Source: NORTH CAROLINA STATE UNIV submitted to NRP
BEST PRACTICES TO REDUCE SALMONELLA IN POULTRY
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1001528
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Oct 23, 2013
Project End Date
Sep 30, 2018
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
NORTH CAROLINA STATE UNIV
(N/A)
RALEIGH,NC 27695
Performing Department
Poultry Science
Non Technical Summary
Understanding the relationship between the chicken gut microbiota, diet composition - including prebiotics and probiotics, and resistance to Salmonella would be of particular interest to the poultry producers and consumers. We therefore plan to study and disseminate knowledge about the best practices for reducing the incidences of Salmonella in poultry and Salmonellosis in humans - caused by the consumption of poultry products including eggs. Our integrated approach will include the best practices for optimizing the chicken's gut microbiota via modulations of the dynamic relationship between prebiotics, probiotics and vaccines.
Animal Health Component
40%
Research Effort Categories
Basic
40%
Applied
40%
Developmental
20%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
7223210110050%
3153299101025%
3053299109025%
Goals / Objectives
Poultry products have been frequently implicated in reported cases of salmonellosis. The goal of this proposal is to develop and communicate a safe, effective and economic Salmonella control program for protecting the safety of the food supply and the health of consumers. To achieve this goal, the proposed studies will develop a novel Salmonella control strategy that promotes the establishment of an intestinal microbiota in the chicken that prevents colonization by pathogenic bacteria and enhances the mucosal immune response to Salmonella vaccination and challenge. Understanding the relationship between the chicken gut microbiota, diet composition - including prebiotics and probiotics, and resistance to Salmonella would be of particular interest to the poultry producers and consumers. We therefore plan to study and disseminate knowledge about the best practices for reducing the incidences of Salmonella in poultry and Salmonellosis in humans - caused by the consumption of poultry products including eggs. Our integrated approach will include the best practices for optimizing the chicken's gut microbiota via modulations of the dynamic relationship between prebiotics, probiotics and vaccines.
Project Methods
Experiment 1: Three hundred 1-day old pullets will be randomly assigned to one of 3 treatment groups (control, prebiotic, and Salmonella vaccine treatment) of 100 birds/group. Within each group, birds will be placed into one of 2 animal isolation chambers (50 birds/isolator). The control group will be fed a standard starter diet, the prebiotic group will be fed a diet supplemented with galactooligosaccharide (GOS, 1.0% w/w) to promote the growth of endogenous Firmicutes, while the vaccine group will receive 108 cfu/bird of an attenuated ST-vaccine by oral gavage. At 4 weeks of age one isolator/treatment group will be challenged with 105 cfu/bird of wild type Salmonella Enteriditis (SE) by oral gavage. To understand how promoting the growth of endogenous bacteria, or the introduction of live attenuated Salmonella vaccine strains affect the diversity of the microbiota, and how those changes are related to colonization by SE, cecal contents will be collected from 5 birds/treatment group at 0, 1, 2, 3, 4, 5, 6, 7, and 8 weeks and analyzed individually by bTEFAP (see Methods). In addition, the cecal content and sections of liver and spleen will be collected at 0, 1, 2, 3, 4, 5, 6, 7, and 8 weeks and analyzed for the presence of SE colonization of the gut (cecal contents) and invasion into the host (liver and spleen). Finally, based on the analysis of the data collected above cecal contents containing specific species found exclusively (or significantly enriched) in animals with the lowest SE colonization levels will be isolated, cultured and characterized for use in Experiment 2. Experiment 2: Four hundred 1-day old pullets will be randomly assigned to one of 4 treatment groups (control, prebiotic, commercial probiotic, candidate probiotic) of 100 birds/group. Within each group, birds will be placed into one of 2 animal isolation chambers (50 birds/isolator). As described above, the control group will be fed a standard starter diet, the prebiotic group will be fed a diet supplemented with GOS (1.0% w/w), the third group will be fed a diet supplemented with FM-B11 (IVS-Wynco LLC, Springdale, AR), a commercially available probiotic previously demonstrated to suppress colonization by SE (See Relevant Body of Knowledge), and the fourth group will receive 108 cfu/bird of the organisms identified in Expt 1 as being associated with decreased SE colonization. Methods: Animals: One-day old female W-36 pullets will be housed under ABLS-2 conditions, in HEAP filtered isolation chambers. These animal isolators have approximately 24 inches of feeder space, 2 nipple drinkers, and 864 sq in of floor space all of which meet