Longitudinal Assessment of Prevalence and Incidence of Salmonella and Escherichia coli O157 Resistance to Antimicrobials in Feedlot Cattle Sourced and Finished in Two Different Regions of the United States
Restricted accessResearch articleFirst published online August, 2023
Longitudinal Assessment of Prevalence and Incidence of Salmonella and Escherichia coli O157 Resistance to Antimicrobials in Feedlot Cattle Sourced and Finished in Two Different Regions of the United States
The objective was to investigate the influence of cattle origin and region of finishing on the prevalence of Salmonella, Escherichia coli O157:H7, and select antimicrobial resistance in E. coli populations. Yearling heifers (n = 190) were utilized in a 2 × 2 factorial arrangement. After determining fecal Salmonella prevalence, heifers were sorted into one of four treatments: heifers originating from South Dakota (SD) and finished in SD (SD-SD); heifers originating from SD and finished in Texas (SD-TX); heifers originating from TX and finished in SD (TX-SD); and heifers originating from TX and finished in TX (TX-TX). Fecal, pen, and water scum line samples were collected longitudinally throughout the study; hide swab and subiliac lymph node (SLN) samples were collected at study end. A treatment × time interaction was observed (p ≤ 0.01) for fecal Salmonella prevalence, with prevalence being greatest for TX-TX and TX-SD heifers before transport. From day (d) 14 through study end, prevalence was greatest for TX-TX and SD-TX heifers compared with SD-SD and TX-SD heifers. Salmonella prevalence on hides were greater (p ≤ 0.01) for heifers finished in TX compared with SD. Salmonella prevalence in SLN tended (p = 0.06) to be greater in TX-TX and SD-TX heifers compared with TX-SD and SD-SD. Fecal E. coli O157:H7 prevalence had a treatment × time interaction (p = 0.04), with SD-TX prevalence being greater than TX-SD on d 56 and SD-SD and TX-TX being intermediate. A treatment × time interaction was observed for fecal trimethoprim-sulfamethoxazole-resistant and cefotaxime-resistant E. coli O157:H7 prevalence (p ≤ 0.01). Overall, these data suggest that the region of finishing influences pathogenic bacterial shedding patterns, with the initial 14 d after feedlot arrival being critical for pathogen carriage.
Get full access to this article
View all access options for this article.
References
1.
ArthurTM, KalchayanandN, BosilevacJM, et al.Comparison of effects of antimicrobial interventions on multidrug-resistant Salmonella, susceptible Salmonella, and Escherichia coli O157:H7. J Food Prot, 2008; 71(11):2177–2181; doi: 10.4315/0362-028x-71.11.2177
2.
AslamM, StanfordK, McAllisterTA. Characterization of antimicrobial resistance and seasonal prevalence of Escherichia coli O157:H7 recovered from commercial feedlots in Alberta, Canada. Lett Appl Microbiol, 2010; 50(3):320–326; doi: 10.1111/j.1472-765x-2010.02798.x
3.
BarhamAR, BarhamBL, JohnsonAK, et al.Effects of transportation of beef cattle from the feedyard to the packing plant on prevalence levels of Escherichia coli O157 and Salmonella spp. J Food Prot, 2002; 65(2):280–283; doi: 10.4315/0362-028x-65.2.280
4.
Barkocy-GallagherGA, ArthurTM, Rivera-BetancourtM, et al.Seasonal prevalence of Shiga toxin-producing Escherichia coli, including O157:H7 and non-157 serotypes, and Salmonella in commercial beef processing plants. J Food Prot, 2003; 66(11):1978–1986; doi: 10.4315/0362-028x-66.11.1978
5.
BerryED, WellsJE. Escherichia coli O157:H7: Recent advances in research on occurrence, transmission, and control in cattle and the production environment. Adv Food Nutr Res, 2010; 60:67–117; doi: 10.1016/s1043-4526(10)60004-6
6.
Brichta-HarhayDM, GueriniMN, ArthurTM. Salmonella and Escherichia coli O157:H7 contamination on hides and carcasses of cull cattle presented for slaughter in the United States: An evaluation of prevalence and bacterial loads by immunomagnetic separation and direct plating methods. Appl Environ Microbiol, 2008; 74(20):6289–6297; doi: 10.1128/aem.00700-08
7.
