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Poult Sci 2008. 87:1947-1954. doi:10.3382/ps.2007-00477
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ENVIRONMENT, WELL-BEING, AND BEHAVIOR

Effects of Social Disruption on Physical Parameters, Corticosterone Concentrations, and Immune System in Two Genetic Lines of White Leghorn Layers

A. G. Fahey*,{dagger} and H.-W. Cheng{dagger},1

* Department of Animal Sciences, Purdue University, West Lafayette, IN 47907; and {dagger} USDA-Agricultural Research Service, Livestock Behavior Research Unit, West Lafayette, IN 47907

1 Corresponding author: Heng-wei.Cheng{at}ars.usda.gov


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Farm management practices such as increasing group size and mixing of unfamiliar chickens may cause social disruption and affect bird well-being. To examine genetic-associated physical and physiological differences in response to social disruption, 2 strains of White Leghorn hens were used in the study [i.e., HGPS (line selected for high group production and survivability) and DXL (DeKalb XL commercial line)]. Social disruption was created when hens were 50 wk of age by increasing group size from 4 hens (control) to 8 hens (experimental) per cage and providing an unstable social environment by moving 2 hens weekly between cages within the same line (experimental hens only). At 58 wk of age, hens were feather-scored. After euthanization, BW and the right adrenal gland weight were collected (n = 10 per treatment). Adrenal gland weight was adjusted for BW, and adjusted adrenal weight was used for analysis. Plasma corticosterone was quantified using RIA. The T-lymphocytes (CD4+ and CD8+) were measured using flow cytometry. Results showed that average feather cover score was greater for DXL hens than HGPS hens in both the unstressed (P < 0.05) and stressed treatment (P < 0.01). There was no difference in BW in DXL and HGPS hens between the control and the social disruption treatments. However, the relative adrenal weight of HGPS hens tended to be lower than control hens after social disruption (0.05 > P < 0.10). Plasma corticosterone was significantly lower in both strains following social disruption (P < 0.01). The T-lymphocyte ratio (CD4+:CD8+) was greater in HGPS hens than DXL hens post social disruption (P < 0.05). The data indicate that the 2 strains of hens reacted differently in terms of the adrenal system and immunity in response to social disruption. Hens selected for longevity with docile behaviors and high productivity, such as HGPS hens, provide a useful tool for improving animal well-being.

Key Words: social disruption • corticosterone • immune parameter • hematology • hen


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Animals have the ability to adapt or habituate to various stressors, and as a result, physiological homeostasis may return to baseline levels or remain unbalanced over extended periods. This is affected by the previous experiences of the animals and characteristics of the stressors (Amario et al., 1984, 1986). Stress susceptibility of poultry is a major problem, and some managerial practices that may subject hens to stress need to be investigated.

It has been suggested that intermittent stressors such as social disruption may be more relevant to modern intensified agricultural systems than other types of stressors (Ladewig, 2000), because animals are often mixed in different groups depending on their life cycle. For example, hens may be mixed with unfamiliar conspecifics when they are transferred from the growing facility to the laying facility. Intermingling of unfamiliar hens has been reported to be stressful (Anthony et al., 1988). Inability of hens to adapt to their social environments results in a greater susceptibility to stimulation and an increase in the frequency of abnormal behaviors, such as feather pecking, aggression, and cannibalism (Guhl, 1964; Bilcik and Keeling, 2000; El-Lethey et al., 2000). Similarly, in other species including rodents, force-mixing during a resident-intruder test resulted in resident rodent males mostly attacking intruder males, causing high mortality (Blanchard et al., 1977, 1985).

Reaction to social stress is a strain-specific interaction between dominance hierarchies and environmental conditions. Differences in behavioral patterns may reflect changes in the social status and neuroendocrine state of animals, such as a change in adrenal functions (Cheng et al., 2001a), immunosuppression (Cheng et al., 2001b), and poor feathering and high mortality (Craig and Muir, 1996a). Genetic selection of hens for a docile phenotype with high resistance to social stress may help to decrease the stress response to social disruption. This may arise by improving the ability of the hens to adapt to environmental stimulations, for example disruption in social structure, in combination with increased group size.

