Skip to main content Accessibility help
×
Home

Effect of threonine deficiency on intestinal integrity and immune response to feed withdrawal combined with coccidial vaccine challenge in broiler chicks

  • Qian Zhang (a1), Xi Chen (a1), Susan D. Eicher (a1) (a2), Kolapo M. Ajuwon (a1) and Todd J. Applegate (a1)...

Abstract

For this study, threonine (Thr) deficiency was hypothesised to exacerbate the intestinal damage induced by feed withdrawal with coccidial infection because of its high obligatory requirement by the gut; two dietary Thr treatments (0·49 and 0·90 %) were applied to chicks from 0 to 21 d of age. At 13 d of age, feed was withdrawn for 24 h from one-half of birds of each dietary treatment with subsequent gavage of a 25× dose of coccidial vaccine. Overall, there were four treatments with eight replicate cages per treatment. Under combined challenge, birds fed the Thr-deficient diet had 38 % lower 13–21-d body weight gain (P≤0·05) compared with birds fed the Thr-control diet. At 21 d, the challenged group fed low Thr had higher number of oocysts (+40 %, P=0·03) and lower crypt depth (−31 %, P<0·01). In addition, birds fed the low-Thr diet had higher gut permeability as measured after 2 h of administration of fluorescein isothiocyanate-dextran (3–5 kDa, P<0·01), which may be attributed to decreased IgA production (P=0·03) in the ileum. In caecal tonsils, the challenged group fed low Thr had lower CD3:Bu-1 ratio (P≤0·05), along with a tendency for lower CCR9 mRNA expression in birds fed the low-Thr diet (P=0·10). In addition, Thr deficiency tended to increase IL-10 mRNA expression regardless of infection (P=0·06), but did not change interferon-γ mRNA expression upon coccidial infection (P>0·05). Overall, Thr deficiency worsened the detrimental effects of combined feed withdrawal and coccidial infection on growth performance and oocyst shedding by impairing intestinal morphology, barrier function, lymphocyte profiles and their cytokine expressions.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Effect of threonine deficiency on intestinal integrity and immune response to feed withdrawal combined with coccidial vaccine challenge in broiler chicks
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Effect of threonine deficiency on intestinal integrity and immune response to feed withdrawal combined with coccidial vaccine challenge in broiler chicks
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Effect of threonine deficiency on intestinal integrity and immune response to feed withdrawal combined with coccidial vaccine challenge in broiler chicks
      Available formats
      ×

Copyright

Corresponding author

* Corresponding author: T. J. Applegate, fax +1 706 542 1827, email applegt@uga.edu

