DEVELOPMENT OF A SYSTEM TO EVALUATE IMPACT OF ON-FARM ANTIMICROBIAL USE ON SWINE HEALTH AND ON EMERGENCE OF ANTIMICROBIAL RESISTANT BACTERIA OF SWINE ORIGIN

• Sponsoring Institution: National Institute of Food and Agriculture
• Project Status: TERMINATED
• Funding Source: ANIMAL HEALTH
• Reporting Frequency: Annual
• Accession No.: 1011262
• Project No.: MIN-62-091
• Project Start Date: Oct 28, 2016
• Project End Date: Sep 30, 2018

Project Director
Perez, AN.

Recipient Organization
UNIV OF MINNESOTA
(N/A)
ST PAUL,MN 55108

Performing Department
Veterinary Population Medicine

Non Technical Summary
The risk posed by misuse and overuse of antimicrobials on food animals on the emergence of antimicrobial resistant(AMR) bacteria of relevance for public and animal health is clearly perceived. However, the exact role that veterinary use of antimicrobials has on this threat remains controversial, partially due to the lack of detailed information on on-farm use. New regulations, leading to the progressive relabeling of antimicrobials so that its use as growth promoters is no longer permitted and its application requires veterinary oversight, have been recently introduced. However, a system for evaluation of those changes in the AMR prevalence but also on the animal health and production is lacking.Here, we are proposing to use swine as a model to assess if the new FDA regulations (leading to a change in the veterinary use of antibiotics) can have an impact on:- Animal health (increased/decreased disease in swine farms)- AMR prevalence (increased/decreased percentage of resistant bacteria recovered from swine farms).To test this hypothesis we will use a double approach: first, we will assess the baseline trends in submission of different types of swine clinical samples as well as detection of relevant swine pathogens in the Minnesota Veterinary Diagnostic Laboratory (MVDL) in the last 10 years and we will compare this baseline with data obtained within the 2017-2018 period. Second, for those routinely subjected to antimicrobial susceptibility testing, we will evaluate the prevalence of resistance to the different antimicrobials before and after the implementation of the new FDA regulations. Finally, we will examine in detail a subset of the swine industry (volunteering systems) to evaluate if their on-farm use of antimicrobials and other management factors (such as increased use of metals) correlates with the resistance patterns found in microorganisms recovered from their sites. This model could be then expanded and applied to other food animals in line with the objectives stated in the National Action Plan for Combating Antibiotic-Resistant Bacteria.

Animal Health Component

100%

Research Effort Categories

Basic

(N/A)

Applied

100%

Developmental

(N/A)

Classification

Knowledge Area (KA)	Subject of Investigation (SOI)	Field of Science (FOS)	Percent
311	3510	1170	100%

Knowledge Area
311 - Animal Diseases;

Subject Of Investigation
3510 - Swine, live animal;

Field Of Science
1170 - Epidemiology;

Keywords

antimicrobial resistance

swine

antimicrobial use

animal health

epidemiology

Goals / Objectives
The overall objective of the study here is to assess, for the first time in quantitative terms, the impact of the new FDA regulations addressing the use of medically important antibiotics in food animals on the animal health and on the prevalence of AMR bacteria in swine. Our hypothesis is that changes in the veterinary use of antibiotics may have an impact on the occurrence of respiratory and/or enteric diseases in swine, and that it may also impact the frequency of isolation of AMR bacteria from swine samples. In order to test this hypothesis, research- and implementation-oriented activities will be conducted to achieve partial sub-objectives. Specificallya) RESEARCH a.1. Establish baseline patterns of submissions of samples associated with respiratory and enteric diseases (i.e., tissue, feces) to the Minnesota Veterinary Diagnostic Laboratory (MVDL) in a 11-year period prior to the effective date of the new FDA regulations (2006-2016), and monitoring of these patterns between January 2017 until the end of the project (October 2018).a.2. Determine the frequency of detection of relevant respiratory (Haemophilus parasuis, Streptococcus suis, Pasteurella multocida, Actinobacillus suis, Mycoplasma hyopneumoniae, M. hyorhinis) and digestive (beta-hemolytic Escherichia coli, Salmonella enterica, Brachyspira spp., Lawsonia intracellularis) bacterial pathogens from clinical samples received at the MVDL before (2006-2016) and after (2017-Oct 2018) the effective date of the FDA new regulations.a.3. Evaluate the patterns of AMR found in bacterial pathogens routinely subjected to antibiotic susceptibility testing (E. coli, S. enterica, P. multocida, S. suis, H. parasuis) at the MVDL in the 2006-2016 and 2017-2018 periods.B IMPLEMENTATION (translation of research):B.1. Develop a production system-oriented monitoring system to evaluate the trends in antibiotic and mineral on-farm use, as well as the prevalence of AMR bacteria recovered from clinical samples originated in each system in collaboration with volunteering swine production companies. This system will cover records collected before and after the effective date of the FDA new regulations.Achievement of those objectives will allow the comparison of i) the patterns of submission of clinical samples associated with respiratory and enteric diseases, ii) the frequency of isolation of relevant respiratory and digestive bacterial pathogens from swine samples and ii) the prevalence of AR-bacteria among relevant swine pathogens, thus providing information on the potential impact of changes in veterinary use of antibiotics in swine in Minnesota. Finally, knowledge gained through this research will be translated through the implementation of a monitoring system to assess the evolution of AMR in the swine industry.

