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ENVIRONMENT, WELL-BEING, AND BEHAVIOR |
Department of Animal Science, McGill University, Sainte-Anne-de-Bellevue, Quebec, Canada, H9X 3V9
1 Corresponding author: ciro.ruiz{at}poultry.tamu.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: antibiotic • mannan oligosaccharide • lignin • gut health • broiler
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Currently, the subtherapeutic usage of antibiotics in livestock production is under severe scientific and public scrutiny, because AGP have been linked to the development of antibiotic-resistant pathogenic bacteria, which pose a threat to human health (Smith et al., 2003). As result of such concerns, in 1997, the European Union initiated a ban on subtherapeutic usage of the antibiotic avoparcin in animal production, and all AGP were banned on January 1, 2006 (Burch, 2006). Although a complete ban on AGP has not been implemented in many countries, international pressure and public health concerns are likely to lead to such a scenario. Consequently, the poultry industry must develop alternatives to AGP to address public health concerns without compromising the efficiency of poultry production.
Prebiotics are nondigestible feed ingredients that beneficially affect the host by selectively stimulating the growth or metabolic activity of a limited number of intestinal microorganisms (Gibson and Roberfroid, 1995). Fructooligosaccharides and mannan oligosaccharides are among the classes of prebiotics that beneficially affect gut health, but they do so by different modes of action (Ferket, 2004). Research comparing BioMos (Alltech Inc., Nicholasville, KY), a commercial mannan oligosaccharide, to AGP shows that it can effectively suppress enteric pathogens, enhance the immune response, and improve the integrity of the intestinal mucosa in broilers (Spring et al., 2000; Iji et al., 2001). However, the effects of mannanoligosaccharides on the beneficial microorganisms in the chicken gut are not very consistent (Spring et al., 2000; Fairchild et al., 2001; Fernandez et al. 2002; Denev et al., 2005).
Lignin has been investigated for its effects on the hind-gut microflora and animal performance and its ability to inhibit the growth of pathogenic enteric bacteria. Lignin is a natural component of plant cell walls, and in its intact form, it represents a barrier to digestion of feedstuffs. Alcell lignin (Alcell Technologies Inc., Montreal, Quebec, Canada) is a coproduct of paper manufacture, composed of low molecular weight polyphenolic fragments (Lora et al., 1993). Alcell lignin (1.25% of DM) has been reported to improve growth performance of veal calves and to inhibit the growth of Escherichia coli in vitro (Phillip et al., 2000). In studies with chickens, the dietary inclusion of Indulin (4 and 8%, Westvaco Corp., Charleston, SC), a purified form of lignin, has been shown to improve weight gain and feed efficiency and to reduce the concentrations of volatile fatty acids in the ceca and large intestine (Ricke et al., 1982). Nelson et al. (1994) reported that Alcell lignin reduced intestinal translocation of pathogenic bacteria following burn injury in rats and inhibited in vitro growth of E. coli, Staphylococcus aureus, and Pseudomonas. It seems likely, therefore, that purified lignin has the potential to improve poultry performance by altering the microbial ecology of the hindgut.
The objectives of this study were to determine the effects of dietary addition of purified lignin (Alcell lignin) or a mannan oligosaccharide (BioMos) to broiler diets free of antibiotics on growth performance, intestinal integrity, and microbial populations in the ceca and litter. The effects of the prebiotics were compared with those of an AGP-supplemented diet.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Birds were randomly assigned to 5 treatments (4 pen replicates; 40 birds per pen). The 5 experimental diets included the following: 1) negative control diet (CTL–), antibiotic-free; 2) positive control diet (CTL+), containing 11 mg/kg of virginiamycin; 3) CTL– with the addition of BioMos (MOS, 0.2% of the starter diet and 0.1% of the grower diet); 4) CTL– with the addtion of Alcell lignin at 1.25% of the diet (LL); 5) CTL– with the addtion of Alcell lignin at 2.5% of the diet (HL). The diets were formulated to be isonitrogenous, isoenergetic, and to meet or exceed NRC (1994) requirements for macro- and micronutrients. The ingredient composition and nutrient content of the diets are shown in Table 1
. A 2-phase feeding program was used with a starter diet from d 1 to 21 and a grower diet from d 22 to 42. Feed consumption and BW (by pen) were recorded at weekly intervals.
