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Poult Sci 2007. 86:1805-1809
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PRODUCTION, MODELING, AND EDUCATION

Effects of Supplemental Dietary Phytase and 25-Hydroxycholecalciferol on the Digestive and Reproductive Organ Characteristics of Commercial Layers Inoculated Before or at the Onset of Lay with the F-Strain of Mycoplasma gallisepticum1,2

E. D. Peebles*,3, 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 39762

3 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 (25-D3) on the digestive and reproductive organ 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 (FMG) were assessed at 58 wk of age. Experimental layer diets that included a basal control diet or a control diet supplemented with 0.025% PHY and 25-D3 were fed from 20 through 58 wk of age. As a percentage of total oviduct weight, magnum weight was lower in birds that were inoculated (sham or FMG) at lay onset compared with those that were inoculated prelay, and in FMG-inoculated birds, relative duodenum length was greater in those inoculated at 12 compared with 22 wk. Also, as percentages of organ weight or length, infundibulum length and isthmus weight were increased, whereas duodenum length was decreased by dietary supplementation with PHY and 25-D3. The overall timing (12 vs. 22 wk) of inoculation can affect the reproductive organ characteristics of layers, whereas, more specifically, the timing of an FMG inoculation may affect their digestive organ structure. Furthermore, independent of inoculation timing and type, the reproductive organ and digestive systems of laying hens may be influenced by dietary supplementation with PHY and 25-D3.

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


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Mycoplasma gallisepticum (MG) may affect the reproductive performance as well as the respiratory function of commercial layers (Mohammed et al., 1987; Burnham et al., 2002a). The vertical transmission of MG from a hen to her eggs is known to occur (Glisson et al., 1984), and MG has been cultured from the periovarian region (Fabricant and Levine, 1963), oviduct (Carlson and Howell, 1967; Domermuth et al., 1967; Nunoya et al., 1997), liver, spleen, uterus, and vagina (Sahu and Olson, 1976), and cloaca of chickens (Amin and Jordan, 1979; MacOwan et al., 1983).

Inoculation of commercial layers with the F-strain of MG (FMG) at 12 wk of age has been reported to delay onset of lay and decrease total egg production (Burnham et al., 2002a). In a companion article, Burnham et al. (2002b) reported that alterations in liver, ovarian, and reproductive organ characteristics were associated with FMG infection in commercial layers. This occurred despite the lack of any concomitant changes in the bird’s intestinal characteristics. More specifically, FMG inoculation at 12 wk resulted in a higher incidence of fatty liver hemorrhagic syndrome (FLHS), ovarian follicular regression, and decreased isthmal and vaginal proportions of the reproductive tract. It was concluded that alterations in the performance and egg characteristics of layers inoculated with FMG at 12 wk of age were related to mutual functional disturbances in the liver, ovary, and oviduct without concomitant intestinal changes.

Although 25-hydroxycholecalciferol (25-D3) is well known as a precursor for dihyroxylated metabolites (i.e., 1, 25-dihydroxycholecalciferol) in the chicken (Holick, 1989), it also has been shown to have biological activity (Olson and DeLuca, 1969), potential clinical significance (Heaney et al., 1997), the capability of inducing calcium ion fluxes in enterocytes (Larsson et al., 2002), and an affinity for binding to specific enterocyte proteins (Teegarden et al., 1997, 2000). Edwards (1993) noted that the addition of 1, 25-dihydroxycholecalciferol to broiler chicken diets allowed for a greater 9-d BW and bone ash content, and a greater retention of total calcium, phosphorus, and phytate phosphorus. Furthermore, Carlos and Edwards (1998) observed that the addition of phytase (PHY), or 1, 25-dihydroxycholecalciferol, or their combination to basal layer diets had a positive effect on BW and prevented a rapid decrease in egg production due to an MG infection. In a recent study, which is a companion to the current one, Peebles et al. (2007) found that the supplementation of layer diets with PHY depressed hematocrit, and that FMG inoculation prelay or at lay onset ameliorated the depressing effects of dietary PHY and 25-D3 supplementation on BW. Although Viveros et al. (2002) observed that PHY supplementation reduced the relative liver weight of broiler chicks, Mattila et al. (2004) reported that no calcification of soft tissues, including the liver, was identified in laying hens fed diets supplemented with vitamin D3 (cholecalciferol).

