Comprehensive Analysis of E. coli, Enterococcus spp., Salmonella enterica, and Antimicrobial Resistance Determinants in Fugitive Bioaerosols from Cattle Feedyards
Abstract
1. Introduction
2. Materials and Methods
2.1. Experimental Design
2.2. Bioaerosol Sampling Methods
Hardware
2.3. Microbiological Processing
2.3.1. Crude Bacterial Quantification
2.3.2. Quantitative Real-Time PCR (qPCR) for Antimicrobial Resistance Genes
Community DNA Extraction for qPCR
Primers and Reaction Setup
Standard Curve Generation
2.3.3. Phenotypic Characterization of Bacteria
Antimicrobial Susceptibility Testing (AST)
2.3.4. Genotypic Characterization of Bacterial Isolates
DNA Extraction for Whole Genome Sequencing (WGS)
Whole Genome Sequencing (WGS)
Bioinformatics Analysis of WGS Data
2.3.5. Dust Mass Calculations
- Mo = mass of filter before sampling (g)
- Me = mass of filter after sampling (g)
- AMCTSP = concentration of bioaerosol captured in TSP filter in grams per m3 of air
- AMCPM10 = concentration of bioaerosol captured in PM10 filter in grams per m3 of air
- TSP(g) = MeTSP − MoTSP
- PM10(g) = MePM10 − MoPM10
- Q = Air sampling flow rate (m3/min)
- = Sampling time (min)
- VA = Volume of air sampled by impinger (L)
- AMTSP = Aerosol mass (AM) derived from co-located high-volume TSP sampler (TSP (g))
- AMCimp = concentration of bioaerosol captured in impinger in grams per m3 of air
- Qimp = Air sampling flow rate through impinger (L/min)
- Δtimp = Impinger sampling time (min)
2.4. Statistical Analyses
2.4.1. Bacterial Count Analyses
- AMimp = Aerosol mass (AM) derived from co-located high-volume TSP sampler (TSP (g))
- V1 = 100 mL of raw sample
- AMmb = Aerosol mass (AM) derived from transmittance measure
- V2 = 150 mL of raw sample
- AMQF = Aerosol mass (AM) derived from quartz filter sampler (g)
- V3 = 200 mL of raw sample
2.4.2. Antimicrobial Susceptibility Analysis
2.4.3. Quantitative Real-Time PCR (qPCR) for Antimicrobial Resistance Genes
3. Results
3.1. Bacterial Prevalence and Quantification
3.1.1. Descriptive Statistics
3.1.2. Hurdle Regression Models
Aerobic Bacteria
E. coli
Enterococcus spp.
