Effect of β-Alanine Metabolite on Gut Integrity and Immunity in Commercial Broiler Chickens Infected with Eimeria maxima
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Experiment 1: In Vitro Study
2.1.1. Anticoccidial Assay
2.1.2. Culture of Epithelial Chicken Cell Line (IEC) and Chicken Macrophage Cell Line (CMC)
2.1.3. Quail Muscle Cell (QMC) Culture
2.1.4. Primary Chicken Embryonic Muscle Cell (PMC) Culture
2.1.5. Reverse Transcription for PCR
2.1.6. Analysis of Cytokines, Tight Junction Proteins, and Muscle Cell Growth Markers Using qRT-PCR
2.2. Experiment 2: In Vivo Study
2.2.1. Chickens and Experimental Design
2.2.2. Determination of Body Weight
2.2.3. Oral Infection with E. maxima
2.2.4. Collection of Intestinal Samples
2.2.5. Jejunal Lesion Scoring
2.2.6. Fecal Oocyst Shedding
2.2.7. RNA Isolation and Reverse Transcription from Jejunal Samples
2.2.8. Gene Expression Analysis via qRT-PCR
2.2.9. Statistical Analysis
3. Results
3.1. Experiment 1
3.1.1. Anti-Coccidial Activity against Sporozoites of E. maxima
3.1.2. Effects of β-Alanine on Chicken Intestinal Epithelial Cells and Chicken Macrophage Cells
3.1.3. Effects of β-Alanine on the Proliferation and Differentiation of Quail Muscle Cells and Primary Chicken Embryonic Muscle Cells
3.2. Experiment 2
3.2.1. Growth of Chickens
3.2.2. Intestinal Lesion Scores and Fecal Oocyst Shedding
3.2.3. Pro-Inflammatory Cytokines
3.2.4. Th1 Cytokines
3.2.5. Tight Junction Proteins
3.2.6. Nutrient Transporters
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Stanton, T.B. A call for antibiotic alternatives research. Trends Microbiol. 2013, 21, 111–113. [Google Scholar] [CrossRef]
- Oviedo-Rondón, E.O. Holistic view of intestinal health in poultry. Anim. Feed Sci. Technol. 2019, 250, 1–8. [Google Scholar] [CrossRef]
- Santos, R.R.; Velkers, F.C.; Vernooij, J.C.M.; Star, L.; Heerkens, J.L.T.; van Harn, J.; de Jong, I.C. Nutritional interventions to support broiler chickens during Eimeria infection. Poult. Sci. 2022, 101, 101853. [Google Scholar] [CrossRef] [PubMed]
- Pan, D.; Yu, Z. Intestinal microbiome of poultry and its interaction with host and diet. Gut Microbes 2013, 5, 108–119. [Google Scholar] [CrossRef] [PubMed]
- Kiela, P.R.; Ghishan, F.K. Physiology of intestinal absorption and secretion. Best Pract. Res. Clin. Gastroenterol. 2016, 30, 145–159. [Google Scholar] [CrossRef]
- Adedokun, S.A.; Olojede, O.C. Optimizing gastrointestinal integrity in poultry: The role of nutrients and feed additives. Front. Vet. Sci. 2019, 5, 348. [Google Scholar] [CrossRef] [PubMed]
- Richards, M.P.; Proszkowiec-Weglarz, M. Mechanisms regulating feed intake, energy expenditure, and body weight in poultry. Poult. Sci. 2007, 86, 1478–1490. [Google Scholar] [CrossRef]
- Wlaźlak, S.; Pietrzak, E.; Biesek, J.; Dunislawska, A. Modulation of the immune system of chickens a key factor in maintaining poultry production—A review. Poult. Sci. 2023, 102, 102785. [Google Scholar] [CrossRef]
- Salminen, S.; Nurmi, J.; Gueimonde, M. The genomics of probiotic intestinal microorganisms. Genome Biol. 2005, 6, 225. [Google Scholar] [CrossRef]
