Effects of the In ovo Administration of L-Ascorbic Acid on Tissue L-Ascorbic Acid Concentrations, Systemic Inflammation, and Tracheal Histomorphology of Ross 708 Broilers Subjected to Elevated Levels of Atmospheric Ammonia †
Abstract
:1. Introduction
2. Materials and Methods
2.1. Egg Incubation
2.2. Posthatch Experimental Design and Atmospheric Ammonia Exposure
2.3. Eye and Liver L-Ascorbic Acid Concentrations
2.4. Plasma NO, Calcium, and Trace Mineral Analyses
2.5. Histopathologic Examination
2.6. Statistical Analysis
3. Results
3.1. Concentrations of Eye and Liver L-AA, and Plasma NO, Ca, Cu, and Zn
3.2. Tracheal Histomorphology
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Williams, C.J. In ovo vaccination and chick quality. Int. Hatch. Pract. 2011, 19, 7–13. [Google Scholar]
- Avakian, A.P. Understanding in ovo vaccination. Int. Hatch. Pract. 2006, 20, 15–17. [Google Scholar]
- Williams, C.J. In ovo vaccination for disease prevention. Int. J. Poult. Sci. 2007, 15, 7–9. [Google Scholar]
- Zhang, H.; Elliott, K.E.C.; Durojaye, O.A.; Fatemi, S.A.; Peebles, E.D. Effects of in ovo-administration of L-ascorbic acid on broiler hatchability and its influence on the effects of pre-placement holding time on broiler quality characteristics. Poult. Sci. 2018, 97, 1941–1947. [Google Scholar] [CrossRef] [PubMed]
- Fatemi, S.A.; Elliott, K.E.C.; Bello, A.; Durojaye, O.; Zhang, H.; Turner, B.; Peebles, E.D. Effects of source and level of in ovo-injected vitamin D3 on the hatchability and serum 25-hydroxycholecalciferol concentrations of Ross 708 broilers. Poult. Sci. 2020, 99, 3877–3884. [Google Scholar] [CrossRef]
- Mousstaaid, A.; Fatemi, S.A.; Elliott, K.E.C.; Alqhtani, A.H.; Peebles, E.D. Effects of the in ovo injection of L-ascorbic acid on broiler hatching performance. Animal 2022, 12, 1020. [Google Scholar] [CrossRef]
- Mousstaaid, A.; Fatemi, S.A.; Elliott, K.E.C.; Levy, A.W.; Miller, W.W.; Gerard, P.D.; Alqhtani, A.H.; Peebles, E.D. Effects of the in ovo and dietary supplementation of L-ascorbic acid on the growth performance, inflammatory response, and eye L-ascorbic acid concentrations in Ross 708 broiler chickens. Animal 2022, 12, 2573. [Google Scholar] [CrossRef]
- Zhang, H.; Elliott, K.E.C.; Durojaye, O.A.; Fatemi, S.A.; Schilling, M.W.; Peebles, E.D. Effects of in ovo injection of L-ascorbic acid on growth performance, carcass composition, plasma antioxidant capacity, and meat quality in broiler chickens. Poult. Sci. 2019, 98, 3617–3625. [Google Scholar]
- Fatemi, S.A.; Elliott, K.E.C.; Bello, A.; Durojaye, O.; Zhang, H.; Turner, B.; Peebles, E.D. The effects of in ovo-injected vitamin D3 sources on the eggshell temperature and early post-hatch performance of Ross 708 broilers. Poult. Sci. 2020, 99, 1357–1362. [Google Scholar] [CrossRef]
- El-Kholy, M.S.; Ibrahim, Z.A.E.G.; El-Mekkawy, M.M.; Alagawany, M. Influence of in-ovo administration of some water-soluble vitamins on hatchability traits, growth, carcass traits and blood chemistry of Japanese quails. Ann. Anim. Sci. 2019, 19, 97–111. [Google Scholar] [CrossRef] [Green Version]
- Fatemi, S.A.; Elliott, K.E.C.; Bello, A.; Peebles, E.D. Effects of the in ovo injection of vitamin D3 and 25-hydroxyvitamin D3 in Ross 708 broilers subsequently challenged with coccidiosis. I. performance, meat yield and intestinal lesion. Poult. Sci. 2021, 100, 101382. [Google Scholar] [CrossRef] [PubMed]
- Zhu, Y.F.; Li, S.Z.; Sun, Q.Z.; Yang, X.J. Effect of in ovo feeding of vitamin C on antioxidation and immune function of broiler chickens. Animal 2019, 13, 1927–1933. [Google Scholar] [CrossRef] [PubMed]