Project Methods
Task 1. Establishment of baseline patterns of submission of respiratory and enteric samples from swine at the MVDL: The MVDL database will be queried to recover information on respiratory (lung), enteric (intestinal tissue, feces) and systemic (liver, spleen, pericardium, peritoneum, pleura, joint, brain) samples submitted to the diagnostic laboratory since 2006. Information on date of submission, origin of the sample (county, farm and/or owner data, coordinates, premise ID when available), sample type and test performed will be extracted and stored using standard software. A first screening to remove all non-diagnostic (i.e., surveillance studies, experimental studies) will be performed by looking for specific signals in the queried fields (pharmaceutical companies, non-agricultural origin of samples, non-clinical samples). Then, scripts developed for integration, filtering and curation of the database that were already developed for a previously funded project on Salmonella will be adapted and optimized. Personal information will be coded prior to further analysis to guarantee confidentiality. The presence of temporal (and whenever possible, spatial) patterns will be assessed using cluster analysis techniques for detection of global and local clustering as well as time uniseries analyses. Information available on animal (age, health status) and farm-level variables will be used as predictors for a classification model that will take advantage of a Machine Learning approach by Random Forest classification as recently described (32).Task 2. Evaluation of the frequency of isolation/detection of relevant swine pathogens: information on the frequency of detection of pathogens of relevance in swine (H. parasuis, S. suis, P. multocida, M. hyopneumoniae, M. hyorhinis, A. suis, E. coli, S. enterica, Brachyspira spp. and L. intracellularis) per sample type will be extracted from the query performed in task 1. The analysis will be performed at the farm-month level (so that pathogens are counted once if they have the same genetic/phenotypic traits and were detected in samples originating in the same farm within the same month) to control for oversampling/overdetection in a given farm. Time uniseries analysis techniques will be applied to assess seasonal components in the longitudinal trends, and the association between the percentage of isolates recovered and associated variables at the different levels (sample, animal and farm) will be assessed using hierarchical generalized linear mixed models separately for each pathogen.Task 3. Assessment of the prevalence of AMR phenotypes in selected microorganisms: information on resistant phenotypes of certain bacteria, selected based on routine AMR typing, will be extracted from the MVDL database and analyzed at the farm-month level as described above. Antimicrobials analyzed will include some of the most commonly used in food animals (both for therapeutic and traditionally for growth promotion purposes) from several classes classified as critically (fluoroquinolones, cephalosporins, macrolides) and highly important (amphenicols, aminoglycosides, tetracyclines, penicillins) by the FDA (33), as well as other drugs routinely used in food animals (sulfonamides, lincosamides and pleuromutilins). Information on the minimum inhibitory concentration (MIC) will be collected and analyzed quantitatively as well as qualitatively using recommended breakpoints developed by the Clinical Laboratory Standards Institute when available (34). Significance of trends in prevalence of resistant isolates will be assessed separately for each bacterial species using chi-square tests for trend and linear regression models controlling for serial correlation.Task 4. Design and test of a system-oriented monitoring system to evaluate impact of new FDA guidance regulations.Subtask 4.1 Surveillance of antimicrobial resistance and antimicrobial use: systems currently enrolled in the Swine Health Monitoring Project (SHMP) (35, 36), that includes approximately 2 million sows (i.e., around 1/3 of the U.S. sow population), will be invited to provide information on their protocols for antimicrobial use in sow farms and nursery and growing pigs, as well as on periodical use of antimicrobials per farm/animal group (last five years and prospectively). This information will be used to assess the impact of the FDA guidance for industry on use practices in each age class. Preliminarily, a number of companies have already expressed their interest to contribute data to the project (see attached letters of support).Permission to access information on their clinical submissions to the MVDL and other veterinary diagnostic laboratories will be also requested in order to collect information on the antimicrobial susceptibility results of bacterial isolates recovered from their farms. This information will be compared with the data on antimicrobial use to evaluate the impact of antimicrobial use practices on resistance trends.Subtask 4.2. Establishing the association between microbial management (disinfection, vaccination, in feed alternatives to antibiotic growth promoters) with prevalence of antibiotic resistance. A survey will be developed to gather information on microbial management practices. Farms from which information on antibiotic use and pravelnce of AMR bacteria is monitored will be requested to share information on the use of feed additives such as Zn and Cu in the diets of pigs during the period previous to sample submission to the MVDL. Additives reported to be used in swine diets will be grouped using chemical and mode of action categories. Categories and frequency of use of alternative products will be analyzed in association with frequency of antibiotic resistance. The current project will be limited to establishing associations and general descriptive statistics of these associations. Future projects could investigate the impact of these associations on animal growth performance, wellbeing, and molecular prevalence of antibiotic resistance.