White Leghorn hens selected for high group productivity and survivability (HGPS) using a genetic selection program called group selection has produced a less aggressive strain (Craig and Muir, 1996a,b; Muir and Craig, 1998; Cheng et al., 2001a,b). Selection was based upon productivity, average rate of lay, and survivability based on days of survival in colony cages. Hens were not beak-trimmed, and high light intensity was used to provide conditions that exacerbated expression of aggressive behavior, stress, and affecting productivity (Craig and Muir, 1996a,b). Compared with the DeKalb XL (DXL) strain, the HGPS strain had better rate of lay, feather score, decreased flightiness, and cannibalism (Craig and Muir, 1996a,b). In addition, HGPS hens were more tolerant of heat and cold stress, indicated by lower mortality and greater egg production compared with the DXL hens under the same conditions (Hester et al., 1996).

Physical and physiological parameters that have been used as stress indicators in poultry are mortality rate, body injury, and feather coverage. Indeed, Moinard et al. (1998) found that hens assessed to have poor welfare had greater mortality rates and poorer feather coverage, which may be due to negative stress. Craig and Muir (1996a) also found in a previous study that DXL hens had greater mortality than HGPS hens due to cannibalism associated with aggression when housed in 12 hen cages. Stress sensitivity in animals is also dependent on changes in the neuroendocrine systems, including altered adrenal functions. Hens selected for high corticosterone concentration exhibited greater social stress than hens selected for low corticosterone concentrations (Gross and Colmano, 1971; Gross and Siegel, 1985), and alteration of plasma corticosterone has been used as an indicator of social stress in chickens (Thompson et al., 1980). Environmental stressors have been shown to have the ability to alter the immune function of the animal (Biondi and Zannino, 1997; Grammatopoulos and Chrousos, 2002; Tsigos and Chrousos, 2002). This has shown to be dependant on the genetic background of the animal and genetic-environmental interactions. In a study comparing diversely selected hen strains, Cheng et al. (2001b) showed that the HGPS strain had a greater T-lymphocyte profile (CD4+:CD8+) than its counterpart, the strain counterselected for low group productivity and survivability (LGPS). Compared with DXL hens, HGPS hens also had a lower heterophil:lymphocyte ratio after heat stress (Hester et al., 1996). In fact, hens that have a low CD4+:CD8+ profile with or without a greater heterophil:lymphocyte ratio have impaired reactions to stress (Hester et al., 1996; Cheng et al., 2001b).

These studies suggest that genetic selection, using the group selection method, is an effective strategy for improving hen well-being by modifying the ability of the hen to adapt to environmental stressors. The current study is one in a series investigating effects of genetic-environmental interactions on well-being in laying hens. The objective of this experiment was to determine the effects of genetic-environmental interactions on the functions of the adrenal and immune systems of hens after an unstable social environment.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Genetic Strain

Hens from the HGPS and DXL strains were used in this study. The HGPS strain was developed by crossing all available commercial strains in 1982, one of which was the DXL commercial strain. The HGPS strain was derived from hens selected for high group egg production and survivability, resulting from decreased aggression and cannibalism (Muir, 1996; Muir and Craig, 1998). The DXL strain was selected based on individual productivity and is known to have high mortality rates, resulting from cannibalism-associated aggression, in group-housing situations (Craig and Muir, 1996a,b). The differences in productivity and survivability of the 2 strains have been reported previously (Craig and Muir, 1996a).

In this study, poultry care was in accordance with the guidelines set by the Federation of Animal Science Societies (http://www.fass.org/facts/poultry.htm). The experimental protocol was approved by the Institutional Animal Care and Use Committee at Purdue University (protocol 00-008-06).

Experimental Design

At 17 wk of age, 120 hens were moved from the growing facility to the laying facility and were randomly assigned to the treatment groups, and treatment groups were randomly distrubted around the laying facility. Hens were not beak-trimmed in this study and had 16 h of light and 8 h of darkness. Hens received an industry standard layer single diet and water ad libitum.

Social disruption was used as stressor in this study. The hens subjected to social disruption were housed in an 8-hen cage (542 cm2/hen, n = 10), whereas control hens were kept in a 4-hen cage (542 cm2/hen, n = 10). At 50 wk of age, hens of the unstressed group (controls) remained in the same cage for the duration of the experiment. In the socially disrupted treatment, 2 hens were sequentially moved weekly among the cages until 58 wk of age.