- Lay, J.O.; Liyanage, R.; Borgmann, S.; Wilkins, C.L. Problems with the “omics”. Trends Anal. Chem. 2006, 25, 1046–1056. [Google Scholar] [CrossRef]
- Veenstra, T.D. Metabolomics: The final frontier? Genome Med. 2012, 4, 40. [Google Scholar] [CrossRef] [PubMed]
- Rattray, N.J.W.; Deziel, N.C.; Wallach, J.D.; Khan, S.A.; Vasiliou, V.; Ioannidis, J.P.A.; Johnson, C.H. Beyond genomics: Understanding exposotypes through metabolomics. Hum. Genom. 2018, 12, 4. [Google Scholar] [CrossRef] [PubMed]
- Caesar, L.K.; Montaser, R.; Keller, N.P.; Kelleher, N.L. Metabolomics and genomics in natural products research: Complementary tools for targeting new chemical entities. Nat. Prod. Rep. 2021, 38, 2041–2065. [Google Scholar] [CrossRef] [PubMed]
- Lin, L.; Zhang, J. Role of intestinal microbiota and metabolites on gut homeostasis and human diseases. BMC Immunol. 2017, 18, 2. [Google Scholar] [CrossRef]
- Oliphant, K.; Allen-Vercoe, E. Macronutrient metabolism by the human gut microbiome: Major fermentation by-products and their impact on host health. Microbiome 2019, 7, 91. [Google Scholar] [CrossRef]
- Bi, C.; Xiao, G.; Liu, C.; Yan, J.; Chen, J.; Si, W.; Zhang, J.; Liu, Z. Molecular immune mechanism of intestinal microbiota and their metabolites in the occurrence and development of liver cancer. Front. Cell Dev. Biol. 2021, 9, 702414. [Google Scholar] [CrossRef]
- Park, I.; Lee, Y.; Goo, D.; Zimmerman, N.P.; Smith, A.H.; Rehberger, T.; Lillehoj, H.S. The effects of dietary Bacillus subtilis supplementation, as an alternative to antibiotics, on growth performance, intestinal immunity, and epithelial barrier integrity in broiler chickens infected with Eimeria maxima. Poult. Sci. 2020, 99, 725–733. [Google Scholar] [CrossRef]
- Park, I.; Zimmerman, N.P.; Smith, A.H.; Rehberger, T.G.; Lillehoj, E.P.; Lillehoj, H.S. Dietary supplementation with Bacillus subtilis direct-fed microbials alters chicken intestinal metabolite levels. Front. Vet. Sci. 2020, 7, 123. [Google Scholar] [CrossRef]
- Sale, C.; Saunders, B.; Harris, R.C. Effect of beta-alanine supplementation on muscle carnosine concentrations and exercise performance. Amino Acids 2010, 39, 321–333. [Google Scholar] [CrossRef]
- Son, D.O.; Satsu, H.; Kiso, Y.; Totsuka, M.; Shimizu, M. Inhibitory effect of carnosine on interleukin-8 production in intestinal epithelial cells through translational regulation. Cytokine 2008, 42, 265–276. [Google Scholar] [CrossRef]
- Tomonaga, S.; Matsumoto, M.; Furuse, M. β-alanine enhances brain and muscle carnosine levels in broiler chicks. Poult. Sci. J. 2012, 49, 308–312. [Google Scholar] [CrossRef]
- Kralik, G.; Sak-Bosnar, M.; Kralik, Z.; Galović, O. Effects of β-alanine dietary supplementation on concentration of carnosine and quality of broiler muscle tissue. Poult. Sci. J. 2014, 51, 151–156. [Google Scholar] [CrossRef]
- Fresta, C.G.; Fidilio, A.; Lazzarino, G.; Musso, N.; Grasso, M.; Merlo, S.; Amorini, A.M.; Bucolo, C.; Tavazzi, B.; Lazzarino, G.; et al. Modulation of pro-oxidant and pro-inflammatory activities of M1 macrophages by the natural dipeptide carnosine. Int. J. Mol. Sci. 2020, 21, 776. [Google Scholar] [CrossRef] [PubMed]
