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United States Department of Agriculture

Agricultural Research Service

Related Topics

Research Project: EPIDEMIOLOGY, ECOLOGY, AND MOLECULAR GENETICS OF ANTIMICROBIAL RESISTANCE IN PATHOGENIC AND COMMENSAL BACTERIA FROM FOOD ANIMALS

Location: Bacterial Epidemiology and Antimicrobial Resistance

2008 Annual Report


1a.Objectives (from AD-416)
1) Use antibiotic resistance data obtained from the Collaboration on Animal Health and Food Safety Epidemiology (CAHFSE) and the National Antimicrobial Resistance Monitoring System - Enteric Bacteria (NARMS) programs and poultry studies to identify sources, reservoirs and amplifiers of resistant food borne and commensal bacteria, as well as the path of dissemination of these resistant bacteria in food producing animals and poultry. Results may be used for risk assessment and in developing mitigation strategies. .
2) Map the spread of antimicrobial resistance throughout the US using molecular epidemiology and population genetic studies of antimicrobial resistant bacterial isolates, including participation in USDA VetNet. .
3) Analyze and differentiate antimicrobial resistance mechanisms, both phenotypically and genotypically, and rapidly identify resistant strains.


1b.Approach (from AD-416)
Under current funding, this research is designed to be conducted by a team of five scientists, each focusing on one particular organism or area. Each SY will design a specific research plan maximizing collaborations within the Unit structure. Although independent research will be conducted, a majority of experiments will be interactive, minimizing the need to repeat experimental samplings, particularly in the field. This research format will also maximize acquisition of data which will provide insight of the interaction between bacterial populations within the host and/or environment, particularly those interactions involving food borne zoonotic and commensal bacteria. Three SYs will focus on the molecular aspects of Antimicrobial Resistance (AR), particularly in Campylobacter, Salmonella and commensal bacteria (E. coli and enterococci). Critical to the molecular research will be epidemiologic studies provided by the CAHFSE program and ecologic (field and environment) studies which will not only provide a source of isolates for the molecular studies, but will also determine prevalence and dissemination of AR attributes within production settings, the environment, and among bacterial populations. Another significant source of isolates will be available from the NARMS program. These isolates will be well characterized to the serotype level and antimicrobial resistance phenotype. Additionally, all isolates will have been subjected to PFGE analysis to determine relatedness among isolates. Specific genotypic characterization will be conducted. Pathogenic studies involving bacterial strains collected from the CAHFSE and the NARMS programs, as well as those which have been genetically modified in the laboratory, will provide information regarding virulence (or lack thereof) associated with the acquisition of AR. Additionally, transfer of resistance genes may be studied under these environments.


3.Progress Report
The mission of the Bacterial Epidemiology and Antimicrobial Resistance Unit is to study antimicrobial resistance (AR) in zoonotic food borne pathogens and commensal bacteria and addresses National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest. To identify food-borne pathogens and gain an understanding of the prevalence of resistance among those pathogens, several methods were developed in 2008 (Problem Statement 1.1.1: Methodology). These included a rapid high-throughput multiplex Polymerase Chain Reaction (PCR) for Salmonella identification, a multiplex PCR for Listeria speciation, microarrays for AR and virulence gene detection, and whole genome DNA microarrays for genotyping food-borne pathogens. Molecular mechanisms associated with the development of 3rd generation cephalosporin resistance in Salmonella and fluoroquinolone and chloramphenicol resistance in Enterococcus were elucidated. These studies addressed the problem of AR (Problem Statement 1.1.5: Antibiotic Resistance). The role commensals may have in the development and transfer of resistance was defined in part using epidemiological studies (Problem Statement 1.1.2: Epidemiology). Prevalence studies of enterococci and staphylococci from companion animals and incidence of Clostridium difficile in swine and dairy herds were performed. Prevalence of Methicillin-Resistant Staphylococcus aureus (MRSA) in retail meat was also determined. As part of the Unit mission, the animal arm of the National Antimicrobial Resistance Monitoring System - Enteric Bacteria (NARMS) is located in our Unit. The goal of the program is to track the development of AR in veterinary isolates and is related to the research needs addressed in Problem Statement 1.1.5: Antibiotic Resistance. In 2008, antimicrobial susceptibility was determined for approximately 5000 Salmonella, 1500 Campylobacter, 8000 generic E. coli, and 4200 Enterococcus; the database now contains antimicrobial susceptibility patterns for over 50,000 Salmonella, 5,500 Campylobacter, 15,000 generic E. coli and 8,200 Enterococcus. Antimicrobial susceptibility patterns from the animal arm of NARMS were complemented by molecular typing information in the form of Pulsed-Field Gel Electrophoresis (PFGE) generated by USDA VetNet. VetNet addresses two Problem Statements in the Action Plan including 1.1.1 Methodology and 1.1.2 Epidemiology and serves to combine information on AR of isolates with genetic attributes to obtain specific characteristics for the isolates. Over 2000 Salmonella isolates submitted to the animal arm of NARMS were submitted to VetNet in 2008 and the VetNet database was used by FSIS and the CDC to assist in the investigation of several Salmonella-related food-borne outbreaks. The results generated by these endeavors will enhance our knowledge of AR and provide the scientific data that is critically needed to direct research among the scientific community and develop policy in the USDA and FDA.


