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Poult Sci 2007. 86:636-642
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IMMUNOLOGY, HEALTH, AND DISEASE

Influence of Hen Age on the Response of Turkey Poults to Cold Stress, Escherichia coli Challenge, and Treatment with a Yeast Extract Antibiotic Alternative1

G. R. Huff*,2, W. E. Huff*, N. C. Rath*, F. Solis de los Santos{dagger}, M. B. Farnell{ddagger} and A. M. Donoghue*

* USDA, Agricultural Research Service Poultry Production and Product Safety Research, Fayetteville, AR 72701; {dagger} Department of Poultry Science, University of Arkansas, Fayetteville 72701; and {ddagger} Department of Poultry Science, Texas A&M University, College Station 77843

2 Corresponding author: grhuff{at}uark.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Two battery experiments were conducted to evaluate a commercial yeast extract feed supplement, Alphamune, in a cold stress-Escherichia coli challenge of 1-wk-old turkeys. Experiment 1 used 1-d-old male poults that were the progeny of 33-wk-old hens in their second week of lay. Experiment 2 used male poults of the same genetic line from 40-wk-old hens in their eighth week of lay. Poults were fed a standard unmedicated turkey starter diet or the same diet with either a low level (504 g/t) or a high level (1,008 g/t) of yeast extract. Challenged birds were exposed to intermittent cold stress during wk 1 to 3 and to a respiratory E. coli challenge at 1 wk of age. In both experiments, BW at wk 1 was increased by feeding yeast extract. In experiment 1, challenged, control-fed birds had decreased BW at wk 3 and feed conversion was protected by both levels of yeast extract supplementation. In experiment 2, challenge had no effect on control-fed birds; however, yeast extract decreased the BW of challenged birds. In experiment 1, total leukocyte numbers were decreased by challenge of control-fed birds only, and there was no effect of challenge on the heterophil/lymphocyte ratio. In experiment 2, total leukocyte numbers were decreased and the heterophil/lymphocyte ratio was increased in challenged, control-fed birds. Percentage mortality was not affected by challenge in experiment 1; however, in experiment 2, mortality was increased by challenge of control-fed birds and those fed the lower level of yeast extract. These results suggest that hen age should be considered when designing studies to evaluate antibiotic alternatives and in making decisions for incorporating such alternatives into production.

Key Words: turkey • yeast extract • hen age • Escherichia coli • cold stress


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Antibiotics have been used in animal production as an economical means of increasing production and preventing disease (Dibner and Richards, 2005). However, the emergence of antibiotic resistance in pathogenic bacteria has led to concern over their use in animal production and has resulted in worldwide consideration of preventing or limiting their use in animal agriculture.

Colibacillosis is a systemic infection by Escherichia coli that is most often acquired from the litter via inhalation through the respiratory tract. It is the most frequently reported poultry disease and requires antibiotics for both treatment and prevention (Barnes et al., 2003). Colibac-illosis can be exacerbated by cold stress, which is one of the many stressors inherent in poultry production that can lead to stimulation or suppression of the immune response and can thereby decrease performance (Hangalapura et al., 2006).

Brewers yeast (Saccharomyces cerevisiae) extracts, which are byproducts of beer manufacturing, have been added to animal feeds for many years for their nutritional content (Westendorf and Wohlt, 2002). Because they also have immunomodulating activity, it is thought that they may serve as alternatives to antibiotics for both growth promotion and disease resistance in poultry production. Brewers dried yeast has been used as a source of mannan oligosaccharides (MOS) and ß-glucans by a number of companies providing antibiotic-replacement products for animal production. Whole yeast or yeast cell walls have been shown to improve growth of both broiler chicks (Zhang et al., 2005) and turkey poults (Bradley et al., 1994).

Mannan oligosaccharides are polysaccharide-protein complexes derived from yeast that are indigestible to non-ruminant animals and can function as prebiotics, providing favorable conditions for beneficial intestinal Lactobacillus spp. (Flickinger and Fahey, 2002). They also provide competitive binding sites for pathogens with mannose-specific fimbriae, causing them to pass through the intestine, thus decreasing attachment and colonization (Newman, 1994). They have been shown to improve BW of turkeys grown to market age (Parks et al., 2001; Sims et al., 2004; Zdunczyk et al., 2005) and to improve feed conversion in turkeys grown to 20 wk (Fritts and Waldroup, 2003).