Mortality

All hens were checked on a daily basis. Dead hens were removed from their cages and recorded. Hens that were severely injured were removed, killed, and then added to the mortality list. Data were presented as percentage mortality [(number of dead hens/total hens of the treatment) x 100].

Body and Organ Weights

At the end of the experiment (58 wk of age), 1 hen was taken randomly from the cages in each treatment and then killed by cervical dislocation (n = 10 per treatment). The BW of each hen was recorded. Based on the asymmetric development of the adrenal glands between the right and left side, and the irregular shape of the left adrenal gland resulting from development of the reproductive system, the right side adrenal gland was dissected without fat and weighed. The relative adrenal weight [(absolute adrenal weight/BW) x 100] was used for statistical analysis.

Blood Sampling

Hens were sedated with sodium pentabarbitol, and a 15-mL blood sample was taken from each hen. Hens within and across treatments were randomly sampled to decrease experimental bias. Blood samples were collected into an EDTA-coated tube via cardiac puncture within 2 min of removal from the cage. Hens were killed after blood sampling.

RIA for Corticosterone

Blood samples were centrifuged for 15 min at 700 x g to obtain plasma, and 300 µL of this plasma was used for RIA analysis of corticosterone. Plasma was kept at –80°C until measurement. Total plasma corticosterone was measured using a commercially available 125I corticosterone RIA kit (catalog no. 07-120122, MP Biomedicals, Solon, OH) as outlined by Cheng et al. (2001a). Plasma samples were randomized before being analyzed by RIA to decrease experimental variation.

Flow Cytometry Analysis for Immunocompetent Cells

Blood samples were centrifuged at 700 x g for 15 min at 20°C. The T-lymphocytes (CD4+ and CD8+) were isolated from the buffy coat layer of the centrifuged blood and analyzed using flow cytometry (Epics XL-MCL, Beckman Coulter Inc., Fullerton, CA). The cell number in the lymphocyte solution was obtained using a Coulter Z1 cell counter, and the cells were then suspended in RPMI Medium 1640 (catalog no. R5886, Sigma-Aldrich, St. Louis, MO) at 1 x 106 cells/mL. Two hundred microliters of the cell suspension of each sample was added into separate tubes for phenotype determination using direct fluorescein isothiocyanate- and phycoerythrin-conjugated antibodies for CD4+ and CD8+ immune cells (Southern Biotechnology Inc., Birmingham, AL), respectively. Based on our preliminary study, the cells were incubated for 1 h at 4°C with antibody concentrations as follows: 50 uL of 1:50 and 1:100 diluted for CD4+ and CD8+ cells, respectively. After washing 3 times with FACS solution (BD Biosciences, San Jose, CA) by centrifugation and then being fixed with 1.0% paraformaldehyde, the percentage of labeled cells was determined using a Coulter XL MCL Flow Cytometer (Beckman Coulter Inc.) with a 488-nm air-cooled argon laser for excitation, a 525-band pass for fluorescein isothiocyanate labels, and a 575-nm band pass for phycoerythrin detection. All necessary negative controls were included (Eicher-Pruiett et al., 1992; Boeker et al., 1999). The results were analyzed using the system II software (Beckman Coulter Inc.), and the results were reported as the percentage of total live cells.

Feather Scores

Feather scoring was used to asses the quality of feather coverage of each hen. Feathers were scored on a 0 to 5 scale, with the best score at 0 and the worst score at 5 (Table 1Go). Seven body regions were assessed, and an average of these was taken as the total feather score for each hen. Feather score data collection was conducted by the same trained person to eliminate interobserver variation.