- Zhu, Y.F.; Bodinga, M.B.; Zhou, J.H.; Zhu, L.Q.; Cao, Y.L.; Ren, Z.Z.; Yang, X.J. Effects of in ovo injection of vitamin C on heat shock protein and metabolic genes expression. Animal 2020, 14, 360–367. [Google Scholar] [CrossRef]
- Fatemi, S.A.; Elliott, K.E.C.; Bello, A.; Zhang, H.; Peebles, E.D. Effects of the in ovo injection of vitamin D3 and 25-hydroxyvitamin D3 in Ross 708 broilers subsequently fed commercial or calcium and phosphorous-restricted diets: II. Immunity and small intestine morphology. Poult. Sci. 2021, 100, 101240. [Google Scholar] [CrossRef] [PubMed]
- Ebrahimi, H.; Shariatmadari, F.; Karimi-Torshizi, M.A. Dietary supplementation and in ovo injection of 1α-OHD3 in a low-calcium and low-phosphorous diets for broilers. J. Appl. Anim. Res. 2016, 44, 113–117. [Google Scholar] [CrossRef] [Green Version]
- Fatemi, S.A.; Elliott, K.E.C.; Bello, A.; Macklin, K.S.; Peebles, E.D. Effects of the in ovo injection of vitamin D3 and 25-hydroxyvitamin D3 in Ross 708 broilers subsequently challenged with coccidiosis: II. Immunological and inflammatory responses and small intestine histomorphology. Animals Basel 2022, 12, 1027. [Google Scholar] [CrossRef]
- Gan, L.; Fan, H.; Mahmood, T.; Guo, Y. Dietary supplementation with vitamin C ameliorates the adverse effects of Salmonella Enteritidis-challenge in broilers by shaping intestinal microbiota. Poult. Sci. 2020, 99, 3663–3674. [Google Scholar] [CrossRef]
- Amer, S.A.; Mohamed, W.A.M.; Gharib, H.S.A.; Al-Gabri, N.A.; Gouda, A.; Elabbasy, M.T.; El-Rahman, G.I.A.; Omar, A.E. Changes in the growth, ileal digestibility, intestinal histology, behavior, fatty acid composition of the breast muscles, and blood biochemical parameters of broiler chickens by dietary inclusion of safflower oil and vitamin C. BMC Vet. Res. 2021, 17, 68. [Google Scholar] [CrossRef]
- Buettner, G.R.; Schafer, F.Q. Ascorbate (vitamin C) as an antioxidant. In Vitamin C: Its Functions and Biochemistry in Animals and Plants; Asard, H., May, J.M., Smirnoff, N., Eds.; BIOS Scientific Publishers: Oxford, UK, 2004; pp. 173–188. [Google Scholar]
- Buettner, G.R. The pecking order of free radicals and antioxidants: Lipid peroxidation, a-tocopherol, and ascorbate. Arch. Biochem. Biophy. 1993, 300, 535–543. [Google Scholar] [CrossRef]
- Padayatty, S.J.; Levine, M. Vitamin C: The known and the unknown and Goldilocks. Oral Dis. 2016, 22, 463–493. [Google Scholar] [CrossRef] [Green Version]
- Orban, J.I.; Roland, D.A.; Cummins, K.; Lovell, R.T. Influence of large doses of ascorbic acid on performance, plasma calcium, bone characteristics, and eggshell quality in broilers and Leghorn hens. Poult. Sci. 1993, 72, 691. [Google Scholar] [CrossRef] [PubMed]
- Hieu, T.V.; Guntoro, B.; Qui, N.H.; Quyen, N.T.K.; Hafiz, F.A.A. The application of ascorbic acid as a therapeutic feed additive to boost immunity and antioxidant activity of poultry in heat stress environment. Vet. World. 2022, 15, 685–693. [Google Scholar] [CrossRef] [PubMed]
- Santos, E.T.; Sgavioli, S.; Castiblanco, D.M.C.; Borges, L.L.; Quadros, T.C.O.; Laurentiz, A.C.; Shimano, A.C.; Baraldi-Artoni, S.M. Glycosaminoglycans and vitamin C affect broiler bone parameters. Poult. Sci. 2019, 98, 4694–4704. [Google Scholar] [CrossRef] [PubMed]
- Atherton, J.G.; Kratzing, C.C.; Fisher, A. The effect of ascorbic acid on infection of chick-embryo ciliated tracheal organ cultures by coronavirus. Arch. Virol. 1978, 56, 195–199. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Constantini, N.W.; Dubnov-Raz, G.; Eyal, B.B.; Berry, E.M.; Cohen, A.H.; Hemilä, H. The effect of vitamin C on upper respiratory infections in adolescent swimmers: A randomized trial. Eur. J. Pediatr. 2011, 170, 59–63. [Google Scholar] [CrossRef]