Progress 10/28/16 to 09/30/18

Outputs
Target Audience:During the second year of the project we have communicated our findings to a wide audience, including the scientific community (through articles submitted to high impact peer-reviewed journals and presentations in scientific meetings), the regulatory agencies (Minnesota Department of Health, through several meetings) and the industry (swine practitioners and swine producers, through presentations at specific conferences and direct contacts/meetings with them). In addition, those contacts were useful also to gather new information to be used in the analysis and/or help in the interpretation of our results. Moreover, we have finalized the design of a webpage with general information on AMR but also some of the results and applications of the research conducted in this project, that will help to reach a wider audience (general public) Changes/Problems:As reported in the first year report, a change in the PI was needed due to the change in the original PI (Alvarez) to a different institution in Europe, which was replaced by Dr. Perez, but this did not impact the progress of the project. Although the project has been successful in achieving its scientific objectives the implementation stage could not be finalized due to the lack of access to farm-level information. An analytical framework to extract AMR information at the farm level from the MVDL database has been nevertheless designed, and this will be helpful looking forward for systems interested in monitoring their AMR patterns and eventually linking data on their on-farm antibiotic use. What opportunities for training and professional development has the project provided?One graduate student has moved into candidacy and is expected to finalize his PhD studies next year. One post doctoral fellow has been awarded with a fellowship from an external institution. How have the results been disseminated to communities of interest?Yes. See results section. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Objectives of the project have been achieved as planned. First, the data on the clinical submissions to the Minnesota Veterinary Diagnostic Laboratory in 2006-2016 from which the selected bacterial pathogens (Actinobacillus suis, Brachyspira spp., Escherichia coli, Haemophilus parasuis, Lawsonia intracellularis, Mycoplasma spp., Pasteurella multocida, Salmonella enterica and Streptococcus suis) were cultured/detected were analyzed in order to establish baseline patterns of submission and detection rates. A mean number of 4,920 submissions/year, mostly containing samples from the lower respiratory tract, that accounted for 36% of all samples received, were analyzed. A seasonal component in sample submission was observed for respiratory and enteric samples (with less samples submitted over the summer). For those pathogens in which at least 500 isolates were retrieved each year (S. suis, P. multocida, E. coli, H. parasuis, S. enterica and A. suis) a large variation between the years was also observed, with no correlation between the rates of isolation of the different pathogens from same samples/years. Finally, results from the antimicrobial susceptibility testing in cultured isolates were also highly heterogeneous, with large increases in resistance to certain antimicrobial classes in certain bacterial species (i.e., fluoroquinolone resistance in enterobacteria) and no trends in the prevalence of resistance in others. Results from the analyses on Salmonella and E. coli data have been included in scientific papers and communications (see above) due to their larger impact as zoonotic pathogens and/or value as indicators of the AMR situation in swine bacteria. When analyzing the data on E. coli a lack of updated information on the global situation regarding prevalence of phenotypic resistance/genetic mechanisms conferring resistance of isolates from swine was detected. In order to provide an adequate context to the findings of our project we have also conducted two systematic literature reviews and meta-analyses to establish the current and historic prevalence of phenotypic/genotypic resistance to cephalosporins, carbapenems, fluoroquinolones and colistin in E. coli of swine origin (Hayer et al., in preparation). For the implementation stage, data from one large swine system was analyzed in order to evaluate the changes in the antimicrobial susceptibility patterns from bacteria recovered from swine clinical samples collected in different production points (i.e., sow farm, nursery, fattening) and submitted to the MVDL (n>1,000 isolates). Data on two specific flows were further analyzed, although the level of stratification require to draw meaningful conclusions at the site level did not allow reaching the required sample size. No data on antibiotic use was finally received during the project, what prevented us from linking results from the analyses on AMR from bacterial isolates recovered from a farm to the farm antibiotic use.

