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Poult Sci 2007. 86:2492-2501. doi:10.3382/ps.2006-00400
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ENVIRONMENT, WELL-BEING, AND BEHAVIOR

Molting in Salmonella Enteritidis-Challenged Laying Hens Fed Alfalfa Crumbles. III. Blood Plasma Metabolite Response

C. S. Dunkley*,1, J. L. McReynolds{dagger},2, K. D. Dunkley*, L. F. Kubena{dagger}, D. J. Nisbet{dagger} and S. C. Ricke*,3

* Texas A&M University, Department of Poultry Science, College Station 77843-2472; and {dagger} USDA-ARS, Southern Plains Agricultural Research Center, Food and Feed Safety Research Unit, College Station, TX 77843

2 Corresponding author: mcreynolds{at}ffsru.usda.gov


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
The objective of this study was to examine an alfalfa crumble diet as an alternative molt diet and compare the physiological response of hens to the responses of feed-deprived molted hens. Hens >50 wk old were placed into 6 treatment groups (12 hens per group in trial 1 and 10 hens per group in trial 2): nonmolted Salmonella enterica serovar Enteritidis positive (FF+), nonmolted Salmonella Enteritidis negative (FF–), feed withdrawal Salmonella Enteritidis positive (FW+), FW Salmonella Enteritidis negative (FW), alfalfa Salmonella Enteritidis positive (ALC+), and ALC Salmonella Enteritidis negative (ALC–). Each hen in the Salmonella Enteritidis-positive groups was challenged on the fourth day of the study with 1 mL of 106-cfu Salmonella Enteritidis. Blood was collected on d 2, 5, 9, and 12 of the trial. Blood plasma was collected and metabolite concentrations were analyzed for glucose, calcium, cholesterol, uric acid, total protein, and triglycerides. The feed intakes of the FF hens were 4- to 6-fold greater (P ≤ 0.05) than those of the ALC birds in both trials. Over the 12 d of molt, the FW+ hens lost more (P ≤ 0.05) BW than all other groups except the FW– hens, whereas the FW–, ALC–, and ALC+ hens lost more BW than the FF hen groups. Uric acid concentrations were generally lower in molted hens compared with the FF hen groups during the initial stages of molt. On d 9 of both trials, concentrations of calcium and total protein were higher (P ≤ 0.05) in the FF hens than in the other groups. The FF hen groups exhibited higher (P ≤ 0.05) concentrations of triglycerides than the FW and ALC groups in both trials on d 5, 9, and 12. Based on the results from these studies, ALC diets can limit some of the potential physiological stress indicators that accompany feed deprivation during an induced molt.

Key Words: alfalfa • laying hen • immune response • molt • Salmonella


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
The practice of feed withdrawal for molt induction has been described as stressful and can lead to increased infection by Salmonella enterica serovar Enteritidis in laying hens (Holt, 2003; Ricke, 2003; Webster, 2003). Given the concerns regarding feed-withdrawal molt induction, researchers over the years have developed various methods to induce a molt by creating diets with nutritional imbalances or feeding high-fiber, low-energy diets (Berry, 2003; Park et al., 2004a,b). A variety of high-fiber diets have been incorporated in poultry feed, including cottonseed meats (Davis et al., 2002), grape pomace (Keshavarz and Quimby, 2002), and wheat middlings (Seo et al., 2001; Biggs et al., 2003). Alfalfa-based diets also have the potential to serve as dietary sources for inducing a molt. When used to induce a molt in laying hens, alfalfa meal limited Salmonella Enteritidis colonization and infection during the molt (McReynolds et al., 2005, 2006; Woodward et al., 2005). Landers et al. (2005a, b) found that hens molted with alfalfa meal or alfalfa pellets had ovary regression responses equivalent to those of hens molted with feed withdrawal, and the hens also retained acceptable egg production characteristics in the second laying cycle. Donalson et al. (2005) observed similar results when they examined molting layer hens fed with different ratios of alfalfa meal and layer ration.