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  		Table 1. Feather score guidelines applied to hens at 58 wk of age
 
Statistical Analysis

All analysis was carried out using the SAS V9.1 software package (SAS Institute Inc., Cary, NC). Histograms, qqplots, and the Kolmogorov-Smirnov goodness-of-fit test for normal distribution in the UNIVARIATE procedure was used to assess if data had a normal distribution. Data that did not approach a normal distribution were transformed using a transformation suggested by the Box-Cox operation in the TRANSREG procedure. It was determined that corticosterone and T-lymphocyte data required a base-10 logarithm transformation. Data (except mortality) were analyzed using the MIXED procedure. Mortality was analyzed using a {chi}2 test using the FREQ procedure. Comparisons were made between genetic lines within treatment and within genetic line across treatment. Corticosterone and T-lymphocyte data presented in this paper show the nontransformed values of the data; however, all P-values were calculated using the corresponding transformed version of the data. A Tukey-Kramer adjustment was used to account for multiple comparisons. Data were analyzed using the model: Yijkl = Sj + Tk + SjTk + cl(sjtk) + {varepsilon}ijkl where Yijkl = the fixed effect of ith physiological indicator from the jth strain given the kth treatment in the lth cage; Sj = the fixed effect of DXL or HGPS chickens; Tk = the fixed effect of the socially disruptive treatment or the control treatment; SjTk = the fixed effect of jth strain in the kth treatment; cl(sjtk) = the random effect of jth strain in the kth treatment in the lth cage; and {varepsilon}ijkl = the residual error. Statistical differences were reported when P-values were <0.05, and statistical trends were reported when P-values were >0.05 and <0.10.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Mortality

Effects of genetic and genetic-environmental social interactions on hen mortality were found in the study (Figure 1Go). In non socially disrupted control hens, there were no differences in mortality between the 2 strains. In addition, there was no difference in mortality between the socially disrupted hens and control hens in the HGPS strain. However, in the DXL strain, the socially disrupted hens had a greater mortality, resulting from cannibalism, than control hens (social disruption:control; 32.5%:12.5%, P < 0.01). These results are in agreement with the data reported by Craig and Muir (1996a), who found mortality due to cannibalism in DXL hens (referred to as strain X) to be greater than HGPS hens (referred to as strain S). The present and previous data suggest that selection for productivity and docile behaviors in hens improves their stress response, which is a universal conclusion regardless of whether they were housed at a stable or unstable social structure in a crowded group setting.


Figure 1
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  		Figure 1. The effect of social disruption on mortality levels in DXL and HGPS hens at 58 wk. There were the effects of genetic and genetic-environmental interactions on hen mortality. There were no differences in mortality between unstressed hens from the 2 strains. However, in the DXL hens but not HGPS hens, the social disruption caused a greater mortality than control hens. a,bP < 0.01 within genetic line; A,BP < 0.01 between genetic lines. DXL (DeKalb XL) is a commercial line individually selected for productivity. HGPS (high group production and survivability) is a group-selected line selected for productivity and survivability. Disrupt is the social disruption of hens due to repeated movement between cages.

 
Feather Scores

There were genetic and genetic-environmental effects on feather score (Table 2Go). Compared with HGPS control hens, DXL control hens had a greater body feather score (greater feather score indicates worse feather coverage; P < 0.05). Feather score was further increased in the DXL hens but not in the HGPS hens after social disruption (P < 0.01). In the social disruption treatment, DXL hens had worse feather coverage on the head and tail compared with their conspecific controls (P < 0.01). These results are in agreement with previous findings (Craig and Muir, 1996a), in which the authors reported that DXL hens had inferior feather coverage compared with HGPS hens in a crowded social environment.


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  		Table 2. The effects of social disruption for feather scores (least squares means ± standard error) for 7 body regions and total feather scores for DXL1 and HGPS2 hens at 58 wk of age
 
It has been suggested that incidence of cannibalism is positively correlated with poor feather coverage, because exposed skin is more easily damaged (Ambrosen and Petersen, 1997). McAdie and Keeling (2000) hypothesized that unprotected skin will bleed when pecked, encouraging cannibalistic behavior. In addition, aggressive pecking is mostly directed at the head, and pecking associated with cannibalism is mostly directed toward the cloaca (cloacal cannibalism, Cloutier and Newberry, 2002). These hypotheses are consistent with the present results, because DXL hens had the worst feather coverage especially on the head and tail with a concurrent greater incidence of cannibalism and greater mortality than HGPS hens. Feather score data further indicated that the well-being of DXL hens was adversely affected by social disruption than HGPS hens. Group selection may have decreased aggressive behaviors in the HGPS hens, resulting in declined feather pecking and removing fewer feathers from conspecifics.

