J. Appl. Poult. Res.
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J APPL POULT RES 2009. 18:530-540. doi:10.3382/japr.2009-00004
© 2009 Poultry Science Association
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Research Reports

Humoral immune response of broilers fed diets containing yeast extract and prebiotics in the prestarter phase and raised at different temperatures

V. K. Silva*,1, J. Della Torre da Silva*, K. A. A. Torres*, D. E. de Faria Filho{dagger}, F. Hirota Hada* and V. M. Barbosa de Moraes*

* Departamento de Zootecnia, Faculdade de Ciências Agrárias e Veterinárias, UNESP, via de Acesso Prof. Paulo Donato Catellane, s/n CEP 14.884-900, Jaboticabal, São Paulo, Brazil; and {dagger} Departamento de Zootecnia, Instituto de Ciências Agrárias, UFMG, CEP 39.404-406, Montes Claros, Minas Gerais, Brazil

1 Corresponding author: vanksilva{at}yahoo.com


   SUMMARY
TOP
 SUMMARY
DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Feedstuffs and additives with immunomodulatory characteristics were investigated to reduce losses caused by disease and to optimize the production potential of the bird. Therefore, the objective of this study was to assess the influence of yeast extract and prebiotics on broilers fed a prestarter diet, and the impact of ambient temperature on maternal and postvaccinal humoral immune responses. The birds were fed diets supplemented with yeast extract, prebiotics, or both in the prestarter phase (1 to 7 d), and from d 8 on, all birds received the same diet. The birds were vaccinated against Newcastle disease virus and infectious bursal disease at 8 and 18 d of age. The addition of yeast extract and prebiotic in the prestarter phase did not change the humoral immune response against Newcastle disease virus or infectious bursal disease throughout the production cycle of the broilers. The higher temperature increased IgG levels, especially maternal antibody titers, despite the immunomodulating effect of heat stress until the second week of life.

Key Words: heat stress • infectious bursal disease • Newcastle disease • mannan oligosaccharide • Saccharomyces cerevisiae


   DESCRIPTION OF PROBLEM
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
The immune system of the newly hatched chick is prepared to fight pathogens in a non-specific manner through innate immunity, and can develop specific modes of defense through cellular and humoral immunity, which requires contact with antigens [1]. Acquired immunity differs from the innate responses by possessing specificity in recognition of foreign invaders (antigens) and the development of memory; therefore, it results in a more rapid response than was elicited during the primary exposure when the bird is reexposed to an antigen [2].

Broilers have lymphoid structures spread throughout the intestinal tract, and these are made up of diffuse and aggregated components. Diffuse components include intraepithelial lymphocytes as well as lymphocytes of the mucosa and lamina propria; aggregated components include Peyer’s patches, cecal tonsils, and the bursa of Fabricius. These tissues capture antigens available in the digestive tract, which stimulate B lymphocyte-derived plasma cell precursors of IgM, IgG, and IgA, and T and B lymphocytes, which activate Peyer’s patches [3, 4] to enhance general and specific immunity.

The immunological stimulation of the mucosa favors the production of IgA antibodies [5–7], mainly in Peyer’s patches [8], which block receptors [9–11] and reduce the number of pathogenic bacteria in the intestinal lumen [12, 13]. The constant production of IgA secreted in large amounts on the surface of the intestinal mucosa occurs because of the continuous stimulation of normal gut microflora [14, 15].

Research has shown that the Harderian gland has large amounts of IgA and B lymphocytes on the surface, which perform a significant migration process to cecal tonsils and, at a lower rate, to the bursa of Fabricius. These data suggest a potential connection between the gut-associated immune system and the ocular immune system [16, 17].

Dietary bioactive food components that interact with the immune response have considerable potential to reduce susceptibility to infectious diseases. In fact, because of the genetically homogenous populations of domestic fowl in the commercial environment, using nutritional dietary intervention strategies could prove to be a cost-effective means of preventing specific infectious diseases and maintaining the health of poultry flocks [18].

Yeast extract is a protein source derived from the cell content of live yeast. It has high nucleotide, inositol, and glutamic acid levels [19]. In previous studies, the addition of yeast extract of Saccharomyces cerevisiae to broiler prestarter diets resulted in beneficial effects on the feed conversion of the birds at 21 d of age [20, 21]. Nucleotides are traditionally used in human diets, particularly in infant diets; they favor the development of the gastrointestinal tract and the immune functions, and they maintain the gut flora [22]. Further studies are required to explain the mechanism through which the immune system is influenced by dietary nucleotides. Although the majority of nucleotides in the diet are metabolized rapidly and then excreted, a significant amount of those retained are found in the gastrointestinal tissue [23]. Several factors, such as food restriction, rapid growth, and certain diseases, may interfere in the endogenous synthesis of these nucleotides; thus, the nucleotide becomes essential under these conditions [24]. Jyonouchi [23] investigated the impact of nucleotides on the immune response in vitro and determined its importance in maintaining the optimal conditions required for the humoral immune response. According to the author, nucleotide deficiency damages cell immunity, and supplementation is therefore recommended.