The development of an alternative to the feed-withdrawal diet is essential to alleviate concerns of reduced animal welfare and increased infectivity. Our overall goal is to examine alfalfa in the form of a crumble diet as an alternative molt-induction diet and to compare the physiological responses of the hens with the responses that hens express during feed deprivation. Stress causes a general deterioration of the well-being of chickens, usually involving a cascade of physiological adaptive responses that include changes in plasma levels of blood metabolites (Puvadolpirod and Thaxton, 2000a,b,c,d; Thaxton and Puvadolpirod, 2000). In this study we determined the effects of alfalfa crumble molt diets on a series of blood plasma metabolites.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Blood Collection and Chemical Analysis

Experiments 1 and 2 were conducted with 250 Single Comb White Leghorn hens >50 wk old, obtained from a local commercial laying flock. Twelve hens were used in each of 6 treatments in trial 1, and 10 hens were used in each of 6 treatments in trial 2. Treatment groups were designated as follows: 1) feed withdrawal Salmonella Enteritidis-positive (FW+), 2) fully fed Salmonella Enteritidis-positive (FF+), 3) 100% alfalfa crumble Salmonella Enteritidis-positive (ALC+), 4) feed withdrawal Salmonella Enteritidis-negative (FW–), 5) fully fed Salmonella Enteritidis-negative (FF–), and 6) 100% alfalfa crumble Salmonella Enteritidis-negative (ALC–). Molt procedures, Salmonella methods, and diets are described elsewhere (Dunkley et al., 2007b). Twenty-one-gauge, 1.5-in. (12.7 mm) needles were used to collect approximately 8 mL of blood from the jugular vein in the neck of 12 birds, which were randomly selected at the beginning of the study, to obtain the baseline data. Eight hens from each treatment group were bled in a similar manner on d 2, 5, 9, and 12 of the molt. Seven-milliliter quantities of blood were placed in 10-mL nonheparinized blood collection tubes (Preanalytical Solutions, BD Vacutainer, Franklin Lakes, NJ) and the remaining 1 mL was placed in EDTA tubes (BD Vacutainer) to be used for smearing microscope slides to determine the heterophil to lymphocyte ratio for experiments described by Dunkley et al. (2007a). The plasma was separated by centrifugation at 610 x g for 15 min. The clear supernatant plasma from each sample was collected, placed in plastic vials, and stored at –20°C until chemical analysis could be conducted.

A clinical chemistry analyzer (Gilford Impact 400E, Ciba Corning Diagnostic Corp., Gilford Systems, Oberlin, OH) was used to analyze spectrophotometrically the concentrations of the plasma metabolite parameters in each of the samples by using methods described previously (Kubena et al., 1985; Park et al., 1999). Chemical reagents obtained from Bayer HealthCare (Bayer Diagnostics, Europe Limited, Chapel Lane, Swords, Co. Dublin, Ireland) were used as outlined in the manufacturer’s manual to determine the concentrations of the following plasma metabolites: calcium, cholesterol, total protein, glucose, triglycerides, and uric acid. Cuvettes were loaded with 1 mL of the respective reagent and 20 µL of the sample. The cuvettes were agitated to ensure proper mixing of the liquids and subsequently allowed to incubate at room temperature for approximately 5 min, after which they were read by the chemical analyzer.

Statistical Analysis

The concentrations of blood plasma metabolites were summarized in each treatment, and means of each metabolite over the 12-d period were analyzed by using a repeated-measures design. The GLM procedure of SAS (SAS version 8.3, SAS Institute Inc., Cary, NC) was used, with treatment, time, the treatment x time interaction, and individual hens nested within treatment as the factors. Hens nested within treatment was used as the error term to test for treatment effects. When significant (P ≤ 0.05) treatment x time interactions were found, means were compared by using the least significant difference.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Feed Intake and Weight Loss

