHMA. Antimicrobial resistance, virulence genes and biofilm formation in Enterococcus species isolated from milk of sheep and goat with subclinical mastitis. PLoS One, 2021; 16(11):e0259584; doi: 10.1371/journal.pone.0259584
24.
EspecheMC, OteroMC, SesmaF, et al.Screening of surface properties and antagonistic substances production by lactic acid bacteria isolated from the mammary gland of healthy and mastitic cows. Vet Microbiol, 2009; 135(3):346–357; doi: 10.1016/j.vetmic.2008.09.078
FioreE, Van TyneD, GilmoreMS. Pathogenicity of Enterococci. Microbiol Spectr, 2019; 7(4):7.4.9; doi: 10.1128/microbiolspec.GPP3-0053-2018
27.
GiraffaG. Functionality of Enterococci in dairy products. Int J Food Microbiol, 2003; 88(2):215–222; doi: 10.1016/S0168-1605(03)00183-1
28.
GiraffaG, CarminatiD, NevianiE. Enterococci isolated from dairy products: A review of risks and potential technological use. J Food Prot, 1997; 60(6):732–738; doi: 10.4315/0362-028X-60.6.732
29.
GöttlingJ, HeckelJ-O, HotzelH, et al.Zoonotic bacteria in clinically healthy goats in petting zoo settings of zoological gardens in Germany. Zoonoses Public Health, 2022; 69(4):333–343; doi: 10.1111/zph.12922
30.
GuptaMD, DasA, IslamMZ, et al.Prevalence of sorbitol non-fermenting Shiga toxin–producing Escherichia coli in Black Bengal Goats on smallholdings. Epidemiol Infect, 2016; 144(12):2501–2508; doi: 10.1017/S0950268816001047
31.
HempsteadSC, GenslerCA, KeelaraS, et al.Detection and molecular characterization of Salmonella species on U.S. goat operations. Prev Vet Med, 2022; 208:105766; doi: 10.1016/j.prevetmed.2022.105766
32.
HershbergerE, OpreaSF, DonabedianSM, et al.Epidemiology of antimicrobial resistance in Enterococci of animal origin. J Antimicrob Chemother, 2005; 55(1):127–130; doi: 10.1093/jac/dkh508
33.
HolmesA, MooreL, SundsfjordA, et al.Understanding the mechanisms and drivers of antimicrobial resistance. Lancet, 2015; 387:176–187; doi: 10.1016/S0140-6736(15)00473-0
34.
IwerieborBC, ObiLC, OkohAI. Macrolide, glycopeptide resistance and virulence genes in Enterococcus species isolates from dairy cattle. J Med Microbiol, 2016; 65(7):641–648.
35.
JacksonCR, LombardJE, DargatzDA, et al.Prevalence, species distribution and antimicrobial resistance of Enterococci isolated from US Dairy Cattle: Enterococci in dairy cattle. Lett Appl Microbiol, 2011; 52(1):41–48; doi: 10.1111/j.1472-765X.2010.02964.x
36.
JacobME, FosterDM, RogersAT, et al.Prevalence and relatedness of Escherichia coli O157:H7 strains in the feces and on the hides and carcasses of U.S. meat goats at slaughter. Appl Environ Microbiol, 2013; 79(13):4154–4158; doi: 10.1128/AEM.00772-13
37.
KritasSK, BurrielAR, TzivaraAH, et al.Prevention of scours in neonatal kids after modification of management and experimental vaccination against Escherichia coli. Small Rumin Res, 2003; 50(1):51–56; doi: 10.1016/S0921-4488(03)00117-2
38.
LandfriedLK, BarnidgeEK, PithuaP, et al.Antibiotic use on goat farms: An investigation of knowledge, attitudes, and behaviors of Missouri goat farmers. Animals, 2018; 8(11):198; doi: 10.3390/ani8110198
39.
LandfriedL, PithuaP, LewisRD, et al.Antibiotic use in goats: Role of experience and education of Missouri Veterinarians. Vet Rec, 2020; 186(11):349; doi: 10.1136/vr.105455
40.
LaukováA, FockováV, Pogány SimonováM. Enterococcus mundtii isolated from slovak raw goat milk and its bacteriocinogenic potential. Int J Environ Res Public Health, 2020; 17(24):9504; doi: 10.3390/ijerph17249504
41.