References

Hide All
1. Lillehoj, HS, Min, W & Dalloul, RA (2004) Recent progress on the cytokine regulation of intestinal immune responses to Eimeria . Poult Sci 83, 611623.
2. Dalloul, RA & Lillehoj, HS (2006) Poultry coccidiosis: recent advancements in control measures and vaccine development. Expert Rev Vaccines 5, 143163.
3. Shivaramaiah, C, Barta, JR, Hernandez-Velasco, X, et al. (2014) Coccidiosis: recent advancements in the immunobiology of Eimeria species, preventive measures, and the importance of vaccination as a control tool against these Apicomplexan parasites. Vet Med Res Rep 5, 2334.
4. Fernando, MA & McCraw, BM (1973) Mucosal morphology and cellular renewal in the intestine of chickens following a single infection of Eimeria acervulina . J Parasitol 59, 493501.
5. Witlock, D & Ruff, M (1977) Comparison of the intestinal surface damage caused by Eimeria mivati, E. necatrix, E. maxima, E. brunetti, and E. acervulina by scanning electron microscopy. J Parasitol 63, 193199.
6. Tan, JZ, Applegate, TJ, Liu, SS, et al. (2014) Supplemental dietary L-arginine attenuates intestinal mucosal disruption during a coccidial vaccine challenge in broiler chickens. Br J Nutr 112, 10981109.
7. Adedokun, SA, Ajuwon, KM, Romero, LF, et al. (2012) Ileal endogenous amino acid losses: response of broiler chickens to fiber and mild coccidial vaccine challenge. Poult Sci 91, 899907.
8. Collier, CT, Hofacre, CL, Payne, AM, et al. (2008) Coccidia-induced mucogenesis promotes the onset of necrotic enteritis by supporting Clostridium perfringens growth. Vet Immunol Immunopathol 122, 104115.
9. Sandberg, FB, Emmans, GC & Kyriazakis, I (2007) The effects of pathogen challenges on the performance of naïve and immune animals: the problem of prediction. Animal 1, 6786.
10. Nichols, NL & Bertolo, RF (2008) Luminal threonine concentration acutely affects intestinal mucosal protein and mucin synthesis in piglets. J Nutr 138, 12981303.
11. Faure, M, Moennoz, D, Montigon, F, et al. (2005) Dietary threonine restriction specifically reduces intestinal mucin synthesis in rats. J Nutr 135, 486491.
12. Law, GK, Bertolo, RF, Adjiri-Awere, A, et al. (2007) Adequate oral threonine is critical for mucin production and gut function in neonatal piglets. Am J Physiol Gastrointest Liver Physiol 292, 12931301.
13. Horn, NL, Donkin, SS, Applegate, TJ, et al. (2009) Intestinal mucin dynamics: response of broiler chicks and White Pekin ducklings to dietary threonine. Poult Sci 88, 19061914.
14. Zhang, Q, Xu, L, Doster, A, et al. (2014) Dietary threonine requirement of Pekin ducks from 15 to 35 days of age based on performance, yield, serum natural antibodies, and intestinal mucin secretion. Poult Sci 93, 19721980.
15. Hamard, AD, Mazuraisc, G, Boudry, IL, et al. (2010) A moderate threonine deficiency affects gene expression profile, paracellular permeability and glucose absorption capacity in the ileum of piglets. J Nutr Biochem 21, 914921.
16. Duval, D, Demangel, C, Munier-Jolain, K, et al. (1991) Factors controlling cell proliferation and antibody production in mouse hybridoma cells: I. Influence of the amino acid supply. Biotechnol Bioeng 38, 561570.
17. Taudou, G, Wiart, J & Panijel, J (1984) Threonine starvation of concanavalin A treated lymphocytes impairs DNA polymerase alpha activity. Mol Immunol 21, 949953.
18. Azzam, MMM, Zou, XT, Dong, XY, et al. (2011) Effect of supplemental L-threonine on mucin 2 gene expression and intestine mucosal immune and digestive enzymes activities of laying hens in environments with high temperature and humidity. Poult Sci 90, 22512256.
19. Tierney, JB, Matthews, E, Carrington, SD, et al. (2007) Interaction of Eimeria tenella with intestinal mucin in vitro . J Parasitol 93, 634638.
20. Thompson, KL & Applegate, TJ (2006) Feed withdrawal alters small-intestinal morphology and mucus of broilers. Poult Sci 85, 15351540.
21. National Research Council (1994) Nutrient Requirements of Poultry, 9th ed. Washington, DC: National Academies Press.
22. Hodgson, JN (1970) Coccidiosis: oocyst counting technique for coccidiostat evaluation. Exp Parasitol 28, 99102.
23. Conway, DP & McKenzie, ME (2008) Examination of lesions and lesion scoring. In Poultry Coccidiosis: Diagnostic and Testing Procedures, 3rd ed, pp. 14–40. Ames, IA: Blackwell Publishing Professional.
24. Vicuña, EA, Kuttappan, VA, Tellez, G, et al. (2015) Dose titration of FITC-D for optimal measurement of enteric inflammation in broiler chicks. Poult Sci 94, 13531359.
25. Mantle, M & Allen, A (1981) Isolation and characterization of the native glycoprotein from pig small-intestinal mucus. Biochem J 195, 267275.
26. Deters, A, Petereit, F, Schmidgall, J, et al. (2008) N-Acetyl-D-glucosamine oligosaccharides induce mucin secretion from colonic tissue and induce differentiation of human keratinocytes. J Pharm Pharmacol 60, 197204.
27. Xu, L, Eicher, SD & Applegate, TJ (2011) Effects of increasing dietary concentrations of corn naturally contaminated with deoxynivalenol on broiler and turkey poult performance and response to lipopolysaccharide. Poult Sci 90, 27662774.
28. Grenier, B, Schwartz-Zimmermann, HE, Caha, S, et al. (2015) Dose-dependent effects on sphingoid bases and cytokines in chickens fed diets prepared with fusarium verticillioides culture material containing fumonisins. Toxins 7, 12531272.
29. Gilbert, ER, Li, H, Emmerson, DA, et al. (2007) Developmental regulation of nutrient transporter and enzyme mRNA abundance in the small intestine of broilers. Poult Sci 86, 17391753.