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Microbial Populations of Cecal Digesta and Litter
At 28 and 42 d of age, the cecal contents from each bird were aseptically emptied into sterile plastic bags and stored at –20°C for later microbiological analysis. Samples of the cecal contents were serially diluted in 0.85% sterile saline solution and used to assay lactobacilli, bifidobacteria, E. coli, and Salmonella. All microbiological analyses were performed in duplicates, and the average value of these were used for statistical analyses. Lactobacilli was anaerobically assayed using lactobacilli MRS agar (Fisher Scientific, Ottawa, Ontario, Canada) and incubated at 37°C for 48 h. Enumeration of bifidobacteria was performed using Wilkins-Chalgren agar (Oxoid, Nepean, Ontario, Canada) supplemented with glacial acetic acid (1 mL/L) and mupirocin (100 mg/L) extracted from antimicrobial discs (Oxoid). Seventy-five discs were placed into 15 mL of Wilkins-Chalgren broth (Oxoid) and shaken for 30 min. Thereafter, 10 mL of this broth was added to 90 mL of agar medium (Rada et al., 1999). The petri dishes were placed in anaerobic jars, using Anaeropacks (Oxoid), and incubated at 37°C for 5 d. Escherichia coli was assayed using Rapid E. coli 2 agar (Bio-Rad Laboratories, Mississauga, Ontario, Canada) modified using E. coli supplement (Bio-Rad) to be selective for E. coli. Populations of Salmonella were assayed using Salmonella Shigella agar (Fischer Scientific).
Litter sampling was performed using a modification of the method described by Rybolt et al. (2005). Litter samples from each pen were taken in the middle of the pen and equidistant from each other at each side end of the pen, using examination gloves. The 5 subsamples were thoroughly mixed by hand, placed into sterile Whirl-Pak microbiological bags (Nasco, Fort Atkinson, WI), and sealed. All samples were kept at –20°C for subsequent enumeration of E. coli and Salmonella. The litter sample (10 g) was serially diluted in sterile saline solution, and E. coli and Salmonella were enumerated as previously described. The 100-mm petri dishes were then incubated at 37°C overnight, and colonies were counted.
Statistical Analysis
Data were analyzed as a one-way ANOVA using the GLM procedure of SAS (SAS Institute, 2003), with pen serving as the experimental unit for performance parameters and bird as the experimental unit for histology and microbiology parameters. Treatment means were separated using Bonferroni’s multiple comparison test. Statistical significance was declared at a probability of P < 0.05. All microbiological concentrations were subject to base-10 logarithm transformation before analysis.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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. Beyond the first week of the experiment, birds fed the CTL– diet were consistently heavier than those fed the diet containing AGP. At 28, 35, and 42 d of age, birds fed the CTL– diet were also heavier than those fed diets containing lignin (LL and HL); only at d 42, birds fed the CTL– diet were heavier than those fed the MOS diet. Throughout the entire 42 d, birds fed the diets containing virginiamycin, MOS, or lignin (LL or HL) exhibited similar growth performance. Before d 28 of the experiment, feed intake was not different among treatment groups (Table 2). However, during the last 2 wk of the study, birds fed the CTL– diet consumed more feed than did those in the other treatment groups. Feed conversion did not differ among dietary treatments at any point during the 6-wk experimental period.
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). However, at d 28, MOS-fed birds had longer villi than birds in any treatment group except the LL group. At d 42, birds fed the CTL+ or HL diet exhibited the smallest villi height. At d 42, there were no differences in villi height among birds fed the CTL– diet or diets containing MOS or LL. The number of goblet cells per villus (GCV) was not different among treatment groups at d 14 (Table 3). At d 28, however, MOS-fed birds had a significantly greater number of GCV than birds in any other treatment group except the LL diet. At this age, birds fed the LL diet had a greater number of GCV than those fed virginiamycin; the number of GCV obtained with the LL diet was not different from those obtained with the HL diet or the CTL– diet. By d 42, birds fed MOS had a greater number of GCV than birds in the other treatment groups. Estimates of crypt depth, muscularis layer thickness, and thickness of the muscularis mucosae were not affected by dietary treatment (Table 3). The whole gut weight; weights of empty duodenum, jejunum, ileum, and ceca; and the pH of the intestinal and cecal digesta were not affected by dietary treatments at any time (data not shown).