4.Accomplishments
1. Antimicrobial susceptibility testing of food-borne pathogens by the animal arm the National Antimicrobial Resistance Monitoring System (NARMS). Objective: To conduct antimicrobial susceptibility testing on Salmonella, Campylobacter, E. coli and Enterococcus from animal and environmental sources. Accomplishment: Since 1996, the animal arm of NARMS has been based in the USDA-ARS at the Richard B. Russell Center in Athens, GA. Salmonella was selected as the sentinel organism and antimicrobial resistance in over 50,000 Salmonella isolates has been determined. Campylobacter, generic E. coli and Enterococcus were added in subsequent years resulting in over 5,500, 15,000 and 8,200, respectively, antimicrobial susceptibility patterns for each of those bacteria. Veterinary Diagnostic Laboratories serve as diagnostic sentinel sites. Impact: This is the only national program for surveillance of resistant bacteria in animals in the U.S. and provides critical information regarding the prevalence and distribution of antimicrobial resistant bacteria in on-farm animals, from diagnostic submissions, and from raw product collected from federally inspected slaughter and processing plants. National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem Statement 1.1.5 Antibiotic Resistance.

2. Swine and dairy studies from the Collaboration in Animal Health Food Safety and Epidemiology (CAHFSE). Objective: To enhance overall understanding of pathogens that pose a food-safety risk and to routinely monitor critical diseases in food-animal production, USDA-ARS, APHIS, and FSIS collectively developed CAHFSE. The goal is to collect information on the prevalence of resistant bacteria and risk factors that may be used to develop mitigation strategies. From the APHIS National Animal Health Monitoring System (NAHMS) samples, a total of 7788 on-farm swine fecal samples from 130 farms were analyzed for Salmonella and about one-fourth of these were analyzed for Campylobacter, E. coli, and enterococci. From the APHIS dairy study, approximately 500 fecal and environmental samples were analyzed for Salmonella with 1/4 of these sampled for the other bacteria. The incidence of Salmonella, E. coli, and enterococci was consistent with previous years; the level of Campylobacter was almost 50% less than in previous years. The predominant Salmonella serotypes from swine samples were S. Derby, S. Typhimurium 5(-), S. Heidelberg, and, S. Mbandaka. Antimicrobial resistance testing and PFGE is being conducted. Results and ability to identify a mechanism for continued sample collection on farm will determine the direction that CAHFSE will pursue in coming years. The goal is to identify and implement mitigation strategies for animal health and food safety issues in a timely manner thereby averting adverse economic, animal well-being and public health consequences. Further, it will provide comprehensive science-based answers regarding animal health and public health, serving as a model for future surveillance and it will complement information obtained from both National Antimicrobial Resistance Monitoring System (NARMS) and USDA VetNet programs. National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem Area 1.1.2 Epidemiology.

3. Molecular typing of Salmonella and Campylobacter using pulsed-field gel electrophoresis (PFGE) by USDA VetNet. Objective: USDA VetNet was established in 2003 and was modeled after PulseNet USA, the national molecular subtyping network for food-borne disease surveillance. The objectives of USDA VetNet are to use PFGE to subtype zoonotic pathogens submitted to the animal arm of the National Antimicrobial Resistance Monitoring System (NARMS), compare USDA VetNet and PulseNet PFGE patterns, and to use the comparative data for surveillance and investigation of food-borne illness outbreaks. Whereas PulseNet subtypes seven food borne disease-causing bacteria: E. coli O157:H7, nontyphoidal Salmonella, Shigella, Listeria monocytogenes, Campylobacter, Yersinia pestis, and Vibrio cholerae, VetNet, at present, subtypes nontyphoidal Salmonella serotypes and Campylobacter from animals including diagnostic specimens, healthy farm animals, and carcasses of food-producing animals at slaughter. Accomplishment: VetNet has two functioning databases including the NARMS Salmonella and Campylobacter databases. The Salmonella database contains over 15,000 Salmonella isolates, while the Campylobacter database contains over 900 Campylobacter isolates. Both databases contain the PFGE Tagged Image File Format (TIFF) images, demographic information, and the antimicrobial resistance profiles assigned by NARMS. In the future, veterinary laboratories will be invited to participate in VetNet. Impact: The establishment of USDA VetNet enhances the mission of the agriculture and public health communities in surveillance and investigation of food borne illness outbreaks. National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem Statement 1.1.1 Methodology and 1.1.2 Epidemiology.