- Hemila, H.; Chalker, E. Vitamin C for preventing and treating the common cold. Cochrane Database Syst. Rev. 2013, 1, CD000980. [Google Scholar] [CrossRef] [Green Version]
- Schefferle, H.E. The decomposition of uric acid in built up poultry litter. J. Appl. Bacteriol. 1965, 28, 412–420. [Google Scholar] [CrossRef]
- Tasistro, A.S.; Ritz, C.W.; Kissel, D.E. Ammonia emissions from broiler litter: Response to bedding materials and acidifiers. Br. Poult. Sci. 2007, 48, 399–405. [Google Scholar] [CrossRef]
- Santoso, U.; Ohtani, S.; Tanaka, K.; Sakaida, M. Dried Bacillus subtilis culture reduced ammonia gas release in poultry house. Asian Austr. J. Anim. Sci. 1999, 12, 806–809. [Google Scholar] [CrossRef]
- Ihrig, A.; Hoffmann, J.; Triebig, G. Examination of the influence of personal traits and habituation on the reporting of complaints at experimental exposure to ammonia. Int. Arch. Occup. Environ. Health 2006, 79, 332–338. [Google Scholar] [CrossRef]
- David, B.; Mejdell, C.; Michel, V.; Lund, V.; Moe, R.O. Air quality in alternative housing systems may have an impact on laying hen welfare. Part II-ammonia. Animal 2015, 5, 886–896. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Almuhanna, E.A.; Ahmed, A.S.; Al-Yousif, Y.M. Effect of air contaminants on poultry immunological and production performance. Int. J. Poult. Sci. 2011, 10, 461–470. [Google Scholar] [CrossRef] [Green Version]
- Elliott, H.A.; Collins, N.E. Factors affecting ammonia release in broiler houses. Trans. ASAE 1982, 25, 413–418. [Google Scholar] [CrossRef]
- Anderson, D.P.; Beard, C.W.; Hanson, R.P. The adverse effects of ammonia on chickens including resistence to infection with Newcastle disease virus. Avian Res. 1964, 8, 369–379. [Google Scholar] [CrossRef]
- Olanrewaju, H.A.; Miller, W.W.; Maslin, W.R.; Thaxton, J.P.; Dozier, W.A., 3rd; Purswell, J.; Branton, S.L. Interactive effects of ammonia and light intensity on ocular, fear and leg health in broiler chickens. Int. J. Poult. Sci. 2007, 6, 762–769. [Google Scholar]
- Xiong, Y.; Tang, X.; Meng, Q. Differential expression analysis of the broiler tracheal proteins responsible for the immune response and muscle contraction induced by high concentration of ammonia using iTRAQ-coupled 2D LC-MS/MS. Sci. China Life Sci. 2016, 59, 1166–1176. [Google Scholar] [CrossRef] [Green Version]
- Zhou, Y.; Zhang, M.; Liu, Q.; Feng, J. The alterations of tracheal microbiota and inflammation caused by different levels of ammonia exposure in broiler chickens. Poult. Sci. 2021, 100, 685–696. [Google Scholar] [CrossRef]
- Oyetunde, O.O.; Thomson, R.G.; Carlson, H.C. Aerosol exposure of ammonia, dust and Escherichia coli in broiler chickens. Can. Vet. J. 1978, 19, 187–193. [Google Scholar]
- Al-Mashhadani, E.H.; Beck, M.M. Effect of atmospheric ammonia on the surface ultrastructure of the lung and trachea of broiler chicks. Poult. Sci. 1985, 64, 2056–2061. [Google Scholar] [CrossRef]
- Ritz, C.W.; Fairchild, B.D.; Lacy, M.P. Implications of ammonia production and Emissions from Commercial poultry Facilities: A review. J. Appl. Poult. Res. 2004, 13, 684–692. [Google Scholar] [CrossRef]
- Wang, M.; Meng, X.; Zhao, Z.; Jing, L. Hazard and prevention of ammonia to poultry industry. China Poult. 2006, 28, 27–28. [Google Scholar]
