NC1206: Antimicrobial Resistance

(Multistate Research Project)

Status: Active

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SAES-422 Reports

Annual/Termination Reports:

[12/22/2022] [07/10/2023]

Date of Annual Report: 12/22/2022

Report Information

Annual Meeting Dates: 10/27/2022 - 10/28/2022
Period the Report Covers: 08/05/2021 - 10/27/2022

Participants

Ganda, Erika (ganda@psu.edu)- Pennsylvania State University;
Okello, Emmanuel (eokello@ucdavis.edu)- University of California, Davis;
Maddock, Kelli (kelli.helgeson@ndsu.edu)- NDSU Veterinary Diagnostic Laboratory;
Plummer, Paul (pplummer@iastate.edu)- Member- Iowa State University;
Ivanek, Renata (evk5387@psu.edu)- Member- Cornell University;
Li, Xu (xuli@unl.edu)- Member- University of Nebraska Lincoln;
Looft, Torey (torey.looft@usda.gov)- Member, USDA, National Animal Disease Center;
Zhang, Qijing (zhang123@iastate.edu)- Member, Iowa State University;
Smith, George (smithge7@anr.msu.edu )- Member, Michigan State University;
Wang, Hua (wang.707@osu.edu)- Member, The Ohio State University;
Wang, Bing (bing.wang@unl.edu)- Member, University of Nebraska Lincoln;
Bearson, Shawn (shawn.bearson@usda.gov)- Member, USDA, National Animal Disease Center;
Johnson, Tim (tjj@umn.edu)- Member, Purdue University;
Cazer, Casey (clc248@cornell.edu)- Member, Cornell University

Participants Attachment:

Annual Report 2022- Multistate Research Project NC1206 Final.docx

Brief Summary of Minutes

Prior to the official start of the meeting, Dr. Paul Plummer coordinated a tour of the National Veterinary Services Laboratory for NC1206 members.

Opening: The meeting started with a welcome by Dr. Erika Ganda, acting president and Dr. Plummer, host. Dr. Ganda passed the president position to Dr. Emmanuel Okello and Drs. Ganda, Plummer, and Okello co-moderated the meeting.

Project Renewal: Dr. George Smith, scientific advisor for the NC 1206 project also attended the meeting. Dr. Smith was pleased with the successful project renewal for the next 5 years, a success credited to Dr. Ganda’s leadership. Dr. Smith reiterated the purpose of the meeting, which is to share results of our research and to develop possible collaborations. He emphasized the importance of leadership submitting the meeting reports and encouraged the group to keep up the good work.
- Question (Dr. Ganda) Signs of project success: True collaborations developing along with joint publications from members in the group.
- Question (Dr. Ganda) How to ensure success/things to avoid: Schedule the next meeting prior to leaving the current one. Emphasize the collaborations made by team members. Carefully elect new leaders.
- Question (Dr. Plummer) Estimated number of multistate projects: 300-400 projects.

Research updates: Drs. Ivanek, Looft, Wang, Li, Okkello, Ganda, Cazer, Plummer, Bearson, and Kelli Maddock presented current research and future collaboration interests.

Guest Speakers:
- Lonty Bryant, Merch Animal Health: Presentation focused on advances in diagnostic medicine and the relevance of antimicrobial resistance (AMR) based on antimicrobial susceptibility test (AST) results or polymerase chain reaction (PCR). Suggested need to explore AMR and treatment outcomes as related to animal health.
  - Discussed ideas regarding measurement of treatment outcomes in relation to AMR and clinical outcome. Discussed use of antibiograms to make treatment choices and the impact of the microbiome and in cases of dysbiosis.
- New leadership: Kelli Maddock will serve as the project Secretary for the next year cycle, which was supported and confirmed by the group.
- Annual meeting schedule, 2023: Two potential meeting dates were presented to the group. A survey with proposed meeting dates was sent to members of the group for follow-up after the meeting.
  - January 25-26, 2023- Chicago, IL with the CRWAD conference (22-24)
  - May 18-19, 2023- Gainesville, FL with the NIAMRRE conference (16-18)
  - With 11 votes, Gainesville, FL was selected as the meeting place for the next NIAMRRE conference.