or exceed the 2010 Federation of Animal Science Societies Guidelines for the care of laying hens up to 6 weeks of age. Chicks will have free access to food and water throughout the duration of the studies. At 0, 3, 7, 14, 21, 28, 31, 35, 42, and 49 days of age) 5 birds per treatment will be weighted, serum collected, and euthanized by CO2 (following approved methods in IACUC protocol), before the tissue samples/organs (liver, spleen, cecum, and crop wash) are collected for bacteriological, microbiota, and immunological analysis. Microbiome Analysis: Isolation of total DNA from cecal digesta will be carried out using a customized isolation protocol on a Qiagen BioRobot Universal and the Qiagen Blood and Tissue Isolation kit using a customized isolation protocol at the UNC Microbiome Core Facility. Approximately 100mg of sample will be resuspended in 100µl of 1X PBS with lysozyme and 200µl of ATL buffer in a 1.5ml microcentrifuge tube and incubated at 37°C for 30 minutes. Following the initial incubation, 20µl of proteinase K will be added and the mix will be incubated overnight at 56°C. Then tubes will be centrifuged at 800g for 5 minutes. The supernatant will be transferred to a Qiagen S-block and sonicated in a VWR B2500A sonicator for 30 minutes at 3 kHz and 65°C. Following the sonication step, the S-block will be transferred to the BioRobot Universal.The V1-V3 region of the bacterial 16S rDNA will be amplified using forward primer composed of the Roche Titanium Fusion Primer A (5'-CGTATCGCCTCCCTCGCGCCATCAG-3'), a 10 basepair MID barcode unique to each of the samples and the universal bacteria primer 27F (5'-AGAGTTTGATCCTGGCTCAG-3'). The reverse primer will be composed of the Roche Titanium Primer B (5'-CTATGCGCCTTGCCAGCCCGCTCAG-3') the identical 10 basepair MID as the forward primer and the reverse bacteria primer 338R (5'-TGCTGCCTCCCGTAGGAGT-3'). Each sample will be gel purified individually using the Qiagen Gel Extraction Kit and then pooled based on equal mass. The pooled 16S rDNA amplicons will be sequenced on a Roche GS FLX plus sequencer using the Titanium sequencing reagents and protocols. Chimeric sequences will be depleted from the trimmed data set using the Black Box Chimera Check (B2C2) tool. Culturing of cecal microbiota: Culturing of samples collected from chicken cecum samples will be carried out essentially as described by Goodman et al.. Freshly collected cecal samples will be transferred into an anaerobic chamber within 30 min of their collection and placed in prereduced PBS with 0.1% cysteine (PBSC). The sample material will be suspended by vortexing for 5 min, and the suspension will be allowed to stand at room temperature for 5 min to permit large insoluble particles to settle to the bottom of the tube. Dilutions of the supernatants will be plated onto prereduced TYG supplementedBrain-Heart-Infusion (BHI), and MRS media, and incubated for 7 days at 42C under an atmosphere of 75% N2, 20% CO2, and 5% H2. Colonies will be collected en masse into 10 ml of prereduced PBSC for preservation of the whole microbial community by adding prereduced glycerol containing 0.1% cysteine samples (final concentration of glycerol, 20%). Additionally, individual colonies will be picked and cultured under the above described conditions in TYGS, BHI, and/or MRS broth. Bacteriological Analysis: Samples of liver, spleen, cecal content, and crop wash will be collected at the specified sampling time points to enumerate viable Salmonella CFUs. The samples will be weighted and diluted 10-fold in PBS - pH 7.4. A Masticator (i.e., stomacher from NEUTEC Group, Inc.) will be used homogenize the samples. The samples will be decimally diluted in PBS buffer. Viable counts will be determined for each bird's organs by plating 0.1 ml aliquots of each dilution in duplicates on LB and XLT-4 media containing the appropriate antibiotics. Plates will be incubated overnight at 37o C before counting. Samples showing no viable counts on the first decimal dilution (i.e., <102 CFU/g) will be enriched overnight at 37oC in Tetrathionate Broth before streaking on XLT-4 agar plates containing the appropriate antibiotics. The presence of Salmonella in the different samples (i.e., from vaccinated and challenged birds) will be confirmed by VITEK®@ REF-21 341 (Biomerieux, Inc.), and published real-time PCR protocols. IgG and IgA titer determinations: Levels of anti-Salmonella IgG and IgA will be assessed in serum, and IgA in crop washes, and intestinal washes by indirect ELISA using killed/sonicated Salmonella cells as the coating antigen as previously described and using HRP labeled anti-chicken IgG or anti-chicken IgA to detect anti-Salmonella IgG and IgA, respectively. Statistical Analysis: Significant differences between the different treatment groups for the mean viable bacterial counts of the ST vaccine(S) and the Salmonella Challenge strains (i.e., WT Virulent S. Typhimurium and WT virulent S. Enteriditidis) in samples taken from the different Organs will be determine by analysis of variance (ANOVA) with Students's test. The limit of significance will be set to p<0.05.