- Valentine, H. A study of the effect of different ventilation rates on the ammonia concentrations in the atmosphere of broiler houses. Br. Poult. Sci. 1964, 5, 149–159. [Google Scholar] [CrossRef]
- Ernst, R.A. The effect of ammonia on poultry. Feedstuffs 1968, 40, 40. [Google Scholar]
- Kling, H.F.; Quarles, C.L. Effect of Atmospheric Ammonia and the Stress of Infectious Bronchitis Vaccination on Leghorn Males. Poult. Sci. 1974, 53, 1161–1167. [Google Scholar] [CrossRef] [PubMed]
- Miles, D.M.; Miller, W.W.; Branton, S.L.; Maslin, W.R.; Lott, B.D. Ocular responses to ammonia in broiler chickens. Avian Dis. 2006, 50, 45–49. [Google Scholar] [CrossRef]
- Kristensen, H.H.; Mathes, C.M. Ammonia and poultry welfare: A review. Worlds Poult. Sci. J. 2000, 56, 235–245. [Google Scholar] [CrossRef]
- Shi, Q.X.; Wang, W.; Chen, M.H.; Zhang, H.F.; Xu, S.W. Ammonia induces Treg/Th1 imbalance with triggered NF-kB pathway leading to chicken respiratory inflammation response. Sci. Total Environ. 2019, 659, 354–362. [Google Scholar] [CrossRef]
- Mousstaaid, A.; Fatemi, S.A.; Elliott, K.E.C.; Levy, A.; Miller, W.W.; Purswell, J.; Olanrewaju, H.A.; Gerard, P.D.; Peebles, E.D. Effects of the in ovo administration of L-ascorbic acid on the performance and incidence of corneal erosion in Ross 708 broilers subjected to elevated levels of atmospheric ammonia. Animal 2023, 13, 399. [Google Scholar] [CrossRef]
- Zhai, W.; Rowe, D.E.; Peebles, E.D. Effects of commercial in ovo injection of carbohydrates on broiler embryogenesis. Poult. Sci. 2011, 90, 1295–1301. [Google Scholar] [CrossRef]
- Keralapurath, M.M.; Corzo, A.; Pulikanti, R.; Zhai, W.; Peebles, E.D. Effects of in ovo injection of L-carnitine on hatchability and subsequent broiler performance and slaughter yield. Poult. Sci. 2010, 89, 1497–1501. [Google Scholar] [CrossRef]
- Keralapurath, M.M.; Keirs, R.W.; Corzo, A.; Bennett, L.W.; Pulikanti, R.; Peebles, E.D. Effects of in ovo injection of L-carnitine on subsequent broiler chick tissue nutrient profiles. Poult. Sci. 2010, 89, 335–341. [Google Scholar] [CrossRef] [PubMed]
- Olanrewaju, H.A.; Thaxton, J.P.; Dozier Iii, W.A.; Purswell, J.; Collier, S.D.; Branton, S.L. Interactive effects of ammonia and light intensity on hematochemical variables in broiler chickens. Poult. Sci. 2008, 87, 1407–1414. [Google Scholar] [CrossRef] [PubMed]
- Bowen, O.T.; Erf, G.F.; Chapman, M.E.; Wideman, R.F., Jr. Plasma nitric oxide concentrations in broilers after intravenous injections of lipopolysaccharide or microparticles. Poult. Sci. 2007, 86, 2550–2554. [Google Scholar] [CrossRef] [PubMed]
- Laur, N.; Kinscherf, R.; Pomytkin, K.; Kaiser, L.; Knes, O.; Deigner, H.-P. ICP-MS trace element analysis in serum and whole blood. PLoS ONE 2020, 15, e0233357. [Google Scholar] [CrossRef] [PubMed]
- Harmon, B.G. Avian heterophils in inflammation and disease resistance. Poult. Sci. 1998, 77, 972–977. [Google Scholar] [CrossRef] [PubMed]
- Herbert, R.A.; Janardhan, K.S.; Pandiri, A.R.; Cesta, M.F.; Miller, R.A. Chapter 22—Nose, larynx, and trachea. In Boorman’s Pathology of the Rat; Elsevier: Amsterdam, The Netherlands, 2018; pp. 391–435. [Google Scholar] [CrossRef]
- Kotani, T.; Odagiri, Y.; Nakamura, J.; Horiuchi, T. Pathological Changes of Tracheal Mucosa in Chickens Infected with Lentogenic Newcastle Disease Virus. Avian Dis. 1987, 31, 491–497. [Google Scholar] [CrossRef]
- Itoo, F.; Mir, M.; Kamil, S.; Khan, H.; Darzi, M. Histopathological profiling of respiratory tract lesions in chickens. SKUAST J. Res. 2014, 16, 93–104. [Google Scholar]
- SAS Institute. SAS Proprietary Software, Release 9.4; SAS Inst. Inc.: Cary, NC, USA, 2013.