ß-Glucans are polymers of glucose that can also be derived from yeast cell walls, bacteria, fungi, and cereals such as oats, barley, and rye. Each type of ß-glucan has a unique structure in which glucose molecules are linked together in different ways, resulting in different physical properties. Variations in molecular weight, degree of branching, conformation, and intermolecular associations can affect their biological activity (Bohn and BeMiller, 1995). One of these molecules, the ß-1,3/1,6-glucan from the cell wall of S. cerevisiae, is recognized as foreign by the immune systems of mammals, fish, and birds and has been shown to be protective in a number of disease challenge studies (Mansell et al., 1978; Williams and Di Luzio, 1979; Reynolds et al., 1980). There is extensive literature describing the immunomodulating effects of ß-glucan in mammals, with most reporting an increase in functional activity of macrophages and neutrophils (Reynolds et al., 1980; Cleary et al., 1999; Tzianabos, 2000). A ß-1,3/1,6-glucan product was recently shown to decrease Salmonella enterica serovar Enteritidis organ invasion and stimulate phagocytosis, bacterial killing, and oxidative burst in heterophils isolated from 4-d-old male Leghorn chickens 24 h after oral challenge (Lowry et al., 2005). In studies evaluating the efficacy of a ß-glucan feed supplement as an antibiotic alternative for broiler chicks it was reported that immunomodulation resulted in protection from the effects of E. coli challenge, but also resulted in lower BW of nonchallenged controls (Huff et al., 2006), probably due to energy reallocation toward the immune response as proposed by Klasing et al. (1987).

The objective of the present study was to evaluate the ability of a commercial brewers yeast extract feed additive (Alphamune, Alpharma Animal Health, Antwerp, Belgium) that combines both the immunomodulatory properties of a standardized level of (1,3)/(1,6) ß-glucans with the performance enhancement of MOS to protect against the effects of a subacute E. coli respiratory challenge and intermittent cold stress of turkey poults.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Experimental Birds
All experimental conditions and animal protocols were approved by the University of Arkansas Institutional Animal Care and Use Committee under Protocol # 06017. In both experiments, male Hybrid Converter turkey poults (Hybrid, Kitchener, Ontario, Canada) of the same genetic lineage were obtained from the same commercial hatchery at day of hatch and were transported to the University of Arkansas Poultry Research Farm. For each experiment, 180 birds were weighed by pen, wing-banded, and placed into randomly assigned brooder battery pens. There were 6 treatments with 3 replicate pens of 10 birds/pen for each treatment in a 3 x 2 (3 feed treatments x 2 challenges) experimental arrangement.

In both experiments, birds were kept under incandescent lighting on a light schedule consisting of 23 h light and 1 h dark. They were provided ad libitum access to water and an unmedicated standard corn and soybean turkey starter diet that met or exceeded the NRC recommended allowances (National Research Council, 1994), and which contained 2,884 kcal of ME/kg and 28.8% CP. Birds were fed an unsupplemented diet or the same diet supplemented with a low level (LL) of 504 g/tonne (1 lb/ton) or a high level (HL) of 1,008 g/tonne (2 lb/ton) of a standardized yeast extract feed supplement (Alphamune). Individual bird weights and feed consumption by pen were determined weekly.

Although every effort was made to duplicate all of the conditions of these 2 experiments, including bird genetics and hatchery source, it was retrospectively determined that the poults in experiment 1 were the progeny of 33-wk-old hens in their second week of lay (referred to herein as younger hens) and the time from lay to set was 2 to 9 d. The poults obtained for experiment 2 were from another flock on the same complex, managed by the same integrator, and were the progeny of 40-wk-old hens in their eighth week of lay (referred to herein as older hens); the time from lay to set was 10 to 13 d. Company management also recorded that the poults in experiment 1 were hatched from lighter eggs and were placed in a cooler brooder house than those from experiment 2. Mean BW at 1 d of age was significantly lower in experiment 1 compared with experiment 2 (48.5 and 52.8 g, respectively, P = 0.004).