The feed intakes of the FF hens were 4- to 6-fold greater (P ≤ 0.05) than those of the ALC hens (Table 1Go). In general, ALC consumption was similar to the feed intake levels reported for 100% alfalfa meal (Woodward et al., 2005). Sen et al. (1998) concluded that reduced feed intake by nonruminant animals fed alfalfa could be due to the low palatability. The slow passage rate of alfalfa through the chickens’ gastrointestinal tract reported by Sibbald (1979) may also reduce feed intake. Over the 12-d molt period, the FW+ hens lost more (P ≤ 0.05) BW (Table 1Go) than all the other groups except the FW– hens, whereas the FW–, ALC–, and ALC+ hens lost more (P ≤ 0.05) weight than the FF hen groups. Landers et al. (2005b) reported that alfalfa meal- and pellet-fed hens lost 15 to 19% of their total BW when compared with FF hens, which actually gained weight. Donalson et al. (2005) observed that feed-deprived hens lost up to one-quarter of their total BW and did not differ from hens fed diets with either 90 or 100% alfalfa meal. Berry and Brake (1985) stated that approximately 25% of the body mass loss can be attributed to liver and reproductive organ weight reductions. The variations in weight loss between the hens in the ALC and FW groups could be due to a combination of factors. Mrosovsky and Sherry (1980) reported that birds generally suppressed their appetites during a natural molt. This, combined with the slow passage of alfalfa through the gastrointestinal tract (Sibbald, 1979) of the ALC hens, could cause their intestines to be heavier in some cases than those of the FW hens.


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  		Table 1. Effects of molting regimen on feed intake and weight loss in laying hens experimentally infected with Salmonella Enteritidis
 
Cholesterol and Glucose Concentrations

There were no treatment x day effects (P > 0.85) in cholesterol concentration, but treatment effects were observed in both trials (P ≤ 0.05). In trial 1, ALC+ hens exhibited lower cholesterol levels than FW+ hens, whereas in trial 2, cholesterol was lower for the FF hen groups than the FW groups (Table 2Go; P ≤ 0.05). Landers et al. (2007) reported higher serum cholesterol levels in FW and alfalfa meal-molted 60-wk-old hens on d 8 compared with FF hens. Walzem et al. (1994) noted that follicular resorption could alter the circulating plasma cholesterol fractions in the laying hen. Mumma et al. (2006) and Puvadolpirod and Thaxton (2000a,b) reported increases in plasma cholesterol levels during stress in broilers and layers. The variable levels of cholesterol observed in the ALC hens could be a result of alfalfa saponins, which can potentially form insoluble complexes with cholesterol in the gut lumen (Coulson and Evans, 1960).


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  		Table 2. Effects of molting regimen on blood cholesterol and glucose levels in laying hens experimentally infected with Salmonella Enteritidis
 
No treatment x day effects (P > 0.2) were observed in glucose concentration in the plasma, but there were treatment effects in trial 1 because the FF hen groups exhibited higher levels of glucose than all the other treatment groups (P ≤ 0.05). Plasma glucose concentrations in chickens have been shown to decline in 6-wk-old broilers at the beginning of feed restriction and in 4-d-fasted 8-wk-old turkeys (Anthony et al., 1999; Edwards et al., 1999). Increased glucose levels in adrenocorticotropic hormone (ACTH) stress-induced broilers and laying hens also have been reported (Puvadolpirod and Thaxton, 2000a,b,c; Mumma et al., 2006). However, Landers et al. (2007) did not observe reductions in glucose concentrations in feed-restricted adult hens on d 8 compared with nonmolted hens. Cherel et al. (1988) reported that glucose did not change substantially during molting fasts in king penguins.