- Kim, W.H.; Lillehoj, H.S.; Min, W. Evaluation of the immunomodulatory activity of the chicken NK-lysin-derived peptide cNK-2. Sci. Rep. 2017, 7, 45099. [Google Scholar] [CrossRef]
- Park, I.; Oh, S.; Goo, D.; Celi, P.; Lillehoj, H.S. Effect of dietary sophorolipids on growth performance and gastrointestinal functionality of broiler chickens infected with Eimeria maxima. Poult. Sci. 2022, 101, 101944. [Google Scholar] [CrossRef]
- Shin, S.; Choi, Y.M.; Suh, Y.; Lee, K. Delta-like 1 homolog (DLK1) inhibits proliferation and myotube formation of avian QM7 myoblasts. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2015, 179, 37–43. [Google Scholar] [CrossRef]
- Park, I.; Nam, H.; Wickramasuriya, S.S.; Lee, Y.; Wall, E.H.; Ravichandran, S.; Lillehoj, H.S. Host-mediated beneficial effects of phytochemicals for prevention of avian coccidiosis. Front. Immunol. 2023, 14, 1145367. [Google Scholar] [CrossRef]
- Hassan, A.; Ahn, J.; Suh, Y.; Choi, Y.M.; Chen, P.; Lee, K. Selenium promotes adipogenic determination and differentiation of chicken embryonic fibroblasts with regulation of genes involved in fatty acid uptake, triacylglycerol synthesis and lipolysis. J. Nutr. Biochem. 2014, 25, 858–867. [Google Scholar] [CrossRef]
- Lee, Y.; Park, I.; Lillehoj, H.S. Oral administration of chicken NK-lysin or recombinant chicken IL-7 improves vaccine efficacy of Eimeria tenella elongation factor-1α (EF-1α) against coccidiosis in commercial broiler chickens. Poult. Sci. 2023, 102, 102611. [Google Scholar] [CrossRef]
- Choi, Y.M.; Suh, Y.; Shin, S.; Lee, K. Skeletal muscle characterization of japanese quail line selectively bred for lower body weight as an avian model of delayed muscle growth with hypoplasia. PLoS ONE 2014, 9, e95932. [Google Scholar] [CrossRef]
- Haug, A.; Thebo, P.; Mattsson, J.G. A simplified protocol for molecular identification of Eimeria species in field samples. Vet. Parasitol. 2007, 146, 35–45. [Google Scholar] [CrossRef] [PubMed]
- Lillehoj, H.S.; Lee, S.H.; Park, S.S.; Jeong, M.; Lim, Y.; Mathis, G.F.; Lumpkins, B.; Chi, F.; Ching, C.; Cravens, R.L. Calcium montmorillonite-based dietary supplement attenuates necrotic enteritis induced by Eimeria maxima and Clostridium perfringens in broilers. Poult. Sci. J. 2016, 53, 329–340. [Google Scholar] [CrossRef] [PubMed]
- Lee, Y.; Park, I.; Wickramasuriya, S.S.; Ben Arous, J.; Koziol, M.E.; Lillehoj, H.S. Co-administration of chicken IL-7 or NK-lysin peptide 2 enhances the efficacy of Eimeria elongation factor-1α vaccination against Eimeria maxima infection in broiler chickens. Poult. Sci. 2022, 101, 102013. [Google Scholar] [CrossRef] [PubMed]
- Cao, Y.; Liu, S.; Liu, K.; Abbasi, I.H.R.; Cai, C.; Yao, J. Molecular mechanisms relating to amino acid regulation of protein synthesis. Nutr. Res. Rev. 2019, 32, 183–191. [Google Scholar] [CrossRef]
- Rezende, N.S.; Swinton, P.; de Oliveira, L.F.; da Silva, R.P.; da Eira Silva, V.; Nemezio, K.; Yamaguchi, G.; Artioli, G.G.; Gualano, B.; Saunders, B.; et al. The muscle carnosine response to beta-alanine supplementation: A systematic review with bayesian individual and aggregate data e-max model and meta-analysis. Front. Physiol. 2020, 11, 913. [Google Scholar] [CrossRef]