- Steel, R.G.D.; Torrie, J.H. Principles and Procedures of Statistics: A Biometrical Approach, 2nd ed.; McGraw-Hill: New York, NY, USA, 1980. [Google Scholar]
- MacMicking, J.; Xie, Q.W.; Nathan, C. Nitric oxide and macrophage function. Ann. Rev. Immunol. 1997, 15, 323–350. [Google Scholar] [CrossRef]
- Stuehr, D.J.; Marletta, M.A. Induction of nitrite/nitrate synthesis in murine macrophages by BCG infection, lymphokines, or interferon-gamma. J. Immunol. 1989, 139, 518–525. [Google Scholar] [CrossRef]
- Shah, S.W.A.; Ishfaq, M.; Nasrullah, M.; Qayum, A.; Akhtar, M.U.; Jo, H.; Hussain, M.; Teng, X. Ammonia inhalation-induced inflammation and structural impairment in the bursa of fabricius and thymus of broilers through NF-κB signaling pathway. Environ. Sci. Pollut. Res. Int. 2020, 27, 11596–11607. [Google Scholar] [CrossRef]
- Osborne, L.C.; Abraham, N. Regulation of memory T cells by γc cytokines. Cytokine 2010, 50, 105–113. [Google Scholar] [CrossRef] [PubMed]
- Ghareeb, K.; Awad, W.A.; Soodoi, C.; Sasgary, S.; Strasser, A.; Böhm, J. Effects of feed contaminant deoxynivalenol on plasma cytokines and mRNA expression of immune genes in the intestine of broiler chickens. PLoS ONE 2013, 8, e71492. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Colditz, I.G. Effects of the immune system on metabolism: Implications for production and disease resistance in livestock. Livest. Prod. Sci. 2000, 75, 257–268. [Google Scholar] [CrossRef]
- Pié, S.S.; Lallès, J.P.; Blazy, F.; Laffitte, J.; Sève, B.; Oswald, I.P. Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. J. Nutr. 2004, 134, 641–647. [Google Scholar]
- Qadir, M.F.; Khan, A.; Kashif, M.; Tehseen, S.G.; Khan, A. Epidemiological and pathological status of Mycoplasma gallisepticum in layer chicks at Faisalabad, Pakistan. Pak. J. Agric. Sci. 2021, 58, 213–218. [Google Scholar]
- Hemilä, H. The effect of vitamin C on bronchoconstriction and respiratory symptoms caused by exercise: A review and statistical analysis. Allergy Asthma Clin. Immunol. 2014, 10, 58–69. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shah, S.W.A.; Chen, J.; Han, Q.; Xu, Y.; Ishfaq, M. Ammonia inhalation impaired immune function and mitochondrial integrity in the broiler’s bursa of Fabricius: Implication of oxidative stress and apoptosis. Ecotoxicol. Environ. Saf. 2020, 190, 110078–110088. [Google Scholar]
- Shah, S.W.A.; Chen, D.; Zhang, J.; Liu, Y.; Ishfaq, M.; Tang, Y.; Teng, X. The effect of ammonia exposure on energy metabolism and mitochondrial dynamic proteins in chicken thymus: Through oxidative stress, apoptosis, and autophagy. Ecotoxicol. Environ. Saf. 2020, 250, 111413–111424. [Google Scholar]
- Devi, G.S.; Prasad, M.H.; Saraswathi, I.; Raghu, D.; Rao, D.N.; Reddy, P.P. Free radicals antioxidant enzymes and lipid peroxidation in different types of leukemias. Clin. Chim. Acta 2000, 293, 53–62. [Google Scholar]
- Thomas, M.J. The role of free radicals and antioxidants. Nutrition 2000, 16, 716–718. [Google Scholar] [CrossRef]