Calcium Concentration

Significant treatment x day effects were observed for calcium concentrations (Figure 1A and 1BGo) in both trials (P ≤ 0.001), and FF hens generally had higher levels of calcium in the blood compared with ALC and FW hens. On d 5 in trial 1, the FF– hens exhibited higher (P ≤ 0.05) concentrations of calcium in the blood than did the other treatment groups, and FW– hens were the lowest except when compared with ALC– hens. In trial 2, FF– hens had the highest levels (P ≤ 0.05) of calcium compared with all the other groups, and the FF+ and ALC– hen groups had higher (P ≤ 0.05) levels than the remaining treatment groups. On d 9 in trial 1, the FF+ hens exhibited higher (P ≤ 0.05) calcium concentrations than the FF– hens, and both were higher than all the other groups, whereas the FW– and ALC– groups were higher than the FW+ and ALC+ hen groups. On d 12 in trial 1, the FF+ hens yielded higher (P ≤ 0.05) levels of calcium than the FF– and FW– hens, but not when compared with hens in the other treatments. In trial 2, calcium concentrations were higher (P ≤ 0.05) in the FF hen groups than in all the other groups for d 9 and 12.


Figure 1
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  		Figure 1. A) Effects of molting regimen on blood calcium levels in molting laying hens on d 2, 5, 9, and 12 after molt initiation. Hens were infected on d 4 of the trial; therefore, there were no Salmonella Enteritidis-positive hens on d 2. a–dTreatments within individual days that have no common letter are different (P ≤ 0.05). B) Effects of molting regimen on blood calcium levels in molting laying hens on d 2, 5, 9, and 12 after molt initiation. Hens were infected on d 4 of the trial; therefore, there were no Salmonella Enteritidis-positive hens on d 2. a–cTreatments within individual days that have no common letter are different (P ≤ 0.05). FW+ = feed withdrawal Salmonella Enteritidis-positive hens; FF+ = fully fed Salmonella Enteritidis-positive hens; ALC+ = alfalfa crumble diet Salmonella Enteritidis-positive hens; FW– = feed withdrawal Salmonella Enteritidis-negative hens; FF– = fully fed Salmonella Enteritidis-negative hens; ALC– = alfalfa crumble diet Salmonella Enteritidis-negative hens.

 
Landers et al. (2007) also reported higher calcium levels when comparing d-8 responses of FF hens with alfalfa meal- and FW– molted 60-wk-old hens. Although alfalfa contains 1.3% calcium (NRC, 1994), it is not known how bioavailable this calcium is to the bird. Calcium is stored in the medullary bones in laying hens for the purpose of eggshell formation (Wilson and Duff, 1990). Medullary bone is formed just before the onset of egg laying and is influenced by estrogen, which reaches very low levels during a molt (Hoshino et al., 1988; Wilson and Thorp, 1998). Calcium is mobilized from the bones and intestines and transported to the reproductive tract for deposition in the shell gland, and decreased levels of eggshell gland and intestinal calbindin occur during molting (Yosefi et al., 2003). Bone weight and density are known to decrease during a molt (Garlich et al., 1984; Park et al., 2004c; Kim et al., 2006, 2007), but Kim et al. (2005) reported that after the end of the second egg-laying cycle (122 wk), there were no significant differences between molted and nonmolted hens in the bone qualities measured.

Total Protein Concentration

Significant treatment x day effects were observed in total protein concentration (Figure 2A and 2BGo) in the plasma (P ≤ 0.001). In trial 2 on d 2, FF– hens exhibited higher (P ≤ 0.05) concentrations of total protein than ALC– and FW– hens. On d 5 in trial 2, FW– and ALC– hens exhibited lower (P ≤ 0.05) total protein concentrations than all the treatment groups except ALC+ hens, whereas in trial 1, FF– hens yielded higher levels than all the other treatment groups. On d 9, the FF hen groups yielded higher total protein levels than all the other treatment groups in both trials. On d 12 of trial 1, the FF hen groups exhibited higher (P ≤ 0.05) protein levels than hens in all the other treatments, whereas in trial 2, ALC+ hens were lower (P ≤ 0.05) than in all treatment groups except FW+ hens. Molting may alter serum protein levels by changes in metabolism as well as indirectly as a result of the stress response. In sparrows, molting has been shown to accelerate fractional synthesis rates of whole-body proteins (Murphy and Taruscio, 1995). Puvadolpirod and Thaxton (2000a,b) have reported elevated levels of total protein in chickens after stress induction by continuous administration of ACTH.


