Epidemiology of antimicrobial resistance (AMR) on California dairies: descriptive and cluster analyses of AMR phenotype of fecal commensal bacteria isolated from adult cows

Essam M Abdelfattah; Pius S Ekong; Emmanuel Okello; Tapakorn Chamchoy; Betsy M Karle; Randi A Black; David Sheedy; Wagdy R ElAshmawy; Deniece R Williams; Daniela Califano; Luis Fernando Durán Tovar; Jonathan Ongom; Terry W Lehenbauer; Barbara A Byrne; Sharif S Aly

doi:10.7717/peerj.11108

Epidemiology of antimicrobial resistance (AMR) on California dairies: descriptive and cluster analyses of AMR phenotype of fecal commensal bacteria isolated from adult cows

PeerJ. 2021 Apr 20:9:e11108. doi: 10.7717/peerj.11108. eCollection 2021.

Authors

Essam M Abdelfattah^{1

2}, Pius S Ekong^{1

3}, Emmanuel Okello^{1

4}, Tapakorn Chamchoy¹, Betsy M Karle⁵, Randi A Black⁶, David Sheedy¹, Wagdy R ElAshmawy^{1

7}, Deniece R Williams¹, Daniela Califano¹, Luis Fernando Durán Tovar¹, Jonathan Ongom¹, Terry W Lehenbauer^{1

4}, Barbara A Byrne⁸, Sharif S Aly^{1

4}

Affiliations

¹ Veterinary Medicine Teaching and Research Center, School of Veterinary Medicine, University of California, Davis, Tulare, CA, USA.
² Department of Animal Hygiene, and Veterinary Management, Faculty of Veterinary Medicine, Benha University, Moshtohor, Qalyubia, Egypt.
³ Department of Epidemiology, National Veterinary Research Institute, Vom, Plateau State, Nigeria.
⁴ Department of Population Health & Reproduction, School of Veterinary Medicine, University of California, Davis, Davis, CA, USA.
⁵ Cooperative Extension, Division of Agriculture and Natural Resources, University of California, Davis, Orland, CA, USA.
⁶ Cooperative Extension, Division of Agriculture and Natural Resources, University of California, Davis, Santa Rosa, CA, USA.
⁷ Department of Internal Medicine and Infectious Diseases, Cairo University, Giza, Giza, Egypt.
⁸ Department of Pathology, Microbiology, and Immunology, School of Veterinary Medicine, University of California, Davis, Davis, CA, USA.

Abstract

Background: This study describes the occurrence of antimicrobial resistance (AMR) in commensal Escherichia coli and Enterococcus/Streptococcus spp. (ES) isolated from fecal samples of dairy cows and assesses the variation of AMR profiles across regions and seasons following the implementation of the Food and Agricultural Code (FAC) Sections 14400-14408 (formerly known as Senate Bill, SB 27) in California (CA).

Methods: The study was conducted on ten dairies distributed across CA's three milk sheds: Northern California (NCA), Northern San Joaquin Valley (NSJV), and the Greater Southern California (GSCA). On each study dairy, individual fecal samples were collected from two cohorts of lactating dairy cows during the fall/winter 2018 and spring/summer 2019 seasons. Each cohort comprised of 12 cows per dairy. The fecal samples were collected at enrollment before calving (close-up stage) and then monthly thereafter for four consecutive time points up to 120 days in milk. A total of 2,171 E. coli and 2,158 ES isolates were tested for antimicrobial susceptibility using the broth microdilution method against a select panel of antimicrobials.

Results: The E. coli isolates showed high resistance to florfenicol (83.31% ± 0.80) and sulphadimethoxine (32.45%), while resistance to ampicillin (1.10% ± 0.21), ceftiofur (1.93% ± 0.29), danofloxacin (4.01% ± 0.42), enrofloxacin (3.31% ± 0.38), gentamicin (0.32% ± 0.12) and neomycin (1.61% ± 0.27) had low resistance proportions. The ES isolates were highly resistant to tildipirosin (50.18% ± 1.10), tilmicosin (48% ± 1.10), tiamulin (42%) and florfenicol (46% ± 1.10), but were minimally resistant to ampicillin (0.23%) and penicillin (0.20%). Multidrug resistance (MDR) (resistance to at least 1 drug in ≥3 antimicrobial classes) was observed in 14.14% of E. coli isolates and 39% of ES isolates. Escherichia coli isolates recovered during winter showed higher MDR prevalence compared to summer isolates (20.33% vs. 8.04%). A higher prevalence of MDR was observed in NSJV (17.29%) and GSCA (15.34%) compared with NCA (10.10%).

Conclusions: Our findings showed high rates of AMR to several drugs that are not labeled for use in lactating dairy cattle 20 months of age or older. Conversely, very low resistance was observed for drugs labeled for use in adult dairy cows, such as cephalosporins and penicillin. Overall, our findings identified important differences in AMR by antimicrobial class, region and season.

Keywords: Antimicrobial resistance; California; Cohort study; Dairy cattle; Enterococcus spp; Escherichia coli; Multidrug resistance; Phenotype; Region; Season.

Grants and funding

This research was funded by the California Department of Food and Agriculture, and the University of California Davis’s School of Veterinary Medicine and Office of Research’s Principal Investigator Bridge Program. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.