4. Development of microarrays for the detection of antimicrobial resistance genes in bacteria. Objective: Develop a technique for identifying and tracking the different genes responsible for antimicrobial resistance and virulence in bacteria. Accomplishment: A DNA microarray was developed to detect 775 resistance and virulence genes simultaneously. Impact: This technique has identify resistance and virulence genes in a variety of bacteria studied by the BEAR-RU, including Campylobacter, Salmonella, E. coli, Enterococcus, Staphylococcus (including MRSA), Listeria and Clostridium. This technique is used to determine the source, spread and epidemiology of these resistance genes, a fundamental component of the unit’s research. Analysis of bacteria collected by CAHFSE with this technique has identified common genes in different species of bacteria co-cultured from the same animal. This microarray is also being used by other scientists in ARS, FDA and research Universities to investigate antimicrobial resistance and to understand how to reduce its spread to bacteria in animal and human populations. National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem Statement 1.1.5 Antimicrobial Resistance.

5. Development of a rapid high-throughput molecular technique to determine the serotype of Salmonella enterica. Objective: Adapt the previously developed multiplex PCR Salmonella serotyping technique to a high-throughput platform. Accomplishment: The multiplex PCR assay can identify the top 31 serotypes which represent 75% of all clinically isolated Salmonella from humans and animals has been adapted to a high-throughput platform by incorporation of capillary analysis of the multiplex PCR products. This allows the determination of up to 90 isolates in a day with very little hands on time at a cost of $1.50/sample as compared to several days and ~$40.00 for traditional serotyping. Impact: The technique requires little training, no specific anti-sera, and works in standard DNA sequencing instruments. Futher, this technique could replace traditional serotyping for most Salmonella isolates implicated in foodborne outbreaks. The technique is currently being tested by several state public health laboratories in the US and also by the Public Health Agency of Canada. National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem Statement 1.1.1 Methodology.

6. Analysis of Salmonella enterica with reduced susceptibility to the 3rd-generation cephalosporin ceftriaxone isolated from U.S. cattle during 2000–2004. Objective: Previous studies had detected increased resistance to cephalosporins in Salmonella isolated from cattle. Therefore, a follow up study was done to characterize the increase in resistance. Accomplishment: Approximately 3,984 cattle isolates were assayed for resistance to Beta-lactams. Ninety-seven were found to have reduced susceptibility to ceftriaxone; however none were found to have an Extended Spectrum Beta-lactamase (ESBL) phenotype or to have genes encoding ESBL enzymes. Impact: ESBLs are a major problem in Europe and Asia; consequently, the lack of ESBLs in cattle isolates from the U.S. is a significant finding that can be used by veterinary drug manufacturers and animal producers to aide in the appropriate stewardship of antimicrobial use in animals. National Program 108 Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem Statement 1.1.2 Epidemiology and 1.1.5 Antibiotic Resistance.

7. Rapid multiplex PCR and Real Time TaqMan assays for detecting Salmonella and the highly virulent serovars Choleraesuis and Paratyphi C. Objective: Develop high-throughput techniques for rapid identification of Salmonella clones and highly virulent serotypes. Salmonella enterica serovars Choleraesuis (Cs) and Paratyphi C (Pc) are food borne pathogens that cause highly invasive infections. To prevent their transmission to humans, a rapid technique is needed to detect them in contaminated foods. Accomplishment: A multiplex polymerase chain reaction (mPCR) assay specific for Cs and Pc including a Salmonella species internal control was determined to be specific by screening over 100 Salmonella strains. The assay was adapted to Real-Time PCR and could detect as few as three colony forming units (CFU) in 10 grams of food in less than two days. Impact: This method can rapidly screen food for contamination with Salmonella Cs and Pc to prevent transmission to humans resulting in improved food safety and consumer confidence. National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem Statement 1.1.1 Methodology.

