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Poult Sci 2007. 86:768-774
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PRODUCTION, MODELING, AND EDUCATION

Effects of Supplemental Dietary Phytase and 25-Hydroxycholecalciferol on the Blood Characteristics of Commercial Layers Inoculated Before or at the Onset of Lay with the F-Strain of Mycoplasma gallisepticum1

E. D. Peebles*,2, S. L. Branton{ddagger}, M. R. Burnham*, S. K. Whitmarsh* and P. D. Gerard{dagger}

* Department of Poultry Science, and {dagger} Experimental Statistics Unit, Mississippi State University, Mississippi State 39762; and {ddagger} Poultry Research Unit, Agricultural Research Service, USDA, Mississippi State, Mississippi 39762

2 Corresponding author: dpeebles{at}poultry.msstate.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
In 3 trials, the effects of dietary supplementation with phytase (PHY) and 25-hydroxycholecalciferol on BW and the blood characteristics of commercial layers that were inoculated prelay (12 wk of age) or at the onset of lay (22 wk of age) with F-strain Mycoplasma gallisepticum were assessed at 34, 50, and 58 wk of age. Experimental layer diets, which included either a basal control diet or the same diet supplemented with 0.025% PHY and 25-hydroxycholecalciferol, were fed from 20 through 58 wk of age. The supplemented diet decreased blood hematocrit values across bird age, inoculation type (sham vs. F-strain M. gallisepticum), and age of inoculation (prelay vs. onset of lay). Phytase- and 25-hydroxycholecalciferol-supplemented diets reduced bird BW in sham-inoculated control birds across bird age and age of inoculation. This effect was not observed in F-strain M. gallisepticum-inoculated birds. Furthermore, across diet (control vs. supplemented) and inoculation type, total plasma protein concentration at 34 wk of age was higher in birds that were inoculated at the onset of lay compared with those inoculated prelay. Diet, inoculation type, and inoculation age had no effect on mortality, reproductive organ histopathological lesion scores, or serum cholesterol and Ca concentrations. In conclusion, throughout lay, the supplementation of commercial layer diets with PHY may lower hematocrit, and inoculation with F-strain M. gallisepticum prelay or at the onset of lay may ameliorate the depressing effects of dietary PHY and 25-hydroxycholecalciferol supplementation on hen BW.

Key Words: F-strain Mycoplasma gallisepticum • inoculation • Mycoplasma gallisepticum • phytase • 25-hydroxycholecalciferol


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Vaccination of commercial layers with a live Mycoplasma gallisepticum vaccine produced from an F-strain of low to moderate virulence has become available to protect flocks against natural M. gallisepticum infections (Branton et al., 1997). The vaccine strain displaces natural field strain infections (Levisohn and Kleven, 1981; Kleven et al., 1990) and is effective in minimizing egg production losses if administered to commercial layers before exposure to more virulent field strains of M. gallisepticum (Luginbuhl et al., 1976). However, inoculation of commercial layers with F-strain M. gallisepticum at 12 wk of age has been reported to delay onset of lay and decrease total egg production (Burnham et al., 2002b). In response to estrogen release and the onset of egg production in the laying hen, a marked increase occurs in liver metabolism (Lorentz et al., 1938; Hillyard et al., 1956) and the production of neutral lipids (Heald and Bandman, 1963), serum triglycerides (ST), and phospholipids (Dashti et al., 1983) destined for subsequent yolk lipid deposition (Nimpf and Schneider, 1991; Walzem et al., 1999). However, colonization of the liver by F-strain M. gallisepticum (Sahu and Olson, 1976) may disrupt yolk lipid synthesis and subsequently reduce egg production.