Accomplishments

Accomplishments Objective 1: Develop knowledge and tools to improve antimicrobial stewardship <ol> <li>iAMResponsible™ is a collaborative education and extension effort about antimicrobial stewardship that was developed by several institutions. [MD, NE, NY, MI] <ol> <li>Activities: Communication strategies and tools to best convey AMR knowledge (prevalence, treatment, stewardship, and perceptions). Well Said Media will create video, web, and print materials. Support and dissemination will occur via iAMResponsible social media accounts.</li> <li>Outputs: Over 150 pieces of content were created and distributed over the past year. Social media platforms are rapidly growing and have a global audience. Based on results of a 2020 survey of social media followers, iAMResponsibleTM has become a trusted resource for communicating AMR-related information and guidance to food producers and consumers worldwide.</li> </ol> </li> <li>One Health Graduate Online Course. [NE, MD]. <ol> <li>Activities: Graduate-level course on the fundamentals of AMR development, transmission, risk to humans, animals, and the environment delivered by experts in the One Health concept (interconnection between people, animals, plants, and their shared environment).</li> <li>Output: Six institutions participated in the Spring 2022 course (University of Nebraska- Lincoln, North Carolina State University, Washington State University, Oklahoma State University, University of Minnesota, University of Maryland) and 18 students were enrolled in the Spring 2022 course. Students learned from academic, industry, and government leaders about multiple elements of the AMR crisis. Students developed communication skills and contributed to new materials for use in the iAMResponsible team’s outreach database and on the website. Additional institutions were invited to participate in the Spring of 2023 course offerings.</li> </ol> </li> </ol>   Objective 2: Develop and evaluate antimicrobial use, resistance transmission, mitigation strategies, and stewardship programs in food systems from a One-Health perspective. <ol> <li>Connecting AntiMicrobial Resistance Agricultural Decisions and Environmental Systems, (CAMRADES) is a project aiming to assess the effectiveness of various mitigation strategies for reducing risk to human health in agro-ecosystems by developing an adaptable framework. [NE, IA] <ol start="2022"> <li>Activities: The project was initiated in Spring 2022. All research groups successfully recruited students for the proposed studies. Both research teams started water sampling and analysis of microbiome and resistome in samples from natural watershed.</li> <li>Output: While research is still on-going, the project will integrate predictive models of AMR transport and associated risk to human health, and improve stakeholder understanding of AMR, potential risks and mitigation strategies, along with motivating adoption of research-based practices to protect human health.</li> </ol> </li> <li>Evaluation of the effect of high temperature treatment of diary manure and modeling antibiotic residual transformation in dairy and beef manure with high temperature and grass strip treatments, respectively, on antibiotic residuals, antimicrobial genes, and bacteria. [MD, NY, NE] <ol> <li>Activities: New extraction techniques will be developed to improve extraction efficiencies of manure to determine antibiotic quantitation in manure and biosolid matrices using LC tandem MS-MS. Thermal-based manure treatment technologies will be employed, including anaerobic digestion, thermophilic digestion, and high-temp, rotary drum processing.</li> <li>Output: While research is on-going, the ultimate impact is to be determined; however, the antibiotic detection method is under review with additional publications to follow.</li> </ol> </li> <li>Environmental fate of antibiotic resistance genes in the bovine and swine agroecosystems. [MI, IN] <ol> <li>Output: Improve understanding of the impact of soil manuring and the environmental fate of antibiotic resistance genes</li> </ol> </li> <li>Plasmid-mediated transfer of antibiotic resistance genes to Enterococcus faecalis JH2-2 in poultry litter. [IN, USDA] <ol> <li>Activities: Quantification and understanding the horizontal transfer of resistance plasmids judge the impact of animal management practices.</li> <li>Output: Development of a novel method to study the ecology of antibiotic resistance genes.</li> </ol> </li> <li>Whole genome sequencing and phenotypic antimicrobial resistance of Salmonella enterica serovar Dublin. [PA, ND] <ol> <li>Activities: Through connections established at the NC1206 meeting, these laboratories will share Salmonella isolates for evaluation of phenotypic and genotypic markers of antimicrobial resistance.</li> <li>Output: Contribution to the body of knowledge surrounding Salmonella Dublin resistance mechanisms and potential mitigation measures.</li> </ol> </li> <li>Integration of a multi-pronged standardized methodology to identify key diseases and prioritized antimicrobial alternatives in production animals. [IA, CA, OH, GA] <ol> <li>Activities: Scoping reviews, expert elicitation, and multi-criteria decision analysis to develop recommendation for alternative practices to manage prioritized diseases that drive the use of medically important antimicrobial agents in production animals.</li> <li>Output: This is an ongoing research project. Expected output include a prioritized list of the diseases that drive the most use of antimicrobials in the four livestock commodities (dairy, beef, poultry, and swine) and a prioritized list of alternative practices to antimicrobial treatments for each of the four livestock commodities</li> </ol> </li> </ol>   Objective 3: Create and deliver programs on antibiotic stewardship in food production systems through education and outreach. <ol> <li>Evaluation of stakeholder perceptions of antimicrobial resistance prevalence and conveyance in the environment. [NY, NE] <ol> <li>Activities: Through interviews, focus groups, surveys, and Q-sort analyses, assessment of farmer and veterinarian perceptions of AMR to develop communication materials that are more tailored to biases, current levels of understanding, and perception.</li> <li>Output: Research is on-going, so impact of the results is still to be determined. The Q-sort analyses paper was submitted and is under review.</li> </ol> </li> <li>Human Dimensions of AMR in Agriculture Workshop. [MD, NE] <ol> <li>Activities: Organized with leaders in AMR social science research and AMR communication to identify current research, identify gaps in the literature, write articles to address limitations of social science-based AMR information in agriculture.</li> <li>Output: Workshop brought together 37 participants, including researchers, students, and agricultural experts focused on surveying and communicating the human and economic dimensions of AMR in agriculture. Working groups allowed for mentoring and collaboration between participants. Three publications with another under review were produced from this workshop.</li> </ol> </li> <li>Improving Antimicrobial Resistance Science Communication Education for Veterinary Students. [IA, CA, OH] <ol> <li>Activities: Focus groups and surveys to identify gaps in knowledge about AMR, antimicrobial stewardship, and communication skills training among current veterinary medicine students with the aim to develop modules that address these knowledge gaps.</li> <li>Output: The research is ongoing. Expected output is online AMR/antimicrobial stewardship communication modules available to all interested individuals and organizations, targeting veterinary students, veterinary technicians, recent graduates, and professional organizations.</li> </ol> </li> </ol>

Publications

<ol> <li>Johnson TA, Sylte MJ, Looft T. In-feed bacitracin methylene disalicylate modulates the turkey microbiota and metabolome in a dose-dependent manner [submitted to Scientific Reports]</li> <li>Carter HF, Wills RW, Scott MA, Thompson AC, Singer RS, Loy JD, Karisch BB, Epperson WB, and Woolums AR. Diversity of antimicrobial resistance phenotypes and genotypes of Mannheimia haemolytica isolates from bovine nasopharyngeal swabs. Front Vet Sci.  2022 May 11;9:883389. doi: 10.3389/fvets.2022.883389</li> <li>Bo Li, Xu Li, Bing Wang, and Tao Yan. A metagenomic approach for characterizing antibiotic resistance genes in specific bacterial populations: demonstration with Escherichia coli in cattle manure. Appl Environ Microbiol. 2022 Apr 12;88(7):e0255421. [NE]</li> <li>Donner L, Staley ZR, Petali J, Sangster J, Li X, Mathews W, Snow D, Howe A, Soupir M, Bartelt-Hunt S. The Human Health Implications of Antibiotic Resistance in Environmental Isolates from Two Nebraska Watersheds. Microbiol Spectr. 2022 Apr 27;10(2):e0208221. doi: 10.1128/spectrum.02082-21. Epub 2022 Mar 21. PMID: 35311538; PMCID: PMC9045274. [NE, IA]</li> <li>Mware NA, Hall MC, Rajendran S, Gilley JE, Schmidt AM, Bartelt-Hunt SL, Zhang Y, Li X. Resistome and mobilome in surface runoff from manured soil as affected by setback distance. J Hazard Mater. 2022 May 5;429:128278. doi: 10.1016/j.jhazmat.2022.128278. Epub 2022 Jan 14. PMID: 35065306. [NE]</li> <li>Kaniyamattam K, Hertl J, Tauer LW, and Grohn YT. (2022). Economics of reducing antibiotic usage for pathogen-specific clinical mastitis through genomic selection and disease management. Prev Vet Med. 2022 Jul;204:105642. doi: 10.1016/j.prevetmed.2022.105642. Epub 2022 Apr 6. PMID: 35430445. [NY]</li> <li>Verteramo Chiu, L. J., Tauer, L. W., & Gröhn, Y. T. (2022). Pricing efficiency in livestock auction markets: A two-tier frontier approach. Agricultural Economics,1–13. <a href="https://doi.org/10.1111/agec.12735">https://doi.org/10.1111/agec.12735</a> [NY]</li> <li>Verteramo Chiu, L.J., Tauer, L.W., Lhermie. G., Kaniyamattam, K., Gröhn Y.T. (2022) Benefits of Preconditioning Cattle under Stochastic Feedlot Performance. Journal of Agricultural and Applied Economics. 1–18 doi:10.1017/aae.2022.32 [NY]</li> <li>Barrett, J. R., Innes, G. K., Johnson, K. A., Lhermie, G., Ivanek, R., Greiner Safi, A., & Lansing, D. (2021). Consumer perceptions of antimicrobial use in animal husbandry: A scoping review. PLOS ONE, 16(12), e0261010</li> </ol>