LaytonBA, WaltersSP, LamLH, et al.Enterococcus species distribution among human and animal hosts using multiplex PCR. J Appl Microbiol, 2010; 109(2):539–547; doi: 10.1111/j.1365-2672.2010.04675.x
42.
LebretonF, WillemsRJL, GilmoreMS. Enterococcus Diversity, Origins in Nature, and Gut Colonization. In: Enterococci: From Commensals to Leading Causes of Drug Resistant Infection. (GilmoreMS, ClewellDB, IkeY, et al. eds.) Massachusetts Eye and Ear Infirmary: Boston; 2014.
43.
MalahlelaMN, Cenci-GogaBT, MarufuMC, et al.Occurrence, serotypes and virulence characteristics of Shiga toxin–producing Escherichia coli isolates from goats on Communal Rangeland in South Africa. Toxins, 2022; 14(5):353; doi: 10.3390/toxins14050353
44.
McAuleyCM, McMillanKE, MooreSC, et al.Characterization of Escherichia coli and Salmonella from Victoria, Australia, Dairy Farm Environments. J Food Prot, 2017; 80(12):2078–2082; doi: 10.4315/0362-028X.JFP-17-044.
45.
MenziesPI, RamanoonSZ. Mastitis of sheep and goats. Vet Clin North Am Food Anim Pract, 2001; 17(2):333–358; doi: 10.1016/S0749-0720(15)30032-3
46.
MillerBA, LuCD. Current status of global dairy goat production: An overview. Asian Australas J Anim Sci, 2019; 32(8):1219–1232; doi: 10.5713/ajas.19.0253
47.
MoghimbeigiA, MoghimbeygiM, DoustiM, et al.Prevalence of vancomycin resistance among isolates of Enterococci in Iran: A systematic review and meta-analysis. Adolesc Health Med Ther, 2018; 9:177–188; doi: 10.2147/AHMT.S180489
48.
MoriartyEM, MackenzieML, KarkiN, et al.Survival of Escherichia coli, Enterococci, and Campylobacter Spp. in sheep feces on pastures. Appl Environ Microbiol, 2011; 77(5):1797–1803; doi: 10.1128/AEM.01329-10
49.
MutuaEN, BettBK, BukachiSA, et al.From policy to practice: An assessment of biosecurity practices in cattle, sheep and goats production, marketing and slaughter in Baringo County, Kenya. PLoS One, 2022; 17(4):e0266449; doi: 10.1371/journal.pone.0266449
NawazF, KhanMN, JavedA, et al.Genomic and functional characterization of Enterococcus mundtii QAUEM2808, isolated from Artisanal fermented milk product Dahi. Front Microbiol, 2019; 10:434.
52.
NicholsMC, GacekP, PhanQ, 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; doi: 10.3389/fvets.2021.744055
53.
NovaisC, FreitasAR, SilveiraE, et al.Spread of multidrug-resistant Enterococcus to animals and humans: An underestimated role for the pig farm environment. J Antimicrob Chemother, 2013; 68(12):2746–2754; doi: 10.1093/jac/dkt289
54.
O'BrienSJ, AdakGK, GilhamC. Contact with farming environment as a major risk factor for Shiga toxin (vero cytotoxin)–producing Escherichia coli O157 infection in humans. Emerg Infect Dis, 2001; 7(6):1049–1051
55.
OrdenJ, CortesC, HorcajoP, et al.A longitudinal study of verotoxin-producing Escherichia coli in two dairy goat herds. Vet Microbiol, 2008; 132:428–34; doi: 10.1016/j.vetmic.2008.05.021
56.
PillayS, ZishiriOT, AdelekeMA. Prevalence of virulence genes in Enterococcus species isolated from companion animals and livestock. Onderstepoort J Vet Res, 2018; 85(1):1583; doi: 10.4102/ojvr.v85i1.1583
57.
PiresAFA, PattersonL, KukielkaEA, et al.Prevalence and risk factors associated with Campylobacter Spp. and Salmonella Enterica in livestock raised on diversified small-scale farms in California. Epidemiol Infect, 2019; 147:e321; doi: 10.1017/S095026881900205X
58.
PoirelL, MadecJ-Y, LupoA, et al.Antimicrobial resistance in Escherichia coli. Microbiol Spectr, 2018; 6(4):6.4.14; doi: 10.1128/microbiolspec.ARBA-0026-2017
59.
QuigleyL, O'SullivanO, StantonC, et al.The complex microbiota of raw milk. FEMS Microbiol Rev, 2013; 37(5):664–698; doi: 10.1111/1574-6976.12030
60.