The positive effect of adding prebiotics to broiler diets on bird performance has been already demonstrated. In a survey conducted to investigate the effects of including mannan oligosaccharides in the prestarter diet of broilers reared under different temperatures (18, 25, and 32°C) [20], improvements in BW gain (5.11%) were observed in birds reared under a high temperature to 42 d of age and improvements in livability (2.80%) were observed until 21 d of age.

By promoting the growth of lactic acid-producing bacteria, prebiotics have an indirect, beneficial effect on the immune system of the host. These bacterial populations produce immunostimulating substances that react with the immune system at different levels, including the production of cytokines, mononuclear cells, and macrophage phagocytosis as well as the induction of synthesis of large amounts of Ig, particularly IgA [25, 26].

Newcastle disease is a contagious, lethal infection that affects all birds. It is caused by Paramyxovirus type 1 (Newcastle disease virus; NDV) [27, 28]. The maternal antibodies protect the chick during the first week of life and may interfere in the development of humoral immunity. However, they cannot invalidate the rapid establishment of vaccine protection [29].

Infectious bursal disease (IBD), also known as Gumboro, is an infectious, contagious disease that affects the bursa of Fabricius, a key organ in the development of the immune system of young birds [30]. In 1-d-old chicks, maternal antibody levels against IBD are high and remain so until d 7, and then they are reduced by approximately 35 d of age. Although these antibodies may be detected until wk 4 of life, protection limits are exhausted in the second week of life [31, 32].

It is widely known that ambient temperatures not only can change broiler susceptibility to infectious diseases, but also can affect the humoral immune response [33]. The effect of ambient temperature on immune response can vary according to the ability of the bird to maintain homeothermy [34]. Exposure of birds to adverse environmental conditions generates adaptive responses such as acclimation, which involves a series of reactions that peak with glucocorticoid secretion [35]. However, it is well known that the action of glucocorticoid is antagonistic to the development of the immune response in birds [36], thereby impairing the expression of the humoral immune response [37].

Considering this, the objective of this study was to assess the effect of yeast extract and prebiotic in a prestarter diet for broilers vaccinated against IBD and NDV, and raised at different temperatures, on maternal and postvaccinal humoral immune response.


   MATERIALS AND METHODS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Birds, Diets, and Management
The experiment was conducted in the experimental poultry house of the Department of Animal Science of the Universidade Estadual Paulista, Jaboticabal Campus, with 1,440 one-day-old male Cobb 500 [38] chicks. The birds were raised in 3 climatic chambers, 1 for each brooding temperature, and chambers were lined with polyurethane and had a heating-cooling system. The chambers were divided into 16 boxes with 2.5 x 1.0 m each. Birds were submitted to different temperatures, as shown in Table 1Go, and received water and feed ad libitum throughout the experimental period of 42 d.


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  		Table 1. Temperatures of the chambers (mean ± SD)
 
The experiment was fully randomized in a factorial design with subdivided plots (3 x 2 x 2 factorial design in the plots), using as factors brooding temperatures (high, control, and low), yeast extract levels (0 and 2%), and prebiotic levels (0 and 0.15%), and with subplots, using ages at blood and tear secretion collection (7, 14, 21, 28, 35, and 42 d of age). Four replicates were used with 30 birds/treatment replicate, totaling 12 treatments.

All the diets (in mash) were either unsupplemented or supplemented with yeast extract and prebiotic and were offered only in the prestarter phase (1 to 7 d). Beginning on d 8, all birds in each treatment were fed the same feed, adjusted according to the breeding phase (1 to 7 d, 8 to 21 d, and 22 to 42 d), as recommended by Rostagno et al. [39] (Table 2Go). The levels of yeast extract and prebiotic followed the directions of the product supplier. The diets were as follows: 1) diet 1: 0% yeast extract and 0% prebiotic; 2) diet 2: 2.0% yeast extract and 0% prebiotic; 3) diet 3: 0% yeast extract and 0.15% prebiotic; 4) diet 4: 2.0% yeast extract and 0.15% prebiotic.


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  		Table 2. Perceptual composition, chemistry composition, and energy value of the experimental diets in the phases at 1 to 7 d, 8 to 21 d, and 22 to 42 d of age
 
The supplements used in the diets were obtained from the processing of the yeast S. cerevisiae strain 1026. The mannan oligosaccharides [40] are derived from the yeast cell wall, and the yeast extract [41] is obtained after removal of the cell wall of yeast by processing with proteolytic enzymes.