Impact Statements

Antimicrobial resistance is a major concern from the One Health perspective, which must be addressed using a multidisciplinary and collaborative approach across the animal, human and environmental health spheres. The NC 1206 Multi-State Research Project has collaborated to accomplish key studies and extension education activities that advance the knowledge, outreach, interdisciplinary collaboration, and mitigation efforts related to antimicrobial resistance. Social sciences have been integrated into education programs to target potential antimicrobial user biases, increase AMR knowledge, and to reach stakeholders across the food chain; the addition of social sciences strengthens the approach and allows for more targeted education of stakeholders. Several mitigation and resistance mechanism collaborations have developed as a result of this collaboration.

Date of Annual Report: 07/10/2023

Report Information

Annual Meeting Dates: 05/15/2023 - 05/16/2023
Period the Report Covers: 10/27/2022 - 05/15/2023

Participants

Okello, Emmanuel (eokello@ucdavis.edu)- University of California, Davis; Outgoing President;
Maddock, Kelli (kelli.helgeson@ndsu.edu)- NDSU Veterinary Diagnostic Laboratory, Incoming President, Secretary;
Cazer, Casey (clc248@cornell.edu)- Member, Cornell University; Incoming Secretary;
Ganda, Erika (ganda@psu.edu)- Member, Pennsylvania State University;
Plummer, Paul (pplummer@iastate.edu)- Member, Iowa State University;
Gill, Jason (jason.gill@ag.tamu.edu) – Member, Texas A&M University;
Ivanek, Renata (evk5387@psu.edu)- Member- Cornell University;
Li, Xu (xuli@unl.edu)- Member- University of Nebraska Lincoln;
Schmidt, Amy (aschmidt@unl.edu) – Member, University of Nebraska Lincoln;
Wang, Hua (wang.707@osu.edu) – Member, The Ohio State University

Brief Summary of Minutes

Brief Summary of Minutes of Annual Meeting:

The meeting started with a brief welcome and introduction of all members. The meeting was moderated by Kelli Maddock and Dr. Emmanuel Okello. Dr. George Smith provided a recorded welcome to NC1206 members.

Dr. George Smith, scientific advisor for the NC1206 project, provided recorded remarks to the group The project was renewed and updated on 10-1-22. There are 24 registered participants in the projects. He encouraged the group to consider putting in an application for the Excellence in Multistate Research Project Award. The impact summary would be a good basis for the application. Need tangible impacts, such as tools and resources that impact industry. Projects grounded in collaboration across multiple stations are imperative. Dr. Smith is willing to assist with application preparation. As a group, members later reviewed the requirements for the 2023 Experiment Station Section Award for Excellence in Multistate Research. Requirements will be shared with the group for review and to determine if we would like to apply.

Research Updates: Drs. Cazer, Ganda, Okello, Ivanek, Plummer, Gill, Schmidt, Wang, Li, and Kelli Maddock presented current research and future collaboration interests.

Guest speakers: Dr. Amy Schmidt, iAMResponsible Project, highlighted resources developed by the iAMResponsible team that are publicly available for use, including social media products, podcasts, and real-life experiences from individuals who have experienced an antimicrobial resistant infection. Dr. Schmidt’s team can develop social media resources for researchers. The group is available as the education/extension component on grants as subcontractors.

Dr. Kathe Bjork, USDA NIFA, provided updates regarding personnel updates at NIFA as well as budgetary notes. Several competitive funding opportunities were included in the update along with program contacts for each program. This update will be provided to meeting members.

New leadership: Kelli Maddock formally transitioned to the role as president of NC1206. Thank you to Dr. Okello for serving as president. Dr. Casey Cazer was unanimously elected as the group secretary.

Annual meeting schedule, 2024: The short time between the 2022 and 2023 meetings limited travel funding for some members as funding was dependent upon fiscal year. Three meeting options were discussed. The final dates and locations will be determined through discussion of members in late 2023.

Cornell- AMR Symposium to be held in Ithaca. March 2024. Could potentially host our group.

NDSU VDL in Fargo is willing to host. Food could be catered by the university and delivered to the laboratory. Would include a tour of the facility. Fargo has a vibrant restaurant scene and is pleasant to visit during the months of May- September.

NIAMRRE: 2024 Meeting scheduled for Ohio. Dr. Paul Plummer offered another joint meeting opportunity if we would like to coordinate the meeting times again.