8. Analysis of Campylobacter jejuni whole genome DNA microarrays to identify gene differences for use in strain subtyping. Objective: Campylobacter jejuni is a common causative agent of bacterial gastroenteritis throughout the world. The development of improved molecular methods for tracing the sources of this ubiquitous pathogen is an essential component in controlling human illness caused by C. jejuni. Accomplishment: In this study, a whole genome DNA microarray typing tool called comparative genome indexing (CGI) was used in conjunction with statistical methods to compare discriminatory power between CGI, fla sequencing, and Pulsed-field Gel Electrophoresis (PFGE). CGI proved to be more discriminatory than the other two methods. Statistical analyses of the whole genome data identified 140 significant genes for use in differentiating C. jejuni isolates by host source and United States geographic region. Impact: Our results demonstrate the discriminatory power of CGI and illustrate that as a molecular subtyping tool for C. jejuni, CGI offers a highly effective and informative means of further understanding the epidemiology and population genetics of this ubiquitous pathogen. National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem Statement 1.1.1 Methodology.

9. A reduced gene set for microarray subyping of Campylobacter jejuni from cattle, chickens and humans. Objective: Campylobacter jejuni is a major cause of bacterial gastroenteritis worldwide. Improved methods for molecular typing of C. jejuni are needed to further our understanding of the epidemiology of this important foodborne pathogen. Accomplishment: A reduced set of genes identified from statistical analyses of whole-genome C. jejuni DNA microarrays was utilized for comparative genome indexing (CGI) and found to be sufficient to differentiate C. jejuni isolates from cattle, humans and chickens. A group of 131 geographically diverse C. jejuni strains were selected from a collection of cattle, chicken and human isolates. Analyses using the whole-genome and the reduced gene set showed that both methods differentiated all isolates as unique subtypes. However, unlike whole-genome CGI, the reduced gene set grouped all human C. jejuni strains in a single major cluster; cattle and chicken isolates were much less clonal by either CGI technique. Impact: The reduced gene set provided isolate discrimination equivalent to the whole-genome method but offers a simplified, more efficient and cost effective CGI technique for genotyping this major food-borne pathogen. National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem Statement 1.1.1 Methodology.

10. Antimicrobial resistance and virulence factors of Enterococcus faecalis isolated from retail food. Objective: The contribution of enterococci to food-borne illnesses via dissemination by retail food remains undefined. This study was conducted to determine prevalence and associations of antimicrobial resistance and virulence factors of Enterococcus faecalis isolated from retail food items. Accomplishment: While the highest rates of resistance were observed for lincomycin and bacitracin, low rates of resistance (<40%) were found for chloramphenicol, ciprofloxacin, erythromycin, gentamicin, nitrofurantoin, penicillin, and tylosin. A number of virulence determinants were present in the retail food enterococci including aggregation protein, toxins, and sex pheromones which facilitate the conjugation process. Statistical associations were found between some virulence factors and antimicrobial resistance. Impact: The presence of virulence determinants in enterococci from retail food suggests that enterococci from these sources may be more pathogenic than previously believed and may pose an increased hazard to humans susceptible to enterococcal infection. National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem Statement 1.1.5 Antibiotic Resistance.

11. Prevalence of antimicrobial resistant enterococci from dogs and cats. Objective: The contribution of dogs and cats as reservoirs of antimicrobial resistant enterococci remains largely undefined. This is increasingly important considering the possibility of transfer of bacteria from companion animals to the human host. In this study, dogs and cats from veterinary clinics were screened for the presence of enterococci. Accomplishment: A total of 420 enterococci were isolated from nasal, teeth, rectal, belly and hindquarter sites of 155 dogs and 121 cats. Of the animals, 80% of dogs and 60% of cats were positive for enterococci. The majority of positive samples were from the rectal, hindquarter, and belly areas. The highest levels of resistance was to ciprofloxacin in Enterococcus faecium, chloramphenicol resistance in E. faecalis and gentamicin resistance in E. faecalis all from dogs and nitrofurantoin resistance in E. faecium from cats. Multi-drug resistance (MDR) (resistance is greater than or equal to 2 antimicrobials) was observed with groups of isolates resistant to as few as two and as many as eight antimicrobials. Impact: Results from this study indicate that healthy dogs and cats are a source of antimicrobial resistant enterococci and may act as a reservoir of antimicrobial resistance that can be transferred to the human host. National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem Statement 1.1.2 Epidemiology.