CallawayTR, CarrMA, EdringtonTS, et al.Diet, Escherichia coli O157:H7, and cattle: A review after 10 years. Curr Issues Mol Biol, 2009; 11(2):67–80; doi: 10.2177/5/cimb.011.067
8.
CameronA, McAllisterTA. Antimicrobial usage and resistance in beef production. J Anim Sci and Biotechnol, 2016; 7:68; doi: 10.1186/s40104-016-0127-3
9.
[CDC] Centers for Disease Control and Prevention. Salmonella. Atlanta, GA; 2022. Available from: https://www.cdc.gov/salmonella/index.html [Last accessed: November22, 2022].
10.
ChoS, BenderJB, Diez-GonzalezF, et al.Prevalence and characterization of Escherichia coli O157 isolates from Minnesota dairy farms and county fairs. J Food Prot, 2006; 69(2):252–259; doi: 10.4315/0362-028x-69.2.252
11.
ConederaG, ChapmanPA, MarangonS, et al.A field study of Escherichia coli O157 ecology on a cattle farm in Italy. Int J Food Microbiol, 2001; 66(1–2):85–93; doi: 10.1016/s0168-1605(00)00489-x
12.
CorrierDE, PurdyCW, DeLoachJR. Effects of marketing stress on fecal excretion of Salmonella spp. in feeder calves. Am J Vet Res, 1990; 51(6):866–869.
13.
DargatzDA, KopralCA, ErdmanMM, et al.Prevalence and antimicrobial resistance of Salmonella isolated from cattle feces in United State feedlots in 2011. Foodborne Pathog Dis, 2016; 13(9):483–489; doi: 10.1089/fpd.2016.2128
14.
DaviesPR, MorrowWEM, JonesFT, et al.Prevalence of Salmonella in finishing swine raised in different production systems in North Carolina, USA. Epidemiol Infect, 1997; 119(2):237–244; doi: 10.1017/s095026889700784x
15.
DewellGA, RansomJR, DewellRD, et al.Prevalence of and risk factors for Escherichia coli O157 in market-ready beef cattle from 12 U.S. feedlots. Foodborne Pathog Dis, 2005; 2(1):70–76; doi: 10.1089/fpd.2005.2.70
16.
DewsburyDMA, RenterDG, ShridharPB, et al.Summer and winter prevalence of Shiga toxin-producing Escherichia coli (STEC) O26, O45, O103, O111, O121, O145, and O157 in feces of feedlot cattle. Foodborne Pathog Dis, 2015; 12(8):726–732; doi: 10.1089/fpd.2015.1987
17.
EdringtonTS, CallawayTR, IvesSE, et al.Seasonal shedding of Escherichia coli O157:H7 in ruminants: A new hypothesis. Foodborne Pathog Dis, 2006; 3(4):413–421; doi: 10.1089/fpd.2006.3.413
18.
ElderRO, KeenJE, SiragusaGR, et al.Correlation of enterohemorrhagic Escherichia coli O157 prevalence in feces, hides, and carcasses of beef cattle during processing. Proc Natl Acad Sci U S A, 2000; 97(7):2999–3003; doi: 10.1073/pnas.97.7.2999
19.
FosslerCP, WellsSJ, KaneeneJB, et al.Herd-level factors associated with isolation of Salmonella in a multi-state study of conventional and organic dairy farms: I. Salmonella shedding in cows. Prev Vet Med, 2005; 70(3–4):257–277; doi: 10.1016/j.prevetmed.2005.04.003
20.
[FSIS] U.S. Department of Agriculture-Food Safety Inspection Service. USDA targeting six additional strains of E. coli in raw beef trim starting Monday: Release 0171.12. Washington, DC; 2012. Available from: https://www.usda.gov/media/press-releases/2012/05/31/usda-targeting-six-additional-strains-ecoli-raw-beef-trim-starting [Last accessed: November12, 2022].
21.
GraggSE, LoneraganGH, BrashearsMM, et al.Cross-sectional study examining Salmonella enterica carriage in subiliac lymph nodes of cull and feedlot cattle at harvest. Foodborne Pathog Dis, 2013a;10(4):368–374; doi: 10.1089/fpd.2012.1275
22.