Accomplishments

Accomplishments: Objective 1: Develop knowledge and tools to improve antimicrobial stewardship, including surveillance and monitoring of antimicrobial resistance, determining the ecology and mechanisms involved in resistance and transmission of resistance, and developing improved diagnostic tests <ol> <li>Integrating online platform to comprehensively assess antibiotic resistance gene pool (AR resistome) by shotgun sequencing analysis [OH] <ol> <li>Activities: assessed total and specified AR gene pools in fermented foods, human and animal gut microbiome.</li> <li>Outputs: Revealed that conventional oral administration of mainstream antibiotics such as ampicillin, vancomycin, clindamycin etc. led to broad disruption of gut microbiota in human and animal hosts, and the changes of antibiotic resistome. Revealed fermented food consumption led to the surge of gut (fecal) antibiotic resistome in most consumers, but the control high plant fiber food consumption didn’t have this effect. Revealed the prevalence of antibiotic resistome in traditionally fermented foods. The method enabled comprehensive assessment of the AR risk.</li> </ol> </li> <li>Antibiotic resistance in fermented foods and the impact on host gut resistome [OH] <ol> <li>Activities: Using culture dependent and independent methods revealed that traditionally fermented foods such as kimchi and artisan cheeses are highly prevalent in antibiotic resistant bacteria and opportunistic pathogens (~90% in retail kimchi and all 4 artisan cheeses assessment) and resistome.</li> <li>Outputs: Supported the finding that fermented foods consumption led to the surge of antibiotic resistome in gut microbiota of consumers. The results revealed a critical avenue of AR transmission and the underestimated food safety and public health risk associated with traditional food fermentation. The results presented a public health warning regarding the aggressive advocacy in recent years promoting fermented food consumption, especially towards targeted susceptible populations with compromised gut and immune functions. The results demand for prompt responses from the federal agencies and industry, in collaboration with academic experts to develop effective and targeted mitigation of antibiotic resistance in food fermentation.</li> </ol> </li> <li>Development of a Matrix-Assisted Laser Desorption Ionization Time-of-Flight (MALDI-TOF) assay to discriminate pathogenic from commensal strains of Histophilus somni: A novel and affordable diagnostic tool for bovine respiratory disease in North Dakota cattle herds. [ND]</li> <li>ORFeome display for the discovery of novel pathogen markers associated with bovine respiratory disease in shipped cattle [TX] <ol> <li>Activities: produced phage display ORFeome libraries for multiple BRD-associated viral and bacterial pathogens and began panning for epitopes in immune sera.</li> <li>Outputs: One candidate epitope, a viral spike in BVDV, has been identified. The ORFeome display platform will be used to identity novel vaccine targets and biomarkers for BRD diagnosis.</li> </ol> </li> <li>Development of bacteriophages as an intervention to control asymptomatic Salmonella carriage in beef cattle [TX] <ol> <li>Activities: Completed trial to assess the effects of phage on Salmonella carriage in the lymph nodes of beef cattle.</li> <li>Outputs: Lymph node carriage of Salmonella was low across the trial, but phages may have modulated Salmonella serovar prevalence.</li> </ol> </li> <li>Development of a targeted sequencing approach for AMR gene profiling [PA] <ol> <li>Activities:</li> <li>Outputs: Targeted sequencing based detection of AMR genes will allow for better characterization and surveillance of AMR, and to identify the impact of different management practices in AMR enrichment.</li> </ol> </li> <li>Characterize the resistome, microbiome, and performance in broilers fed various feed supplements. [PA] <ol> <li>Activities: Performed experiment feeding broilers with 4 different antibiotic free feed additives</li> <li>Outputs: Knowledge on antibiotic free feed additives for use in poultry will help producers decide which type of additive to use. Understanding the impact of these additives on antimicrobial resistance will allow for rational decisions regarding the potential of off-target antimicrobial resistance selection that might happen when certain antibiotic free feed additives are used, such as in the case of heavy metals.</li> </ol> </li> </ol> <ol> <li>Assess the impact of FDA antimicrobial use (AMU) regulations on antimicrobial resistance (AMR) and multidrug resistance (MDR) in Salmonella Dublin. [NY]</li> </ol> <ol> <li>Activities: Assess the impact of FDA antimicrobial use (AMU) regulations on antimicrobial resistance (AMR) and multidrug resistance (MDR) in Salmonella</li> <li>Output: Assess the impact of FDA antimicrobial use (AMU) regulations on antimicrobial resistance (AMR) and multidrug resistance (MDR) in Salmonella</li> </ol>   Objective 2: Develop and evaluate antimicrobial use, resistance transmission, mitigation strategies, and stewardship programs in food systems from a One-Health perspective. Includes antimicrobial use and stewardship, and AMR transmission and mitigation strategies. <ol> <li>Determine phylogenetic relationships, antimicrobial resistance determinants, and virulence potential ofDublin from cattle and humans in the United States. [PA, ND, USDA] <ol> <li>Activities: Analyzed >2,100 Salmonella Dublin genomes to determine phylogenetic relationships between isolates from bovine or human sources.