Publications

• Type: Journal Articles Status: Published Year Published: 2018 Citation: 1. Elnekave E., Hong S., Mather A.E., Boxrud D., Taylor A.J., Lappi V., Johnson T.J., Vannucci F., Davies P., Hedberg C., Perez A., Alvarez J. Salmonella enterica serotype 4,[5],12:i:- in swine in the United States Midwest: an emerging multidrug resistant clone. Clinical Infectious Diseases, 2018 66(6):877-885. doi: 10.1093/cid/cix909
• Type: Journal Articles Status: Submitted Year Published: 2018 Citation: 2. Elnekave E, Hong S, Lim S. et al. Circulation of plasmids harboring resistance genes to quinolones and/or extended spectrum cephalosporins in nontyphoidal Salmonella enterica serotypes from swine in the Midwestern United States. Under review at mBio
• Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: 1. Elnekave E, Hong S, Hayer SS, et al. Genetic resistance for quinolones and 3rd generation cephalosporins in Salmonella serotypes circulating in the Midwest swine. September 2018. Leman conference. The Allen D. Leman Swine Conference. St Paul, Minnesota, USA.
• Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: 2. Hayer SS, Lim S, Hong S, et al. Genomic basis of emerging fluoroquinolone and third generation cephalosporin resistance in Escherichia coli isolated from swine clinical samples collected across USA. The Allen D. Leman Swine Conference. St Paul, Minnesota, USA
• Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: 3. Hayer SS, Machado G, Vannucci F,et al. Changes in fluoroquinolone and cephalosporin resistance in Escherichia coli isolates collected from swine clinical accessions at MVDL from 2006-2016. Poster and oral presentation at American Society of Microbiology Microbe conference. June, 2018 Atlanta, Georgia, USA
• Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: 4. Elnekave, E., Ding, T., Hong, S., et al. Use of Genome Scale Metabolic Models (GEMs) to understand the emergence of Salmonella I 4,[5],12:i:-. April 2018. 3rd International Conference on One Medicine One Science (iCOMOS). Minneapolis, Minnesota, USA