This study was designed to characterize possible changes in the digestive and reproductive organ characteristics of commercial layers in response to FMG inoculation and dietary supplementation with PHY and 25-D3 throughout a complete egg laying cycle. The organs examined included the liver, small intestine, ovary, and oviduct. Furthermore, the relative lengths and weights of the individual segments that make up the small intestine and oviduct were examined. Because it has been suggested that timing of inoculation (12 vs. 22 wk) may affect the blood characteristics of layers (Peebles et al., 2007), the additional effects of FMG inoculations given prelay (12 wk of age) and at onset of lay (22 wk of age) were also determined.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Bird Management
All trials were conducted under an approved USDA Animal Care and Use protocol. In the pretreatment pullet period, chickens were vaccinated, and sample testing procedures, materials, and specificity for the presence of MG and Mycoplasma synoviae were performed as described by Peebles et al. (2003). Ingredient percentages and calculated analyses of the basal starter and grower diets used during the pretreatment pullet period are also provided by Peebles et al. (2003). These diets were formulated to meet or exceed NRC (1994) specifications. No medications were administered during any of the trials. A full description of all the other pretreatment pullet management procedures is provided by Peebles et al. (2007).

In each trial, 240 birds were randomly placed in individual cages 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 FMG-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, feed, and water were provided as described by Peebles et al. (2007). Ingredient percentages and calculated analyses of the basal developer and prelay diets used are provided by Peebles et al. (2003). These diets were also formulated to meet or exceed NRC (1994) specifications.

FMG Inoculation and Mycoplasma Identification
At 12 and 22 wk of age, pullets treated with FMG 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 FMG (99th passage above the unknown passage level; provided by S. H. Kleven, University of Georgia, Athens, GA). Similarly, pullets designated as controls were sham inoculated via eye drop in the right eye with 0.04 mL of sterile Frey’s broth media (Frey et al., 1968). The FMG inoculation titers, titer determination procedures, and testing procedures for the presence of Mycoplasma species in hens at 20 and 58 wk of age were as described by Peebles et al. (2007).

Experimental Diets
Experimental layer diets were made available throughout each entire trial period, beginning at 20 wk of age, and continuing through 58 wk of age. Both diets were isocaloric and isonitrogenous; however, one diet served as a basal control diet and the other was the basal diet supplemented with PHY (0.025%; 600 FTU phytase units/ kg of diet; BASF, Corp., Florham Park, NJ) and 25-D3 (diluted premix, 0.025%; pure crystalline, 34.5 µg/kg of diet; Hoffmann-La Roche Inc., Parsippany, NJ). Feed adjustments and mixing frequency, and 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 by Peebles et al. (2007). The diets were formulated to meet or exceed NRC (1994) specifications. Determined analyses of the diets were performed according to the methods of the Association of Official Analytical Chemists (1980).

Data Collection
At 58 wk of age, in all 3 trials, 1 tagged hen from each replicate treatment group of birds representing each treatment combination (diet, inoculation type, and inoculation age) was euthanized by cervical dislocation following an overnight fast. The birds were then weighed and their organs harvested. Organ analyses included liver weight; liver moisture and lipid concentration; incidence of FLHS; ovary weight, histology, and mature follicle quantitation; total oviduct weight and length; weights, lengths, and histologies of the infundibulum, magnum, isthmus, uterus, and vagina; small intestine weight and length; and weights and lengths of the duodenum, jejunum, and ileum. Liver, ovary, oviduct, and small intestine weights were expressed as percentages of BW. The FLHS incidence was expressed as the percentage of birds exhibiting FLHS to any degree. Weights of the various regions of the oviduct and small intestine were expressed as percentages of BW and total organ weight. Lengths of the various regions of the oviduct and small intestine were expressed as percentages of total organ length.

Statistical Analysis
A randomized complete block experimental design, with trial as a block, was utilized. Weights, lengths, and histologies of the isthmus and uterus were examined in 2 trials. Whereas, liver weight; liver moisture and lipid concentration; FLHS incidence; ovary weight, histology, and mature follicle quantitation; total oviduct weight and length; weights, lengths, and histologies of the infundibulum, magnum, and vagina; small intestine weight and length; and weights and lengths of the duodenum, jejunum, and ileum were examined in all 3 trials. The data of all trials (2 or 3 depending upon parameter) were pooled and then analyzed together. Therefore, results from the individual trials were not reported independently but were reported over all the 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. The data for all parameters were subjected to 1-way ANOVA. The effects of dietary treatment (control vs. PHY and 25-D3), age of inoculation (12 vs. 22 wk), type of inoculation (sham vs. FMG), and their interactions were tested. Fixed effects were inoculation type, age of inoculation, and diet 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
 
Tests for the presence of Mycoplasma species in the birds from all 3 trials indicated that there was no cross contamination between FMG-inoculated and FMG-clean birds (Peebles et al., 2007). Therefore, treatment differences attributed to inoculation (type or timing) were not influenced by miss-exposure of the experimental birds to MG. There was a significant main effect due to age of inoculation (P ≤ 0.04) for magnum weight as a percentage of total oviduct weight. Percentage magnum weight was lower in birds that were inoculated (sham or FMG) at lay onset (22 wk of age) compared with those that were inoculated prelay (12 wk of age). Percentage magnum weights in birds inoculated prelay and at onset of lay were 46.8 and 43.8%, respectively (pooled SEM = 1.58%).

The effects of the age at which an inoculation is given, irrespective of inoculum content, on the digestive or reproductive organ characteristics of commercial layers have not previously been determined. Nevertheless, these current data indicate that the proportion of the total weight of the oviduct contributed by the magnum was reduced by inoculating (sham or FMG) birds at 22 rather than at 12 wk of age. Because there was no associated change in the weight of the total oviduct relative to BW, an internal shift or repartitioning of regions within the oviduct may have occurred. Also, because there was no concomitant effect on the relative lengths of the various oviductal segments, it is suggested that the size or numbers of the cells lining the walls of the magnum were decreased by inoculating at the later time.

The basis for the effect of age of inoculation on this specific component of the reproductive tract is not known; however, lay onset represents a physiological transition that can be particularly demanding to the bird (Klasing, 1998). Contrasts in the physiological state of the birds at these 2 different ages of inoculation may have, therefore, played a role in the differential effects of the 12 and 22 wk inoculations on oviduct structure. In a companion article by Peebles et al. (2007) describing the blood characteristics of the birds used in the current study, it was shown that total plasma protein concentration at 34 wk of age was higher in the birds that were inoculated at the onset of lay compared with those inoculated prelay. These current results support the contention that the age at which inocula are administered to layers should be given careful consideration because of possible subsequent effects on oviduct anatomy.

There was a significant inoculation type x age of inoculation interaction for duodenum length as a percentage of total small intestine length (P ≤ 0.03). Duodenum length as a percentage of organ length in birds inoculated with FMG at 12 wk was greater than those inoculated with FMG at 22 wk, with 12 and 22 wk sham-inoculated birds intermediate. Percentage duodenum lengths in 12 and 22 wk sham-inoculated birds were 22.1 and 22.9%, respectively, and in 12 and 22 wk FMG-inoculated birds were 23.3 and 21.9%, respectively (pooled SEM = 1.18%). Conversely, although the virulence of the S6-strain of MG (S6MG) is considered to be greater than that of FMG (Levisohn et al., 1986), in a report provided by Peebles et al. (2006), in which layers were sham inoculated at 10 wk of age or inoculated with S6MG at 10, 22, or 45 wk of age, there were no noted effects on the digestive tracts of the birds. Also, despite noted effects of a 12-wk FMG inoculation on the hen’s reproductive tract (relative magnum length, and isthmus and vagina weights relative to body and oviduct weight) when compared with 12-wk sham-inoculated controls, Burnham et al. (2002b) noted no effects of the 12-wk FMG inoculation on the digestive system. The results of Burnham et al. (2002b) and those of the current study regarding the effects of a 12-wk FMG-inoculation on specific oviduct characteristics do not agree. However, the present results and those of Burnham et al. (2002b) do indicate that the gross intestinal characteristics of layers inoculated with FMG at 12 wk are not different when compared with 12-wk sham-inoculated controls. Furthermore, although the age of S6MG inoculation, as reported by Peebles et al. (2006), did not affect the gross characteristics of the small intestine, the current results do show that the timing (12 vs. 22 wk) of an FMG inoculation may differentially influence relative duodenal length.

There was a significant main effect due to diet for infundibulum length as a percentage of total oviduct length (P ≤ 0.03), isthmus weight as a percentage of total oviduct weight (P ≤ 0.05), and duodenum length as a percentage of total small intestine length (P ≤ 0.02; Table 1Go). Infundibulum length and isthmus weight percentages were increased, whereas duodenum length percentage was decreased by dietary supplementation with PHY and 25-D3 (Table 1Go). An association between oviduct structure and dietary PHY or 25-D3 has not been previously reported; however, these data suggest that the dietary combination of PHY and 25-D3 can affect oviductal as well as intestinal anatomy. More specifically, the relative contribution of the infundibulum to total oviduct length and the isthmus to total oviduct weight in the layer may be increased by supplemental PHY and 25-D3.


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  		Table 1. Infundibulum length as a percentage of oviduct length (INFL), isthmus weight as a percentage of oviduct weight (ISTW), and duodenum length as a percentage of small intestine length (DUOL) in commercial layers fed control or phytase (PHY) and 25-hydroxycholecalciferol (25-D3) supplemented diets1,2
 
In the companion article by Peebles et al. (2007), dietary supplementation with PHY and 25-D3 was shown to decrease BW in sham-inoculated controls and decrease blood hematocrit values in sham and FMG inoculation treatments (across type of inoculation). The bases for the association between these effects and the changes in the relative weight of the isthmus and relative lengths of the infundibulum and duodenum are not evident. Nevertheless, Wu et al. (2004) reported that the addition of microbial PHY improved the performance of broiler chickens fed diets containing adequate phosphorus levels. The improvement in performance with PHY supplementation was associated with a reduction in the relative weight and length of the small intestine, in an increase in villus height in the duodenum, and in a decrease in the number of goblet cells in the jejunum. Supplemental PHY reduced the relative weight and length of the small intestine by 11.4 and 14.1%, respectively. When fed adequate diets, birds absorb phosphate in the upper jejunum (Levin, 1984) and secrete phosphate in the duodenum (Denbow, 2000). However, when fed phosphorus-deficient diets, a net absorption of phosphate takes place in the duodenum (Denbow, 2000). In the control birds of the current investigation, which were fed basal diets adequate in phosphorus, a normal exchange of phosphate in the upper jejunum and duodenum would be expected. However, supplementation of the basal diets with PHY and 25-D3 led to a decrease in the length of the duodenum relative to the length of the entire small intestine.

Carlos and Edwards (1998) reported that the supplementation of diets with PHY and 1, 25-dihydroxycholecalciferol positively affected BW and prevented a rapid decrease in egg production that had been observed in MG-infected commercial layers. An increase in calcium and phosphate uptake efficiency in the duodenum in response to PHY and 25-D3 would therefore be expected to be accentuated in MG-infected birds. However, there was no interaction between the effects of inoculation type and diet (PHY and 25-D3 supplementation) on relative duodenum length as well as on relative infundibulum length or isthmus weight. Furthermore, the effects of PHY and 25-D3 on the reproductive and digestive organs of the hens were completely independent of those due to age of inoculation as well as those due to type of inoculation.


   ACKNOWLEDGMENTS
 
The authors express appreciation to Jerry H. Drott (Poultry Research Unit, ARS, USDA) for his expert technical assistance in this project.


   FOOTNOTES
 
1 This is journal article No. J-11057 from the Mississippi Agricultural and Forestry Experiment Station supported by MIS-321010. Back

2 Use of trade names in this publication does not imply endorsement by Mississippi Agricultural and Forestry Experiment Station of these products, nor similar ones not mentioned. Back

Received for publication February 6, 2007. Accepted for publication March 21, 2007.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
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E. D. Peebles, S. L. Branton, M. R. Burnham, S. K. Whitmarsh, and P. D. Gerard
Effects of Supplemental Dietary Phytase and 25-Hydroxycholecalciferol on the Performance Characteristics of Commercial Layers Inoculated Before or at the Onset of Lay with the F-Strain of Mycoplasma gallisepticum,
Poult. Sci., March 1, 2008; 87(3): 598 - 601.
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