At 8 d of age, the birds were vaccinated with live vaccine virus against NDV (La Sota strain) and IBD (intermediate strain Lukert), and at 18 d, the birds were vaccinated against IBD (strong strain Australia V-877). All vaccines were administered ocularly, diluted according to the recommendations of the manufacturer, at 30 mL/1,000 vaccine doses, or 30 µL/bird, based on the method described by Paulillo [42].

Analytical Procedures
Blood samples for antibody analysis were taken by puncture of the brachial vein, and for IgA analysis, the lacrimal secretions were collected by irritating the eye of the bird with glycerin. The samples were always taken from the same broilers by plot, at 7, 14, 21, 28, 35, and 42 d of age. Once serum and lacrimal secretions were taken, the samples were frozen at –20°C until they were submitted to analyses.

Serum antibody titers against NDV were measured by the hemagglutination inhibition test (HI) [43], and HI antibodies were then converted into log2. Immunoglobulin G titers against IBD were measured by the indirect enzyme-linked immunosorbent assay (ELISA) with a commercial kit [44]. Determination of IgA against the IBD found in lacrimal secretions was also measured by an indirect ELISA commercial kit [45] and a commercial goat anti-chicken IgA horse-radish peroxidase conjugate (chain specific) [46]. The HI titers were transformed into log2, and in the ELISA test, the optical density was converted into titer values based on the calculation recommended by the kit manufacturer.

The methodology for IgA analysis was adapted to the commercial kit used to determine IgG levels in IBD, and only plates coated with the kit antigen were used. Substrate and reagents were the same as used in the indirect ELISA. For that purpose, the plates were incubated with a 1 M bicarbonate buffer solution (pH 7.4) and skimmed powdered milk (SPM) for 45 min at 37°C. The plates were then washed with PBS-Tween 20 (PBST; pH 7.4) and, after a PBST and SPM solution was added to the plate, samples were distributed in the solution. The plate was then placed in an oven at 37°C for 60 min. After this procedure, the plate was washed again with PBST, followed by addition of PBST and SPM and finally the anti-IgA conjugate. The plate was placed back into the oven at 37°C for 120 min. After incubation, the plate was again washed with PBST, followed by the addition of a substrate solution containing O-phenylenediamine dihydrochloride, citrate buffer, and oxygenated water. After 15 min, 1 M HCl was added to stop the reaction. The reading was carried out at 490 nm with a microplate reader [47].

Statistical Analyses
Prior to statistical analyses, the authors checked for the presence of outliers and normality assumptions of Studentized errors (Cramérvon-Mises test) and for homogeneity of variances (Brown and Forsythe test). Analysis of variance was conducted with the GLM, a procedure of the SAS program [48]. Whenever significant differences were found, mean values were compared by Tukey’s test (5%).


   RESULTS AND DISCUSSION
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
The results for serum antibody titers (IgG) against NDV and IBD and lacrimal titers (IgA) in broilers supplemented with prebiotic and yeast extract in the prestarter diet and raised at different temperatures are presented in the Table 3Go.


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  		Table 3. Serum antibody titers (IgG) against Newcastle disease virus (NDV) and infectious bursal disease virus (IBD), and lacrimal titers (IgA) in broilers supplemented with prebiotic and yeast extract in the prestarter diet and raised at different temperatures
 
No significant effects of the prebiotic and yeast extract on the analyzed parameters were observed; however, it is important to highlight that according to preliminary trials [20, 49], the addition of yeast extract to broiler prestarter diets promoted better feed conversion and better livability at 21 d of age.

Although there was no significant effect of prebiotic on the immune response, it is important to note that additives such as prebiotics with high mannose levels increase the protective antibody response and improve resistance to diseases while reducing the acute response [20, 50]. By direct action, we can assume that some specific prebiotics may reduce pathogen translocation in the intestine [51]. These compounds would bind to macrophage reception sites by recognizing specific sugars found in glucoproteins of the epithelial surface, triggering a cascading reaction that would eventually activate macrophages and release cytokines, thereby activating the acquired immune response [52].

Various experiments have been conducted to examine the effect of mannan oligosaccharides on humoral and cell immunity. Lilburn et al. [53] demonstrated that inclusion at 0.5 and 1 g/kg enhanced the serum antibody titer against sheep erythrocyte antigen administered 1 wk before evaluation when using a microtiter procedure. The stimulatory effect of mannan oligosaccharide on antibody titer was statistically significant 7 d after sensitization, and numerical differences persisted throughout the following 4 wk as titers waned. Inclusion of mannan oligosaccharide at 1 g/kg of diet enhanced both IgG and IgA serum antibody levels in turkey poults, and statistically significant increases in both Ig were detected at 7.5 wk of age [54].

Swanson et al. [55], who supplemented the diet of adult dogs with 2 g/d of prebiotics, found increased IgA levels in the ileum. However, when prebiotics were added to the prestarter diet in the present study (when the immune system was preparing to begin its activity), the humoral immune response was not affected; however, the response after inclusion must be followed up in later phases of the production cycle.