Cold Stress and Respiratory Challenge
In both experiments, challenged birds were exposed to intermittent cold stress during wk 1 to 3 for increasing periods as described in Table 1Go. The need for an increasing level of cold stress to affect immune and production values was determined in preliminary experiments that showed either no effects or an improvement in disease resistance when birds were cold-stressed for constant periods over 3 wk (data not shown). The first 4 cold-stress treatments included a handling stress component, as birds were removed from their pens and each pen of 10 birds was placed in an individual basket, which was then transported to the cold room. Birds were returned to their original pens following cold stress. The final cold-stress treatment (d 19) entailed placing each treatment group of birds (3 pens, 30 birds) into a commercial transport coop, a process which included cold stress, handling stress, and social stress, and then placing the coops in the cold room. Mean RH of the cold room was 61.4 ± 5%. Controls were not subjected to stressors and were not inoculated. The temperature of the control room was maintained according to established standard operating procedures. Brooders were set at 32.3°C for the first week, after which room temperature was maintained at 24.8°C ± 1.5 and RH at 63 ± 2.3% for the remainder of the study using an automated air handling system.


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  		Table 1. Intermittent cold stress schedule for experiments 1 and 2
 
At 7 d of age, during the cold-stress treatment, birds were challenged by coarse spray inoculation of eyes and nares with approximately 3 to 4 x 108 cfu of a nonmotile serotype O2 strain of E. coli that had originally been isolated from chickens with colisepticemia and has been used to reproduce turkey osteomyelitis complex (Huff et al., 1998, 2000). The inoculum was prepared by adding 2 loops of a fresh 18-h culture that was grown on Columbia sheep blood agar at 37°C to 100 mL of tryptose phosphate broth and incubating for 2.5 h in a 37°C shaking waterbath. The culture was serially diluted and held overnight for 18 to 20 h at 4°C while a standard plate count was made and counted.

Mortality data were collected twice each day after challenge and birds were weighed and examined for lesions of airsacculitis. The following key, modified from that described by Piercy and West (1976), was used to score lesions of airsacculitis and pericarditis observed in both mortalities and at necropsy: 0 = no inflammation; 1 = opacity and thickening of the inoculated air sac; 2 = mild airsacculitis and mild pericarditis; 3 = moderate airsacculitis or pericarditis with spread to liver or abdominal cavity (perihepatitis or peritonitis); 4 = severe fibrinous airsacculitis and severe pericarditis; and 5 = severe airsacculitis or pericarditis with spread to liver or abdominal cavity.

Hematology and Necropsy
At 13 d postchallenge, 3 birds/pen (9 birds/treatment) were bled by venipuncture into EDTA-coated Vacutainer tubes (Becton Dickinson, Franklin Lakes, NJ). Total leukocyte counts and the proportions of heterophils, lymphocytes, monocytes, eosinophils, and basophils were determined using a Cell-Dyn 3500 blood analysis system (Abbott Diagnostics, Abbott Park, IL), which uses both electronic impedance and laser light scattering and was standardized for analysis of chicken and turkey blood. Heterophil/lymphocyte ratios (H/L) were determined by dividing the number of heterophils in 1 mL of peripheral blood by the number of lymphocytes. The following day all surviving birds were euthanized, weighed, and scored for lesions of colibacillosis.

Statistical Analysis
Data were analyzed by pen as a 3 x 2 factorial arrangement (3 treatments x 2 challenges) using the GLM procedure of SAS software (SAS Institute, 1999) for ANOVA. Means were separated using Duncan’s multiple range test and the least squares means procedure (SAS Institute, 1999) with pen as the experimental unit. Data comparing values between experiment 1 and experiment 2 were determined using the t-test procedure of SAS. A P-value of less than 0.05 was considered significant unless otherwise stated.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
In experiment 1 the prechallenge BW (wk 1) of poults from younger hens was increased more by LL yeast extract (P < 0.0001) than by HL yeast extract (P = 0.05; Figure 1aGo). In experiment 2 the prechallenge BW (wk 1) of poults from older hens was increased by HL yeast extract (P < 0.02; Figure 1bGo). In experiment 1 the wk-3 BW of poults from younger hens was decreased by cold stress-E. coli (P = 0.005); this decrease was prevented by both levels of yeast extract (Figure 1cGo). In experiment 2 the wk-3 BW of poults from older hens was not decreased by cold stress-E. coli. However, E. coli challenge decreased BW of birds fed LL (P = 0.002) or HL yeast extract (P = 0.0002) relative to their unchallenged controls (Figure 1dGo).