Progress 10/28/16 to 09/30/17

Outputs
Target Audience:During the first year of the project we have contacted members of the industry, the regulatory agencies and general public in an effort to i) obtain the necessary data to fulfill the objectives of the project and ii) to ensure the communication of our work. Since October 2016 we have maintained several meetings with a number of swine clinics in the Midwest to discuss our plan of action and the possibility of sharing information on antibiotic use/antibiotic resistance. Similarly, we have presented our findings in meetings with the industry (Swine Disease Eradication Center annual meeting, held in Saint Paul on June 20; Allen D. Leman swine conference, held in Saint Paul in September 16-19). In addition, we have been sharing our plan of action and progress in meetings with members of the Minnesota Department of Health (director of the One Health Antibiotic Stewardship; head of the Foodborne Vectorborne and zoonotic diseases unit; supervisor of Molecular Epidemiology in the Public Health Laboratory) in which we have been able to coordinate the research and get input from the public health side regarding AMR trends in animal pathogens. Part of the work carried out in this project has been also used in presentations used for training of DVM veterinary students (courses on clinical epidemiology and public health) and in outreach talks given internationally (at the Universidad Autonoma de Mexico, September 2017, and at the Safepork conference in Brazil in August 2017). Changes/Problems:Guaranteeing the needed industry of the industry to develop the activities listed under Task 4 has been challenging so far due to difficulties getting access to private data, although we expect to be successful in year 2 of the project. The PI of the proposal (Alvarez) will move to a different institution in Spain, and for this reason a change in the PI has been requested (to replace Dr. Alvarez with Dr. Perez).Dr. Perez is associate professor at the CVM and currently a co-I of the project, so he is aware of the progress that has been made and the steps that need to be performed for the duration of the project. Therefore, no impact on the progress of the project due to this change is expected. What opportunities for training and professional development has the project provided?During the first year of the project we received the visit of a PhD student from Spain (Universidad de Zaragoza), Dr. Alejandro Casanova, who did a training stay for 5 months and was trained on data and trend analysis and collaborated in the laboratory work needed for the good functioning of the project. One of the collaborators of the project, Dr. Elnekave, participated in the Workshop 'TamingtheBEAST' on Bayesian Phylogenetics that took place in London(July 24-28, 2017). He was trained on phylodynamic analytic techniques that will be useful for the project, since this will help us monitoring the dynamics of spread of antimicrobial resistance genes in the pathogens under evaluation. Mr. Hong, that is in charge of database curation and assembly and the pipeline for detection of antimicrobial resistance genes through Whole Genomic Sequencing, participated in the UCLA Computational Genomics Summer Institute in Los Angeles (July 10-15,2017). Finally, Dr. Paladino, that is currently working on the analysis of the baseline data on submission and isolation rates at the UMN Veterinary Diagnostic Laboratory, has taken the course "Introduction to data analysis with R and reproducible data science" organized by the Institue for Research in Statistics and its Applications (IRSA) of the UMN on August 31-September 1 2017. The work of this project is part of the doctoral theses of two PhD students at the UMN, and their work has been translated into posters and communications presented in conferences and also seminars presented internally at the University of Minnesota (two seminars at the graduate student seminar rounds of the CVM). How have the results been disseminated to communities of interest?Results have been disseminated mainly through three ways: - Scientific articles in high-impact peer-reviewed journals: one manuscript has been already accepted (Clinical Infectious Diseases, impact factor=8.2) and there are two other manuscripts already in preparation. - Outreach communications in journals for the general public: our results have been included in XX communications published in different journals (National Hog Farmer, Science page of the Swine Health Monitoring Project weekly report) directed specifically to the swine industry, one of the main targets of our research. - Oral presentations: we have shared our results internally at the University through 2 presentations in graduate seminars at the College of Veterinary Medicine and another seminar presented at the Veterinary Diagnostic Laboratory, and results were also presented in two international scientific conferences (International Symposium on the Epidemiology and Control of Biological, Chemical and Physical Hazards in Pigs and Pork - Safepork; Allen D. Leman swine conference). In addition, results were also presented in an international seminar presented at the Universidad Autonoma de Mexico (Mexico). What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? The objectives planned for year 1 have been accomplished as expected. Activities performed have allowed to demonstrate that for most of the swine bacterial pathogens under study and the antibiotics evaluatedin this project the proportion of antimicrobial resistance organisms did not increase (or even experienced a moderate decrease) during the study period (2006-2017). In contrast, only for a specific family of antimicrobials (fluoroquinolones) a significant increase in the proportion of resistant isolates was observed for both Escherichia coli (indicator bacteria) and Salmonella enterica (foodborne pathogen). This information is very valuable since it provides a baseline to compare the trends in the current and next years, once that the new regulations on antibiotic use have been fully implemented. In addition, we have demonstrated at least one of the mechanisms behind the fluoroquinolone resistance observed in Salmonella (genes from a family of plamid-mediated genes, Qnr), what has large implications in terms of animal and public health since these genes can be highly transferable and thus may represent an important concern for preventing the emergence of antimicrobial resistance. More specifically, we have completed the assembly of the database containing information on sample submission and pathogen isolation that is necessary to achieve objectives a.1 and a.2. We have already performed some initial descriptive analysis that have been presented in oral communications presented at the University of Minnesota as internal research seminars but also in a scientific conference (Allen D. Leman swine conference, 2017). This newly generated information will allow the evaluation of the impact of the new regulations since define the expected variability in terms of sample submission and pathogen isolation. In addition, the data for the achievement of Objective a.3 has been also generated, and several analysis already conducted for two of the bacterial species of higher importance (E. coli and Salmonella). Our results have demonstrated that trends in both pathogens were similar for most of the antibiotics, with no change or slight decrease in the proportion of resistant strains for most of them and a marked increase in resistance for fluoroquinolones. These results have been translated already in a publication (accepted) and several communications through outreach communications as detailed in the "products" section. The implementation phase of the project is under development. Several meetings with swine clinics have taken place and data sharing has been discussed, though progress is expected to be achieved in year 2 of the project as originally planned.