We found no studies in the literature in which yeast extract was used only in the starter diet, nor did we find studies that used the additive at different temperatures, with the supply of the products only in the prestarter. In the few existing studies, yeast extract was fed to broiler chickens during the whole cycle of production (1 to 42 d).

There was no systemic response to the 8-d NDV vaccination, whereas the IBD vaccination at 8 d decreased antibodies but increased them when injected on d 18. These results support interference caused by passive antibodies. Maternal protection is essential to protect the birds in their first days of life against challenges in the field, but it has now been proven that immunity also acts to interfere with the virus vaccine in vaccination success.

There was a significant interaction between brooding temperature and age at collection on the humoral immune response in all the parameters assessed (see Tables 4Go, 5Go, and 6Go). It is important to emphasize that the temperatures in this study were not repeated in other climate chambers or through repetition over time because these procedures are costly owing to the number of animals with which we work. In this context, it would be good to note that several researchers conducted their field testing with the procedures used in this experiment.


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  		Table 4. Interaction of the effects of higher temperature on serum antibody titers (IgG) against Newcastle disease virus1 in broilers supplemented with prebiotics and yeast extract in the prestarter fraction and raised at different temperatures
 

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  		Table 5. Interaction of the effects of higher temperatures on serum antibody levels (IgG) against infectious bursal disease1 in broilers supplemented with prebiotics and yeast extract in the prestarter phase and raised at different temperatures
 

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  		Table 6. Interaction of the effects of higher temperature on lacrimal antibody titers (IgA) against infectious bursal disease1 in broilers supplemented with prebiotics and yeast extract in the prestarter fraction and raised at different temperatures
 
Given the ability of broilers to respond with active immunity as of the second week of life, and given that innate immunity and maternal antibodies are active in previous stages [56], a plausible explanation for the differences in NDV-IgG at 7 d of age for high and low temperatures (Table 2Go) would be that the transfer of IgG in the yolk sac membrane to the blood occurs until d 2 posthatch [57], when the yolk sac is absorbed. Environmental changes affect circulating hormones, such as T3 and T4, which in turn may affect the speed of yolk sac absorption [1, 58]. In addition, the exposure of young birds to high ambient temperatures prior to primary antigenic changes inhibits the development of the primary immune response [59].

Stress influences the immune system function by stimulating the hypothalamic-pituitary-adrenal axis [60], which stimulates the secretion of corticosterone and adrenocorticotropic hormone (ACTH). High corticosterone levels cause involution of lymphoid organs, such as the thymus, bursa, and spleen, and the redistribution of sub-populations of T lymphocytes [61, 62]. The bursa is an essential organ in the differentiation process of B lymphocytes and in the diversification of specificity in specific antibodies [63, 64], and the microenvironment of the thymus allows for the clonal formation of specific T-lymphocyte receptors, turning them into T-helper (CD4+) and T-cytotoxic (CD8+) lymphocytes [65].

The data collected contrast with those reported by Oba [66], who assessed the immune response to NDV in birds submitted to different temperatures and supplemented with chromium, and found the lowest titer value for NDV at 7 d under cool temperatures.

At 42 d of age, antibody titers for NDV were the highest at control temperatures, whereas the lowest titers were found at low temperatures (Table 4Go). The antibody titers for NDV at high temperatures were not statistically different from those found at low and control temperatures. The decrease found at 42 d of age at low temperatures was probably related to the greater susceptibility of birds to low temperatures because of the stronger adrenal activity triggered by stress.

Overall, the study showed the influence of ambient temperature on the immune system at critical ages, that is, over the first 2 wk. In addition, the low temperature acted as an immunomodulator, improving the humoral immune response to NDV when compared with thermoneutral conditions, and these results support the findings of Henken et al. [34] and Oba [66].

The lower humoral immune response of broilers raised at low temperatures, compared with thermoneutral conditions, can be explained by an association between the stress on the hypothalamic-pituitary-adrenal axis [60] and the production of IL-1 (IL-1) by macrophages, stimulated by antigen. Interleukin-1 stimulates the hypothalamus, leukocytes, or both to produce the corticotropin-releasing factor, which stimulates the production of ACTH by the anterior pituitary, leukocytes, or both. In addition, corticotropin-releasing factor can directly increase lymphocyte activity in the spleen, causing ACTH to stimulate the production of corticosteroids, which in turn will redistribute secondary lymphocytes, such as to the spleen, to process the antigen and produce antibodies against the invading antigen [67].

The breakdown study with different temperature ranges for antibody titers against IBD showed a statistical difference among the 3 temperatures at 7 and 42 d of age (Table 3Go). At 7 d, the birds raised at low temperatures had lower antibody titers for IBD when compared with the birds raised at high and control temperatures. The findings are different from those shown by others [66], who assessed the immune response for IBD and found no statistical difference among these temperatures and ages.