- Cinar, M.; Yildirim, E.; Yigit, A.A.; Yalcinkaya, I.; Duru, O.; Kisa, U.; Atmaca, N. Effects of dietary supplementation with Vitamin C and Vitamin E and their combination on growth performance, some biochemical parameters, and oxidative stress induced by copper toxicity in broilers. Biol. Trace. Elem. Res. 2014, 158, 186–196. [Google Scholar] [CrossRef] [PubMed]
Cilial erosion | 0 = normal, 1 = focal (mild), 2 = multifocal (moderate), 3 = diffuse (severe) |
Gland assessment | 0 = normal, 1 = depletion (mild), 2 = hyperplasia (moderate), 3 = both depletion and hyperplasia (severe) |
Inflammation | 0 = normal, 1 = mild lymphocytes, 2 = moderate lymphocytes, 3 = heterophils/moderate lymphocytes |
Attenuation | 0 = normal, 1 = focal (mild), 2 = multifocal (moderate), 3 = diffuse (severe) |
Ulceration | 0 = normal, 1 = focal (mild), 2 = multifocal (moderate), 3 = diffuse (severe) |
Eye | |||||
---|---|---|---|---|---|
Treatment | 0 doa | 7 doa | 14 doa | 21 doa | 28 doa |
--------------------------------- (μmol) --------------------------------- | |||||
Non-injected 1 | 4.48 | 4.51 | 2.94 | 3.09 | 2.15 |
Saline 2 | 4.15 | 4.23 | 3.25 | 3.41 | 2.16 |
L-AA 12 3 | 3.96 | 4.25 | 3.27 | 3.05 | 1.99 |
L-AA 25 4 | 4.47 | 3.82 | 2.95 | 3.17 | 1.97 |
Pooled SEM | 0.456 | 0.488 | 0.291 | 0.295 | 0.283 |
p-Value | 0.607 | 0.795 | 0.522 | 0.628 | 0.861 |
Liver | |||||
0 doa | 7 doa | 14 doa | 21 doa | 28 doa | |
--------------------------------- (μmol) --------------------------------- | |||||
Non-injected | 24.6 | 20.3 | 14.8 | 12.7 | 7.09 |
Saline | 24.8 | 20.2 | 14.0 | 12.2 | 8.22 |
L-AA 12 | 27.1 | 20.9 | 16.9 | 11.9 | 7.53 |
L-AA 25 | 27.4 | 21.1 | 16.1 | 12.4 | 8.26 |
Pooled SEM | 1.36 | 2.12 | 3.02 | 1.34 | 0.908 |
p-Value | 0.109 | 0.968 | 0.773 | 0.948 | 0.511 |
Treatment | 0 doa | 14 doa | 21 doa | 28 doa |
---|---|---|---|---|
--------------------------------- (μmol) --------------------------------- | ||||
Non-injected 1 | 7.04 | 6.93 | 6.05 | 5.90 |
Saline 2 | 6.78 | 6.68 | 6.48 | 6.97 |
L-AA 12 3 | 6.95 | 7.52 | 7.19 | 6.17 |
L-AA 25 4 | 7.09 | 5.55 | 9.13 | 5.59 |
Pooled SEM | 1.135 | 0.745 | 0.958 | 0.846 |
p-Value | 0.998 | 0.317 | 0.154 | 0.661 |
Treatment | 0 doa | ||
---|---|---|---|
Ca (ppm) | Cu (ppm) | Zn (ppm) | |
Non-injected 1 | 100 | 0.06 | 3.25 |
Saline 2 | 102 | 0.07 | 3.39 |
L-AA 12 3 | 102 | 0.08 | 3.31 |
L-AA 25 4 | 101 | 0.10 | 3.34 |
Pooled SEM | 2.6 | 0.056 | 0.313 |
p-Value | 0.805 | 0.809 | 0.977 |
21 doa | |||
Non-injected | 92 | 0.09 | 2.35 |
Saline | 97 | 0.06 | 2.37 |
L-AA 12 | 90 | 0.08 | 2.22 |
L-AA 25 | 99 | 0.09 | 2.30 |
Pooled SEM | 6.9 | 0.018 | 0.133 |
p-Value | 0.769 | 0.596 | 0.865 |
Treatment | Cilial Erosion 6 | Glands 7 | Inflammation 8 | Attenuation 9 | Ulceration 10 |
---|---|---|---|---|---|
0 doa | |||||
Non-injected 2 | 1.50 | 0.58 | 0.58 | 2.42 a | 0.83 |
Saline 3 | 0.83 | 1.00 | 1.00 | 2.08 a | 0.50 |
L-AA 12 4 | 1.33 | 1.00 | 1.00 | 1.25 b | 0.25 |
L-AA 25 5 | 0.83 | 0.83 | 0.83 | 1.25 b | 0.17 |
Pooled SEM | 0.307 | 0.265 | 0.265 | 0.391 | 0.265 |
p-Value | 0.072 | 0.359 | 0.359 | 0.007 | 0.068 |
21 doa | |||||
Non-injected | 0.67 | 1.00 | 1.67 | 0.92 b | 0.33 |
Saline | 0.58 | 0.92 | 0.92 | 1.58 a | 0.25 |
L-AA 12 | 0.58 | 1.33 | 1.33 | 2.08 a | 0.17 |