</li> <li>Outputs: Salmonella Dublin is highly multidrug resistant and virulent. It has been increasingly isolated from human bloodstream infections. Better understanding the genomic epidemiology of this pathogen might aid in better prevention strategies.</li> </ol> </li> <li>One Health Analysis of Salmonella enterica Serotype Newport Isolated from Humans and Exotic Felids. Pecoraro HL, Stenger BLS, Maddock KA, Evans D, Breuer A, and Rickey C. [ND] <ol> <li>Activities: Coordinated a One Health response and investigation of a multi-drug resistant Salmonella Newport impacting human and animal species.</li> </ol> </li> <li>Genomic sequencing has been leveraged to identify genotypes of Moraxella bovis and utilized to inform strain typing tools and to improve vaccine and other prevention strategies to decrease antimicrobial usage. [NE]</li> <li>Investigate the transmission and persistence of antimicrobial resistant genes, resistant indicate bacteria and antibiotics in the natural environment and the impact on human health risks, and translate the science to enhance stakeholders understanding of and behaviors toward AMR risks. [NE, IA, NY]</li> <li>Determine ideal sampling strategies and strains variation between cattle with different antimicrobial treatments and detection of AMR strains of Mannheimia haemolytica. [NE, TX, MS]</li> <li>Investigate the role of insertional elements in antimicrobial resistance in Salmonella. In addition, machine learning and classifier models have been used to predict AMR phenotypes in Salmonella strains using Fourier transform infrared spectrometry. [NE]</li> <li>New generation of antibiotic to mitigation antibiotic resistome in host gut microbiome [OH] <ol> <li>Activities: First pilot study in poultry to study the effect of the patented OSU new generation of probiotic on the most troublesome AR gene pools (for beta-lactams and multidrug).</li> <li>Outputs: the probiotic effectively mitigated the most troublesome AR gene pools (for beta-lactams and multidrugs) up to 3 logs with short-term treatment and further significantly improved weight gain in experimental chickens</li> </ol> </li> <li>Evaluated alternative to antibiotics and their impact on development/propagation of antimicrobial resistance in both cattle and swine production systems. [KS] <ol> <li>Outputs: Improved understanding and knowledge on antibiotic alternatives and their use in food animals.</li> </ol> </li> <li>Evaluate dietary interventions to enhance intestinal health of nursery pigs without antimicrobial growth promoters in feeds [NC]</li> <li>Determine Dublin prevalence in Salmonella enrichments from cattle clinical specimens in Pennsylvania and establish antimicrobial resistance genotype-phenotype relationship in S. Dublin from agricultural and food sources [PA]</li> </ol> <ol> <li>Develop a framework for benchmarking antimicrobial use in New York State dairy cattle and collect data on antimicrobial use on 5 dairy farms [NY]</li> <ol> <li>Activities: Evaluated 16 indicators (count-based, mass-based, and dose-based) for quantifying antimicrobial use on U.S. dairy farms and systematized them to improve interchangeability, interpretation, and comparability. </li> <li>Outputs: Systematized indicators will benefit One Health by aiding the uptake of farm-level antimicrobial use indicators by U.S. dairy farms.</li> </ol> <li>QMRA of antimicrobial-resistant Campylobacter jejuni infections associated with unpasteurized milk consumption in the United States [NY]</li> <ol> <li>Activities: developed preliminary QMRA for Campylobacter jejuni in raw milk</li> <li>Outputs: Identified knowledge gaps regarding human exposure to Campylobacter jejuni via consumption of raw milk</li> </ol> <li>Design and develop a novel multimodal sensing technology to characterize and quantify changes in suckle behavior in dairy breed calves that experience pre-weaning morbidity events [NY]</li> </ol> <ol> <li>Activities: Prototype development for novel precision livestock technology in progress</li> </ol> <ol> <ol> <li>Outputs: Develop a novel precision livestock technology for early disease detection with the goal of early intervention and reduction of antimicrobial use in neonatal calves</li> </ol> </ol>   Objective 3: Create and deliver programs on antibiotic stewardship in food production systems through education and outreach. <ol> <li>iAMResponsible™, a collaborative education and extension effort about antimicrobial stewardship that was developed by several institutions. [MD, NE, NY, MI] <ul> <li>Activities: Developing communication strategies and tools to best convey AMR knowledge (prevalence, treatment, stewardship, and perceptions). Supporting and disseminating research via iAMResponsible social media accounts. The iAMResponsible project team recognizes that audiences often respond best to peer-to-peer interactions or interactions with already trusted members of their personal networks for their decision-making. Thus, helping citizens, educators, and advisors articulate among themselves and to their communities the key actions they could take to slow AMR infections is a major emphasis area of iAMResponsible outreach and education efforts. To that end the team is focused on improving access to information, tools, and resources to improve both stakeholder understanding and communication of AMR-related risks.</li> </ul> </li> </ol> <ol> <li>Outputs: <ol> <li>Over 25 new pieces of outreach content [videos, infographics, podcast episodes, etc.] were created during the reporting period for distribution on social media and added to the existing database of media and research related to AMR curated by the iAMResponsible team and available to the public at <a href="https://lpelc.org/antimicrobial-resistance-resource-library/">go.unl.edu/amrlibrary</a></li> <li>Four on-line social media outlets for dissemination of AMR related materials are managed with regular (monthly, weekly, or daily) outputs, roughly 5000 persons (4971 as of 4/11/2022) follow one or more of these accounts.