Publications

• Type: Conference Papers and Presentations Status: Other Year Published: 2016 Citation: Hayer S.S., Hong S., Alshalchi S., Rovira A, Olsen K., Perez A., Vidovic S., Alvarez J. Antimicrobial susceptibility and virulence profiles of non typhoidal Salmonella enterica isolates obtained from porcine clinical samples received at the Minnesota Veterinary Diagnostic Laboratory. Allen D. Leman Swine Conference, September 17-20 2016, St Paul, Minnesota, US
• Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Elnekave E., Hong S., Perez A., Davies P., Boxrud D., Taylor A.J., Lappi V., Alvarez J. Genotypic characterization of a monophasic variant of Salmonella enterica serotype Typhimurium in swine in USA Midwest. 12th International Symposium on the Epidemiology and Control of Biological, Chemical and Physical Hazards in Pigs and Pork, Foz do Icua�u (Brazil), August 21-24, 2017
• Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Paladino, E. How the GFI#213/VFD Affected the Pattern of Submissions at the UMNVDL
• Type: Other Status: Published Year Published: 2017 Citation: E. Elnekave, S. Hong, P. Davies and J. Alvarez. Emerging Salmonella isolated from Midwest Swine. Published in the National Hog Farmer (February 14, 2017). Available at http://www.nationalhogfarmer.com/animal-health/emerging-salmonella-isolated-midwest-swine
• Type: Other Status: Published Year Published: 2017 Citation: Emerging Salmonella 4,[5],12:i:? and antimicrobial resistance in Salmonella serovars isolated from swine in the Midwest. Ehud Elnekave, Samuel Hong, Albert Rovira, Julio Alvarez. Science page of the weekly report of the Swine Health Monitoring Project in September 2017 (available at https://www.vetmed.umn.edu/sites/vetmed.umn.edu/files/shmp_2017l18.12_antimicrobial_resistance_in_salmonella_-_science_page.pdf)
• Type: Journal Articles Status: Accepted Year Published: 2017 Citation: Elnekave E., Hong S., Mather A.E., Boxrud D., Taylor A.J., Lappi V., Johnson T.J., Vannucci F., Davies P., Hedberg C., Perez A., Alvarez J. Salmonella enterica serotype 4,[5],12:i:- in swine in the United States Midwest: an emerging multidrug resistant clone. Clinical Infectious Diseases
• Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Ehud Elnekave Samuel Hong, Peter Davies, Dave Boxrud, Angela Taylor, Victoria Lappi, Fabio Vannucci, Andres Perez, Julio Alvarez. Tracking the evolutionary pathway of Salmonella 4,[5],12:i:- circulating in the Midwestern swine. Poster presentation at the Allen D. Leman Swine Conference, September 16-19 2017, St Paul, Minnesota.
• Type: Other Status: Published Year Published: 2017 Citation: S. Hayer, S. Hong, M. Thurn, A. Perez and J. Alvarez. Antibiotic susceptibility in Pasturella multocida and Streptococcus suis isolated at the Minnesota Veterinary Diagnostic Laboratory (2006-2016). Science page of the weekly report of the Swine Health Monitoring Project in July 2017. Available at https://www.vetmed.umn.edu/sites/vetmed.umn.edu/files/shmp_2017l18.4_antibiotic_susceptibility_in_pasturella_multocida_and_streptococcus_suis_-_science_page.pdf
• Type: Other Status: Published Year Published: 2017 Citation: S. Hayer, A. Perez, J. Torrison and J. Alvarez. Time trend analysis of antibiotic resistance in Beta-hemolytic Escherichia coli isolated at MVDL (2006-2016). Science page of the weekly report of the Swine Health Monitoring Project in January 2017. Available at https://www.vetmed.umn.edu/sites/vetmed.umn.edu/files/shmp_2016l17.31_time_trend_antiobiotic_resistance_sciencepage.pdf
• Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: S. Hayer, G. Machado, F. Vannucci, A. Perez and J. Alvarez. Changes in fluoroquinolone and cephalosporin resistance in Escherichia coli isolates collected from swine clinical accessions at MVDL from 2006-2016. Poster presentation at Allen D. Leman Swine conference, September 2017, St. Paul, USA.