L-AA 25 | 0.75 | 1.17 | 1.17 | 1.67 a | 0.25 |
Pooled SEM | 0.363 | 0.30 | 0.319 | 0.298 | 0.221 |
p-Value | 0.961 | 0.514 | 0.632 | 0.004 | 0.902 |
28 doa | |||||
Non-injected | 1.25 | 0.92 | 1.33 | 0.92 | 0 |
Saline | 1.33 | 0.92 | 1.58 | 0.92 | 0 |
L-AA 12 | 0.58 | 1.1 | 2.08 | 1.08 | 0 |
L-AA 25 | 1.00 | 1.0 | 1.92 | 1.00 | 0.25 |
Pooled SEM | 0.368 | 0.220 | 0.310 | 0.220 | 0.127 |
p-Value | 0.187 | 0.851 | 0.086 | 0.851 | 0.137 |
Treatments | |||||||
---|---|---|---|---|---|---|---|
Non-Injected 1 | Saline 2 | L-AA 12 3 | L-AA 25 4 | Pooled SEM | p-Value | ||
Cilial Erosion 5 (%) | Score 0 | 16.7 | 25.0 | 8.3 | 36.4 | 17.13 | 0.261 |
Score 1 | 25.0 | 66.7 | 50.0 | 36.4 | 20.10 | 0.180 | |
Score 2 | 50.0 | 8.0 | 41.7 | 27.3 | 18.69 | 0.130 | |
Score 3 | 8.3 | 0 | 0 | 0 | 5.89 | 0.402 | |
Glands 6 (%) | Score 0 | 50.0 | 25.0 | 8.3 | 27.3 | 17.99 | 0.152 |
Score 1 | 41.7 | 58.3 | 83.3 | 72.7 | 19.37 | 0.212 | |
Score 2 | 8.3 | 8.3 | 8.3 | 0 | 10.32 | 0.822 | |
Score 3 | 0 | 8.3 | 0 | 0 | 5.96 | 0.402 | |
Inflammation 7 (%) | Score 0 | 50.0 | 16.7 | 8.3 | 27.3 | 17.35 | 0.103 |
Score 1 | 41.7 | 66.7 | 83.3 | 72.7 | 19.12 | 0.210 | |
Score 2 | 8.3 | 8.3 | 8.3 | 0 | 10.32 | 0.800 | |
Score 3 | 0 | 8.3 | 0 | 0 | 5.96 | 0.402 | |
Attenuation 8 (%) | Score 0 | 8.3 | 0.0 | 8.3 | 9.1 | 10.31 | 0.801 |
Score 1 | 58.3 a | 41.7 a | 8.3 b | 0 b | 16.17 | 0.010 | |
Score 2 | 25.0 | 58.3 | 50.0 | 72.7 | 20.03 | 0.208 | |
Score 3 | 8.3 | 0.0 | 33.3 | 18.2 | 14.22 | 0.123 | |
Ulceration 9 (%) | Score 0 | 50.0 | 58.3 | 75.0 | 81.8 | 19.49 | 0.306 |
Score 1 | 16.7 | 33.3 | 25.0 | 18.2 | 17.85 | 0.783 | |
Score 2 | 33.3 a | 8.3 b | 0 b | 0 b | 11.79 | 0.019 | |
Score 3 | 0 | 0 | 0 | 0 | - | - | |
Thickness 10 (μm) | 25.8 | 24.4 | 25.7 | 20.9 | 2.44 | 0.186 |
Treatments | |||||||
---|---|---|---|---|---|---|---|
Non-Injected 1 | Saline 2 | L-AA 12 3 | L-AA 25 4 | Pooled SEM | p-Value | ||
Cilial Erosion 5 (%) | Score 0 | 50.0 | 50.0 | 75.0 | 75.0 | 38.19 | 0.835 |
Score 1 | 27.3 | 8.3 | 8.3 | 8.3 | 14.14 | 0.460 | |
Score 2 | 18.2 | 25.0 | 25.0 | 33.3 | 18.89 | 0.884 | |
Score 3 | 0 | 0 | 0 | 0 | - | - | |
Glands 6 (%) | Score 0 | 18.2 | 8.3 | 0.0 | 16.7 | 13.08 | 0.478 |
Score 1 | 72.7 | 91.7 | 83.3 | 66.7 | 17.35 | 0.475 | |
Score 2 | 0 | 0 | 0 | 0 | - | - | |
Score 3 | 9.1 | 0 | 16.7 | 16.7 | 13.11 | 0.521 | |
Inflammation 7 (%) | Score 0 | 18.2 | 8.3 | 0 | 16.7 | 13.08 | 0.478 |
Score 1 | 63.6 | 91.7 | 83.3 | 66.7 | 17.77 | 0.337 | |
Score 2 | 0 | 0 | 0 | 0 | - | - | |
Score 3 | 27.3 | 0 | 16.7 | 16.7 | 14.94 | 0.340 | |
Attenuation 8 (%) | Score 0 | 27.3 | 16.7 | 0 | 16.7 | 14.95 | 0.340 |
Score 1 | 36.4 a | 8.3 b | 0 b | 8.3 b | 13.32 | 0.017 | |
Score 2 | 27.3 b | 66.7 a | 91.6 a | 66.6 a | 18.48 | 0.006 | |
Score 3 | 9.1 | 0 | 8.3 | 8.3 | 10.54 | 0.793 | |
Ulceration 9(%) | Score 0 | 54.6 | 83.3 | 83.3 | 83.3 | 17.70 | 0.288 |
Score 1 | 36.4 | 8.3 | 16.7 | 8.3 | 15.65 | 0.254 | |
Score 2 | 0 | 8.3 | 0 | 8.30 | 8.62 | 0.595 | |
Score 3 | 3.9 | 0 | 0 | 0 | 2.63 | 0.360 | |
Thickness 10 (μm) | 37.3 | 39.8 | 35.4 | 40.5 | 5.60 | 0.778 |
Treatments | |||||||
---|---|---|---|---|---|---|---|