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. At both d 28 and 42, birds fed the CTL+ diet had the lowest population of lactobacilli. At d 28, the population of lactobacilli in MOS-fed birds exceeded only that of birds fed the CTL+ diet; however, at d 42, birds fed the MOS diet had the largest population of lactobacilli among all dietary treatments. At d 42, birds fed both levels of lignin also had greater populations of lactobacilli in the ceca than those fed the CTL+ diet. However, there were no differences in the cecal population of lactobacilli between the 2 levels of lignin or between lignin and the CTL– diet, whether the measurements were made at d 28 or 42.
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). At d 28, the population of bifidobacteria was not different in birds fed MOS or CTL–. At d 42, birds fed the MOS diet had a higher population of bifidobacteria than those fed the CTL+ or the HL diet but not different from birds fed the CTL– diet nor the LL diet. Populations of E. coli and Salmonella could not be enumerated, because it appears that the concentrations in the cecal digesta were too low to be enumerated.
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). At d 28, birds fed LL or HL had lower populations of E. coli loads in the litter than birds fed the CTL– or CTL+ diet, but the effects were not significant. Birds fed the HL diet had a lower population of E. coli in the litter than those fed the CTL– but only at d 42. At both d 28 and 42, the effects of MOS and lignin (LL and HL) were similar.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Feed efficiency was not affected by any of the additives. In studies with broilers fed MOS, AGP, a combination of MOS and AGP, or an AGP-free diet, Waldroup et al. (2003) reported no improvement in growth performance and feed efficiency. However, based on a meta-analysis of 44 research trials with broilers, Hooge (2004) concluded that birds fed MOS showed improved growth performance and feed efficiency compared with those fed AGP-free diets; performance was similar between MOS and AGP. In a study with broiler chickens, Ricke et al. (1982) reported that dietary addition of indulin improved weight gain and feed efficiency. However, indulin is a different source of lignin than the one used in this study, which may explain the different results.
It is reported that AGP (Sims et al., 2004) and most beneficial additives (Hooge, 2004) are most effective under disease and stress conditions, such as extremes of ambient temperature, crowding, and poor management, which are invariably present in commercial broiler production. The present study was conducted under good hygienic conditions (new experimental facility, strict bio-security measures, clean litter, good ventilation, and low stocking density), thus implying minimum bacterial challenge. Under such conditions, the birds may not have required any feed additive for maximum productive response.
Dietary addition of MOS caused a major increase in the height of the villi in the jejunum when compared with AGP and AGP-free diets. The effect of feeding the low level of lignin was similar to that of MOS. An increase in villi height in the duodenum has been previously reported in broilers fed a prebiotic-based diet compared with an antibiotic-free diet (Solis de los Santos et al., 2005) and has been explained by indigenous microbes that stimulate vascularization and development of the intestinal villi, thus enhancing the efficiency of digestion and absorption (Stappenbeck et al., 2002). Thus, our findings suggest that lactobacilli and bifidobacteria, among other types of beneficial bacteria favored by the dietary addition of MOS or LL, have important contributions to villi height. Because long villi are correlated with improved gut health, MOS and LL diets offer a comparative advantage over the CTL+ diet in improving the gut health status of the birds. However, at d 42, birds fed the CTL+ or HL diet had shorter villi than those fed the CTL– diet. Miles et al. (2006) also reported that virginiamycin-fed broilers had shorter villi in the ileum and duodenum than when fed an AGP-free diet. Both diets (CTL+ and HL) had lower cecal populations of beneficial bacteria, and this could explain the shorter villi.
The results revealed that the addition of MOS also increased the number of GCV when compared with all other dietary treatments. Compared with the CTL+ diet, the LL diet also had a positive effect on the number of GCV but only at d 28. In studies with turkeys, Ferket et al. (2002) reported that, when compared with an AGP-free diet, MOS significantly increased the goblet cell numbers. Goblet cells are responsible for the production of mucins, which bind pathogenic microorganisms and reduce their colonization of the gut mucosa (Blomberg et al., 1993). The mechanism by which MOS increases mucin production is through stimulation of the immune system (Janeway, 1993). Because LL also increased goblet cell numbers, it may be possible that low levels of lignin act via a mechanism similar to MOS.