Figure 1
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  		Figure 1. Effects of yeast extract treatment and age of breeder hen on performance characteristics of poults challenged by cold stress and Escherichia coli infection. Birds were fed an unmedicated standard corn and soybean turkey starter diet (control feed) or the control diet supplemented with a low level (LL) or high level (HL) of yeast extract. Prechallenge BW (wk 1) of poults from a) younger hens and b) older hens (b); wk 3 BW of poults from c) younger hens and d) older hens; feed conversion of poults from e) younger hens and f) older hens. Each bar represents the pen mean ± SEM of 3 pens of 10 birds each. a,bWithin each graph, bars with differing letters are significantly different (P ≤ 0.05).

 
In experiment 1 the feed:gain ratio of poults was increased by cold stress-E. coli (P = 0.004), and this increase was prevented by both levels of yeast extract (Figure 1eGo). In experiment 2 the feed:gain ratio was not affected by cold stress-E. coli challenge or by yeast extract treatment (Figure 1fGo).

In experiment 1 the number of leukocytes in peripheral blood was decreased by cold stress-E. coli in control-fed poults from younger hens (P = 0.04) and marginally decreased in birds fed LL yeast extract (P = 0.1) but was protected by HL yeast extract (P = 0.79; Figure 2aGo). However, the H/L ratio was not affected by either cold stressE. coli or by yeast extract treatment (Figure 2cGo). In experiment 2 the number of leukocytes in peripheral blood was decreased by cold stress-E. coli in control-fed poults from older hens (P = 0.03) but was not decreased in challenged birds fed either LL or HL yeast extract (Figure 2bGo). In experiment 2 the H/L ratio of control fed poults was increased by cold stress-E. coli challenge (P = 0.0003) and the basal H/L ratio was increased in birds fed both levels of yeast extract (P = 0.01; Figure 2dGo).


Figure 2
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  		Figure 2. Effects of yeast extract treatment and age of breeder hen on total leukocyte counts and heterophil/lymphocyte ratio (H/L) of poults challenged by cold stress and Escherichia coli infection. Birds were fed an unmedicated standard corn and soybean turkey starter diet (control feed) or the control diet supplemented with a low level (LL) or high level (HL) of yeast extract. Total leukocyte counts of poults from a) younger hens and b) older hens; H/L of poults from c) younger hens and d) older hens. Each bar represents the pen mean ± SEM of values obtained from blood samples of 9 birds. a,bWithin each graph, bars with differing letters are significantly different (P ≤ 0.05).

 
There were no significant differences due to treatment or challenge in either percentage mortality (Figure 3aGo) or airsacculitis scores (Figure 3cGo) in experiment 1. In experiment 2, overall percentage mortality was increased by the cold stress-E. coli challenge (P = 0.0001) (Figure 3bGo) and was higher in both control-fed and LL yeast extract birds relative to their respective controls. In experiment 2, overall airsacculitis scores were nominally higher in stressed birds (P = 0.06), although there were no significant differences between feed treatments (Figure 3dGo).


Figure 3
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  		Figure 3. Effects of yeast extract treatment and age of breeder hen on percentage mortality and airsacculitis scores of poults challenged by cold stress and Escherichia coli infection. Birds were fed an unmedicated standard corn and soybean turkey starter diet (control feed) or the control diet supplemented with a low level (LL) or high level (HL) of yeast extract. Percentage mortality of poults from a) younger hens and b) older hens; airsacculitis scores of poults from c) younger hens and d) older hens. Birds were scored on a scale of 1 to 5. Each bar represents the pen mean ± SEM of 3 pens of 10 birds each. a,bWithin each graph, bars with differing letters are significantly different (P ≤ 0.05).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In these 2 experiments, genetics and hatchery source, treatment and challenge conditions, and all management and environmental variables were highly controlled. Nonetheless, there were highly significant differences in the poults’ responses to the cold stress-E. coli challenge as well as to supplementation with yeast extract. Retrospectively, it was determined that the poults in experiment 1 were the progeny of younger hens, and that the initial BW were significantly lower than the poults obtained in experiment 2, which were the progeny of older hens. The experiment 1 hens fall into the E (33 to 38 wk) age category and the experiment 2 hens fall into the M (39 to 44 wk) age category as defined by Christensen et al. (1996), who showed that poults from E hens had lower BW and higher blood glucose and heart glycogen levels than did poults from M hens. Fairchild et al. (2001) suggested that poults from young hens might be less able to cope with environmental stressors than those from older hens. They found that supplementation with MOS increased BW of 2-wk-old turkeys from young hens (33 wk) but did not affect BW of poults from older hens (58 wk). In the same study MOS significantly increased the mortality of poults given an oral E. coli challenge, but in that study hen age did not significantly affect the mortality or BW of challenged poults.