GraggSE, LoneraganGH, NightingaleKK, et al.Substantial within-animal diversity of Salmonella isolates from lymph nodes, feces, and hides of cattle at slaughter. Appl Environ Microbiol, 2013b;79(15):4744–4750; doi: 10.1128/aem.01020-13
23.
HancockDD, BesserTE, RiceDH, et al.A longitudinal study of Escherichia coli O157 in fourteen cattle herds. Epidemiol Infect, 1997; 118(2):193–195; doi: 10.1017/s0950268896007212
24.
HuQ, TuJ, HanX, et al.Development of multiplex PCR assay for rapid detection of Riemerella anatipestifer, Escherchia coli, and Salmonella enterica simultaneously from ducks. J Microbiol Methods, 2011; 87(1):64–69; doi: 10.1016/j.mimet.2011.07.007
25.
KhaitsaML, KegodeRB, BauerML, et al.A longitudinal study of Salmonella shedding and antimicrobial resistance patterns in North Dakota feedlot cattle. J Food Prot, 2007; 70(2):476–481; doi: 10.4315/0362-028x-70.2.476
26.
KoohmaraieM, ScangaJA, De La ZerdaMJ, et al.Tracking the sources of Salmonella in ground beef produced from nonfed cattle. J Food Prot, 2012; 75(8):1464–1468; doi: 10.4315/0362-028x.jfp-11-540
27.
LauferAS, GrassJ, HoltK, et al.Outbreaks of Salmonella infections attributed to beef-United States, 1973–2011. Epidemiol Infect, 2015; 143(9):2003–2013; doi: 10.1017/s0950268814003112
28.
LeventG, SchlochtermeierA, IvesSE, et al.Population dynamics of Salmonella enterica within beef cohorts followed from single-dose metaphylactic antibiotic treatment until slaughter. Appl Environ Microbiol, 2019; 85(23):e01386-19; doi: 10.1128/aem.01386-19
29.
LiM, MalladiS, HurdHS, et al.Salmonella spp. in lymph nodes of fed and cull cattle: Relative assessment of risk to ground beef. Food Control, 2015; 50(2015):423–434; doi: 10.1016/j.foodcont.2014.09.011
30.
LongNS, WellsJE, BerryED, et al.Metaphylactic antimicrobial effects on occurrences of antimicrobial resistance in Salmonella enterica, Escherichia coli, and Enterococcus spp. measured longitudinally from feedlot arrival to harvest in high-risk beef cattle. J Appl Microbiol, 2022; 133(3):1940–1955; doi: 10.1111/jam.15691
31.
MatthewsL, ReeveR, GallyDL, et al.Predicting the public health benefit of vaccinating cattle against Escherichia coli O157. Proc Natl Acad Sci U S A, 2013; 110(40):16265–16270; doi: 10.1073/pnas.1304978110
32.
MillerMF, LoneraganGH, HarrisDD, et al.Environmental dust exposure as a factor contributing to an increase in Escherichia coli O157 and Salmonella populations on cattle hides in feedyards. J Food Prot, 2008; 71(10):2078–2081; doi: 10.4315/0362-028x-71.10.2078
33.
MolinaF, López-AcedoE, TablaR, et al.Improved detection of Escherichia coli and coliform bacteria by multiplex PCR. BMC Biotechnol, 2015; 15:48; doi: 10.1186/s12896-015-0168-2
34.
[NASEM] Nutrient Requirements of Beef Cattle. 8th Revised edition. National Academies of Sciences, Engineering, and Medicine. Natl. Acad. Press: Washington, DC; 2016.
35.
NickelsonKJ, TaylorTM, GriffinDB, et al.Assessment of Salmonella prevalence in lymph nodes of U.S. and Mexican cattle presented for slaughter in Texas. J Food Prot, 2019; 82(2):310–315; doi: 10.4315/0362-028x.jfp-18-288
36.
Rivera-BetancourtM, ShackelfordSD, ArthurTM, et al.Prevalence of Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella in two geographically distant commercial beef processing plants in the United States. J Food Prot, 2004; 67(2):295–302; doi: 10.4315/0362-028x-67.2.295
37.