Figure 2
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  		Figure 2. A) Effects of molting regimen on blood protein levels in molting laying hens on d 2, 5, 9, and 12 after molt initiation. Hens were infected on d 4 of the trial; therefore, there were no Salmonella Enteritidis-positive hens on d 2. a–cTreatments within individual days that have no common letter are different (P ≤ 0.05). B) Effects of molting regimen on blood protein levels in molting laying hens on d 2, 5, 9, and 12 after molt initiation. Hens were infected on d 4 of the trial; therefore, there were no Salmonella Enteritidis-positive hens on d 2. a–cTreatments within individual days that have no common letter are different (P ≤ 0.05). FW+ = feed withdrawal Salmonella Enteritidis-positive hens; FF+ = fully fed Salmonella Enteritidis-positive hens; ALC+ = alfalfa crumble diet Salmonella Enteritidis-positive hens; FW– = feed withdrawal Salmonella Enteritidis-negative hens; FF– = fully fed Salmonella Enteritidis-negative hens; ALC– = alfalfa crumble diet Salmonella Enteritidis-negative hens.

 
Triglyceride Concentration

Significant treatment x day effects (P ≤ 0.0002) were observed in the levels of triglycerides (Figure 3A and 3BGo) found in the blood plasma. Triglycerides were generally higher in FF hens compared with molted hens. On d 5 in trial 1, all the FF hens exhibited higher (P ≤ 0.05) blood triglyceride levels than the FW and ALC hens. Similar results were observed in trial 2 on d 5, but the FF– hens exhibited higher (P ≤ 0.05) levels than all the other groups, and the FF+ hens exhibited higher (P ≤ 0.05) levels than the FW and ALC hen groups. On d 9 and 12, both FF groups yielded higher (P ≤ 0.05) triglyceride levels than any of the other treatment groups in both trials, whereas the ALC and FW hens were not different (P > 0.05) from each other. Puvadolpirod and Thaxton (2000a, b) observed an elevation in triglyceride levels in ACTH-stressed broilers, but not in ACTH-treated layers (Mumma et al., 2006). Anthony et al. (1999) observed reduced plasma concentrations of triglycerides in fasted hens that were challenged with Pasteurella multocida. However, we did not generally observe differences between Salmonella Enteritidis-positive and Salmonella Enteritidis-negative birds in the current study.


Figure 3
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  		Figure 3. A) Effects of molting regimen on blood triglyceride levels in molting laying hens on d 2, 5, 9, and 12 after molt initiation. Hens were infected on d 4 of the trial; therefore, there were no Salmonella Enteritidis-positive hens on d 2. a,bTreatments within individual days that have no common letter are different (P ≤ 0.05). B) Effects of molting regimen on blood triglyceride levels in molting laying hens on d 2, 5, 9, and 12 after molt initiation. Hens were infected on d 4 of the trial; therefore, there were no Salmonella Enteritidis-positive hens on d 2. a–cTreatments within individual days that have no common letter are different (P ≤ 0.05). FW+ = feed withdrawal Salmonella Enteritidis-positive hens; FF+ = fully fed Salmonella Enteritidis-positive hens; ALC+ = alfalfa crumble diet Salmonella Enteritidis-positive hens; FW– = feed withdrawal Salmonella Enteritidis-negative hens; FF– = full fed Salmonella Enteritidis-negative hens; ALC– = alfalfa crumble diet Salmonella Enteritidis-negative hens.