- Perim, P.; Marticorena, F.M.; Ribeiro, F.; Barreto, G.; Gobbi, N.; Kerksick, C.; Dolan, E.; Saunders, B. Can the skeletal muscle carnosine response to beta-alanine supplementation be optimized? Front. Nutr. 2019, 6, 135. [Google Scholar] [CrossRef]
- Qi, B.; Wang, J.; Ma, Y.B.; Wu, S.G.; Qi, G.H.; Zhang, H.J. Effect of dietary β-alanine supplementation on growth performance, meat quality, carnosine content, and gene expression of carnosine-related enzymes in broilers. Poult. Sci. 2018, 97, 1220–1228. [Google Scholar] [CrossRef]
- Lackner, J.; Albrecht, A.; Mittler, M.; Marx, A.; Kreyenschmidt, J.; Hess, V.; Sauerwein, H. Effect of feeding histidine and β-alanine on carnosine concentration, growth performance, and meat quality of broiler chickens. Poult. Sci. 2021, 100, 101393. [Google Scholar] [CrossRef]
- Chen, L.; Zhong, Y.; Ouyang, X.; Wang, C.; Yin, L.; Huang, J.; Li, Y.; Wang, Q.; Xie, J.; Huang, P.; et al. Effects of β-alanine on intestinal development and immune performance of weaned piglets. Anim. Nutr. 2023, 12, 398–408. [Google Scholar] [CrossRef]
- Teng, P.Y.; Choi, J.; Tompkins, Y.; Lillehoj, H.; Kim, W. Impacts of increasing challenge with Eimeria maxima on the growth performance and gene expression of biomarkers associated with intestinal integrity and nutrient transporters. Vet. Res. 2021, 52, 81. [Google Scholar] [CrossRef]
- Wickramasuriya, S.S.; Park, I.; Lee, Y.; Richer, L.M.; Przybyszewski, C.; Gay, C.G.; van Oosterwijk, J.G.; Lillehoj, H.S. Orally delivered Bacillus subtilis expressing chicken NK-2 peptide stabilizes gut microbiota and enhances intestinal health and local immunity in coccidiosis-infected broiler chickens. Poult. Sci. 2023, 102, 102590. [Google Scholar] [CrossRef] [PubMed]
- Goo, D.; Choi, J.; Ko, H.; Choppa, V.S.R.; Liu, G.; Lillehoj, H.S.; Kim, W.K. Effects of Eimeria maxima infection doses on growth performance and gut health in dual-infection model of necrotic enteritis in broiler chickens. Front. Physiol. 2023, 14, 1269398. [Google Scholar] [CrossRef]
- Klasing, K.C. Nutrition and the immune system. Br. Poult. Sci. 2007, 48, 525–537. [Google Scholar] [CrossRef] [PubMed]
- Broom, L.J.; Kogut, M.H. Inflammation: Friend or foe for animal production? Poult. Sci. 2018, 97, 510–514. [Google Scholar] [CrossRef]
- Vermette, D.; Hu, P.; Canarie, M.F.; Funaro, M.; Glover, J.; Pierce, R.W. Tight junction structure, function, and assessment in the critically ill: A systematic review. Intensive Care Med. Exp. 2018, 6, 37. [Google Scholar] [CrossRef] [PubMed]
- Edelblum, K.L.; Turner, J.R. The tight junction in inflammatory disease: Communication breakdown. Curr. Opin. Pharmacol. 2009, 9, 715–720. [Google Scholar] [CrossRef]
- Ni, Y.; Teng, T.; Li, R.; Simonyi, A.; Sun, G.Y.; Lee, J.C. TNFα alters occludin and cerebral endothelial permeability: Role of p38MAPK. PLoS ONE 2017, 12, e0170346. [Google Scholar] [CrossRef]
- Li, G.; Li, Z.; Liu, J. Amino acids regulating skeletal muscle metabolism: Mechanisms of action, physical training dosage recommendations and adverse effects. Nutr. Metab. 2024, 21, 41. [Google Scholar] [CrossRef]