Burnham et al. (2003) recently reported that hematocrits (HCT) were increased in layers inoculated with F-strain M. gallisepticum at 12 wk of age. Furthermore, ST and total plasma protein (PPRO) concentrations were significantly increased at 22 wk by the prelay F-strain M. gallisepticum inoculation, whereas ST and PPRO were decreased in F-strain M. gallisepticum-treated hens at wk 54 and 52, respectively. Age of inoculation may also have differential effects on the blood characteristics of layers. Compared with 12-wk inoculations, Burnham et al. (2002a) showed that 22-wk inoculations (sham or F-strain M. gallisepticum) increased serum cholesterol (SCHOL) and ST from 20 to 58 wk; decreased serum Ca (SCA) at 44, 50, and 58 wk; and increased PPRO at 34 wk of age. Additional information regarding the hematological and noncellular blood characteristics of birds infected with F-strain M. gallisepticum is lacking in the literature.

When broiler chickens received diets containing 1,25-dihydroxycholecalciferol, maximum bone ash was obtainable with diets containing two-thirds as much Ca as was needed to obtain maximum bone ash when no 1, 25-dihydroxycholecalciferol was present in the diets (Edwards et al., 1992). Edwards (1993) noted that the addition of 1,25-dihydroxycholecalciferol to broiler chicken diets allowed for a greater retention of total Ca and that dietary 1,25-dihydroxycholecalciferol in the presence of phytase (PHY) resulted in greater BW and bone ash and a lower incidence of rickets. Furthermore, Carlos and Edwards (1998) observed that the addition of PHY or 1,25-dihydroxycholecalciferol, or their combination, to basal layer diets prevented a rapid decrease in egg production due to an M. gallisepticum infection. The addition of PHY was also shown to have a positive effect on BW, tibia bone ash, and plasma Ca.

The objective of the current investigation was to determine the effects of F-strain M. gallisepticum inoculations given prelay (12 wk of age) and at onset of lay (22 wk of age) in commercial layers fed either a basal control diet or the same diet supplemented with PHY and 25-hydroxycholecalciferol (D3) on mortality, BW, HCT, SCHOL, ST, PPRO, and SCA.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Pretreatment Pullet Management
In each of 3 trials, 1,000 Hy-Line W-36 pullets were obtained at 1 d of age from a commercial source that was monitored and certified free of M. gallisepticum and Mycoplasma synoviae (USDA-APHIS-VS, 2003). Chickens were vaccinated as specified by Peebles et al. (2003). At 5 wk of age, 10 randomly selected pullets were bled from the left cutanea ulna wing vein to test for antibodies to M. gallisepticum and M. synoviae. At the same time, birds were swabbed from the choanal cleft (Branton et al., 1984) to test for the presence of Mycoplasma species. Detailed descriptions of sample testing procedures, materials, and specificity are provided by Peebles et al. (2003).

Pullet chicks (1,000) on arrival were initially placed on clean, dry litter in a 5.5 x 6.1 m section of a conventional house, resulting in a flock density of 0.034 m2/bird. A daily artificial lighting schedule followed a 13L:11D cycle. One 75-W incandescent light bulb was used to illuminate each 8.4 m2 of floor space, providing an intensity of 35.5 lx at bird level. Light intensity was measured in foot candles by light meter and was then converted to lux. Feed and water were provided for ad libitum consumption. Ingredient percentages and calculated analyses of the basal starter and grower diets used are provided by Peebles et al. (2003). These diets were formulated to meet or exceed NRC (1994) recommendations. No medications were administered during any of the trials.

Pullet Housing in Caged Layer Facility
In each trial, 240 birds were randomly placed in individual cages (25.4 cm wide x 40.6 cm deep; 1,031 cm2) in a commercial caged layer facility. Birds were equally divided into 2 isolated ends of the facility and were watered, fed, and ventilated separately beginning at 12 wk of age. One end housed uninoculated or control birds (120), and the other end housed F-strain M. gallisepticum-inoculated birds (120). In each end, birds were inoculated at 1 of 2 time (bird age) periods and were fed 1 of 2 experimental diets. There were 10 individually caged birds within each of 3 replicate groups belonging to each diet and age of inoculation treatment combination. Artificial lighting schedules were increased 15 min/d beginning at 18 wk of age until a 16 h 15 min of light-7 h 45 min of dark cycle was achieved. Chickens were maintained on that schedule through the remainder of the experiment. Feed and water were provided for ad libitum consumption. Ingredient percentages and calculated analyses of the basal developer and prelay diets used are provided by Peebles et al. (2003). These diets were formulated to meet or exceed NRC (1994) recommendations.

F-strain M. gallisepticum Inoculation
At 12 and 22 wk of age, pullets receiving F-strain M. gallisepticum vaccines in all 3 trials were inoculated via eye drop in the right eye with 0.04 mL of a 24-h broth culture of high-passage F-strain M. gallisepticum (99th passage above the unknown passage level; provided by S. H. Kleven, University of Georgia, Athens). In trial 1, inoculum titers at 12 and 22 wk, respectively, were 2 x 106 and 1 x 106 cfu/mL. Inoculum titers at both 12 and 22 wk in trials 2 and 3, respectively, were 1 x 105 and 1 x 107 cfu/mL. Vaccine titers were determined by plate count after incubating the inoculum on plated agar containing Frey’s broth medium (Frey et al., 1968) for a minimum of 4 d and a maximum of 28 d. Similarly, pullets designated as controls were sham-inoculated via eye drop in the right eye with 0.04 mL of sterile Frey’s broth medium (Frey et al., 1968).

Mycoplasma Identification
At 20 and 58 wk, 1 randomly selected hen from each replicate group in each treatment was bled, swabbed, and tested for the presence of Mycoplasma species as for pullets at 5 wk of age.

Experimental Diets
Experimental layer diets were made available throughout each trial period, beginning at 20 wk of age and continuing through 58 wk of age. Both diets were isocaloric and isonitrogenous; however, 1 diet served as a basal control diet, and the other was the same diet supplemented with PHY (0.025%; 600 PHY units/kg of diet; BASF Corp., Florham Park, NJ) and D3 (diluted premix, 0.025%; pure crystalline, 34.5 µg/kg of diet; Hoffmann-La Roche Inc., Parsippany, NJ). To ensure efficacy of the supplements, new feed batches were mixed every 28 d. Available protein and Lys percentages in the layer diet were adjusted when feed batches were mixed according to the past amount of feed consumed per bird. Ingredient percentages, calculated analyses, and determined analyses of the CP, crude fat, crude fiber, ash, and moisture contents of the basal control and supplemented layer diets at wk 36 are provided in Table 1Go. The diets were formulated to meet or exceed NRC (1994) recommendations. Determined analyses of the diets were performed according to the methods of the Association of Official Analytical Chemists (1980).


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  		Table 1. Ingredient percentages and calculated analyses of experimental layer diets at wk 36
 
Data Collection
Mortality was monitored daily for determination of cumulative bird mortality at the end of each trial. In each trial, hens were weighed and then bled at 34, 50, and 58 wk of age. In all 3 trials, BW was determined for all hens, and blood samples, which were harvested from 2 hens per replicate group of birds representing each treatment combination (diet, inoculation type, and inoculation age), were utilized to conduct the following 5 analyses. Hematocrit values were expressed as percentage of blood packed cell (primarily red blood cell) volume and were determined using capillary tubes that were centrifuged in a micro-HCT centrifuge and were then read with a microcapillary reader. Serum cholesterol and ST expressed in milligrams per deciliter and PPRO expressed in grams per deciliter were determined by placing 10 µL of serum or plasma for each test on test slides that were analyzed on a Kodak Ektachem DT-60 analyzer (Eastman Kodak Co., Rochester, NY) as described by Latour et al. (1996). Similarly, SCA concentrations expressed in milligrams per deciliter were determined by placing 10 µL of serum on a test slide that was analyzed on a Kodak Ektachem DTSC module analyzer (Eastman Kodak Co.) according to the procedures of Tietz (1986). Control analyses were performed to assure that each sample was in the appropriate test range for accurate analysis. At the termination of each trial, 1 hen from each replicate treatment group was euthanized by cervical dislocation. Ovary, infundibulum, magnum, isthmus, uterus, and vagina tissue specimens were collected for histopathological examination as described in detail by Peebles et al. (2004).

Statistical Analysis
A randomized complete block experimental design, with trial as a block, was utilized. The data of all 3 trials were pooled then analyzed together. Therefore, results from trials 1, 2, and 3 were not reported independently but were reported over all 3 trials. A split-plot treatment structure was used, with inoculation type as the whole plot factor and age of inoculation and diet as subplot factors. Body weight, HCT, SCHOL, ST, PPRO, and SCA data were subjected to a repeated measures analysis to account for the fact that the same experimental units were observed over multiple age periods. The effects of dietary treatment (control vs. PHY and D3), age of inoculation (12 vs. 22 wk), type of inoculation (sham vs. F-strain M. gallisepticum), hen age (34, 50, and 58 wk), and their interactions were tested. Reproductive organ histopathology and cumulative mortality data were analyzed by 1-way analysis. Fixed effects were inoculation type, age of inoculation, diet, hen age, and their interactions. Trial and interactions between fixed effects and trial were considered random effects. Replicate means for each parameter were used in all data analyses. Least squares means were compared in the event of significant global effects (Steel and Torrie, 1980). All data were analyzed using the MIXED procedure of SAS software (SAS Institute, 2000). Statements of significance were based on P ≤ 0.05 unless otherwise stated.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
In all 3 trials, all initial mycoplasmal cultures as well as serum plate agglutination and hemagglutination-inhibition (HI) test results obtained from 5-wk-old pullets were negative for M. gallisepticum and M. synoviae. Control serum samples obtained at 20 and 58 wk of age were serum plate agglutination- and HI-negative for M. gallisepticum, whereas the same tests were positive for M. gallisepticum in the 12- and 22-wk F-strain M. gallisepticum-inoculated hens. Hens were considered F-strain M. gallisepticum-free when they exhibited no detectable HI titers. All F-strain M. gallisepticum-inoculated hens had HI titers ≥ 1:80. Similarly, fluorescent antibody culture results for swabs obtained at 20 and 58 wk of age in each trial were negative for Mycoplasma species growth for 12 out of 12 F-strain M. gallisepticum-free hens tested, whereas growth was evident for 12 out of 12 F-strain M. gallisepticum-inoculated hens tested. No significant differences were demonstrated among the treatments (diet, inoculation type, or inoculation age) on cumulative bird mortality or for the assessed reproductive organ histopathological lesion scores within any of the tissues sampled (data not shown). These results verified systemic infections in F-strain M. gallisepticum-inoculated birds and indicated that there was no cross-contamination between F-strain M. gallisepticum-inoculated and F-strain M. gallisepticum-clean birds. Nevertheless, similar to that reported by Burnham et al. (2002c), infection did not increase mortality or the incidence of recognizable lesions in the reproductive system of the birds. Dietary treatment or age of inoculation also did not cause or promote any effect of F-strain M. gallisepticum infection on mortality or reproductive organ histopathology.

There was a significant main effect due to hen age for BW (P ≤ 0.0001), HCT (P ≤ 0.04), and SCA (P ≤ 0.0003; Table 2Go). Hen BW at 50 and 58 wk were not different, but BW at both those times was significantly higher than that at wk 34. Hematocrit and SCA levels at wk 50 and 58 were also not different; conversely, HCT and SCA at both those times were significantly lower than those at wk 34. The overall increase in BW, experienced by the hens from 34 to 58 wk in the current study, was similar to those reported by Burnham et al. (2002b) except that the BW of the birds in this study were generally heavier during that period. The difference in overall BW may be related to housing, in that the birds in this investigation were individually caged, whereas those in the other investigation were held as a group of 10 birds in biological isolation units (1.16 m2/unit). The birds in the isolation units gained less weight, having had less restricted movement and the opportunity for more exercise. Because of a significant hen age x type of inoculation interaction for HCT, Burnham et al. (2003) did not report an age main effect for HCT; however, similar to this study, HCT values were numerically lower at the end of the first trial in that study (wk 54) than at wk 32 and 36. Furthermore, as in this study, Burnham et al. (2003) also found a significant age main effect on SCA and showed that SCA levels at wk 54 were lower than those at wk 28 across both trials examined.


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  		Table 2. Body weight, hematocrit (HCT), and serum Ca (SCA) in commercial layers at 34, 50, and 58 wk of age1
 
There was a significant inoculation type x diet interaction for BW (P ≤ 0.05; Table 3Go). The BW of sham-inoculated control birds was significantly reduced by dietary PHY and D3 supplementation, whereas dietary treatment had no effect in F-strain M. gallisepticum-inoculated hens (Table 3Go). Carlos and Edwards (1998) observed a positive effect of supplementing either 1,25-dihydroxycholecalciferol, or PHY, or their combination, on the BW of laying hens, with the addition of PHY alone significantly increasing BW. In broiler chickens, BW and bone ash were observed to increase by the addition of supplementary PHY and D3 to their diets (Edwards, 1993). Huff et al. (1998) likewise observed an increase in the 49-d BW of broilers fed PHY-treated diets since hatch. Conversely, in the current investigation, the supplementation of basal diets with both PHY and D3 caused a significant decrease in the BW of F-strain M. gallisepticum-clean hens. The basis for this BW suppression is not understood; however, Viveros et al. (2002) observed that the supplementation of broiler chick diets with microbial PHY suppressed relative liver weight. In response to PHY, a relative decrease in the liver weights of the laying hens in this study could have directly reduced BW. Their BW could have also been indirectly decreased by suppression of total liver metabolic activity in association with a decrease in hepatic tissue.


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  		Table 3. Body weight of sham- and F-strain Mycoplasma gallisepticum-inoculated commercial layers fed control or phytase and 25-hydroxycholecalciferol-(D3) supplemented diets1
 
Furthermore, there was no effect of F-strain M. gallisepticum inoculation across diet on BW in this study, and Burnham et al. (2002b) and Peebles et al. (2003) also saw no significant effect of a 12-wk F-strain M. gallisepticum inoculation on hen BW. However, the laying hens observed by Carlos and Edwards (1998) lost weight during an experimental 9-wk feeding period due to an M. gallisepticum infection, whereas the addition of either 1,25-dihydroxycholecalciferol, PHY, or their combination decreased the magnitude of weight loss as compared with hens fed control basal diets. The contrasting effect of M. gallisepticum infection on BW between this study and that of Carlos and Edwards (1998) is likely due to an M. gallisepticum strain difference. The strain of M. gallisepticum that infected the hens examined by Carlos and Edwards (1998) was not identified but was probably a field strain with greater virulence than the F-strain M. gallisepticum that infected the birds in this study.

Although the effect of dietary PHY and D3 supplementation on BW in control birds was opposite to that of Carlos and Edwards (1998), the current results do confirm that an interaction between F-strain M. gallisepticum inoculation and supplemental PHY and D3 occurs and that one may influence the effect of the other on BW. Either the diet can diminish the negative effect of F-strain M. gallisepticum on BW or F-strain M. gallisepticum can negate the negative effect of PHY and D3 supplementation on BW. The precise metabolic mechanisms at play in this interaction are not clear, although Carlos and Edwards (1998) have shown that the combination of 1,25-dihydroxycholecalciferol and PHY improve P retention, and 1,25-dihydroxycholecalciferol increases the absorption and retention of Ca. Changes in the absorption and retention of these 2 minerals have the potential to affect BW, and Cowieson et al. (2006) have shown that supplemental dietary PHY can increase the digestibility of amino acids in broilers. However, the lack of change in SCA and PPRO in response to diet or F-strain M. gallisepticum inoculation does not support the involvement of Ca or protein in this interaction.

There was a significant (P ≤ 0.03) main effect due to diet for HCT such that HCT in hens fed a control diet was significantly higher than that in hens fed diets supplemented with PHY and D3. Mean HCT in birds fed control diets and diets supplemented with PHY and D3 were 26.7 and 26.1% (pooled SEM = 0.583), respectively. Percentage packed cell volume (HCT) usually increases to a lesser degree than PPRO during dehydration (Boyd, 1981). Therefore, a decrease in HCT in response to supplementary PHY and D3 would be expected to be associated with a decrease in PPRO, particularly if supplementation resulted in a hydration effect in the birds. Because of this incongruity, it is suggested that the decrease in HCT in response to PHY and D3 is not a hydration effect but may be due to an effect on blood cell formation. Supplemental dietary D3 has been shown to provide protection against immunological suppression and increase disease resistance in turkeys (Huff et al., 2000) and has also been observed to have no effect on red blood cell count or HCT, as well as plasma Ca, in fish (Horvli et al., 1998). Therefore, a depression of the white or red blood cell count by D3 would not be expected. However, Czech and Grela (2004) noted that the addition of microbial PHY to high native PHY diets diminished white blood cell numbers in pigs. This would implicate PHY as a possible factor leading to the decrease in HCT in birds fed supplemental PHY and D3. Further research in birds is needed to establish the individual effects of PHY and D3 on white and red blood cell numbers and the relative contributions of these cells to the effects of the supplements on HCT.

There was a significant age x diet interaction for ST (P ≤ 0.03; Table 4Go). However, despite the significant interaction, supplementation of diets with PHY and D3 did not significantly influence ST in 34-, 50-, or 58-wk-old hens (Table 4Go). The effects of dietary vitamin D3 on ST in birds is apparently lacking in the literature; nevertheless, supplemental dietary PHY has been shown to have no significant effect on ST as well as SCA and serum total protein in broilers (Huff et al., 1998) or on liver lipid content in fish (Robiana et al., 1998; Kim and Shin, 2001). In addition, Gannage-Yared et al. (2003) found no effect of dietary 1,25-dihydroxycholecalciferol supplementation on ST in humans.


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  		Table 4. Serum triglyceride levels at 34, 50, and 58 wk of age in commercial layers fed control or phytase and 25-hydroxycholecalciferol-(D3) supplemented diets1
 
There was a significant age x age of inoculation interaction for PPRO (P ≤ 0.01; Table 5Go). The effect observed for PPRO was only in hens that were 34 wk of age, and the effect was due to the inoculation process itself across sham and F-strain M. gallisepticum treatments. Total plasma protein levels at 34 wk were higher in birds that were inoculated (sham or F-strain M. gallisepticum) during lay onset (22 wk of age) compared with those that were inoculated before lay (12 wk of age; Table 5Go). Burnham et al. (2002a) earlier noted that age of inoculation exerted differential effects on the blood characteristics of layers. Similar to the current investigation, it was likewise shown in that study that compared with inoculations at 12 wk, inoculations at 22 wk of age (sham or F-strain M. gallisepticum) increased PPRO at 34 wk. However, unlike this study, Burnham et al. (2002a) also showed that 22-wk inoculations increased SCHOL and ST from 20 to 58 wk and decreased SCA at 44, 50, and 58 wk compared with 12-wk inoculations. Perhaps relative differences in the stress levels of these 2 periods of inoculation on the bird was the basis of the effect on these blood parameters. Nevertheless, the results in this report specifically suggest that hen age must be considered when determining the effects of age of inoculation on PPRO and that these effects may become ameliorated in older hens past peak production (50 and 58 wk of age). In conclusion, F-strain M. gallisepticum inoculation and PHY and D3 dietary supplementation may interact to influence the BW of commercial egg-laying hens, with the current results specifically showing that F-strain M. gallisepticum inoculation can negate the negative effect of PHY and D3 supplementation on BW. Furthermore, supplemental PHY may depress HCT levels in layers throughout lay, whereas possible effects of age of inoculation on PPRO may not occur past peak production.


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  		Table 5. Total plasma protein levels at 34, 50, and 58 wk of age in commercial layers given 12-wk (prelay) or 22-wk (onset of lay) inoculations1
 


   ACKNOWLEDGMENTS
 
We thank Jerry H. Drott for his expert technical assistance in this project.


   FOOTNOTES
 
1 This is journal article number J-11005 from the Mississippi Agricultural and Forestry Experiment Station supported by MIS-321010. Use of trade names in this publication does not imply endorsement by the Mississippi Agricultural and Forestry Experiment Station of these products nor similar ones not mentioned. Back

Received for publication September 25, 2006. Accepted for publication December 4, 2006.


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