Population Dynamics of Salmonella enterica within Beef Cattle Cohorts Followed from Single-Dose Metaphylactic Antibiotic Treatment until Slaughter

Abstract

Antibiotic use in cattle can select for multidrug-resistant Salmonella enterica, which is considered a serious threat by the U.S. Centers for Disease Control and Prevention. A randomized controlled longitudinal field trial was designed to determine the long-term effects of a single dose of ceftiofur or tulathromycin on Salmonella population characteristics in cattle feces and peripheral lymph nodes and on hides. A total of 134 beef cattle from two sources were divided among 12 pens, with cattle in each of the 3-pen blocks receiving a single dose of either ceftiofur or tulathromycin or neither (control) on day 0. Fecal samples were collected before treatment (day 0) and repeatedly following treatment until slaughter (day 99+). Hide and lymph node samples were collected at slaughter age. Salmonella prevalence, phenotypic antimicrobial resistance, serotype, and phylogenetic relationships were examined. Multilevel mixed logistic regression models indicated no significant effects (P ≥ 0.218) of metaphylactic antibiotics on the prevalence of Salmonella across sample types. However, there was a significant time effect observed, with prevalence increasing from spring through the midsummer months (P < 0.0001) in feces. The majority of Salmonella isolates were pansusceptible to a panel of 14 antibiotics both before and after treatment. Highly prevalent Salmonella serotypes were Salmonella enterica serovar Montevideo, Salmonella enterica serovar Anatum, Salmonella enterica serovar Cerro, and Salmonella enterica serovar Lubbock across all sample types. Strong pen and cattle source serotype clustering effects were observed among Salmonella isolates originating from fecal, lymph node, and hide samples; however, the potential role of Salmonella isolates from the pen environment prior to animal placement was not assessed in this study. IMPORTANCE Salmonella is a leading bacterial foodborne pathogen, causing a significant number of human infections and deaths every year in the United States. Macrolides and 3rd-generation cephalosporins play critical roles in the treatment of human salmonellosis. Use of these antibiotics in beef cattle can select for resistant bacteria that may enter the food chain or spread from the farm via manure. There is a lack of longitudinal research concerning the long-term effects of metaphylactic antibiotic administration. Here, we assessed Salmonella population dynamics during the feeding period until slaughter following single-dose antibiotic treatment. We found no long-term effects of antibiotic use early in the cattle-feeding period on Salmonella prevalence and antimicrobial resistance at slaughter. We identified the pens in which cattle were housed as the factor that contributed most to Salmonella serotypes being shared; importantly, the dominant strain in each pen changed repeatedly over the entire feeding period.

Genomic surveillance of antimicrobial resistance shows cattle and poultry are a moderate source of multi-drug resistant non-typhoidal Salmonella in Mexico

“…However, there is limited evidence linking food consumption with AMR emergence in humans [1,2]. Moreover, an increasing number of studies in developed countries have found that AMU in food animals has a limited impact on the AMR profile of foodborne pathogens [3][4][5][6]. However, this situation is probably different in low and middle-income countries (LMIC), where controls of AMU in veterinary practice and human health are less rigorous.…”

High-resolution genomic comparisons within Salmonella enterica serotypes derived from beef feedlot cattle: parsing the roles of cattle source, pen, animal, sample type and production period

“…What varied instead, was the distinct serotype distribution patterns observed across sampling days and sample types among the 12 pens, four experimental blocks, and the two sources the cattle were purchased from, which merited further investigation into how the subpopulations within the serotypes were influenced when a higher resolution was obtained. The isolates identified as Anatum, Lubbock, Cerro, Montevideo, Kentucky, and Newport serotypes each appeared in their own same legacy 7-gene MLST groups, which initially suggested clonal dissemination of Salmonella within the cohorts of cattle throughout the feeding period and at slaughter (25).…”

“…Salmonella isolates derived from fecal samples during the early feeding period (Day 0 and 7) and fecal, sub-iliac lymph node, and hide swab samples obtained at slaughter included for analysis in this study are previously reported in detail by Levent et al (2019). A total of 399 isolates was previously isolated, sequenced, serotyped and sequence typed (using legacy 7-gene MLST [multi-locus sequence type]), and were identified as Lubbock ST413 (n =136), Anatum ST64 (n=113), Montevideo ST138 (n=68), Cerro ST138 (n=64), Kentucky ST152 (n=11), Newport ST118 (n=6), and Norwich ST2119 (n=1).…”

“…Previous work by our group measured the effects of single-dose metaphylactic antibiotic treatments on Salmonella prevalence in beef feedlot cattle feces, hides, and lymph nodes, and reported no treatment effects on the prevalence or phenotypic antibiotic resistance profiles of Salmonella (25). However, the serotype-level distribution of Salmonella (Anatum, Lubbock, Cerro, Montevideo, Kentucky, Newport, and Norwich) that corresponded to a single sequence type was found to be mostly influenced by the geographical origin of the cattle and the experimental blocks of pens that housed them through the study period.…”

“…In an effort to minimize public-health risks of Salmonella originating from cattle, multiple teams of researchers have previously explored serotype-level dynamics of Salmonella in healthy cattle among samples taken from feces, lymph nodes and hides, as well as from feedlot pen environments. These teams have documented not only a shift of the serotype-level population as influenced by geographical, ecological, and seasonal (or temporal) changes, but also an elevated association between specific antibiotic resistance profiles found in specific serotypes (10,15,(21)(22)(23)(24)(25) Pathogenicity (virulence) and antibiotic resistance are two of the major adaptation, survival, and defense mechanisms of Salmonella. These mechanisms are located on bacterial chromosomes or plasmids, and are considered among either the core-or accessory-genomes of Salmonella (26)(27)(28)(29)(30)(31)(32).…”