- Zhang, S.; Zeng, X.; Ren, M.; Mao, X.; Qiao, S. Novel metabolic and physiological functions of branched chain amino acids: A review. J. Anim. Sci. Biotechnol. 2017, 8, 10. [Google Scholar] [CrossRef]
- Criado-Mesas, L.; Abdelli, N.; Noce, A.; Farré, M.; Pérez, J.F.; Solà-Oriol, D.; Martin-Venegas, R.; Forouzandeh, A.; González-Solé, F.; Folch, J.M. Transversal gene expression panel to evaluate intestinal health in broiler chickens in different challenging conditions. Sci. Rep. 2021, 11, 6315. [Google Scholar] [CrossRef]
- Stevens, B.R. Amino acid transport by epithelial membranes. In Epithelial Transport Physiology; Gerenscer, G.A., Ed.; Springer Nature Publishing: New York, NY, USA, 2010; pp. 353–378. [Google Scholar]
- Dave, M.H.; Schulz, N.; Zecevic, M.; Wagner, C.A.; Verrey, F. Expression of heteromeric amino acid transporters along the murine intestine. J. Physiol. 2004, 558, 597–610. [Google Scholar] [CrossRef]
Type | Target Gene | Samples | Primer Sequence (5′-3′) | Accession Number or References |
---|---|---|---|---|
Reference | GAPDH | F-GGTGGTGCTAAGCGTGTTAT | K01458 | |
R-ACCTCTGCCATCTCTCCACA | ||||
Proinflammatory | IL-1β | CMCs and Jejunum | F-TGGGCATCAAGGGCTACA | Y15006 |
R-TCGGGTTGGTTGGTGATG | ||||
IL-6 | CMCs and Jejunum | F-CAAGGTGACGGAGGAGGAC | AJ309540 | |
R-TGGCGAGGAGGGATTTCT | ||||
IL-8 | CMCs and Jejunum | F-GGCTTGCTAGGGGAAATGA | AJ009800 | |
R-AGCTGACTCTGACTAGGAAACTGT | ||||
TNFSF15 | Jejunum | F-CCTGAGTATTCCAGCAACGCA | AB194710 | |
R-ATCCACCAGCTTGATGTCACTAAC | ||||
Th | IFN-γ | Jejunum | F-AGCTGACGGTGGACCTATTATT | NM_205149 |
R-GGCTTTGCGCTGGATTC | ||||
IL-10 | Jejunum | F-CGGGAGCTGAGGGTGAA | AJ621614 | |
R-GTGAAGAAGCGGTGACAGC | ||||
TJ proteins | Claudin-1 | Jejunum | F-TGGAGGATGACCAGGTGAAGA | NM_001013611.2 |
R-CGAGCCACTCTGTTGCCATA | ||||
Claudin-2 | Jejunum | F-CCTGCTCACCCTCATTGGAG | NM_001277622.1 | |
R-GCTGAACTCACTCTTGGGCT | ||||
JAM-2 | Jejunum | F-AGCCTCAAATGGGATTGGATT | NM_001006257.1 | |
R-CATCAACTTGCATTCGCTTCA | ||||
Occludin | IECs and jejunum | F-GAGCCCAGACTACCAAAGCAA | NM205,128.1 | |
R-GCTTGATGTGGAAGAGCTTGTTG | ||||
ZO-1 | IECs and jejunum | F-CCGCAGTCGTTCACGATCT | XM01,527,8981.1 | |
R-GGAGAATGTCTGGAATGGTCTGA | ||||
ZO-2 | Jejunum | F-ATCCAAGAAGGCACCTCAGC | NM_204918.1 | |
R-CATCCTCCCGAACAATGC | ||||
Mucin | MUC2 | IECs | F: GCCTGCCCAGGAAATCAAG | NM0,013,18434.1 |
R: CGACAAGTTTGCTGGCACAT | ||||
Muscle cell | MyoG | QMCs and PMCs | F-CTGCCCAAGGTGGAGATCCT | Choi et al. [30] |
R-CTGGAGTTTGGCACCAACCC | ||||
Pax7 | QMCs and PMCs | F- TCGATTAGCCGTGTGCTACG | NM_205065.1 | |
R-GCCATCTATGCTGTGCTTGG | ||||
Nutrient transports | BAT1 | Jejunum | F-GGGTTTTGTGTTGGCTTAGGAA | XM_419056.6 |
R-TCCATGGCTCTGGCAGAGAT | ||||
B0AT | Jejunum | F-CAGTAGTGAATTCTCTGAGTGTGAAGCT | NM_001199133.1 | |
R-GCAATGATTGCCACAACTACCA | ||||
CAT1 | Jejunum | F-CCAAGCACGCTGATAAAG | XM_015277945.2 | |
R-TACTCACAATAGGAAGAAGGG | ||||
EAAT | Jejunum | F-TGCTGCTTTGGATTCCAGTGT | XM_424930.6 | |
R-AGCAATGACTGTAGTGCAGAAGTAATATATG | ||||
GLUT1 | Jejunum | F-CTTTGTCAACCGCTTTGG | NM_205209.1 | |
R-TGTGCCCCGGAGCTTCT | ||||