There are genetic differences in the time required to transfer the breeder’s antibodies to the egg by breeder immunization [67]. The percentage of eggs laid and the yolk weight are also important factors in the efficiency of IgG deposition in the egg [68], hence in the IgG available in the yolk subsequently to be transferred to the embryo. According to Shephard and Shek [69], cold stress suppresses lymphocyte proliferation, promotes a negative feedback of the immunological cascade, and reduces the number of natural killer cells and cytolytic activity.

The hypothalamus translates stress stimuli into neuroendocrine factors that can change the immune function [1, 70]. Under specific circumstances, corticosteroids may act as immunostimulants or immunomodulators, and they may regulate the development of both cellular and humoral immune responses, favoring and challenging the resistance to several pathogens [71]. During early response to stress, ACTH is released, leading to, among other physiological changes, increased blood lymphocyte levels to repair any possible physical damage and to fight any occasional aggressive agent [69]. This explains why the best maternal antibody values are found at high temperatures at 7 d of age.

At 42 d of age, birds raised at high temperatures had lower antibody titers for IBD when compared with birds raised at control temperatures. This can be explained by the greater sensitivity of the birds to heat stress at this age. This may have triggered the release of corticosterone, which in turn promoted the involution of lymphoid organs and, consequently, a lower humoral immune response to IBD.

On studying different ages for variable IgA, we found the only statistical difference at 14 and 35 d, when the birds raised at control and low temperatures, respectively, had higher IgA values (Table 6Go). Despite the lack of statistical difference in IgA titer values in the lacrimal secretion of birds raised at low temperatures, these values tended to remain higher from 21 to 42 d of age when compared with other temperatures. There was a difference in the titer values of the birds at 14 d of age, indicating that the high and low temperatures affected the systemic response of the birds at this age.


   CONCLUSIONS AND APPLICATIONS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
REFERENCES AND NOTES
 

  1. The addition of yeast extract and pre-biotic in the prestarter phase had no effect on the humoral immune response to NDV and IBD throughout the production cycle of the broilers.
  2. The higher temperature increased the IgG values, because it particularly affected maternal antibodies, despite the immunomodulating effect caused by heat stress until the wk 2 of life.
  3. Low temperatures favored higher and constant IgA levels in lacrimal secretion during the growth phase of the broilers.
  4. Further studies are required to assess the potential benefit of low broiler brooding temperatures on mucosal protection.


   ACKNOWLEDGMENTS
 
The authors thank Alltech do Brasil Agroindustrial Ltda and Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP) for financial support, and Conselho Nacional de Desenvolvimento Técnico e Pesquisa (CNPq) for student support.