Progress 10/01/17 to 09/30/18

Outputs
Target Audience:Poultry producers; Poultry Scientist; Poultry consumers; Regulatory agents; and The public at large Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?We provided training and professional development for 3 undergraduate students and one postdoctoral fellow. How have the results been disseminated to communities of interest?The results have been dissemenated via: 1- scientifis publication; 2- Presentations at scientific meetings and seminars; What do you plan to do during the next reporting period to accomplish the goals?We plan to: 1. continue the studies on the composition of the chicken gut microbiome 2. continue our studies on the use of Salmonella vaccines and Prebiotics.probiotics.

Impacts
What was accomplished under these goals? - We developed and patented an attenuated strain ofSalmonellato be used as vaccine. The strain is different from the current available vaccines. The authenticity and efficacy of the vaccine was first tested in the Mice model of Salmonellosis before it was successfully tested in poultry. - The complete genome of the patentedSalmonellavaccine strain was sequenced.

Publications

  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Hosni Hassan 12:22 PM (1 minute ago) to me M. Andrea Azcarate-Peril*, Natasha Butz, Maria Belen Cadenas, Matthew Koci, Anne Ballou, Mary Mendoza, Rizwana Ali, and Hosni Hassan* (2018). An attenuated Salmonella enterica Serovar Typhimurium strain and galacto-oligosaccharides accelerate clearance of Salmonella infections in poultry through modifications to the gut microbiome. Appl. Environ. Microbiol. 84: e02526-17  doi:10.1128/AEM.02526-17


Progress 10/01/16 to 09/30/17

Outputs
Target Audience:1. Poultry Science researchers 2. Microbiology and molecular biology researchers 3. Poultry Industry - Meat and Egg producers 4. Poultry consumers 5. The regulatory agents 6. The Scientific community at large Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?We continue to provide training and professional development for several undergraduate students, 4-H clubs, one graduate student, and postdoctoral fellows. How have the results been disseminated to communities of interest?Yes, our 4-H team in collaboration with the Kenan Institute Fellows developed and published a "Food Safety/Salmonella" curricula for K-12 and 4-H education settings. Also we published two scientific publication and presented seminars (2) and posters (2) at local and national meetings. What do you plan to do during the next reporting period to accomplish the goals?1. We will continue our studies on gut microbiota and its role in preventing Salmonella presence in poultry and poultry products. 2. We will continue the development of effective Salmonella Vaccines for poultry and Farm Animals. 3. We will continue the studies on the efficacy of the host-specific Lactobacilli on fighting Salmonella infections without the use of antibiotics.

Impacts
What was accomplished under these goals? Preventing Salmonella colonization in young birds is key to reducing contamination of poultry products for human consumption (eggs and meat). While several anti-Salmonella vaccines have been developed that are capable of yielding high systemic antibodies, it is not clear how effective these approaches are at controlling or preventing Salmonella colonization of the intestinal tract. Effective alternative control strategies are needed to help supplement the bird's ability to prevent Salmonella colonization, specifically by making the cecum less hospitable to Salmonella. In this study we investigated the effect the prebiotic galacto-oligosaccharide (GOS) has on cecal microbiome and ultimately the carriage of Salmonella. Day-old pullet chicks were fed control diets or diets supplemented with GOS (1 % w/w) and then challenged with a cocktail of Salmonella Typhimurium and S. Enteritidis. Changes in cecal tonsil gene expression, cecal microbiome, and levels of cecal and extraintestinal Salmonella were assessed at 1, 4, 7, 12, and 27 days post infection. While the Salmonella counts were generally lower in the GOS treated birds, the differences were not significantly different at the end of the experiment. However, the data demonstrated that treatment with the prebiotic GOS can modify both cecal tonsil gene expression and the cecal microbiome, suggesting that type of treatment may be useful as a tool for altering the carriage of Salmonella in poultry.