12. Presence of a qnr-like gene in enterococci isolated from animals and foods conferring resistance to fluoroquinolones. Objective: Previous studies have found the presence of a homologue of the qnr gene in the genome of Enterococcus faecalis V583 and evaluated its role in the intrinsic resistance of enterococci to fluoroquinolones. In this study, enterococci from various animal and food sources that had shown resistance to ciprofloxacin by broth microdilution were examined for qnr1, qnr2, and qnrX (fluoroquinolone resistance genes) as well as a chloramphenicol acetyltransferase (CAT) gene. Accomplishment: From 2000-2007, enterococci were isolated from swine and cattle fecal samples on-farm, poultry carcass rinsates, fruits, vegetables, retail meats, and environmental sources. Ciprofloxacin resistant isolates were tested for qnr-like genes and CAT genes using PCR. Approximately 5.2% of the isolates contained qnr1, 4.9% had qnr2, 5.8% had qnrX, and none had the CAT gene. Impact: The intrinsic resistance of E. faecalis could be due to a qnr-like gene that may be transferred to other bacterial organisms increasing their resistances to fluoroquinolones. National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem Statement 1.1.5 Antibiotic Resistance.

13. Detection and prevalence of Methicillin-Resistant Staphylococcus aureus (MRSA) from retail meat. Objective: Recently, methicillin-resistant Staphylococcus aureus (MRSA) have been found in swine in a number of European countries. These MRSA have also been found in the swine farmers, their families, and veterinarians who have had contact with those farms and in retail pork products. The spread of MRSA originating from animals appears to be a source of MRSA in humans and may have the potential to threaten human health. Accomplishment: One hundred samples of retail pork and beef samples were collected and tested for the presence of MRSA. Three percent of retail pork and 4% of retail beef samples were positive for MRSA. Impact: Because none of these studies have been performed in the United States and the United States imports a number of swine from Canada, the extent of MRSA in swine and pork products as well as in the human population remains unknown. This information will be useful in evaluating the extent of MRSA from animal sources. National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem statement 1.1.2 Epidemiology.

14. Characterization of Methicillin-Resistant Staphylococcus aureus (MRSA) from companion animals. Objective: The contribution of companion animals as reservoirs of MRSA remains largely undefined. This is increasingly important considering the possibility of transfer of bacteria from companion animals to the human host. In this study, MRSA from companion dogs and cats were isolated and characterized. Accomplishment: MRSA were isolated from various sites on ill and healthy animals. All isolates were of the same staphylococcal chromosome cassette (SCC) mec type. Susceptibility of MRSA isolates was performed to determine the range of resistance and of the 18 antimicrobials tested, all exhibited resistance to the same nine drugs. Impact: MRSA causes severe to fatal infections among high risk populations and healthy individuals. Sources of community-acquired MRSA infections vary and the current study shows that companion animals may harbor the organism. National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem Statement 1.1.5 Antibiotic Resistance.

15. Development of a microarray for genotyping Listeria monocytogenes. Objective: A whole-genome DNA microarray was developed as a means of genotyping Listeria monocytogenes. Accomplishment: Listeria isolates were tested against a Listeria specific whole-genome DNA microarray. The whole-genome DNA microarray provided an efficient and effective means for genotyping and performing comparative genomics of Listeria species. Impact: Listeria monocytogenes is a common foodborne pathogen that exhibits a high mortality rate (> 25%). The whole-genome DNA array provides a method for genotyping L. monocytogenes to further understand the epidemiology, genetic basis of antimicrobial resistant strains, and comparative genomics between Listeria species. National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem Statement 1.1.1 Methodology.

16. Development of a multiplex PCR reaction for speciation of Listeria. Objective: To develop a multiplex PCR method was developed for rapid speciation of Listeria. Accomplishment: The multiplex reaction used conserved and variable regions of the iap gene to distinguish the six species of Listeria. The reaction produced distinct banding patterns that were easily interpreted. Impact: Listeria monocytogenes is a common foodborne pathogen that exhibits a high mortality rate (> 25%). Biochemical methods, such as API strips, can be costly, time-consuming, and prone to contamination. The speciation reaction is rapid (approximately 2 hours), less expensive, and can be highly effective, especially when combined with preliminary biochemical testing. National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem Statement 1.1.1 Methodology.