</li> </ol> </li> </ol> <ul> <li>The fourth annual offering of a multi-university graduate seminar on AMR from a one-health perspective was delivered in the Spring of 2023 [Banerjee ND, Harrison WA]</li> </ul> <ol> <li>One Health Graduate Online Course, available to graduate students and others on the fundamentals of AMR development and spread. One Health experts collaborate to deliver the course content.</li> <li>Resources and webinars: <a href="https://lpelc.org/tag/iamresponsible/">https://lpelc.org/tag/iamresponsible/</a>; <a href="http://www.iamrproject.com/">http://www.iamrproject.com/</a>; Podcast: Tales of the Resistance; Partnership with the Livestock and Poultry Environmental Learning Community (LPELC).</li> </ol> <ol start="2"> <li>Evaluate veterinary students’ preparedness in antimicrobial stewardship topics and develop educational interventions. [NY] <ol> <li>Activities: Adaptation and implementation of case-based antimicrobial stewardship lessons in a required veterinary public health course. A fully-virtual/online based case was implemented during the COVID-19 pandemic. This year it was adapted to be in-person with role-play that encourages veterinary students to practice communication skills. Data on graduating veterinary students’ antimicrobial stewardship knowledge was analyzed.</li> <li>Outputs: Developing and implementing new educational modules, topic rounds, and lectures on antimicrobial stewardship will increase veterinarians’ competency and confidence in being antimicrobial stewards.</li> </ol> </li> </ol>   Funding: <ol> <li>CAMRADES connecting antimicrobial resistance, agricultural decisions, and environmental systems: A tool for mitigating AMR and assessing risk to human health in agro-ecosystems. Duration: 01/01/2022-12/31/2026. Amount: $1,000,000. USDA NIFA. PI and Co-PIs: Michelle Soupir (ISU, PI), Daniel Anderson (ISU), Adina Howe (ISU), Diana Aga (U of Buffalo), Shannon Bartelt-Hunt (UNL), Amy Schmidt (UNL), Bing Wang (UNL).</li> <li>AMR Gene Reservoirs and Bacterial Host-AMR Gene Associations in Swine Production Systems. Amount: $999,981. USDA-NIFA. PI: Fernando; Co-PIs: A. Schmidt.</li> <li>Gut check: innovative mitigation of antibiotic resistance. Duration: 2020-2023. OSU Women & Philanthropy. PI: Wang</li> <li>IFT Feeding Tomorrow E. Caldwell fellowship. Duration: 2022-2023. PI: Yu L (Advisor, Wang H).</li> <li>Antibiotic Resistome in Fermented Foods and Probiotics for Mitigation. Duration: 2023-2025. OARDC Seed grant immediate needs. PI: Wang H, Pascall.</li> <li>Whole genome sequence analysis of Staphylococcus aureus, Staphylococcus pseudintermedius, and Group B Streptococcus isolated from veterinarians and veterinary technicians in the upper Midwest. Amount: $20,000. PI: Kelli Maddock (PI), Brianna Stenger, Teckla Webb, Gerald Stokka, Paul Carson.</li> <li>Development of a Matrix-Assisted Laser Desorption Ionization Time-of-Flight (MALDI-TOF) assay to discriminate pathogenic from commensal strains of Histophilus somni: A Novel and affordable diagnostic tool for bovine respiratory disease in North Dakota cattle herds. Amount: $5,000. SBARE. PI: Kelli Maddock (Co-PI), Brett Webb. 2023-2024.</li> <li>ORFeome Display for the Discovery of Novel Pathogen Markers Associated with Bovine Respiratory Disease in Shipped Cattle Duration: 2022-2025. Amount: $589,000. Chancellors research initiative, Texas A&M University. PI: Gill </li> <li>rhAMR: A comprehensive and cost-effective method refined and applied to understand the impact of feed additives on antimicrobial resistance. Duration: March 1, 2023 - February 29, 2028. Amount: $1,000,000. USDA National Institute of Food and Agriculture, Federal Agencies. PI: Ganda, E. (Principal Investigator), Boney, J. (Co-Principal Investigator), Kovac, J. (Co-Principal Investigator)</li> <li>Salmonella Dublin: Data-Driven Mitigation of an Emerging Pathogen in North-Eastern US Dairy Farms. Duration: February 28, 2023 - February 27, 2025. Amount: $300,000. USDA National Institute of Food and Agriculture, Federal Agencies. PI: Ganda, E. (Principal Investigator), Barragan, A. (Co-Principal Investigator), Hovingh, E. P. (Co-Principal Investigator), Springer, H. (Co-Principal Investigator), Surendran Nair, M. (Co-Principal Investigator)</li> <li>Promoting poultry health and productivity through feed additives," Duration: July 1, 2022 - June 30, 2024. Amount: $40,757. COP: Department of Agriculture, Commonwealth of Pennsylvania. PI: Ganda, E. (Principal Investigator), Kuchipudi, V. (Co-Principal Investigator),</li> <li>Impact of antibiotic use restrictions on antibiotic resistance in Salmonella Duration: 10/1/2021 – 9/30/2024. Amount: $90,000. USDA-NIFA Federal Formula Funds #NYC-478449, accession number 7000403. PI: Cazer, Cummings (Co-PI)</li> <li>Revealing Antimicrobial Resistance Trends in the Food Chain with Machine Learning Tools. Duration: 9/30/2023 – 9/29/2025. Amount: $300,000. USDA-AFRI. PI: Cazer, Goodman (Co-PI).</li> <li>Benchmarking Antimicrobial use in New York State Dairy Cattle. USDA-NIFA Federal Formula Funds #NYC-478945, accession number 7000433. PI: Ivanek</li> </ol> Design and development of a multimodal sensing technology to characterize and quantify changes in suckle behavior in dairy breed calves that experience pre-weaning morbidity events. Duration: 10/1/2022 – 9/30/2024. Cornell Institute of Digital Agriculture. PI: von Königslöw & Bhattacharjee