Gut weight and other measures of gut integrity (crypt depth, muscularis thickness, and muscularis mucosae thickness) were not influenced by either lignin, MOS, or AGP at any stage of the experiment. Ferket et al. (2002) reported that intestinal weight and crypt depth were similar when turkeys were fed MOS or an AGP-free diet; however, muscularis thickness was significantly reduced. Broilers fed diets containing the AGP virgin-iamycin or bacitracin had reduced length and weight of the intestinal tract (Stutz et al., 1983; Dafwang et al., 1985; Miles et al., 2006). Increases in gut mass are associated with inflammation following bacterial infection (Walton, 1988), and this notion is supported by the observation that germ-free birds have thinner muscularis mucosae than conventional birds (Gordon and Bruckner-Kardoss, 1961). The reason for the lack of an effect of the feed additives on gut parameters may be that under the conditions of this experiment the pathogen load in the gut was low.
The cecal population of lactobacilli, at d 42 of the study, was highest in birds fed MOS. At this age, adding an AGP to the diet caused a major reduction in lactobacilli population. The effects of MOS on the population of beneficial bacteria in the gut of broilers are inconsistent. Fernandez et al. (2002) and Denev et al. (2005) reported increases in lactobacilli and bifidobacteria populations in the ceca of broilers fed MOS compared with an AGP-free diet. Sims et al. (2004) observed increased cecal population of bifidobacteria in turkeys fed MOS compared with an AGP-free diet, but there were no differences in cecal load of lactobacilli. Spring et al. (2000) also reported no effect of MOS on lactobacilli populations in the ceca of broilers. In studies with turkeys, Fairchild et al. (2001) reported that intestinal populations of lactobacilli and bifidobacteria did not differ among an AGP-free diet or those containing MOS or flavomycin. Factors contributing to variability in the effects of MOS on population of beneficial bacteria in the gut may include differences in experimental conditions, diet formulation, seasonal effects, and health status of the flock. Published data on the effects of lignin on the populations of lactobacilli and bifidobacteria in the gut of chickens are not available. The fact that when compared with the AGP, lignin had a positive effect on the population of lactobacilli in the ceca is a novel finding from this study. We observed that HL inhibited the growth of bifidobacteria in the ceca, which implies that lignin was beneficial only at the low level.
Then MOS, and to a less extent LL, increased villi height, goblet cell numbers, and the population of beneficial bacteria (lactobacilli and bifidobacteria) in the ceca of broiler chickens. These events may be linked. For instance, there is evidence that lactobacilli and bifidobacteria can increase the synthesis and secretion of mucin in the gut (Smirnov et al., 2005) as a result of an increase in goblet cell number (Ferket et al., 2002). Hence, the greater populations of lactobacilli and bifidobacteria in the ceca of birds fed MOS or the low level of lignin could explain the increased number of GCV associated with these treatments. There is also evidence that lactobacilli and bifidobacteria promote gut health by competing against potential pathogens for nutrients and binding sites and by producing bacteriocins, which act as antimicrobial compounds to control pathogens in the gut (Gibson and Wang, 1994; Kawai et al., 2004). Therefore, the use of MOS and low levels of lignin in the diet may be an effective strategy to maintain the integrity and health of the gut in chickens.
We could not enumerate E. coli and Salmonella in the cecal digesta, and this was probably due to undetectably low concentrations of these pathogenic bacteria under the conditions of this experiment. The use of an enrichment medium before the samples were plated may have allowed for detection of low numbers of E. coli and Salmonella. However, this approach was not adopted.
Chicken litter is a potential reservoir and transmission vehicle for pathogens and potential pathogens and a major source of E. coli (Garrido et al., 2004; Schrader et al., 2004). Our results reveal that the litter from MOS-fed birds showed a reduced population of E. coli when compared with birds fed the CTL+ or CTL– diet. According to Newman (1994), E. coli and Salmonella adsorb to MOS in the chicken gut, and less is excreted in feces. This explains the reduced population of E. coli in the litter of MOS-fed birds. The effect of MOS in reducing E. coli load in the litter is consistent with the results of Stanley et al. (2000). It is possible that E. coli remains bound to MOS, thereby limiting E. coli proliferation in the litter. Compared with CTL–, adding AGP to the diet did not influence the E. coli load in litter. Gram-negative pathogenic bacteria, such as E. coli, are resistant to most of the AGP used in poultry production (Page, 2003), and therefore, our finding is expected.
There was a tendency for lignin to reduce E. coli load in the litter. Although not statistically different from the control diets, the effects were comparable to that of MOS. Research conducted in vitro with the lignin product used in this study has demonstrated that it has inhibitory effects on growth of E. coli, S. aureus, and Pseudomonas (Nelson et al., 1994; Phillip et al., 2000). Nelson et al. (1994) reported that addition of lignin to the diet had a tendency to inhibit growth of aerobic bacteria in the cecum of rats and reduced the translocation of these bacteria in lymph nodes and the liver. Although the exact mechanism of lignin action remains unclear, it has been suggested that the phenolic compounds in lignin cause cell membrane damage and lysis of bacteria (Jung and Fahey, 1983). Lignin could, therefore, be a dietary strategy to reduce E. coli load in the gut and litter of chickens.
Escherichia coli is the principal pathogenic organism implicated in cellulitis, the major cause of carcass condemnation at the processing plants in Canada (Kumor et al., 1998). Cellulitis is characterized by s.c. inflammatory reaction resulting from an infection by E. coli associated with litter (Schrader et al., 2004). The findings from this study indicate that MOS, and to a less extent lignin, can be used to reduce E. coli proliferation in poultry litter. This would offer an opportunity for dietary control of the cellulitis problem.
In conclusion, adding MOS or low levels of lignin (1.25%) to broiler diets improved gut integrity, as measured by changes in villi height, goblet cell number, and populations of the beneficial bacteria, lactobacilli and bifidobacteria, in the ceca; MOS also resulted in a major reduction in E. coli load in the litter, and this might have implications for the control of cellulitis in chickens. The effect of lignin in reducing E. coli load in litter was similar to that of MOS. Under the conditions of this study, AGP failed to improve growth performance and feed efficiency when compared with an antibiotic-free diet or one containing MOS or lignin. The addition of MOS and perhaps low levels of lignin to the diet could be an alternative to the use of antibiotics as growth promoters in poultry production.
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ACKNOWLEDGMENTS |
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Received for publication September 1, 2006. Accepted for publication January 29, 2007.
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REFERENCES |
|---|
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Blomberg, L., H. C. Krivan, P. S. Cohen, and P. L. Conway. 1993. Piglet ileal mucus protein and glycolipid (galactosylceramide) receptors specific for Escherichia coli K88 fimbriae. Infect. Immun. 61:2526–2531.
Burch, D. 2006. Anticipated effects of the withdrawal of antibiotic growth promoters (AGPs) from pigs in the European Union on 1st January 2006. http://www.octagon-services.co.UK/articles/withdrawalAGP.htm. Accessed Aug. 2006.
CEAS. 1991. The impact on animal husbandry in the European community of the use of growth promoters. Pages 1–319 in Growth Promoters in Animal Feed. Rep. Eur. Comm. London Univ. Press, UK.
Dafwang, I. I., M. E. Cook, M. L. Sunde, and H. R. Bird. 1985. Bursal, intestinal, and spleen weights and antibody response of chicks fed sub-therapeutic levels of dietary antibiotics. Poult. Sci. 64:634–639.[ISI][Medline]
Denev, S. A., I. Dinev, I. Nikiforov, and V. Koinarski. 2005. Effects of mannan oligosaccharides on composition of cecal microflora and performance of broiler chickens. Pages 351–353 in 15th Eur. Symp. Poult. Nut., Balatonfüred, Hungary. World’s Poult. Sci. Assoc., Budapest, Hungary.
Emborg, H., A. K. Ersboll, and O. E. Heuer. 2001. The effect of discontinuing the use of antimicrobial growth promoters on the productivity in the Danish broiler production. Prev. Vet. Med. 50:53–70.[ISI][Medline]
Engster, H., D. Marvil, and B. Stewart-Brown. 2002. The effect of withdrawing growth promoting antibiotics from broiler chickens: A long term commercial industry study. J. Appl. Poult. Res. 11:431–436.
Fairchild, A. S., J. L. Grimes, F. T. Jones, M. J. Wineland, F. W. Edens, and A. E. Sefton. 2001. Effects of hen age, Bio-Mos and Flavomycin on poult susceptibility to oral Escherichia coli challenge. Poult. Sci. 80:562–571.
Ferket, P. R. 2004. Alternatives to antibiotics in poultry production: Responses, practical experience and recommendations. Pages 56–67 in Re-imaging the feed industry. Proc. Alltech’s 20th Annu. Symp. T. P. Lyons and K. A. Jacques, ed. Nottingham Univ. Press, UK.
Ferket, P. R., C. W. Parks, and J. L. Grimes. 2002. Benefits of dietary antibiotic and mannan oligosaccharide supplementation for poultry. http://www.feedinfo.com/files/multi2002-ferket.pdf Accessed Jun. 2006.
Fernandez, F., M. Hinton, and B. Van Gils. 2002. Dietary mannan-oligosaccharides and their effect on chicken caecal microflora in relation to Salmonella Enteritidis colonization. Avian Pathol. 31:49–58.[ISI][Medline]
Garrido, M. N., M. Skjervheim, H. Oppegaard, and H. Sorum. 2004. Acidified litter benefits the intestinal flora balance of broiler chickens. Appl. Environ. Microbiol. 70:5208–5213.
Gibson, G. R., and M. B. Roberfroid. 1995. Dietary modulation of the human colonic microbiotica: Introducing the concept of prebiotica. J. Clin. Nutr. 125:1404–1412.
Gibson, G. R., and X. Wang. 1994. Regulatory effects of bifidobacteria on the growth of other colonic bacteria. J. Appl. Bacteriol. 77:412–420.[Medline]
Gordon, H. A., and E. Bruckner-Kardoss. 1961. Effect of normal microflora on intestinal surface area. Am. J. Physiol. 201:175–178.
Hooge, D. M. 2004. Meta-analysis of broiler chicken pen trials evaluating dietary mannan oligosaccharides, 1993–2003. Int. J. Poult. Sci. 3:163–174.
Iji, P., A. A. Saki, and D. R. Trivey. 2001. Intestinal structure and function of broiler chickens on diets supplemented with a mannanoligosaccharide. J. Sci. Food Agric. 81:1186–1192.[ISI]
Janeway, C. A. 1993. How the immune system recognizes invaders. Sci. Am. 269:72–79.[ISI][Medline]
JETACAR. 1999. The use of antibiotics in food-producing animals: Antibiotic-resistant bacteria in animals and humans. Rep. Joint Expert Advis. Comm. Antibiot. Resist. Commonw. Aust., Canberra.
Jung, H. G., and G. C. Fahey. 1983. Nutritional implications of phenolic monomers and lignin: A review. J. Anim. Sci. 57:206–219.
Kawai, Y., Y. Ishii, K. Arakawa, K. Uemura, B. Saitoh, J. Nishimura, H. Kitazawa, Y. Yamazaki, Y. Tateno, T. Itoh, and T. Saito. 2004. Structural and functional differences in two cyclic bacteriocins with the same sequences produced by lactobacilli. Appl. Environ. Microbiol. 70:2906–2911.
Kumor, L. W., A. A. Olkowski, S. M. Gomis, and B. J. Allan. 1998. Cellulitis in broiler chickens: Epidemiological trends, meat hygiene, and possible human health implications. Avian Dis. 42:285–291.[ISI][Medline]
Lora, J. H., A. W. Creamer, L. C. F. Wu, and G. C. Goyal. 1993. Industrial scale production of organosolv lignins: Characteristics and applications. Pages 252–256 in Cellulosics: Chemical, Biochemical and Material Aspects. J. F. Kennedy, G. O. Phillips, and P. A. Williams, ed. Ellis Horwoods Ltd., West Sussex, UK.
Miles, R. D., G. D. Butcher, P. R. Henry, and R. C. Littell. 2006. Effect of antibiotic growth promoters on broiler performance, intestinal growth parameters and qualitative morphology. Poult. Sci. 85:476–485.
Nelson, J. L., J. W. Alexander, L. Gianotti, C. L. Chalk, and T. Pyles. 1994. Influence of dietary fiber on microbial growth in vitro and bacterial translocation after burn injury in mice. Nutrition 10:32–36.[ISI][Medline]
Newman, K. 1994. Mannanoligosaccharides: Natural polymers with significant impact on the gastrointestinal microflora and the immune system. Pages 167–174 in Biotechnology in the feed industry. Proc. Alltech’s 10th Annu. Symp. T. P. Lyons and K. A. Jacques, ed. Nottingham Univ. Press, UK.
NRC. 1994. Nutrient Requirements of Poultry. 9th rev. ed. Natl. Acad. Press, Washington, DC.
Page, S. W. 2003. The role of enteric antibiotics in livestock production. Pages 1–13 in A Review of Published Literature. Avcare Ltd., Canberra, Australia.
Phillip, L. E., E. S. Idziak, and S. Kubow. 2000. The potential use of lignin in animal nutrition, and in modifying microbial ecology of the gut. Pages 1–9 in East. Nutr. Conf. Anim. Nutr. Assoc. of Canada, Montreal, Quebec, Canada.
Rada, V., K. Sirotek, and J. Petr. 1999. Evaluation of selective media for bifidobacteria in poultry and rabbit caecal samples. J. Vet. Med. 46:369–373.
Ricke, S. C., P. J. van der Aar, G. C. Fahey, and L. Berger. 1982. Influence of dietary fibres on performance and fermentation characteristics of gut contents from growing chicks. Poult. Sci. 61:1335–1343.[ISI]
Rybolt, M. L., R. W. Wills, and R. H. Bailey. 2005. Use of secondary enrichment for isolation of Salmonella from naturally contaminated environmental samples. Poult. Sci. 84:992–997.
SAS Institute. 2003. SAS User’s Guide. Version 9.1 ed. SAS Inst. Inc., Cary, NC.
Schrader, J. S., R. S. Singer, and E. R. Atwill. 2004. A prospective study of management and litter variables associated with cellulites in California broiler flocks. Avian Dis. 48:522–530.[ISI][Medline]
Sims, M. D., K. A. Dawson, K. E. Newman, P. Spring, and D. M. Hooge. 2004. Effects of mannanoligosaccharide, bacitracin methylene disalicyclate, or both on live performance and intestinal microbiology of turkeys. Poult. Sci. 83:1148–1154.
Smirnov, A., R. Perez, E. Amit-Romach, D. Sklan, and Z. Uni. 2005. Mucin dynamics and microbial populations in chicken small intestine are changed by dietary probiotic and antibiotic growth promoter supplementation. J. Nutr. 135:187–192.
Smith, D. L., J. A. Johnson, A. D. Harris, J. P. Furuno, E. N. Perencevich, and J. G. Morris. 2003. Assessing risks for a pre-emergent pathogen: Virginiamycin use and the emergence of streptogramin resistance in Enterococcus faecium. Lancet Infect. Dis. 3:241–249.[ISI][Medline]
Solis de los Santos, F., M. B. Farnell, G. Tellez, J. M. Balog, N. B. Anthony, A. Torres-Rodriguez, S. Higgins, B. M. Hargis, and A. M. Donoghue. 2005. Effect of prebiotic on gut development and ascites incidence of broilers reared in a hypoxic environment. Poult. Sci. 84:1092–1100.
Spring, P., C. Wenk, K. A. Dawson, and K. E. Newman. 2000. The effects of dietary mannan-oligosaccharides on cecal parameters and the concentrations of enteric bacteria in the ceca of Salmonella challenged broiler chicks. Poult. Sci. 79:205–211.
Stanley, V. G., C. Brown, and A. E. Sefton. 2000. Comparative evaluation of a yeast culture, mannan-oligosaccharide and an antibiotic on performance of turkeys. Poult. Sci. 79(Suppl. 1):117. (Abstr.)
Stappenbeck, T. S., L. V. Hooper, and J. I. Gordon. 2002. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc. Natl. Acad. Sci. USA 99:15451–15455.
Stutz, M. W., S. L. Johnson, and F. R. Judith. 1983. Effects of diet, bacitracin, and BW restrictions on the intestine of broiler chicks. Poult. Sci. 62:1626–1632.[ISI][Medline]
Valencia, Z., and E. R. Chavez. 1997. Lignin as a purified dietary fiber supplement for piglets. Nutr. Res. 17:1517–1527.[ISI]
Waldroup, P. W., C. A. Fritts, and F. Yan. 2003. Utilization of Bio-Mos mannan oligosaccharide and Bioplex copper in broiler diets. Int. J. Poult. Sci. 2:44–52.
Walton, J. R. 1988. The modes of action and safety aspects of growth promoting agents. Pages 92–97 in Proc. Maryland Nutr. Conf. Univ. Maryland, College Park.
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  B. Baurhoo, A. Letellier, X. Zhao, and C. A. Ruiz-Feria Cecal Populations of Lactobacilli and Bifidobacteria and Escherichia coli Populations After In Vivo Escherichia coli Challenge in Birds Fed Diets with Purified Lignin or Mannanoligosaccharides Poult. Sci., December 1, 2007; 86(12): 2509 - 2516. [Abstract] [Full Text] [PDF]
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