   REFERENCES AND NOTES
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 

  1. Torres, K. A. A. 2006. Influência do estresse térmico no nascedouro sobre a imunidade humoral e as características zootécnicas de frangos de corte. MS Thesis, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista, Jaboticabal, São Paulo, Brazil.
  2. Kogut, M. H., and K. Klasing. 2009. An immunologist’s perspective on nutrition, immunity, and infectious diseases: Introduction and overview. J. Appl. Poult. Res. 18:103–110.[Abstract/Free Full Text]
  3. Montassier, H. J. 1998. Importância da imunidade em pintos na primeira semana de vida. Pages 99–120 in Simpósio Internacional Sobre Manejo de Pintos de Corte, Conferência Apinco. FACTA, Campinas, São Paulo, Brazil.
  4. Montassier, H. J. 2004. Imunologia do aparelho digestório das aves. In Curso de Fisiologia da Digestão e Metabolismo dos Nutrientes em Aves, 2004, Jaboticabal. Anais Jaboticabal, Centro Virtual de Ciência Avícola, Jaboticabal, São Paulo, Brazil [CD-Rom].
  5. Brandtzaeg, P., T. S. Halstensen, P. Krajci, D. Kvale, T. O. Rognum, H. Scott, and L. M. Sollid. 1989. Immunobiology and immunopathology of human gut mucosa: Humoral immunity and intraepithelial lymphocytes. Gastroenterology 97:1562–1584.[Web of Science][Medline]
  6. Salminen, S., C. Bouley, M. C. Boutron-Ruault, J. H. Cummings, A. Franck, G. R. Gibson, E. Isolauri, M. C. Moreau, M. Roberfroid, and I. Rowland. 1998. Functional food science and gastrointestinal physiology and function. Br. J. Nutr. 80:147–171.[CrossRef]
  7. Bengmark, S. 2000. Gut microbial ecology in critical illness: Is there a role for pre-, pro-, and synbiotics. Curr. Opin. Crit. Care 8:145–151.[CrossRef]
  8. Gebert, A., S. Fassbender, K. Werner, and A. Weissferdt. 1999. The development of M cells in Peyer’s patches is restricted to specialized dome-associated crypts. Am. J. Pathol. 154:1573–1582.[Abstract/Free Full Text]
  9. Perdigón, G., E. Vintiñ, S. Alvarez, M. Medina, and M. Medici. 1999. Study of the possible mechanisms involved in the mucosal immune system activation by lactic acid bacteria. J. Dairy Sci. 82:1108–1114.[Abstract]
  10. Shu, Q., F. Qu, and H. S. Gill. 2001. Probiotic treatment using Bifidobacterium lactis HN019 reduces weanling diarrhea associated with rotavirus and Escherichia coli infection in a piglet model. J. Pediatr. Gastr. Nutr. 33:171–177.[CrossRef][Web of Science][Medline]
  11. Yasui, H., S. Shida, T. Matsuzaki, and T. Yokokura. 1999. Immunomodulatory function of lactic acid bacteria. Antonie Leeuwenhoek 76:383–389.[CrossRef][Web of Science][Medline]
  12. Jin, L. Z., Y. W. Ho, N. Abdullah, and S. Jalaludin. 1997. Prebiotics in poultry? Modes of actions. World’s Poult. Sci. J. 53:351–368.[CrossRef][Web of Science]
  13. Perozo, F., G. Finol, and Y. Mavarez. 2007. Niveles de inmunoglobulina A en muestras de tráquea, intestino y bilis provenientes de aves vacunadas contra la enfermedad de Newcastle. Rev. Cient. 17:226–230.
  14. Falk, P. G., L. V. Hooper, T. Midtvedt, and J. I. Gordon. 1998. Creating and maintaining the gastrointestinal ecosystem: What we know and need to know from gnotobiology. Microbiol. Mol. Biol. Rev. 62:1157–1170.[Abstract/Free Full Text]
  15. Franco, M. A., and H. B. Greenberg. 1999. Immunity to rotavirus infection in mice. J. Infect. Dis. 179:S466–S469.[CrossRef][Web of Science][Medline]
  16. Muir, W. I., W. L. Bryden, and A. J. Husband. 2000. Immunity, vaccination and avian intestinal tract. Dev. Comp. Immunol. 24:325–342.[CrossRef][Web of Science][Medline]
  17. Yun, C. H., H. S. Lillehoj, and E. P. Lillehoj. 2000. Intestinal immune responses to coccidiosis. Dev. Comp. Immunol. 24:303–324.[CrossRef][Web of Science][Medline]
  18. Kogut, M. H. 2009. Impact of nutrition on the innate immune response to infection in poultry. J. Appl. Poult. Res. 18:111–124.[Abstract/Free Full Text]
  19. Rutz, F., J. L. Rech, E. G. Xavier, M. A. Anciuti, and P. Rossi. 2005. Cuidados críticos na nutrição inicial de aves: Alternativas para melhorar o desempenho e o papel essencial dos nucleotídeos. Pages 19–39 in Simpósio Brasileiro da Indústria de Alimentação Animal, Ronda Latino Americana da Alltech, Curitiba, Paraná, Brazil.
  20. Silva, V. K. 2006. Extrato de levedura (Saccharomyces cerevisiae) e prebiótico na dieta préinicial para frangos de corte criados em diferentes temperaturas. PhD Thesis. Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista, Jaboticabal, São Paulo, Brazil.