Publications

  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Allali, I., J.W. Arnold, J. Roach, M.B. Cadenas, N. Butz, H.M Hassan, M.D. Koci, A.L. Ballou, M. Mendoza, R. Ali, and M.A. Azcarate-Peril. (2017). A Comparison of sequencing platforms and bioinformatics pipelines for compositional analysis of the gut microbiome. BMC Microbiology 17:194 (doi: 10.1186/s12866-017-1101-8).
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Hughes,R-A., R.A. Ali, M.A. Mendoza, H.M. Hassan, and M.D. Koci (2017). Impact of dietary galacto-oligosaccharide (GOS) on chickens gut microbiota, mucosal gene expression, and Salmonella colonization. Frontiers in Veterinary Science Volume 4  article 192 (doi: 10.3389/fvets.2017.00192).


Progress 10/01/15 to 09/30/16

Outputs
Target Audience:1. The Scientific Community at large 2. Poultry Science 3. Poultry Producers (Meat & Eggs) 4. Poultry consumers 5. Regulatory Agents Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This Progect continues to provide training and professional development for several undergraduate students, one graduate student, and onepostdoctoral fellow. How have the results been disseminated to communities of interest?1. Scintific publications (6). 2. Presentations at local (2), National (2), and International (1) meetings. What do you plan to do during the next reporting period to accomplish the goals?1. Continue our studies on the gut microbiome and its relationsship to Salmonella infection/persistance in poultry. 2. We will study the effect of vaccination on the gut microbiome and Salmonella infection. 3. We will study the efficacy of the poultry-specific Lactobabacillus isolates, the we isolated, characterized, and sequenced as potential probiotic additives to fight Salmonella infection without the use of antibiotics.

Impacts
What was accomplished under these goals? We sequenced the genome of our patentend Salmonella strain we are using in our current studies. This gives us a complete understanding of the attenuated genes that make this strain a good vaccine strain. We isolated more than 100 potential probiotic lactic acid bacteria strains from the cecal content of chickens used in our studies. We studied the physilogy and metabolism of six of the Lactobacillus isolates. We sequenced the genomes of three unique isolates of the isolated Lactobacillus strain for use in future studies. Our collaborators, the Kenan institute and the 4-H team continue with their efforts to develop and revise the the "Foos Safety/Salmonella" curricula for K-12 and 4-H education setttings.

Publications

  • Type: Theses/Dissertations Status: Accepted Year Published: 2016 Citation: Daron, Caitlyn S. (2016). Characterization of Lactobacillus isolates from chickens
  • Type: Journal Articles Status: Accepted Year Published: 2016 Citation: Rezvani, M., M. Mendoza, M.D. Koci, C. Daron, J. Levy, and H.M. Hassan (2016). Draft Genome sequence of Lactobacillus crispatus C25 Isolated from Chicken Cecum. Genome Announc 4(6):e01223-16. doi:10.1128/genomeA.01223-16.
  • Type: Journal Articles Status: Accepted Year Published: 2016 Citation: Rezvani, M., M. Mendoza, M.D. Koci, C. Daron, J. Levy, and H.M. Hassan (2016). Draft Genome Sequences of Lactobacillus animalis P38 and Lactobacillus reuteri P43 Isolated from Chicken Cecum. Genome Announc 4(6):e01229-16. Doi: 10.1128/genomeA.01229-16.
  • Type: Journal Articles Status: Accepted Year Published: 2016 Citation: Troxell, B., R.C. Fink, A.N. Dickey, E.H. Scholl, and H.M. Hassan (2016) Complete Genome Sequence of NC983, a Live-Attenuated Strain of Salmonella enterica serovar Typhimurium. Genome Announc 4(5):e01074-16. doi: 10.1128/genomeA.01074-16.
  • Type: Book Chapters Status: Published Year Published: 2016 Citation: Troxell, B., and H.M. Hassan (2016). Interplay between Oxygen and Iron in Gene Expression: Environmental Sensing by FNR, ArcA, and Fur in Bacteria. Book Chapter In Stress and Environmental Control of Gene Expression in Bacteria; Frans J. De Bruijn, Editor. John Wiley & Sons.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Ballou, A.L., R.A. Ali, M.A. Mendoza, H.M. Hassan, W.J. Croom, and M.D. Koci (2016). Development of the chick microbiome: How early exposure influences future microbial diversity. Frontiers in Veterinary Science Volume 3  doi: 10:3389/fvets.2016.00002


Progress 10/01/14 to 09/30/15

Outputs
Target Audience:1. The Scientific community 2. Poultry producers (Meat & Eggs) 3. Poultry consumers Regulatory Agents Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project provides training and professional development for several undergraduate, graduate and postdoctoral students. In addition it provides training for 9 Kenan Fellows from K-12 School teachers. How have the results been disseminated to communities of interest?1. Scientific Publications 2. Presentations at local and national meetings What do you plan to do during the next reporting period to accomplish the goals?Continue our studies on the gut microbiome and its effect on Salmonella in poultry. We will finish the genomic sequences of Three Poultry-specific Lactobacillus (probiotic) isolates. We will feed these poultry probiotics to the chicken and study their effects on the microbiome and resistance to Salmonella challenges.