RodriquesGL, PanzenhagenP, FerrariRG, et al.Frequency of antimicrobial resistance genes in Salmonella from Brazil by in silico whole-genome sequencing analysis: An overview of the last four decades. Front Microbiol, 2020; 11:1864; doi: 10.3389/fmicb.2020.01864
38.
SamuelsonKL, HubbertME, GalyeanML, et al.Nutritional recommendations of feedlot consulting nutritionists: The 2015 New Mexico State and Texas Tech University survey. J Anim Sci, 2016; 94(6):2648–2663. doi: 10.2527/jas.2016-0282
39.
ScallanE, HoekstraRM, AnguloFJ, et al.Foodborne illness acquired in the United States-Major pathogens. Emerg Infect Dis, 2011; 17(1):7–15; doi: 10.3201/eid1701.P11101
40.
SchmidtJW, AggaGE, BosilevacJM, et al.Occurrence of antimicrobial-resistant Escherichia coli and Salmonella enterica in the beef cattle production and processing continuum. Appl Environ Microbiol, 2015; 81(2):713–725; doi: 10.1128/aem.03079-14
41.
SmithD, BlackfordM, YountsS, et al.Ecological relationships between the prevalence of cattle shedding Escherichia coli O157:H7 and characteristics of the cattle or conditions of the feedlot pen. J Food Prot, 2001; 64(12):1899–1903; doi: 10.4315/0362-028x-64.12.1899
42.
StevensMP, HumphreyTJ, MaskellDJ. Molecular insights into farm animal and zoonotic Salmonella infections. Philos Trans R Soc Lond B Biol Sci, 2009; 364(1530):2709–2723; doi: 10.1098/rstb.2009.0094
43.
[USDA] US Department of Agriculture-Animal and Plant Health Inspection Service: Veterinary Services. Escherichia coli O157 in United States feedlots: N345.1001. Fort Collins, CO; 2001. Available from: https://www.aphis.usda.gov/animal_health/nahmsfeedlot/downloads/feedlot99/Feedlot99_is_Ecoli.pdf [Last accessed: November22, 2022].
44.
VikramA, RoviraP, AggaGE, et al.Impact of “raised without antibiotics” beef cattle production practices on occurrences of antimicrobial resistance. Appl Environ Microbiol, 2017; 83(22):e01682-17; doi: 10.1128/aem.01682-17
45.
WebbHE, Brichta-HarhayDM, BrashearsMM, et al.Salmonella in peripheral lymph nodes of healthy cattle at slaughter. Front Microbiol, 2017; 8:2214; doi: 10.3389/fmlcb.2017.02214
46.
WellsJE, BerryED, KimM, et al.Determination of gastrointestinal tract colonization sites from feedlot cattle transiently shedding or super-shedding Eshcerchia coli O157:H7 at harvest. J Appl Microbiol, 2020; 129(5):1419–1426; doi: 10.1111/jam.14684
47.
WellsJE, ShackelfordSD, BerryED, et al.Prevalence and level of Escherichia coli O157:H7 in feces and on hides of feedlot steers fed diets with or without wet distillers grains with solubles. J Food Prot, 2009; 72(8):1624–1633; doi: 10.4315/0362-028x-72.8.1624
48.
WellsJE, ShipmanLD, GreeneKD, et al.Isolation of Escherichia coli serotype O157:H7 and other Shiga-like-toxin-producing E. coli from dairy cattle. J Clin Microbiol, 1991; 29(5):985–989; doi: 10.1128/jcm.29.5.985-989.1991
49.
WheelerTL, KalchayanandN, BosilevacJM. Pre- and post-harvest interventions to reduce pathogen contamination in the U.S. beef industry. Meat Sci, 2014; 98(3):372–382; doi: 10.1016/j.meatsci.2014.06.026
50.
WilkersonS, BroadwayPR, CarrollJA, et al.Translocation of orally inoculated Salmonella following mild immunosuppression in holstein calves and the presence of the Salmonella in ground beef samples. Foodborne Pathog Dis, 2020; 17(9):533–540; doi: 10.1089/fpd.2019.2761
51.
WottlinLR., EdringtonTS, AndersonRC.Salmonella carriage in peripheral lymph nodes and feces of cattle at slaughter is affected by cattle type, region, and season. Front Anim Sci, 2022; 3:859800; doi: 10.3389/fanim.2022.859800