  21. Rutz, F., M. A. Anciuti, J. L. Rech, F. M. Gonçalves, A. D. Delgado, E. R. Rosa, N. Zauk, C. L. G. Ribeiro, R. R. Silva, and P. R. Dallmann. 2006. Desempenho e característica de carcaça de frangos de corte recebendo extrato de levedura na dieta. Ciênc. Anim. Bras. 7:349–355.
  22. Uauy, R., G. Stringel, R. Thomas, and R. Quan. 1990. Effect of dietary nucleosides of growth and maturation of the developing gut in rat. J. Pediatr. Gastroenterol. Nutr. 10:497–503.[Web of Science][Medline]
  23. Jyonouchi, H. 1994. Nucleotide actions on humoral immune responses. J. Nutr. 124(Suppl. 1):138–143.
  24. Carver, J. D., and W. A. Walker. 1995. The role of nucleotides in human nutrition. J. Nutr. Biochem. 6:58–72.[CrossRef][Web of Science]
  25. Yasui, H., and M. Ohwaki. 1995. Enhancement of immune response in Peyer’s patch cells cultured with Bifidobacterium breve. J. Dairy Sci. 74:1187–1195.
  26. Macfarlane, G. T., and J. H. Cummings. 1999. Probiotics and prebiotics: Can regulating the activities of intestinal bacteria benefit health? Br. Med. J. 318:999–1003.[Free Full Text]
  27. Grando, N. 2002. Doença de Newcastle. Pages 66–72 in Simpósio Brasil Sul de Avicultura, 3. Empresa Brasileira de Pesquisa Agropecuária, Chapecó, Santa Catarina, Brazil.
  28. Ali, A. S., M. O. Absalla, and M. E. H. Mohammed. 2004. Interaction between Newcastle disease and infectious bursal disease vaccines commonly used in Sudan. Int. J. Poult. Sci. 3:300–304.[CrossRef]
  29. Kouwenhoven, B. 1993. Newcastle disease. p. 341–361 in J. B. McFerran and M. S. Nulty. Virus Infections of Birds. Elsevier Science Publishers, Amsterdam, the Netherlands.
  30. Kneipp, Z. A. F. 2000. Doença de Gumboro no Brasil. Pages 79–88 in Simpósio de Sanidade Avícola, 2. EMBRA-PA, Santa Maria, Rio Grande do Sul, Brazil.
  31. Lukert, P. D., and Y. M. Saif. 1997. Infections Bursal Disease. 9th ed. Iowa State University Press, Ames.
  32. Zaheer, A., and S. Akhter. 2003. Role of maternal antibodies in protection against infectious bursal disease in commercial broilers. Int. J. Poult. Sci. 2:251–255.[CrossRef]
  33. Beard, C. W., and B. W. Mitchell. 1987. Influence of environmental temperatures on the serologic responses of broiler chickens to inactivated and viable Newcastle disease vaccines. Avian Dis. 31:321–326.[CrossRef][Web of Science][Medline]
  34. Henken, A. M., A. M. J. Groote Schaarsberg, and M. G. B. Nieuwland. 1983. The effect of environmental temperature on immune response and metabolism of the young chicken 3. Effect of environmental temperature on the humoral immune response following injection of sheep red blood cells. Poult. Sci. 62:51–58.[Web of Science][Medline]
  35. Geraert, P. A., J. C. F. Padilha, and S. Guillaumin. 1996. Metabolic and endocrine changes induced by chronic heat exposure in broiler chickens: Biological and endocrinological variables. Br. J. Nutr. 75:205–216.[CrossRef][Web of Science][Medline]
  36. Tankson, J. D., Y. Vizzier-Thaxton, J. P. Thaxton, J. D. May, and J. A. Cameron. 2001. Stress and nutritional quality of broilers. Poult. Sci. 80:1384–1389.[Abstract/Free Full Text]
  37. Thaxton, P., and H. S. Siegel. 1973. Modification of high temperature and ACTH induced immunodepression by Metyrapone. Poult. Sci. 52:618–624.[Web of Science][Medline]
  38. Cobb do Brasil, Guapiaçu, São Paulo, Brazil.
  39. Rostagno, H. S., L. F. T. Albino, J. L. Donzele, P. C. Gomes, R. F. Oliveira, A. S. Ferreira, and S. L. T. Barreto. 2000. Tabelas brasileiras para aves e suínos: Composição dos alimentos e exigências nutricionais. Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.
  40. Bio-Mos, Alltech do Brasil Agroindustrial Ltda., Araucária, Paraná, Brazil.
  41. Nupro, Alltech do Brasil Agroindustrial Ltda., Araucária, Paraná, Brazil.
  42. Paulillo, A. C. 1987. Doença de Newcastle. IV. Ensaio experimental de diferentes vias de vacinação com estirpe lentogênica LaSota em frangos de corte. Ars. Vet. 3:73–79.
  43. Cunningham, C. H. 1971. Virologia Practica. 6th ed. Editora Acribia, Saragossa, Spain.
  44. ProFLOK IBD ELISA kit, Synbiotics Corporation, Via Frontera, San Diego, CA.
  45. ND ProFLOk, Synbiotics Corporation, San Diego, CA.
  46. Bethyl Laboratories Inc., Montgomery, TX.
  47. Model 550, Bio-Rad, Hercules, CA.
  48. SAS Institute. 2004. SAS/STAT Version 9.1 User’s Guide. SAS Inst. Inc., Cary, NC.
  49. Silva, V. K., J. D. T. Silva, R. A. Gravena, R. H. Marques, F. H. Hada, and V. M. B. Moraes. 2009. Desempenho de frangos de corte de 1 a 21 dias de idade alimentados com extrato de leveduras e prebiótico e criados em diferentes temperaturas. R. Bras. Zootec. 38:690–696.