Publications

Appendix I: Publications <ol> <li>Ruzante J.M., Harris B., Plummer P., Raimeri R.R., Loy J.D., Jacob M., Sahin O. and Krueder A.J. (2022) Surveillance of Antimicrobial Resistance in Veterinary Medicine in the United States: Current Efforts, Challenges, and Opportunities. Frontiers in Veterinary Science. DOI: 10.3389/fvets.2022.1068406</li> <li>Lewis, G.L., Fenton R.J., Moriyama E.N., Loy J.D., and Moxley R.A. (2023). Association of ISVsa3 with Multidrug Resistance in Salmonella enterica Isolates from Cattle (Bos taurus). Microorganisms.  Microorganisms 2023, 11, x. <a href="https://doi.org/10.3390">https://doi.org/10.3390</a></li> </ol> <ol start="3"> <li>Bo Li, Min Ki Jeon, Xu Li, and Tao Yan.   Differential impacts of salinity on antibiotic resistance genes during cattle manure stockpiling are linked to mobility potential revealed by metagenomic sequencing.  Journal of Hazardous Materials, 445: 130590.</li> <li>Yangjunna Zhang, John W. Schmidt, Terrance M. Arthur, Tommy L. Wheeler, Qi Zhang, Bing Wang. A farm-to-fork quantitative microbial exposure assessment of β-lactam-resistant Escherichia coli among U.S. beef consumers. Microorganisms. 2022; 10(3): 661. <a href="https://doi.org/10.3390/microorganisms10030661">https://doi.org/10.3390/microorganisms10030661</a></li> <li>Li Y, Fu S, Klein M, Wang H. 2023. <a href="https://www.biorxiv.org/content/10.1101/2023.04.21.537834v1#:~:text=This%20study%20examined%20traditionally%20fermented%20foods%20and%20the,in%20the%20gut%20microbiota%20of%20most%20human%20subjects.">Traditionally fermented foods still as a critical avenue impacting host gut antibiotic resistome | bioRxiv</a></li> <li>Wang H, Li Y, Fu 2023. Food safety and host health: hazards, risks, challenges and mitigation of antibiotic resistance. Food Safety Management in Practice. (Revision in review).</li> <li>Maddock K, Gefroh S, Burbick C. Beta-lactam resistance in veterinary beta-hemolytic Streptococcus species: Are we experiencing a public health or test method crisis? J Am Vet Med Assoc.2023 May 23; 1-4. doi: 10.2460/javma.23.03.0172. Online ahead of print.</li> <li>Sun R, Cummings KJ, Beukema A, Hinckley-Boltax AL, Korich JA, & Cazer CL. 2023. Veterinary Students’ Knowledge and Awareness of Antimicrobial Stewardship before and after Clinical Rotations. J Vet Med Educ e20220125</li> <li>Loy, JD., Clawson M.L., Adkins P.R.F., and Middleton J.R. (2023) Current and Emerging Diagnostic Approaches to Bacterial Diseases of Ruminants.  Veterinary Clinics of North America: Food Animal Practice.  Vol 39. 93-114</li> <li>Wynn E.L., Hille M.M., Loy J.D., Schuller G., Kuhn K.L., Dickey A.M., and Clawson M.L. (2022) Whole Genome Sequencing of Diverse Moraxella bovis Strains Reveals Two Genotypes with Different Genetic Determinants.  BMC Microbiology.  Vol 22 (258) DOI: 10.1186/s12866-022-02670-3</li> <li>Olson H.G., Loy J.D., Clawson M.L., Wynn E.L., and Hille M.W. (2022) Genotype classification of Moraxella bovis isolates using MALDI-TOF MS profiles.  Frontiers in Microbiology.  13:1057621 DOI: 10.3389/fmicb.2022.10576215</li> <li>Nickodem C, Arnold AN, Gehring KB, Gill JJ, Richeson JT, Samuelson KL, Scott HM, Smith JK, Taylor TM, Vinasco J, Norman KN. 2023. A Longitudinal Study on the Dynamics of Salmonella enterica Prevalence and Serovar Composition in Beef Cattle Feces and Lymph Nodes and Potential Contributing Sources from the Feedlot Environment. Appl Environ Microbiol. 89(4):e0003323. doi: 10.1128/aem.00033-23.</li> <li>Cull, C. A., V. K. Singu, B. J. Cull, K. F. Lechtenberg, G. Amachawadi, J. S. Schutz, and K. A. Bryan. 2022. Efficacy of two probiotic products fed daily to reduce Clostridium perfringens- based adverse health and performance effects in dairy calves. MDPI Antibiotics. 11:1513. DOI: 10.3390/antibiotics11111513</li> <li>Cull, C. A., V. K. Singu, B. J. Cull, K. F. Lechtenberg, G. Amachawadi, J. S. Schutz, and K. A. Bryan. 2022. Efficacy of Lactobacillus animalis and Propionibacterium freudenreichii-based feed additives in reducing Salmonella-associated health and performance effects in commercial beef calves. MDPI Antibiotics. 11:1328. DOI: DOI: 10.3390/antibiotics11101328.</li> <li>Cull, C. A., V. K. Singu, J. J. Bromm, K. F. Lechtenberg, G. Amachawadi, and B. J. Cull. 2023. Effects of core antigen bacterin with an immunostimulant on piglet health and performance outcomes when challenged with enteric and respiratory pathogens. Antibiotics. 12:599. <a href="https://doi.org/10.3390/antibiotics12030599/">https://doi.org/10.3390/antibiotics12030599/</a>.</li> <li>Yadav, A., B. R. Singh, A. M. Pawde, P. Thomas, V. Singh, R. Singh, S. Singh, K. Ravichandran, H. Agri, V. Jayakumar, and R. G. Amachawadi*. 2023. Draft genome sequence of a Pasteurella multocida strain isolated from a Spotted Deer (Axis axis) in India. Microbiology Resource Announcements. <a href="https://doi.org/10.1128/mra.01297-22">https://doi.org/10.1128/mra.01297-22</a>.</li> <li>Duarte, M. E., C. H. Stahl, and W. Kim. 2023. Intestinal oxidative damages by F18+ Escherichia coli and its amelioration with an antibacterial bacitracin fed to nursery pigs. Antioxidants (in press) [NC, MD]</li> <li>Moita, V. H., and W. Kim. 2023. Efficacy of a bacterial 6-phytase supplemented beyond traditional dose levels on jejunal mucosa-associated microbiota, ileal nutrient digestibility, bone and intestinal health, and growth performance of nursery pigs. Journal of Animal Science 101:skad134. <a href="https://doi.org/10.1093/jas/skad134">https://doi.org/10.1093/jas/skad134</a> [NC]</li> <li>Choi, H., Y. Chen, F. Longo, and W. Kim. 2023. Comparative effects of benzoic acid and sodium benzoate in diets for nursery pigs on growth performance and acidification of digesta and urine. Journal of Animal Science 101:skad116. <a href="https://doi.org/10.1093/jas/skad116">https://doi.org/10.1093/jas/skad116</a> [NC, Brazil]</li> <li>Deng, Z., M. E. Duarte, Y. Kim, Y. Hwang, and S. W. Kim. 2023. Comparative effects of soy protein concentrate, enzyme-treated soybean meal, and fermented soybean meal replacing animal protein supplements in feeds on growth performance and intestinal health of nursery pigs. Journal of Animal Science and Biotechnology (in press) [NC, Korea]</li> <li>Vanessa Lagos, L., J. C. Woodworth, W. Kim, and H. H. Stein. 