RademacherC, PudenzC, SchulzL. Impact assessment of new US Food and Drug Administration regulations on antibiotic use: A post-enactment survey of swine practitioners. J Swine Health Prod, 2019; 27(4):11.
61.
SahinO, YaegerM, WuZ, et al.Campylobacter-associated diseases in animals. Annu Rev Anim Biosci, 2017; 5(1):21–42; doi: 10.1146/annurev-animal-022516-022826
62.
SchillingA-K, HotzelH, MethnerU, et al.Zoonotic agents in small ruminants kept on city farms in Southern Germany. Appl Environ Microbiol, 2012; 78(11):3785–3793; doi: 10.1128/AEM.07802-11
63.
ScottL, MenziesP, Reid-SmithRJ, et al.Antimicrobial resistance in fecal generic Escherichia coli and Salmonella spp. obtained from Ontario sheep flocks and associations between antimicrobial use and resistance. Can J Vet Res, 2012; 76:109–119.
64.
ShabanaII, Al-EnaziAT. Investigation of plasmid-mediated resistance in E. coli isolated from healthy and diarrheic sheep and goats. Saudi J Biol Sci, 2020; 27(3):788–796; doi: 10.1016/j.sjbs.2020.01.009
65.
StanfordK, BryanM, PetersJ, et al.Effects of long- or short-haul transportation of slaughter heifers and cattle liner microclimate on hide contamination with Escherichia coli O157. J Food Prot, 2011; 74(10):1605–1610.
66.
SunC, WangY, MaS, et al.Surveillance of antimicrobial resistance in Escherichia coli and Enterococci from food products at retail in Beijing, China. Food Control, 2021; 119:107483; doi: 10.1016/j.foodcont.2020.107483
67.
TeunisP, TakumiK, ShinagawaK. Dose response for infection by Escherichia coli O157:H7 from outbreak data. Risk Anal, 2004; 24(2):401–407; doi: 10.1111/j.0272-4332.2004.00441.x
68.
TorresC, AlonsoCA, Ruiz-RipaL, et al.Antimicrobial resistance in Enterococcus spp. of animal origin. Microbiol Spectr, 2018; 6(4):6.4.24; doi: 10.1128/microbiolspec.ARBA-0032-2018
U.S. Food and Drug Administration (FDA). Antibiotic Stewardship—Sheep and Goats. 2022. Available from: https://www.fda.gov/media/162673/download [Last accessed: March4, 2024].
75.
VancanneytM, ZamfirM, DevrieseLA, et al.Enterococcus saccharominimus Sp. Nov., from dairy products. Int J Syst Evol Microbiol, 2004; 54(Pt 6):2175–2179; doi: 10.1099/ijs.0.63193-0
76.
VihanVS, KalaSN, SinghVP. Epidemiological investigation of neonatal kid mortality due to enteropathogenic colibacillosis. Prev Vet Med, 1992; 13(3):179–183; doi: 10.1016/0167-5877(92)90102-L
77.
WallaceMJ, FishbeinSRS, DantasG. Antimicrobial resistance in enteric bacteria: Current state and next-generation solutions. Gut Microbes, 2020; 12(1):1799654; doi: 10.1080/19490976.2020.1799654
78.
WattsJL. Evaluation of the rapid strep system for identification of gram-positive, catalase-negative cocci isolated from bovine intramammary infections. J Dairy Sci, 1989; 72(10):2728–2732; doi: 10.3168/jds.S0022-0302(89)79416-9
YoussefDM, WielandB, KnightGM, et al.The effectiveness of biosecurity interventions in reducing the transmission of bacteria from livestock to humans at the farm level: A systematic literature review. Zoonoses Public Health, 2021; 68(6):549–562; doi: 10.1111/zph.12807
81.
ZaheerR, CookSR, BarbieriR, et al.Surveillance of Enterococcus spp. reveals distinct species and antimicrobial resistance diversity across a One-Health Continuum. Sci Rep, 2020; 10(1):3937; doi: 10.1038/s41598-020-61002-5
82.
ZschöckM, HamannHP, KloppertB, et al.Shiga toxin–producing Escherichia coli in faeces of healthy dairy cows, sheep and goats: Prevalence and virulence properties. Lett Appl Microbiol, 2000; 31(3):203–208; doi: 10.1046/j.1365-2672.2000.00789.x
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