GLUT2 | Jejunum | F-TCATTGTAGCTGAGCTGTT | NM_207178.1 | |
R-CGAAGACAACGAACACATAC | ||||
GLUT5 | Jejunum | F-TTGCTGGCTTTGGGTTGTG | XM_417596.6 | |
R-GGAGGTTGAGGGCCAAAGTC | ||||
LAT1 | Jejunum | F-GATTGCAACGGGTGATGTGA | NM_001030579.2 | |
R-CCCCACACCCACTTTTGTTT | ||||
LAT2 | Jejunum | F-TCAGCTTCAGTTACTGGTT | XM_025154295.1 | |
R-GCACAACCACGAGAAATAC | ||||
SGLT | Jejunum | F-GCCGTGGCCAGGGCTTA | NM_001293240.1 | |
R-CAATAACCTGATCTGTGCACCAGT |
Ingredients (%) | Basal Diet |
---|---|
Corn | 55.78 |
Soybean meal | 37.03 |
Soybean oil | 2.97 |
Dicalcium phosphate | 1.80 |
Calcium carbonate | 1.51 |
Salt | 0.38 |
Poultry Vit Mix 1 | 0.22 |
Poultry Mineral Mix 2 | 0.15 |
DL-Methionine | 0.10 |
Choline-chloride, 60% | 0.06 |
Total | 100 |
Calculated values (%) | |
CP, % | 24.00 |
Ca, % | 1.20 |
AP, % | 0.51 |
Lys, % | 1.40 |
Met, % | 0.49 |
Cys + Met, % | 0.80 |
ME, Mcal/kg | 3.5 |
Treatment | NC | PC | H-ALA | L-ALA | SEM | p-Value |
---|---|---|---|---|---|---|
BW, g | ||||||
Initial | 36.6 | 36.6 | 36.6 | 36.6 | 0.7 | 1.000 |
d 7 | 157 | 159 | 160 | 160 | 2.5 | 0.822 |
d 14 (0 dpi) | 461 | 457 | 464 | 475 | 8.1 | 0.448 |
d 20 (6 dpi) | 860 a | 743 b | 738 b | 764 b | 16 | <0.001 |
d 22 (8 dpi) | 1017 a | 763 c | 843 b | 839 b | 22 | <0.001 |
ADG, g | ||||||
d 0 to 7 | 20.0 | 20.4 | 20.6 | 20.6 | 0.3 | 0.475 |
d 7 to 14 | 43.5 | 41.9 | 43.5 | 45.1 | 0.9 | 0.109 |
d 0 to 14 1 | 32.7 | 32.2 | 32.9 | 33.8 | 0.6 | 0.291 |
d 14 to 20 | 66.5 a | 47.7 b | 45.5 b | 47.2 b | 1.6 | <0.001 |
d 14 to 22 2 | 69.4 a | 38.2 c | 47.3 b | 43.3 b | 1.7 | <0.001 |
NC | PC | H-ALA | L-ALA | SEM | p-Value | |
---|---|---|---|---|---|---|
Nutrient transporters, mean normalized expression | ||||||
BAT1 | 0.43 a | 0.13 c | 0.29 b | 0.16 c | 0.04 | 0.001 |
B0AT1 | 0.074 a | 0.027 c | 0.053 ab | 0.035 bc | 0.009 | 0.008 |
CAT1 | 0.031 | 0.016 | 0.033 | 0.021 | 0.008 | 0.380 |
EAAT | 0.041 | 0.034 | 0.034 | 0.035 | 0.009 | 0.940 |
GLUT1 | 0.0057 a | 0.0013 b | 0.0033 ab | 0.0014 b | 0.001 | 0.011 |
GLUT2 | 0.022 a | 0.007 b | 0.008 b | 0.008 b | 0.004 | 0.023 |
GLUT5 | 0.073 a | 0.016 b | 0.038 b | 0.035 b | 0.010 | 0.007 |
LAT1 | 0.070 a | 0.015 c | 0.05 ab | 0.03 bc | 0.009 | 0.004 |
LAT2 | 0.0072 a | 0.0014 b | 0.0050 a | 0.0018 b | 0.001 | 0.001 |
SGLT | 0.14 | 0.11 | 0.12 | 0.12 | 0.03 | 0.963 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Park, I.; Nam, H.; Lee, Y.; Smith, A.; Rehberger, T.; Lillehoj, H. Effect of β-Alanine Metabolite on Gut Integrity and Immunity in Commercial Broiler Chickens Infected with Eimeria maxima. Animals 2024, 14, 2558. https://doi.org/10.3390/ani14172558
Park I, Nam H, Lee Y, Smith A, Rehberger T, Lillehoj H. Effect of β-Alanine Metabolite on Gut Integrity and Immunity in Commercial Broiler Chickens Infected with Eimeria maxima. Animals. 2024; 14(17):2558. https://doi.org/10.3390/ani14172558
Chicago/Turabian StylePark, Inkyung, Hyoyoun Nam, Youngsub Lee, Alexandra Smith, Thomas Rehberger, and Hyun Lillehoj. 2024. "Effect of β-Alanine Metabolite on Gut Integrity and Immunity in Commercial Broiler Chickens Infected with Eimeria maxima" Animals 14, no. 17: 2558. https://doi.org/10.3390/ani14172558