 
Uric Acid Concentration

Significant treatment x day effects (P < 0.0001) were observed in uric acid concentration responses (Figure 4A and 4BGo). On d 2, uric acid concentrations of both the FW– and ALC– hens were reduced (P ≤ 0.05) when compared with the FF– hens in both trials. On d 5 in trial 1, the FF+ hens had higher (P ≤ 0.05) uric acid concentrations when compared with the other treatment groups, and FW– hens yielded lower concentrations than the remainder of the treatments except when compared with the FW+ and ALC– hens. In trial 2, the FF hen groups had higher (P ≤ 0.05) levels of uric acid than all the other treatment groups, whereas the ALC and FW hen groups did not differ (P > 0.05). On d 9, the FW hen groups exhibited lower (P ≤ 0.05) uric acid concentrations than all the other treatments except the ALC– hens in trial 1. In trial 2, the FW hen groups exhibited lower (P ≤ 0.05) uric acid concentrations than any of the other treatment groups. On d 12 of trial 1, the FW hen groups exhibited lower (P ≤ 0.05) levels of uric acid than all except the FF+ hens. Landers et al. (2007) observed a considerable reduction in serum uric acid in 60-wk-old FW hens on d 8 of the molt period compared with hens on alfalfa meal or FF diets. Although a general initial reduction in the uric acid concentration was observed in both the FW and ALC hens, only uric acid concentrations of the FW hens tended to remain lower throughout the trial. For the FW hens, this could have been the result of the lack of a dietary protein source. Although alfalfa contains protein, ALC hens initially did not accept the alfalfa diet as a feed source, which could account for the reduction in uric acid concentration observed at the beginning of the trial. Cherel et al. (1988) found that plasma concentrations of uric acid were highly variable, increasing after the 13th day of the fast, which was an indication of the utilization of endogenous proteins. Anthony et al. (1999) observed uric acid increases early after initiation of feed deprivation in 8-wk-old turkeys and reported that the rate of protein degradation increased with the duration of feed withdrawal, as indicated by increased plasma uric acid levels. This would correspond with the increasing levels of serum protein in FW hens observed toward the end of the molt.


Figure 4
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  		Figure 4. A) Effects of molting regimen on blood uric acid levels in molting laying hens on d 2, 5, 9, and 12 after molt initiation. Hens were infected on d 4 of the trial; therefore, there were no Salmonella Enteritidis-positive hens on d 2. a–dTreatments within individual days that have no common letter are different (P ≤ 0.05). B) Effects of molting regimen on blood uric acid levels in molting laying hens on d 2, 5, 9, and 12 after molt initiation. Hens were infected on d 4 of the trial; therefore, there were no Salmonella Enteritidis-positive hens on d 2. a,bTreatments within individual days that have no common letter are different (P ≤ 0.05). FW+ = feed withdrawal Salmonella Enteritidis-positive hens; FF+ = fully fed Salmonella Enteritidis-positive hens; ALC+ = alfalfa crumble diet Salmonella Enteritidis-positive hens; FW– = feed withdrawal Salmonella Enteritidis-negative hens; FF– = fully fed Salmonella Enteritidis-negative hens; ALC– = alfalfa crumble diet Salmonella Enteritidis-negative hens.

 
Thaxton and Puvadolpirod (2000) advised caution when attempting to diagnose stress by using physiological changes, because stress consists of a series of nonspecific adaptive responses that can enable a return to homeostasis (Puvadolpirod and Thaxton, 2000a,b,c,d). In general, the nonchallenged hens exhibited levels of blood plasma metabolites that were comparable to those of their Salmonella Enteritidis-challenged counterparts; therefore, the presence of an infective organism in the hens did not appear to alter the results. The results indicate that alfalfa can induce a molt as effectively as feed deprivation without resulting in additional physiological stresses to the birds. However, stress responses need to be studied further by evaluating immunological and behavioral responses of molting hens fed an alfalfa diet.


   ACKNOWLEDGMENTS
 
This research was supported by Hatch grant no. H8311 administered by the Texas Agricultural Experiment Station, USDA-NRI grant no. 2002–0614, and U.S. Poultry and Egg Association grant no. 485.


   FOOTNOTES
 
1 Current address: Department of Poultry Science, University of Georgia, P.O. Box 748, Tifton, GA 31793-0478. Back

3 Current address: University of Arkansas, Center for Food Safety and Microbiology, IFSE, 2650 N. Young Ave., Fayetteville, AR 72704. Back

Received for publication November 20, 2006. Accepted for publication September 13, 2007.


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
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