30. Paris, NE & Wong, EA (2013) Expression of digestive enzymes and nutrient transporters in the intestine of Eimeria maxima infected chickens. Poult Sci 92, 13311335.
31. Hong, YH, Lillehoj, HS, Lee, SH, et al. (2006) Analysis of chicken cytokine and chemokine gene expression following Eimeria acervulina and Eimeria tenella infections. Vet Immunol Immunopathol 114, 209223.
32. Annamalai, T & Selvaraj, RK (2011) Chemokine receptor CCR7 and CXCR5 mRNA in chickens following inflammation or vaccination. Poult Sci 90, 16951700.
33. Annamalai, T & Selvaraj, RK (2012) Interleukin 4 increases CCR9 expression and homing of lymphocytes to gut-associated lymphoid tissue in chickens. Vet Immunol Immunopathol 145, 257263.
34. Livak, KJ & Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402408.
35. Pastorelli, H, van Milgen, J, Lovatto, P, et al. (2012) Meta-analysis of feed intake and growth responses of growing pigs after a sanitary challenge. Animal 6, 952961.
36. Aviagen (2014) Ross 708 parent stock performance objectives. http://en.aviagen.com/assets/Tech_Center/Ross_Broiler/Ross-708-Broiler-PO-2014-EN.pdf (accessed July 2016).
37. Burkholder, KM, Thompson, KL, Einstein, ME, et al. (2008) Influence of stressors on normal intestinal microbiota, intestinal morphology, and susceptibility to Salmonella enteritidis colonization in broilers. Poult Sci 87, 17341741.
38. Kansagra, K, Stoll, B, Rognerud, C, et al. (2003) Total parenteral nutrition adversely affects gut barrier function in neonatal piglets. Am J Physiol Gastrointest Liver Physiol 285, G1162G1170.
39. Kaetzel, CS (2005) The polymeric immunoglobulin receptor: bridging innate and adaptive immune responses at mucosal surfaces. Immunol Rev 206, 8399.
40. Zhang, Q, Eicher, SD & Applegate, TJ (2014) Development of intestinal mucin 2, IgA, and polymeric Ig receptor expressions in broiler chickens and Pekin ducks. Poult Sci 94, 172180.
41. Poritz, LS, Harris, LR III, Kelly, AA, et al. (2011) Increase in the tight junction protein claudin-1 in intestinal inflammation. Dig Dis Sci 56, 28022809.
42. Johansen, F-E & Kaetzel, CS (2011) Regulation of the polymeric immunoglobulin receptor and IgA transport: new advances in environmental factors that stimulate pIgR expression and its role in mucosal immunity. Mucosal Immunol 4, 598602.
43. Phalipon, A & Corthésy, B (2003) Novel functions of the polymeric Ig receptor: well beyond transport of immunoglobulins. Trends Immunol 24, 5558.
44. Chen, J, Tellez, G, Richards, JD, et al. (2015) Identification of potential biomarkers for gut barrier failure in broiler chickens. Front Vet Sci 2, 14.
45. Wils-Plotz, EL & Dilger, RN (2013) Combined dietary effects of supplemental threonine and purified fiber on growth performance and intestinal health of young chicks. Poult Sci 92, 726734.
46. Su, SC (2013) Expression of digestive enzymes and nutrient transporters in the intestine of Eimeria-challenged chickens. Master Thesis, Virginia Polytechnic Institute and State University.
47. Wigley, P & Kaiser, P (2003) Avian cytokines in health and disease. Rev Bras Cienc Avic 5, 114.
48. Walston, MWS (2014) Studies on T-cell properties during coccidiosis and a vitamin E supplement to an in ovo coccidiosis vaccine. Master Thesis, The Ohio State University.
49. Papadakis, KA, Prehn, J, Nelson, V, et al. (2000) The role of thymus-expressed chemokine and its receptor CCR9 on lymphocytes in the regional specialization of the mucosal immune system. J Immunol 165, 50695076.
50. Ebert, LM, Schaerli, P & Moser, B (2005) Chemokine-mediated control of T cell traffic in lymphoid and peripheral tissues. Mol Immunol 42, 799809.
51. Laurent, F, Mancassola, R, Lacroix, S, et al. (2001) Analysis of chicken mucosal immune response to Eimeria tenella and Eimeria maxima infection by quantitative reverse transcription-PCR. Infect Immun 69, 25272534.
52. Yun, CH, Lillehoj, HS & Choi, KD (2000) Eimeria tenella infection induces local gamma interferon production and intestinal lymphocyte subpopulation changes. Infect Immun 68, 12821288.
53. Lillehoj, HS & Choi, KD (1998) Recombinant chicken interferon gamma-mediated inhibition of Eimeria tenella development in vitro and reduction of oocyst production and body weight loss following Eimeria acervulina challenge infection. Avian Dis 42, 307314.
54. Schoenborn, JR & Wilson, CB (2007) Regulation of interferon-γ during innate and adaptive immune responses. Adv Immunol 96, 41101.
55. Ding, X, Lillehoj, HS, Quiroz, MA, et al. (2004) Protective immunity against Eimeria acervulina following in ovo immunization with a recombinant subunit vaccine and cytokine genes. Infect Immun 72, 69396944.
56. Rothwell, L, Young, JR, Zoorob, R, et al. (2004) Cloning and characterization of chicken IL-10 and its role in the immune response to Eimeria maxima . J Immunol 173, 26752682.
57. Haritova, AM & Stanilova, SA (2012) Enhanced expression of IL-10 in contrast to IL-12B mRNA in poultry with experimental coccidiosis. Exp Parasitol 132, 378382.
58. Zhang, L, Liu, R, Song, M, et al. (2013) Eimeria tenella: interleukin 17 contributes to host immunopathology in the gut during experimental infection. Exp Parasitol 133, 121130.
59. Konkel, JE & Chen, W (2011) Balancing acts: the role of TGF-β in the mucosal immune system. Trends Mol Med 17, 668676.

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed