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METABOLISM AND NUTRITION |
* Department of Animal Science, University of Manitoba, Winnipeg, Canada R3T 2N2; Nutreco Canada Agresearch, Burford, Ontario, Canada N0E 1A0; Department of Food Science, University of Manitoba, Winnipeg, Canada R3T 2N2; and Canadian Bio-Systems Inc., Calgary, Canada T2C 0J7
1 Corresponding author: b_slominski{at}umanitoba.ca
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: enzyme • Clostridium perfringens • broiler chicken
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Carbohydrase enzymes have a direct, positive effect on animal performance by improving nutrient digestion and absorption, thereby reducing substrate availability for microbial growth in the ileum (Choct et al., 1999; Bedford and Apajalahti, 2001); therefore, these enzymes may be beneficial for maintaining a healthy environment in the gastrointestinal tract of growing broiler chickens. Conventional carbohydrase supplements are mainly composed of xylanase and glucanase, enzymes that have been found effective in improving growth performance because of a reduction in digesta viscosity. However, a new generation of enzyme supplements is now being developed for specific use in the feed industry. This includes a multicarbohydrase blend of activities that, in our laboratory, has been proven to be effective in cell wall polysaccharide depolymerization (Meng et al., 2005), with the hydrolysis products potentially having a direct effect on animal health by manipulating the growth of pathogenic and nonpathogenic gastrointestinal microorganisms. Such effects mainly originate from the chemical nature of the substrates produced via enzymatic action on feed components. Among the feedstuffs commonly used in Canada, wheat, barley, corn, soybean meal, peas, canola meal, and wheat byproducts contain significant amounts of NSP such as arabinoxylans, β-glucans, galactans, galactomannans, rhamnogalacturonans, arabinogalactans, mannans, and arabinans (Theander et al., 1989). In addition, these feedstuffs are rich in certain galactooligosaccharides, which, along with resistant starch and glycoproteins, represent components poorly metabolized by poultry (Slominski, 1991). In the process of depolymerizing various polysaccharides in the diet, exogenous enzymes may produce galacto-, gluco-, manno-, or xylooligomers, which are similar to prebiotics and which may facilitate the proliferation of health-promoting bacteria such as Bifidobacterium and Lactobacillus (Monsan and Paul, 1995). In this context, the enzyme hydrolysis products may indirectly prohibit the growth of certain pathogenic species by stimulating the growth of lactic acid bacteria in the lower gut (Gibson and Roberfroid, 1995). Monsan and Paul (1995) demonstrated that glucooligosaccharides could be assimilated well by Bifidobacterium spp. In contrast, pathogenic species, including Clostridium and Salmonella, showed poor assimilation. In addition, certain enzyme hydrolysis products may attract microbes away from the intestinal binding sites by means of competitive exclusion, thereby reducing colonization and disease and releasing the mucosa to perform its function of secretion, digestion, and nutrient absorption (Iji and Tivey, 1998). For example, a reduced colonization of Salmonella was shown for diets after the addition of mannanoligosaccharides (MOS; Spring et al., 2000). Therefore, we hypothesized that the NSP hydrolysis products may serve as prebiotics and indirectly prohibit the growth of certain pathogenic species.
Reports on the effects of enzyme supplementation on the growth of C. perfringens and the incidence of NE are scarce. Therefore, the objective of this study was to investigate the effects of diet and a multicarbohydrase enzyme supplement on growth performance, gut health, and the incidence of NE in broiler chickens during C. perfringens challenge.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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A total of 1,216 male Ross-308 broiler chickens, vaccinated for Marek’s disease and infectious bronchitis, were purchased from a commercial hatchery. The broiler chicken research facility at Nutreco Canada Agresearch in Burford, Ontario, Canada, was used to conduct this study. Sixty-four pens were randomly assigned to treatment groups, with 19 birds per pen. Each pen provided 0.75 m2 of floor space, with a concrete floor and new wood shavings for bedding. A solid 12-inch-high (31 cm) plastic barrier separated adjacent pens. Precautions such as changing gloves and food coverings between treatment pens were taken to avoid accidental contamination of unchallenged pens with the challenge organism. Lighting program, heating, ventilation, and other management procedures were typical of broiler chicken producers in the local geographic area of Ontario, Canada. Water was provided by nipple-type drinker and feed was provided by trough-type feeders ad libitum. All animal procedures were conducted according to the guidelines of the Canadian Council on Animal Care (1993).
Experimental Design and Diets
A 2 x 2 x 2 factorial arrangement of treatments was used in a randomized complete block design to study the effects of diet type (corn- or wheat-based), enzyme addition (none or multicarbohydrase enzyme supplement), pathogen challenge, and their interactions. There were 8 blocks of 8 pens per block, with 1 pen of each treatment in each block, and each replicate pen consisted of 19 birds, for a total of 152 birds per treatment. The carbohydrase enzyme supplement supplied 60 U of cellulase, 1,400 U of pectinase, 1,200 U of xylanase, 800 U of glucanase, 500 U of mannanase, 30 U of galactanase, and other minor enzyme activities per kilogram of diet. Antibiotic- and coccidiostat-free diets were formulated to contain 3,000 kcal of ME/kg and 23% CP in the starter phase and 3,000 kcal of ME/ kg and 20% CP in the grower phase (Table 1
). All diets were pelleted and crumbled, and the pelleting temperature did not exceed 75°C.
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The experiment lasted for 39 d and consisted of 2 phases (0 to 21 d, starter; 21 to 39 d, grower-finisher). The C. perfringens challenge model used in the study was originally developed based on the method of Prescott et al. (1978) and has been described in several publications (Brennan et al., 2001a,b). The C. perfringens strain used was originally isolated from a field case of NE in Ontario and was known to produce lesions typical of NE, with mild suppression of growth rate and minimal mortality. Feed was withdrawn from all birds approximately 8 h before challenge. Inoculum was mixed with feed, and the feed was offered on the afternoon of d 13. Inoculation lasted for 16 h, and the remaining inoculum-containing feed was weighed and discarded on the morning of d 14. The calculated inoculation dose ranged from 6.7 x 108 to 8.9 x 108 cfu/ bird. During inoculation, the control birds received their regular feed.
Feed consumption and BW were measured on a pen basis on d 0, 13, 21, and 40, whereas mortality was recorded daily. Average daily feed intake, average daily gain, and the feed conversion ratio (FCR) were calculated for each period (d 0 to 13, d 13 to 21, d 21 to 39, and d 0 to 39). On d 17, 40 birds per treatment (5 birds per pen) were randomly selected and killed by asphyxiation with carbon dioxide. After euthanasia, the small intestine from each bird was removed, opened, and subjected to scoring by the same poultry pathologist for NE and coccidiosis lesions using the following scale: 0, no gross lesions; 1, thin, friable small intestine; 2, focal necrosis, ulceration, or both; 3, patchy necrosis; 4, severe, extensive mucosal necrosis (Johnson and Reid, 1970; Prescott et al., 1978). The intestinal contents were collected, and samples from 10 birds were pooled to yield 4 replicates per treatment for enumeration of bacteria. Subsamples (1.5 g from each pooled sample) were frozen in liquid nitrogen and stored at –20°C until needed for viscosity and pH measurements. The thawed samples were centrifuged at 3,600 x g at room temperature for 10 min, and viscosity of the supernatant was determined at 40°C by using a Brookfield digital viscometer (model DV-II+LV, Brookfield Engineering Laboratories, Stoughton, MA). The pH was determined by using a conventional pH meter.
Enumeration of Bacteria
Pooled digesta (10 g) were transferred into 90 mL of sterile peptone containing 0.5% cysteine hydrochloride and serially diluted. For C. perfringens enumeration, dilutions were plated on Perfringens agar base (OPSP, Oxoid Inc., Nepean, Ontario, Canada) containing supplements SR 76 and SR 7 (Oxoid Inc.) and were incubated at 38°C for 48 h in jars containing gas generation kits (BBL GasPak Plus, Becton Dickinson, Sparks, MD). Lactic acid bacteria were enumerated by using de Man, Rogosa, Sharpe agar (Difco, Detroit, MI) after incubation at 37°C for 48 h. Each sample was plated in duplicate.
Statistical Analysis
Statistical analysis was conducted by the SAS program (SAS Institute, 2003). Bacterial enumeration data were converted to log10 cfu/g before analysis. Because of the presence of a random effect (block), the performance parameters and lesion score data were analyzed by the MIXED procedure. The fixed effects in the model for performance parameters included diet, enzyme, challenge, and the associated 2- and 3-way interactions. Because no lesions were observed in the unchallenged birds, the model simply included diet, enzyme, and the 2-way interaction. Analyses based on pooled samples (bacterial numbers, pH, and viscosity) were tested by the GLM procedure, and the model included diet, enzyme, challenge, and the associated 2- and 3-way interactions. Mortality was tested by the same model but was subjected to the FREQ and GENMOD procedures. The results are presented with actual frequencies with SE. The GENMOD analysis was performed by using the binomial distribution and the logit function. Contrasts of enzyme effects (i.e., without vs. with enzyme addition) within each diet type and pathogen treatment (none or challenge) were made. All statements of significance were based on P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Feed intake was not affected by dietary treatments in the starter phase, except that from d 0 to 13, birds consumed slightly but significantly more corn-based diets than wheat-based diets, regardless of enzyme addition or disease challenge (Table 2). In the grower phase, a significant interaction between enzyme addition and diet type was observed. Enzyme addition resulted in an increase in feed consumption in birds fed corn-based diets (187.8 vs. 183.0 g; P = 0.01), whereas a reduction in feed intake was observed among birds fed wheat-based diets from 21 to 40 d (178.3 vs. 183.8 g; P < 0.01), regardless of disease challenge. Over the entire trial (0 to 40 d), birds consumed less of the wheat-based diets when enzyme was added (101.8 vs. 104.8 g; P = 0.04), but no difference was found in those consuming corn-based diets (106.7 vs. 104.2 g; P = 0.09), irrespective of pathogen challenge. Clostridium perfringens challenge significantly suppressed BW gain during the postchallenge period (13 to 21 d) in both the corn (55.3 vs. 60.1 g; P < 0.01) and the wheat group (47.2 vs. 55.3 g; P < 0.01), regardless of enzyme addition. An increased BW gain was observed in challenged birds consuming enzyme-supplemented corn-based diets (57.6 vs. 53.0 g), and this positive effect of enzyme addition was maintained throughout the grower phase. As a result, the final BW at the end of the trial was similar to that of the unchallenged birds (corn + enzyme, challenged vs. corn, unchallenged; 2.62 vs. 2.60 kg; P > 0.05). Over the entire trial, birds fed corn-based diets had a greater average daily gain than those fed the wheat-based diets. Clostridium perfringens challenge caused significant growth inhibition, and enzyme addition resulted in increased average BW gain (58.5 vs. 57.2 g) as well as increased final BW (2.57 vs. 2.51 kg). Feed conversion ratio was affected by the pathogen challenge from d 13 to 21 of the experiment, with a more pronounced effect observed for the wheat-based diets (none vs. challenge; 1.53 vs. 1.79; P < 0.0001) than for the corn-based diets (1.44 vs. 1.53; P = 0.11), regardless of enzyme addition. The effect of enzyme on feed utilization was significant and interacted with the diet type during each period, except from d 13 to 21. Enzyme addition significantly decreased FCR from d 0 to 13 of the experiment (1.36 vs. 1.44; P < 0.01) in birds consuming corn-based diets, irrespective of the disease challenge group. For those consuming wheat-based diets, FCR was decreased by 5.1 and 4.5% from d 21 to 40, and by 4.9 and 3.7% for the entire trial in unchallenged and challenged birds, respectively.
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Total mortality increased from 0.8 to 3.8% because of the pathogen challenge (Table 3). Neither diet type nor enzyme addition affected the mortality rate. The number of C. perfringens was below the detection limit among the unchallenged birds (Table 3). Among the challenged birds, those consuming wheat-based diets had greater C. perfringens counts than those consuming corn-based diets, regardless of enzyme addition. No intestinal lesions were observed in birds from the unchallenged groups (Table 3). For those exhibiting intestinal lesions, all were scored as focal necrosis, except that one bird consuming the wheat-based diet was scored as patchy necrosis. The average lesion score was greater in birds consuming wheat-based diets than in birds consuming corn-based diets. Addition of enzyme did not affect the C. perfringens numbers or lesion score. The number of lactic acid bacteria was similar among the treatment groups, except that a reduction in bacteria number was found because of enzyme addition in the unchallenged birds consuming wheat-based diets. When compared with corn-based diets, digesta viscosity was greater in birds consuming wheat-based diets (Table 3) and was reduced significantly after enzyme addition (from 4.1 to 2.7 mPa·s; P < 0.01), regardless of pathogen challenge. No differences in pH values were observed among the treatments.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). However, the decrease in FCR reached the level of significance only in birds fed the wheat-based diets in the grower phase, despite the fact that birds at this phase of production are known to be able to tolerate high intestinal viscosity (Salih et al., 1991). In addition, enzyme supplementation resulted in a decreased FCR in birds consuming corn-based diets from d 0 to 13, given that minimal amounts of water-soluble NSP are present in this type of diet. The results of the current study indicated that the cell wall-degrading activities are at least of equal importance as the viscosity-reducing properties. In the current study, C. perfringens challenge caused an inhibition of BW gain and inferior FCR over the entire trial, regardless of diet type. No overt behavioral signs or death caused by NE were observed, although macroscopically visible focal or patchy necrosis in the small intestinal mucosa and increased numbers of intestinal C. perfringens were noted in birds from the challenge group. Such responses would reflect a subclinical form of NE (Kaldhusdal and Hofshagen, 1992). The presence of typical intestinal lesions was used to diagnose whether the mortality was due to NE. In the current study, C. perfringens challenge significantly increased mortality even though no lesions were observed in dead birds, indicating that nonspecific, subtle histological changes may exist (Wilson et al., 2005; Olkowski et al., 2008). There are some concerns within the poultry industry that the subclinical form of NE may contribute to poor flock health (J. Wilson, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada, personal communication). Clinical outbreaks of NE may cause high mortality; however, subclinical NE may also lead to severe economic losses. Because NE is not usually detected in broiler chickens unless there are associated mortalities, it is often untreated; thus, performance and bird welfare could be greatly affected and associated with high condemnation rates at slaughter (Mcdevitt et al., 2006).
Numerous studies have shown that birds consuming diets with high amounts of wheat and barley, which are known to increase the viscosity of the intestinal contents, have a greater incidence of NE than those fed corn-based diets (Branton et al., 1987; Kaldhusdal and Hofshagen, 1992). Kaldhusdal and Skjerve (1996) concluded that the ratio of wheat plus barley to corn was positively correlated with the incidence of NE. The results from the current study support these findings, because greater C. perfringens numbers and average lesion scores were observed in birds fed the wheat-based diets. Despite considerable research efforts, the actual mechanisms underlying this cereal effect are still not fully understood (Dahiya et al., 2006). It has been suggested that high intestinal viscosity reduces nutrient absorption by the host animal, increases the rate of feed passage (Gohl and Gohl, 1977; Johnson and Gee, 1981; Edwards et al., 1988; Fengler and Marquardt, 1988; Ikegami et al., 1990), and may enhance mucus production (Larsen et al., 1993; Langhout et al., 1999; Piel et al., 2005), which could lead to increased numbers of anaerobic bacteria in the small intestine, particularly C. perfringens (Wagner and Thomas, 1978; Langhout et al., 1999). A study by Deplancke et al. (2002) showed that C. perfringens had significant acidomucolytic potential and grew rapidly on mucin-containing medium. Therefore, Collier et al. (2003) suggested that C. perfringens may be particularly mucolytic and its growth would be favored by the increased host mucus production associated with coccidiosis or a viscous intestinal environment.
Carbohydrase enzyme supplementation is known to accelerate dietary nutrient utilization by the host, which may reduce microbial activity as a result of substrate limitation in the ileum (Choct et al., 1999). Bedford and Apajalahti (2001) demonstrated that in birds fed wheat-based diets, addition of a xylanase-based enzyme preparation resulted in a 60% reduction in bacterial numbers, and research by Hubener et al. (2002) supported this finding. Any potential reduction in ileal fermentation could, in fact, be beneficial, because the substrates being fermented in this region are mainly undigested or encapsulated starch and protein, which would otherwise be available to the bird (Bedford, 2000). Furthermore, in the process of depolymerizing various NSP in the diet, the enzyme may produce galacto-, gluco-, manno-, or xylooligomers (De Silva et al., 1983), which could serve as prebiotics because of their ability to selectively stimulate the growth, activity, or both of beneficial lactic acid bacteria (Gibson and Roberfroid, 1995; Monsan and Paul, 1995). The use of both undefined competitive exclusion products (Elwinger et al., 1992; Craven et al., 1999) and defined bacterial cultures, including Lactobacillus acidophilus, Streptococcus faecalis, and Bacillus subtilis (Fukata et al., 1991; La Ragione and Woodward, 2003), have shown promising results in suppressing the proliferation of C. perfringens. Hofacre et al. (2003) reported that a lactic acid-producing bacterial culture alone or in combination with the MOS was effective at reducing C. perfringens-associated mortality and the subclinical effects on feed utilization, but addition of neither MOS nor fructooligosaccharides alone had any positive effects. In contrast, Sims et al. (2004) observed reduced C. perfringens numbers in the large intestine of turkey at 6 wk of age when MOS was included in the diets. In another study, Monsan and Paul (1995) demonstrated that glucooligosaccharides were assimilated well by beneficial Bifidobacterium spp., whereas Clostridium and Salmonella showed poor assimilation. In this context, we hypothesized that enzyme hydrolysis products may facilitate proliferation of lactic acid bacteria, thereby reducing C. perfringens growth. The results of the current study, however, do not fully support this hypothesis, because parameters such as C. perfringens numbers, digesta pH, lesion score, or mortality in birds consuming enzyme-supplemented diets did not differ significantly from those consuming diets without the enzyme. Only a few studies exist in the literature on the effects of enzyme supplementation on NE incidence, and the results have been contradictory and very difficult to compare because of the use of different disease challenge models, diet types, and enzyme supplements. Riddell and Kong (1992), who used a similar in-feed C. perfringens challenge model as that in the present study, found that the addition of pentosanase to a wheat-based diet did not affect NE mortality. However, no C. perfringens enumeration was performed in their study. In contrast, Choct et al. (2006) reported that xylanase supplementation reduced C. perfringens numbers in the ceca of healthy broiler chickens fed wheat-based diets. In another study, Jackson et al. (2003) showed that the addition of β-mannanase to corn-based diets improved performance and reduced lesion scores in birds challenged with both Eimeria and C. perfringens. They postulated that the benefits of enzyme addition were due to the depolymerization of β-mannans, which may exacerbate the disease symptoms via a stimulatory effect on the immune system. In the current study, enzyme supplementation did not affect the growth of C. perfringens. However, it ameliorated the growth inhibition of disease challenge by increasing the BW gain in birds consuming the corn-based diets and improving the FCR in those consuming the wheat-based diets. The different responses of birds to enzyme supplementation may be due to the different natures of the diets (i.e., wheat vs. corn) and the content of water-soluble NSP.
Some earlier studies demonstrated that xylanase addition stimulates the growth of lactic acid bacteria in the small intestine (Vahjen et al., 1998; Engberg et al., 2004). However, the results of the current study demonstrated that the number of lactic acid bacteria was slightly but significantly reduced by enzyme addition in the nonchallenged birds consuming the wheat-based diets. Whether this is the true microbial response is difficult to determine because it was observed only in one enzyme-supplemented group, and further research may be needed.
Overall, enzyme supplementation minimized the growth suppression associated with the C. perfringens challenge, with the most pronounced effect observed in birds fed the wheat-based diet. The beneficial effect of enzyme addition was likely due to enhanced nutrient utilization as a consequence of reduced intestinal viscosity and elimination of the nutrient-encapsulating effect of the cell wall polysaccharides. This finding may assist in the development of nutritional strategies to maintain performance in broiler chickens without using antibiotic growth promoters.
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ACKNOWLEDGMENTS |
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Received for publication May 21, 2008. Accepted for publication September 8, 2008.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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