2023. Short communication: Commercial diets for pigs in the United States contain more calcium than formulated. Journal of Animal Science 100:(in press) [IL, NC, KS]</li> <li>Jang, K. B., V. H. C. Moita, N. Martinez, A. Sokale, and W. Kim. 2023. Efficacy of zinc glycinate reducing zinc oxide on intestinal health and growth of nursery pigs challenged with F18+ Escherichia coli. Journal of Animal Science 101:skad035. <a href="https://doi.org/10.1093/jas/skad035">https://doi.org/10.1093/jas/skad035</a> [NC]</li> <li>Jang, K. B., and W. Kim. 2022. Evaluation of standardized ileal digestibility of amino acids in fermented soybean meal for nursery pigs using direct and difference procedures. Animal Bioscience 36:275-283. <a href="https://doi.org/10.5713/ab.22.0269">https://doi.org/10.5713/ab.22.0269</a> [NC]</li> <li>Rocha, G. C., M. E. Duarte, and W. Kim. 2022. Advances, implications, and limitations of low crude protein diets in pig production. Animals12:3478 <a href="https://doi.org/10.3390/ani12243478">https://doi.org/10.3390/ani12243478</a> [NC, Brazil]</li> <li>Cheng, Y. C., H. L. Lee, Y. Hwang, and W. Kim. 2022. The effects of SID His to Lys ratio on growth performance, intestinal health, and mobilization of histidine-containing proteins in pigs at 7 to 11 kg body weight. Journal of Animal Science 100:skac396 <a href="https://doi.org/10.1093/jas/skac396">https://doi.org/10.1093/jas/skac396</a> [NC, Korea]</li> <li>Moita, V. H. C., and W. Kim. 2022. Nutritional and functional roles of phytase and xylanase enhancing the intestinal health of nursery pigs and broiler chickens. Animals 12:3322 <a href="https://doi.org/10.3390/ani12233322">https://doi.org/10.3390/ani12233322</a> [NC]</li> <li>Cheng, Y. C., and W. Kim. 2022. Use of microorganisms as nutritional and functional feedstuffs for nursery pigs and broilers. Animals 12:3141 <a href="https://doi.org/10.3390/ani12223141">https://doi.org/10.3390/ani12223141</a> [NC]</li> <li>Duarte, M. E., and W. Kim. 2022. Phytobiotics from oregano extracts enhance intestinal health and growth performance of pigs. Antioxidants 11:2066 <a href="https://doi.org/10.3390/antiox11102066">https://doi.org/10.3390/antiox11102066</a> [NC]</li> <li>Boston, T. E., F. Wang, X. Lin, Leonard, S. W. Kim, D. McKilligan, V. Fellner, and J. Odle. 2022. Gruel creep feeding accelerates growth and alters intestinal health of young pigs. Animals 12:2408. <a href="https://doi.org/10.3390/ani12182408">https://doi.org/10.3390/ani12182408</a> [NC]</li> <li>Niu, Q., G. Pu, L. Fan, C. Gao, T. Lan, C. Liu, T. Du, W. Kim, P. Niu, Z. Zhang, P. Li, and R. Huang. 2022. Identification of gut microbiota affecting fiber digestibility in pigs. Current Issues in Molecular Biology 44:4557-4569 <a href="https://doi.org/10.3390/cimb44100312">https://doi.org/10.3390/cimb44100312</a> [NC, China]</li> <li>Deng, Z., M. E. Duarte, K. B. Jang, and W. Kim. 2022. Soy protein concentrate replacing animal protein supplements and its impacts on intestinal health, mucosa-associated microbiota, and growth performance of nursery pigs. Journal of Animal Science 100:skac255. <a href="https://doi.org/10.1093/jas/skac255">https://doi.org/10.1093/jas/skac255</a> [NC]</li> <li>Xu, X., M. E. Duarte, and W. Kim. 2022. Postbiotics effects of Lactobacillus fermentate on intestinal health, mucosa-associated microbiota, and growth efficiency of nursery pigs challenged with F18+ Escherichia coli. Journal of Animal Science 100:skac210. <a href="https://doi.org/10.1093/jas/skac210">https://doi.org/10.1093/jas/skac210</a> [NC]</li> <li>Moita, V.H.C., M.E. Duarte, and S.W. Kim. 2022. Functional roles of xylanase enhancing intestinal health and growth performance of nursery pigs by reducing the digesta viscosity and modulating the mucosa-associated microbiota in the jejunum. Journal of Animal Science 100:skac116. <a href="https://doi.org/10.1093/jas/skac116">https://doi.org/10.1093/jas/skac116</a> [NC]</li> <li>Holanda, D. M., and W. Kim. 2022. Impacts of weaning weights and mycotoxin challenges on jejunal mucosa-associated microbiota, intestinal and systemic health, and growth performance of nursery pigs. Journal of Animal Science and Biotechnology 13:43. <a href="https://doi.org/10.1186/s40104-022-00691-6">https://doi.org/10.1186/s40104-022-00691-6</a>. [NC]</li> <li>Cheng, Y. C., M. E. Duarte, and W. Kim. 2022. Effects of Yarrowia lipolytica supplementation on growth performance, intestinal health, and apparent ileal digestibility of diets fed to nursery pigs. Animal Bioscience 35:605-613. <a href="https://doi.org/10.5713/ab.21.0369">https://doi.org/10.5713/ab.21.0369</a> [NC]</li> <li>Duarte, M. E., and W. Kim. 2022. Intestinal microbiota and its interaction to intestinal health in nursery pigs. Animal Nutrition 8:169-184. <a href="https://doi.org/10.1016/j.aninu.2021.05.001">https://doi.org/10.1016/j.aninu.2021.05.001</a>. [NC]</li> <li>Jang, K. B., and W. Kim. 2022. Role of milk carbohydrates in intestinal health of nursery: a review. Journal of Animal Science and Biotechnology 13:6. <a href="https://doi.org/10.1186/s40104-021-00650-7">https://doi.org/10.1186/s40104-021-00650-7</a> [NC]</li> <li>Ganda E, Chakrabarti A, Sardi MI, Tench M, Kozlowicz BK, Norton SA, Warren LK, Khafipour E. Saccharomyces cerevisiae fermentation product improves robustness of equine gut microbiome upon stress. Front Vet Sci. 2023 Feb 24;10:1134092. doi: 10.3389/fvets.2023.1134092. PMID: 36908513; PMCID: PMC9998945.</li> </ol>

Impact Statements

According to the World Health Organization and the Centers for Disease Control and Prevention, antimicrobial resistance is one of the greatest threats to the health of humans, animals, and the environment. When considering health across humans, animals, and plants, the approach should be viewed from a “One Health” perspective, which must be addressed using a multidisciplinary and collaborative approach. Members of the NC 1206 Multi-State Research Project have collaborated to accomplish key studies and extension education activities that advance the knowledge, outreach, interdisciplinary collaboration, and mitigation efforts related to antimicrobial resistance. Social sciences have been integrated into education programs to target potential antimicrobial user biases, increase AMR knowledge, and to reach stakeholders across the food chain. The addition of social sciences strengthens the approach and allows for more targeted education of stakeholders.