  50. Rutz, F., and S. R. Collet. 2006. Alternativas para o desenvolvimento e função intestinal, visando a digestão e a absorção na ausência de aditivos químicos. Pages 139–159 in Conferência Apinco de Ciência e Tecnologia Avícolas. FACTA, Santos, São Paulo, Brazil.
  51. Silva, E. N., and R. L. Andreatti Filho. 2000. Probióticos e prebióticos na avicultura. Pages 45–54 in Simpósio de Sanidade Avícola, 2. Santa Maria, Rio Grande do Sul, Brazil.
  52. Collet, S. 2000. Nutrição, imunidade e produtividade. Pages 20–30 in Ronda Latino-americana Alltech: O futuro da alimentação. Alltech Biotechnology, Campinas, São Paulo, Brazil.
  53. Lilburn, M., J. Dixon, P. Cotter, B. Paluch, A. Malzone, T. Sefton, and A. Connolly. 2000. Modulation of humoral immunity in commercial laying hens by a dietary probiotic. Poult. Sci. 79(Suppl. 1):38. (Abstr.)
  54. Savage, T. F., P. F. Cotter, and E. I. Zakrzewska. 1996. The effects of feeding a mannan oligosaccharide on immunoglobulins, plasma IgG and bile IgA, of Wrolstad MW male turkeys. Poult. Sci. 75:143–148.
  55. Swanson, K. S., C. M. Grieshop, E. A. Flickinger, L. L. Bauer, H. P. Healy, K. A. Dawson, N. R. Merchen, and G. C. F. Fahey Jr.. 2002. Supplemental fructooligosaccharides and mannanoligosaccharides influence immune function, ileal and total tract nutrient digestibilities, microbial populations and concentrations of protein catabolites in the large bowel of dogs. J. Nutr. 132:980–989.[Abstract/Free Full Text]
  56. Friedman, A., E. Bar-Shira, and D. Sklan. 2003. Ontogeny of gut associated immune competence in the chick. World’s Poult. Sci. J. 59:209–219.[CrossRef][Web of Science]
  57. Nakano, T., H. H. Sunwoo, B. H. Paek, H. S. Chae, and J. S. Sim. 1998. Effects of egg and yolk (IgY) production in laying chickens. Poult. Sci. 77:266–270.[Abstract/Free Full Text]
  58. Iqbal, A., E. Decuypere, A. Abd El Azim, and E. R. Kühn. 1990. Pre- and post- hatch high temperature exposure affects the thyroid hormones, and corticosterone responses to acute heat stress in growing chicken (Gallus domesticus). J. Therm. Biol. 15:149–153.[CrossRef][Web of Science]
  59. Thaxton, P., C. R. Sadler, and B. Glick. 1968. Immune response of chickens following heat exposure or injections with ACTH. Poult. Sci. 47:264–266.[Web of Science][Medline]
  60. Thaxton, P., and H. S. Siegel. 1970. Immunodepression in young chickens by high environmental temperature. Poult. Sci. 49:202–205.[Web of Science][Medline]
  61. Marsh, J. A., and C. C. Scanes. 1994. Neuroendocrine-immune interactions. Poult. Sci. 73:1049–1061.[Web of Science][Medline]
  62. Trout, J. M., and M. M. Mashaly. 1994. The effects of adrenocorticotropic hormone and heat stress in the distribution of lymphocyte populations in immature male chickens. Poult. Sci. 73:1694–1698.[Web of Science][Medline]
  63. Paramithiotis, E., and M. J. H. Ratcliffe. 1994. Survivors of bursal B cell production and emigration. Poult. Sci. 73:991–997.[Web of Science][Medline]
  64. Glick, B. 1995. Embryogenesis of the bursa of Fabricius: Stem cell, microenvironment, and receptor-paracrine pathways. Poult. Sci. 74:419–426.[Web of Science][Medline]
  65. Glick, B. 2000. Immunophysiology. Pages 657–670 in Sturkie’s Avian Physiology. 5th ed. San Diego, CA.
  66. Oba, A. 2004. Utilização do crômio na dieta de frangos de corte criados sob diferentes condições de ambiente. PhD Thesis. Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista, Jaboticabal, São Paulo, Brazil.
  67. Mashaly, M. M., J. M. Trout, G. L. Hendricks Iii, L. M. Al-Dokhi, and A. Gehad. 1998. The role of neuroendocrine immune interactions in the initiation of humoral immunity in chickens. Domest. Anim. Endocrinol. 15:409–422.[CrossRef][Web of Science][Medline]
  68. Boa-Amponsem, K., E. A. Dunnington, and P. B. Siegel. 1997. Antibody transmitting ability of hens from lines of chickens differing in response to SRBC antigen. Br. Poult. Sci. 38:480–484.[CrossRef][Web of Science][Medline]
  69. Shephard, R. J., and P. N. Shek. 1998. Cold exposure and immune function. Can. J. Physiol. Pharmacol. 76:826–836.
  70. Ballone, G. J. 2006. Estresse. PsiqWeb Psiquiatria Geral, 2002. Disponível em http://www.psiqweb.med.br/site/?area=NO/LerNoticia&idNoticia=64 Accessed May 2006.
  71. Morgulis, M. S. 2002. Imunologia aplicada. Pages 231–245 in M. Macari, R. L. Furlan, and E. Gonzales. Fisiologia Aplicada a Frangos de Corte. FUNEP/UNESP, Jaboticabal, São Paulo, Brazil.




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