Impacts
What was accomplished under these goals? We identified the host immune responses towards Salmonella Vaccination and prebiotic (GOS) treatment. We isolated , purified and characterized six probiotic lactobacilli from the chicken ceca. Work on progress to sequence the genomes of representative isolates. In collaboration with the 4-H team, 9 Kenan Fellowsbcompleted the development of "Food Safety/Salmonella" curricula suitable for both formal (K-12) and non-formal (4-H) education settings. The Kenan Fellows completed the pre-pilot of their curricula in their classrooms and used the results along with guidance and suggestions from the curriculum advisory team to revise the curricula.

Publications

  • Type: Journal Articles Status: Accepted Year Published: 2015 Citation: Troxell, B., N. Petri, C. Daron, R. Pereira, M. Mendoza, H.M. Hassan, and M.D. Koci (2015). Poultry body temperature contributes to invasion control through reduced expression of Salmonella Pathogenicity Island -1 genes in Salmonella enterica serovars Typhimurium and Enteritidis. Appl. Environ. Microbiol. 81:8192-8201
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Caldwell, J. M., I. M. P�rez-D�az, K. P. Sandeep, J. Simunovic, K. Harris, J. Osborne, and H. M. Hassan. (2015). Mitochondrial DNA Fragmentation as a Molecular Tool to Monitor Plant-Derived, Low-Acid Thermal Processes. J. Food Sci. 80: 1804-1814  doi: 10.1111/1750-3841.12937
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Caldwell, J. M., I. M. P�rez-D�az, K. Harris, H. M. Hassan, J. Simunovic, and K. P. Sandeep (2015). Mitochondrial DNA Fragmentation to Monitor Processing Parameters in High Acid, Plant-Derived Foods. J. Food Sci. 80: 2892-2898 - doi:10.1111/1750-3841.13139
  • Type: Book Chapters Status: Published Year Published: 2015 Citation: Leite, M. C.T., Troxell, B., Bruno-B�rcena, J. M., and H. M. Hassan (2015). Biology of Reactive Oxygen Species, Oxidative Stress, and Antioxidants in Lactic Acid Bacteria. Chapter 14 (pp205-218). In Probiotics and Prebiotics: Current Research and Future Trends; Koen Venema and Ana Paula do Carmo, Eds.; Caister Academic Press.


Progress 10/23/13 to 09/30/14

Outputs
Target Audience: 1. The scientific community 2. Poultry producers (mear and Eggs) 3. Poultry consumers 4. Regulatory agents Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? This project provided training and professional development for two undergraduates and a postdoctoral fellow who participated in the studies. How have the results been disseminated to communities of interest? 1. Scientific publication 2. presentation at US Animal Health Annual meeting 3. Presentations at local and National Symposia What do you plan to do during the next reporting period to accomplish the goals? 1. Continue to study and analyze the gut microbiome and its effect on protecting the poultry products from salmonella contamination. We will test the effects of the different treatments on the persistance of Salmonella in the birds and eggs.

Impacts
What was accomplished under these goals? 1. We sequenced and mapped the microbiome of the chicken gut as a function of time (during 8 weeks). 2. we examined the effects of age, added prebiotic (GOS), and the use of Salmonella vaccine on the gut microflora. 3. The effects of changes in gut microflora on Salmonella infections are being studied.

Publications

  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Husain, M., J. Jones-Carson, L. Liu, M. Song, J. R. Saah, B. Troxell, M. Mendoza, H. Hassan, and A. V�zquez-Torres (2014). Ferric uptake regulator-dependent antinitrosative defenses in Salmonella pathogenesis. Infect. & Immun. 82: 333-340 (doi:10.1128/IAI.01201-13)
  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: H. M. Hassan. (2014). The Chicken Gut Microbiome and Salmonella. United State Animal Health Association  Annual Meeting, Arkansas, MO, October 21, 2014 (Invited Presentation)