Body Weight, Relative Adrenal Weight, and RIA for Corticosterone

There were no significant differences for BW of hens within or between treatments (P > 0.05, Table 3Go). Relative adrenal gland weights were not different between the HGPS and DXL controls (P > 0.05). Compared with their controls, the relative adrenal gland weight was decreased in the HGPS hens (0.05 > P < 0.10) but not in the DXL hens (P > 0.10) post social disruption.


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  		Table 3. The effects of social disruption for body weight, relative adrenal weight,1 and corticosterone for DXL2 and HGPS3 hens at 58 wk of age
 
The reasons for the social disruptive effects on BW are unclear. Although it was not examined in this study, social disruption could cause an initial decrease in BW in hens immediately after the first time movement of hens, when creating an unstable social environment. However, this effect could be overcome by the repeated movement of hens among the cages. There is abundant evidence that acute and chronic stress have different effects on BW. A study comparing weaning age in beef calves found that compared with conventionally weaned calves, early weaned calves had an initially decreased BW (Arthington et al., 2005) but weighed as much or more as conventionally weaned calves at a later age (Arthington et al., 2005; Rasby 2007). Marin et al. (2007) reported that in rats, chronic restraint did not cause BW loss. Moreover, in rats, weight loss produced by short-term food restriction can be prevented by repeated handling for 20 d (Carrera et al., 2006). These results indicate that stress-caused changes of BW and organ weights are affected by multiple factors, including the type, degree, and duration of the stressors. The current and previous results suggest that BW may not be a good indicator for stress due to repeated social disruption in many species, including hens.

There were no differences in the baseline plasma concentrations of corticosterone between HGPS and DXL controls (P > 0.05, Table 3Go). However, plasma corticosterone levels were significantly decreased in both HGPS and DXL hens after social disruption (P < 0.01). Similar to the present results, chronic or intermittent stress caused reduction of corticosterone response after an initial increase was found in rodents (File, 1982; Armario et al., 1986), monkeys (Levine and Mody, 2003), and humans (Lehmann and Feldon, 2000; Pryce et al., 2001). In a study in which dairy heifers were tethered, their cortisol response to adrenocorticotropic hormone (ACTH) injections decreased over time (Redbo, 1993). Results from these previous studies further indicate that in hens, similar to mammals, intermittent exposure to the same type of stressful stimulus, such as social disruption, can lead to decreased physiological and neuroendocrine responses, including the hypothalamic-pituitary-adrenal (HPA) axis.

It is interesting to note that correlations between relative adrenal weight and corticosterone were negative for HGPS hens, whereas they were positive for DXL hens (Table 3Go). Various stress-associated correlations between changes in adrenal weight (hypertrophy, hypotrophy, or no change) and corticosterone concentrations (increase, decrease, or no change) have been reported previously and are affected by several factors such as experimental animal (species, age, sex, and experience), stressors (type, intensity, duration, interval, and number of stressors), and environment (single and group). Gross and Siegel (1979) and Siegel and Gould (1982) reported that adrenal atrophy and secretion of glucocorticoids were negatively correlated in hens subjected to repeated stressors over a prolonged period. In humans, a 50% reduction in adrenal size was positively correlated with lower cortisol levels in patients suffering from chronic fatigue syndrome (Scott et al., 1999), in which the authors suggested that people with chronic fatigue syndrome had a reduction in adrenocortical tissue, which would decrease the cortisol synthesis capacity. A similar cellular mechanism may be present in the HGPS hens stressed by repeated social disruption. It is possible that repeated exposure to stress caused a gradual decrease in the responsiveness of the HPA axis, which can lead to the development of habituation in HGPS hens. Through this regulation system, HGPS may have a decreased stress response indicating an ability to cope with a changing social environment. In contrast, stressed DXL hens had a tendency to have heavier adrenal glands with decreased corticosterone synthesis post social disruptive treatment, which may indicate the HPA axis of the DXL hens was at a hypofunctional state (adrenocortical insufficiency). The cellular mechanism of the reaction is still unclear, but it could be similar to the less efficient negative corticosterone-ACTH-corticotropin-releasing hormone feedback regulation in mammals [i.e., low levels of corticosterone stimulates releasing ACTH from the pituitary, then high levels of ACTH lead to hypertrophy of the adrenal glands, but the cells of the adrenal cortex are insufficient to synthesize corticosterone (LiVoisi et al., 1993)]. Our results suggest that stressed DXL hens may be in an adrenal insufficiency state compared with the HGPS hens. However, the hypothesis needs to be tested in future studies.