Non-Injected 1 | Saline 2 | L-AA 12 3 | L-AA 25 4 | Pooled SEM | p-Value | ||
Cilial Erosion 5 (%) | Score 0 | 25.0 | 16.7 | 58.3 | 41.7 | 19.22 | 0.152 |
Score 1 | 33.3 | 33.3 | 25.0 | 25.0 | 19.30 | 0.945 | |
Score 2 | 33.3 | 50.0 | 16.7 | 25.0 | 19.05 | 0.353 | |
Score 3 | 8.3 | 0 | 0 | 8.3 | 8.33 | 0.577 | |
Glands 6 (%) | Score 0 | 0 b | 8.3 b | 66.7 a | 41.7 ab | 18.21 | 0.018 |
Score 1 | 33.3 | 33.3 | 16.7 | 25.0 | 18.72 | 0.780 | |
Score 2 | 33.3 | 58.3 | 16.7 | 25.0 | 18.97 | 0.161 | |
Score 3 | 8.3 | 0 | 0 | 8.3 | 8.33 | 0.577 | |
Inflammation 7 (%) | Score 0 | 8.3 | 8.3 | 25.0 | 8.3 | 13.76 | 0.538 |
Score 1 | 91.7 a | 91.7 a | 50.0 b | 83.3 a | 15.69 | 0.033 | |
Score 2 | 0 | 0 | 16.7 | 8.3 | 9.89 | 0.286 | |
Score 3 | 0 | 0 | 8.3 | 0 | 5.89 | 0.402 | |
Attenuation 8 (%) | Score 0 | 8.3 | 8.3 | 33.3 | 25.0 | 15.99 | 0.313 |
Score 1 | 8.3 | 0.0 | 16.7 | 33.3 | 14.10 | 0.123 | |
Score 2 | 16.7 | 66.7 | 41.7 | 33.3 | 19.38 | 0.089 | |
Score 3 | 66.7 a | 25.0 b | 8.3 b | 8.3 b | 15.99 | 0.002 | |
Ulceration 9 (%) | Score 0 | 100.0 | 100.0 | 100.0 | 83.3 | 7.95 | 0.102 |
Score 1 | 0 | 0 | 0 | 8.3 | 5.89 | 0.402 | |
Score 2 | 0 | 0 | 0 | 8.3 | 5.89 | 0.402 | |
Score 3 | 17.3 | 14.3 | 15.6 | 17.4 | 2.24 | 0.446 | |
Thickness 10 (μm) | 25.8 | 24.4 | 25.7 | 20.9 | 2.44 | 0.186 |
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Mousstaaid, A.; Fatemi, S.A.; Levy, A.W.; Purswell, J.L.; Olanrewaju, H.A.; Baughman, B.; McNulty, K.; Gerard, P.D.; Peebles, E.D. Effects of the In ovo Administration of L-Ascorbic Acid on Tissue L-Ascorbic Acid Concentrations, Systemic Inflammation, and Tracheal Histomorphology of Ross 708 Broilers Subjected to Elevated Levels of Atmospheric Ammonia. Poultry 2023, 2, 158-173. https://doi.org/10.3390/poultry2020014
Mousstaaid A, Fatemi SA, Levy AW, Purswell JL, Olanrewaju HA, Baughman B, McNulty K, Gerard PD, Peebles ED. Effects of the In ovo Administration of L-Ascorbic Acid on Tissue L-Ascorbic Acid Concentrations, Systemic Inflammation, and Tracheal Histomorphology of Ross 708 Broilers Subjected to Elevated Levels of Atmospheric Ammonia. Poultry. 2023; 2(2):158-173. https://doi.org/10.3390/poultry2020014
Chicago/Turabian StyleMousstaaid, Ayoub, Seyed Abolghasem Fatemi, April Waguespack Levy, Joseph L. Purswell, Hammed A. Olanrewaju, Brittany Baughman, Kaylin McNulty, Patrick D. Gerard, and Edgar David Peebles. 2023. "Effects of the In ovo Administration of L-Ascorbic Acid on Tissue L-Ascorbic Acid Concentrations, Systemic Inflammation, and Tracheal Histomorphology of Ross 708 Broilers Subjected to Elevated Levels of Atmospheric Ammonia" Poultry 2, no. 2: 158-173. https://doi.org/10.3390/poultry2020014
APA StyleMousstaaid, A., Fatemi, S. A., Levy, A. W., Purswell, J. L., Olanrewaju, H. A., Baughman, B., McNulty, K., Gerard, P. D., & Peebles, E. D. (2023). Effects of the In ovo Administration of L-Ascorbic Acid on Tissue L-Ascorbic Acid Concentrations, Systemic Inflammation, and Tracheal Histomorphology of Ross 708 Broilers Subjected to Elevated Levels of Atmospheric Ammonia. Poultry, 2(2), 158-173. https://doi.org/10.3390/poultry2020014