Salmonella
Coliforms
3.2. Bacterial Resistance Gene Quantification in Dust
3.3. Phenotypic Characterization
Evaluation of Antimicrobial Resistance in E. coli and Salmonella
3.4. Genotypic Characterization
3.4.1. Antimicrobial Resistance Genes
3.4.2. Salmonella Serovars
3.4.3. Plasmid Analysis
4. Discussion
4.1. Bacterial Quantification in Dust
4.2. Bacterial Gene Quantification in Dust
4.3. Phenotypic and Genotypic Characterization of E. coli and Salmonella Isolates
4.3.1. Evaluation of Antimicrobial Resistance in E. coli and Salmonella spp.
4.3.2. Salmonella Serovars
4.3.3. Bacterial Antimicrobial Resistance Genes
4.3.4. Plasmids
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Campaign | Sample Type | Δt (min) 4 | Δt (h) 4 |
---|---|---|---|
1 | Impinger, QF 1 (PM10 2, TSP 3), and marbles | 215–249 | 3.58–4.15 |
2 | QF (TSP) | 149–215 | 2.48–3.58 |
3 | Impinger, QF (PM10, TSP), and marbles | 184–192 | 3.07–3.20 |
4 | Impinger, QF (PM10 and TSP), and marbles | 142–148 | 2.37–2.47 |
5 | Impinger, QF (PM10 and TSP), and marbles | no recorded | no recorded |
6 | Impinger, QF (PM10 and TSP) and marbles | 195–205 | 3.25–3.42 |
Plate Type | CDTC 1 | CDEC 2 | CDSL 3 |
---|---|---|---|
Bacteria | Total Aerobic | Coliforms and E. coli | Salmonella |
Temperature (°C) | 37 °C | 37 °C | 42 °C |
Incubation time (h) | 18 | 18 | 24 |
Expected phenotypic results | Most colonies will be red | Pink and purple colonies are coliforms and blue-colored colonies are E. coli | Green or blue colonies with and without the black center on a yellow background |
Antimicrobial Class | Antimicrobial Agent | Breakpoints (µg/mL) | ||
---|---|---|---|---|
Susceptible | Intermediate | Resistant | ||
Aminoglycosides | Gentamicin | ≤4 | 8 | ≥16 |
Streptomycin 1 | ≤16 | N/A | ≥32 | |
β-Lactam/β-Lactamase Inhibitor Combinations | Amoxicillin–Clavulanic Acid | ≤8/4 | 16/8 | ≥32/16 |
Cephems | Cefoxitin | ≤8 | 16 | ≥32 |
Ceftriaxone | ≤1 | 2 | ≥4 | |
Ceftiofur | ≤2 | 4 | ≥8 | |
Folate Pathway Inhibitors | Sulfisoxazole | 256 | N/A | ≥512 |
Trimethoprim–Sulfamethoxazole | ≤2/38 | N/A | ≥4/76 | |
Macrolides | Azithromycin 1 | ≤16 | N/A | ≥32 |
Penicillins | Ampicillin | ≤8 | 16 | ≥32 |
Phenicols | Chloramphenicol | ≤8 | 16 | ≥32 |
Quinolones | Ciprofloxacin 2 | ≤0.06 | 0.12–0.5 | ≥1 |
Nalidixic acid | ≤16 | N/A | ≥32 | |
Tetracyclines | Tetracycline | ≤4 | 8 | ≥16 |
Direction | Sample Type | Observations | Mean | Std. Dev. | Min | Max |
---|---|---|---|---|---|---|
downwind | PM10 | 33 | 0.00080 | 0.00111 | 0.00003 | 0.00380 |
downwind | TSP | 42 | 0.00227 | 0.00279 | 0.00006 | 0.01006 |
downwind | impinger | 33 | 0.00276 | 0.00297 | 0.00006 | 0.01006 |
upwind | PM10 | 21 | 0.00008 | 0.00009 | 0.000004 | 0.00023 |
upwind | TSP | 21 | 0.00009 | 0.00005 | 0.00003 | 0.00018 |
upwind | impinger | 21 | 0.00009 | 0.00005 | 0.00003 | 0.00018 |
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Leon, I.M.; Auvermann, B.W.; Bush, K.J.; Casey, K.D.; Pinchak, W.E.; Levent, G.; Vinasco, J.; Lawhon, S.D.; Smith, J.K.; Scott, H.M.; et al. Comprehensive Analysis of E. coli, Enterococcus spp., Salmonella enterica, and Antimicrobial Resistance Determinants in Fugitive Bioaerosols from Cattle Feedyards. Appl. Microbiol. 2025, 5, 63. https://doi.org/10.3390/applmicrobiol5030063
Leon IM, Auvermann BW, Bush KJ, Casey KD, Pinchak WE, Levent G, Vinasco J, Lawhon SD, Smith JK, Scott HM, et al. Comprehensive Analysis of E. coli, Enterococcus spp., Salmonella enterica, and Antimicrobial Resistance Determinants in Fugitive Bioaerosols from Cattle Feedyards. Applied Microbiology. 2025; 5(3):63. https://doi.org/10.3390/applmicrobiol5030063
Chicago/Turabian StyleLeon, Ingrid M., Brent W. Auvermann, K. Jack Bush, Kenneth D. Casey, William E. Pinchak, Gizem Levent, Javier Vinasco, Sara D. Lawhon, Jason K. Smith, H. Morgan Scott, and et al. 2025. "Comprehensive Analysis of E. coli, Enterococcus spp., Salmonella enterica, and Antimicrobial Resistance Determinants in Fugitive Bioaerosols from Cattle Feedyards" Applied Microbiology 5, no. 3: 63. https://doi.org/10.3390/applmicrobiol5030063
APA StyleLeon, I. M., Auvermann, B. W., Bush, K. J., Casey, K. D., Pinchak, W. E., Levent, G., Vinasco, J., Lawhon, S. D., Smith, J. K., Scott, H. M., & Norman, K. N. (2025). Comprehensive Analysis of E. coli, Enterococcus spp., Salmonella enterica, and Antimicrobial Resistance Determinants in Fugitive Bioaerosols from Cattle Feedyards. Applied Microbiology, 5(3), 63. https://doi.org/10.3390/applmicrobiol5030063