Flow Cytometry Analysis for Subpopulation of T Cells

The CD4+ cells are helper T lymphocytes that activate CD8+ cells to become activated cytotoxic T cells and B lymphocytes to develop into antibody-producing plasma cells and to secrete cytokines, which in turn activate macrophages and natural killer cells. The CD8+ cells are cytotoxic T cells, which are involved in the cell-mediated response, by directly targeting infected cells (Janeway et al., 2001). Stress results in the increase of the ratio of CD4+:CD8+, indicating an increase in the efficiency of cell-mediated immunity as a result of stress. In supporting the suggestion, it has been found that dexamethasone is a compound that increases HPA axis activity in a similar way to stress. When 1-yr-old beef steers were injected with dexamethasone, there was a transient increase in CD4+:CD8+ ratio through an increase in CD4+ and a decrease in CD8+ cells (Anderson et al., 1999). In another study that looked at the effects of transportation stress in dairy steers, transportation increased the CD4+:CD8+ ratio in bronchoalveolar fluid (Ishizaki et al., 2005). A metaanalysis study using 834 human patients across 16 studies that suffered from stress showed that the CD4+:CD8+ ratio was increased by stress (Zorrilla et al., 2001). Levinson and Jawetz (1996) suggested that a CD4+:CD8+ ratio greater than 1.5 was required for efficient cell-mediated immunity. The current data showed that compared with the strain controls, the percentage of CD4+ cells was greater in HGPS hens after repeated social disruption (P < 0.05, Table 4Go). Stressed DXL hens had a significant increase in the percentage CD8+ cells (P < 0.05), but there were no changes of CD8+ cells in HGPS hens as a result of repeated social disruption. Compared with its controls, CD4+:CD8+ ratio increased numerically in HGPS hens, whereas it decreased numerically in DXL hens after social disruption (P > 0.05), by which the HGPS hens had a significantly greater CD4+:CD8+ ratio than DXL hens (P < 0.05). The contrasting numerical changes in CD4+:CD8+ ratio between DXL and HGPS hens may suggest that group selection for productivity and survivability results in altered immune response to stress.


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  		Table 4. The effects of social disruption for T-lymphocyte (CD4+ and CD8+) percentages (least squares means ± standard error) for DXL1 and HGPS2 hens at 58 wk of age
 
In conclusion, results from this study show that there are strain differences in mortality, feather scores, and the regulation of the adrenal function and cell-mediated immunity. The DXL hens were more adversely affected by intermittent social disruption than HGPS hens. These results suggest different selection strategies (group selection versus individual selection) have altered behavioral and immune responses of hens to stress. The selection-associated physiological differences may be involved in regulating the unique characteristics of each strain in productivity and survivability, along with different coping strategies for various environmental stressors. The current strains, HGPS and DXL, could be used as animal models to investigate the cellular and molecular mechanisms underlying the effects of genotype x environment interactions on the functions of the neuroimmunoendocrine system in controlling domestic behavior, productivity, and longevity as related to adaptation to the current egg production systems.


   ACKNOWLEDGMENTS
 
We are grateful to students and employees of the USDA-Agricultural Research Service Livestock Behavioral Research Unit for their assistance in the collection of data. We would also like to thank Fred Haan and all the employees of the Purdue University poultry farm for their assistance. Thank you to Mark Einstein in the Animal Sciences Department (Purdue University) for his statistical advice. We would also like to express gratitude to Don Lay (USDA-Agricultural Research Service) for his assistance in manuscript preparation. This work was supported by a USDA-National Research Initiative grant.

Received for publication November 24, 2007. Accepted for publication June 13, 2008.


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H.-W. Cheng and A. Fahey
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Poult. Sci., October 1, 2009; 88(10): 2018 - 2025.
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