Recently, Siegel et al. (2006) have suggested that poults from younger hens may be less fit than those from older hens, and thus may receive more benefit from supplementation with vitamin E. They also comment that there is an increasing body of information suggesting that hen age is relevant when comparing genetic stocks. This study agrees with that observation and suggests further that the physiological response to stress may be directly affected by hen age.

Paradoxically, in the present study, the cold stress-E. coli challenge increased mortality (P = 0.0001) and airsacculitis scores (P = 0.06) in poults from older hens but not in those from younger hens. The poults from older hens had a 3-fold higher response to the cold stress-E. coli challenge than those from younger hens as determined by both the H/L ratio, a standard measure of the stress response of birds, and the nominal increases in airsacculitis scores. Because the challenge was the same in both experiments, this finding may indicate that because the poults from younger hens were less able to mount an inflammatory response to the challenge compared with poults from older hens, they had less airsac inflammation and therefore less mortality. We have previously documented that an enhanced inflammatory response increases mortality due to colibacillosis in turkeys, because the pathology is immune mediated (Bayyari et al., 1997). An immune-mediated pathology due to inflammation may also have led to the reported increase in mortality in MOS-supplemented poults that were orally challenged with E. coli (Fairchild et al., 2001).

Yeast extract supplementation significantly improved both the BW and the feed:gain ratio of the poults challenged in experiment 1. Neither the cold stress-E. coli challenge nor the yeast extract treatment affected production values of nonchallenged birds in experiment 2; however, the challenge did decrease the BW of birds provided with yeast extract relative to their respective unchallenged controls. The decrease in BW seen with yeast extract supplementation of these birds may reflect the costs of overenhancing the immune response of birds that were already well equipped to respond to the challenge. Stress has variable effects on the immune system and can both enhance and suppress responses depending on the type and degree of stress and individual variation in the host response (Siegel, 1995). Cold stress has been shown to have variable results that can both stimulate and suppress the immune response in chickens (Regnier and Kelley, 1981; Hangalapura et al., 2006). Additive effects of cold stress and yeast extract on the immune response may have been responsible for the decrease in BW seen in supplemented birds in experiment 2. Yalçin et al. (2005) reported that broiler chickens from younger breeder flocks are less able to thermoregulate than those from older parents. Their report concluded that the age of the parent plays an important role in the ability of broilers to adapt to heat stress. Similarly, these studies suggest that turkey poults from young and inexperienced breeder hens may also have a differential response to cold stress and a blunted inflammatory response compared with those from older hens. Immunostimulation using yeast extract supplements may protect poults from young breeder flocks from some of the production loss due to cold stress and E. coli infection but may sometimes be detrimental to birds not needing immunostimulation.

The effects of hen age on the stress response of progeny is an often-overlooked experimental variable that may explain some of the variability seen in experiments testing the value of antibiotic-alternative products with immunomodulatory effects such as yeast extracts. These results suggest that hen age should be considered when designing studies to evaluate antibiotic alternatives and also in making management decisions for incorporating such alternatives into production.


   ACKNOWLEDGMENTS
 
We are grateful to Steven Clark and Kurt Dobson, Alpharma Animal Health, for providing Alphamune for these studies and also for their advice and assistance in this project. We also gratefully acknowledge the excellent technical assistance of Dana Bassi, Sonia Tsai, Scott Zornes, David Horlick, and Wally McDonner.


   FOOTNOTES
 
1 Mention of a trade name, proprietary product, or specific equipment does not constitute a guarantee or warranty by the USDA and does not imply its approval to the exclusion of other products that may be suitable. Back

Received for publication September 29, 2006. Accepted for publication December 8, 2006.


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TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
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