17. Determining the incidence of Clostridium difficile in swine and dairy herds: Objective: Clostridium difficile causes a severe colitis which is typically thought to be nosocomial. However, there is some indication that some portion of the infections may be community acquired. Fecal and environmental samples from the National Animal Health Monitoring System (NAHMS) swine and dairy samples were analyzed to determine incidence rate and to compare the strains from these sources to those causing human illness. Accomplishment: Approximately six percent of swine fecal and 1% of dairy environmental samples were found to contain C. difficile. Further studies are being conducted to determine the relatedness of these animal associated strains to human disease strains. Impact: If animal related strains are the same or closely related to human disease strains, there are potentially very great implications to human health. If they are not related, then the concerns being raised by public health agencies will be substantially alleviated. National Program 108-Food Safety, Component 1.1 Pathogens, Toxins and Chemical Contaminants Preharvest, Problem statement 1.1.2 Epidemiology.


5.Significant Activities that Support Special Target Populations
None.


6.Technology Transfer

Number of Non-Peer Reviewed Presentations and Proceedings2
Number of Other Technology Transfer1

Review Publications
Cox Jr, N.A., Richardson, L.J., Buhr, R.J., Northcutt, J.K., Bailey, J.S., Cray, P.J., Hiett, K.L. 2007. Recovery of Campylobacter and Salmonella serovars from the spleen, liver and gallbladder, and ceca of six and eight week old commercial broilers. Journal of Applied Poultry Research. 16(4):477-480.

Jenkins, M., Truman, C.C., Siragusa, G.R., Line, J.E., Bailey, J.S., Frye, J.G., Endale, D.M., Franklin, D.H., Schomberg, H.H., Fisher, D.S., Sharpe, R.R. 2008. Rainfall and tillage effects on transport of fecal bacteria and sex hormones 17ß-estradiol and testosterone from broiler litter applications to a Georgia Piedmont Ultisol. Science of the Total Environment. 403(1-3):154-163.

Line, J.E., Bailey, J.S., Berrang, M.E. 2008. Addition of sulfamethoxazole to selective media aids in the recovery of campylobacter spp. from broiler rinses. Journal of Rapid Methods and Automation in Microbiology. 16(1):2-12.

Hiett, K.L., Stern, N.J., Cray, P.J., Cox Jr, N.A., Seal, B.S. 2007. Molecular phylogeny of the flaa short variable region (svr) among campylobacter spp isolates collected during an annual evaluatoin of poultry flocks in the southeastern united states. Foodborne Pathogens and Disease. 4(3):339-347.

Bouldin, J.G., Morales, C., Frye, J.G., Gast, R.K., Musgrove, M.T. 2007. Detection of Salmonella enterica subpopulations by phenotype microarray antibiotic resistance patterns. Applied and Environmental Microbiology. 73(23):7753-7756.

Douris, A., Cray, P.J., Jackson, C.R. 2008. Characterization of salmonella enterica serovar agona slaughter isolates from the animal arm of the national antimicrobial resistance monitoring system - enteric bacteria (narms): 1997 through 2003. Microbial Drug Resistance. 14(1):55-63.

Douris, A., Cray, P.J., Jackson, C.R. 2007. Detection of Plasmids and Class 1 Integrons in Salmonella enterica serovar Agona Isolated from NARMS Slaughter Samples Collected in Years 1997 through 2003. Microbial Drug Resistance.13(3):212-219.

Wagner, B., Straw, B.E., Cray, P.J., Dargatz, D. 2008. Effect of antimicrobial dosage regimen on salmonella and escherichia coli isolats from feeder swine. Applied and Environmental Microbiology. 74(6):1731-1739

Jackson, C.R., Cray, P.J., Barrett, J.B., Hiott, L.M., Woodley, T.A. 2008. First report of vatB and vgaB from Enterococcus gallinarum in the USA.International Journal of Antimicrobial Agents. 31(2):175-187.

Mcgowan-Spicer, L., Cray, P.J., Frye, J.G., Meinersmann, R.J., Barrett, J.B., Jackson, C.R. 2008. Antimicrobial resistance and virulence of Enterococcus faecalis isolated from retail food. Journal of Food Protection. 71(4):760-769.

Lundin, J., Dargatz, D., Wagner, B., Lombard, J., Hill, A., Ladely, S.R., Cray, P.J. 2008. Antimicrobial Drug Resistance of Fecal Escherichia coli and Salmonella spp. Isolates from United States Dairy Cows. Foodborne Pathogens and Disease. 5(1):7-19.

Last Modified: 7/31/2014
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