Does dietary fiber change resistance to enteric disease?

Those who provide daily care for animals in production agriculture are acutely aware of the importance of animal health. From an economic perspective, as record systems (both performance and financial) used in animal agriculture have become markedly more sophisticated during the last two decades, they have increasingly shown the importance of keeping animals healthy for the economic strength of the production unit and the industry.

Indeed, the willingness of animal producers to make dramatic investments in depopulation/ repopulation procedures to eliminate specific diseases from herds or flocks highlights the importance they attach to maintenance of a high level of animal health.

The importance of herd/flock health has driven the development of innovative management schemes that protect animal health. Notable among these in the pig industry are all-in/all-out animal flow (by room, building or site), segregated weaning, intense biosecurity procedures, careful attention to disinfection, and vaccination. There have been orchestrated industry programs for elimination of specific diseases from an industry (e.g., pseudorabies in pigs).

There have been efforts at the farm level to eliminate specific diseases from individual herds by the aforementioned depopulation/repopulation or by less aggressive means such as test and removal programs. All of these technologies are powerful, but collectively they still cannot guarantee freedom from disease for all animals. There remains a pressing need for additional measures.

Animal agriculture has made very effective use of antibiotics in maintaining animal health for half a century, but concerns about development of resistance to those antibiotics now compel the industry to minimize the use of these powerful tools, and that development only emphasizes the need for innovative approaches to disease control in livestock.

The industry now has available a rich supply of feed ingredients and feeding management technologies purported to improve the health and productive performance of animals, ingredients that may be considered functional foods for animals. Bio-Mos® (Alltech Inc.) is an important one. Examples of other such products that have been widely adopted include spray-dried animal plasma, acids, high levels of zinc oxide or copper sources, probiotics and enzymes. A wide range of others have been proposed. Many of these products are thought to act by altering the microbial populations in the digestive tract, with resulting benefits to the animal.

While these ingredients may change microbial populations in the digestive tract in important ways, it is likely that the substrate (nutrient) supply available to microbes in the several parts of the digestive tract is one of the most powerful factors affecting those populations. That substrate supply depends on the diet composition, with type and level of dietary fiber being especially important. The relationship of dietary fiber to digestive tract microbial populations and then to the animal’s ability to resist enteric infection is controversial, as reviewed below.


Distillers dried grains with solubles (DDGS)

The anticipated diversion of startling amounts of US corn to ethanol production and the associated availability of enormous quantities of DDGS for use in animal feeds is the most dramatic change now underway in US agriculture. Indeed, it may change the nature of US agriculture. We must find means to replace the corn starch that is diverted from animal feeds to ethanol and we must find ways to use the DDGS. We suggest that DDGS may be related to the need for innovative approaches to disease control in livestock.

There is a popular notion in the US swine industry that inclusion of DDGS in the diet helps to protect pigs against ileitis, an enteric disease caused by the intracellular pathogen Lawsonia intracellularis. A series of challenge experiments (Whitney et al., 2006a,b,c) failed to show such protection clearly, as described below. However, the notion persists, perhaps because of perceived benefits in practice. It appears likely that any protective effect of DDGS derives from its high fiber content, although effects of residual yeast from the fermentation cannot be discounted.

The persistence of the notion that DDGS protects against one enteric disease coupled with the controversy about the connection between dietary fiber and resistance to enteric infection invites a broader consideration of the impact of DDGS and other fibrous ingredients on enteric infections in animals.


Concepts of fiber effects on resistance to enteric disease

Dietary fiber consists mainly of non-starch polysaccharides (NSP), which are carbohydrates that are not digested by the enzymes produced by animals. Because they escape digestion in the upper digestive tract, they are available for fermentation by the microbes that inhabit the lower gut in large numbers to support their proliferation.

In very general terms, fiber can be divided into soluble and insoluble NSP. The microbes can ferment most soluble NSP rapidly, but ferment most insoluble NSP slowly if at all. DDGS contains a relatively high level of fiber, and the NSP are mostly insoluble.

At least three concepts of the relationship of dietary fiber to enteric disease have been proposed:

1. Fermentable (soluble) fiber is beneficial because it supports the proliferation of commensal (normal) bacteria, and these bacteria inhibit the growth of pathogens.

2. Fermentable (soluble) fiber is detrimental because it serves as a substrate for pathogens.

3. Nonfermentable (insoluble) fiber is beneficial because of a variety of physiological effects.

The controversy surrounding the relationship of dietary fiber and enteric disease was highlighted at the 10^th International Symposium on Digestive Physiology in Pigs, held last year in Vejle, Denmark. That symposium included a workshop on this topic. The lively discussion made it clear that many of the scientists participating assume that fiber is beneficial, but also that empirical support for that assumption is difficult to find.

In fact, Dr. K.E. Bach- Knudsen, who chaired the session, concluded with the observation that there have been many studies of various carbohydrates but there are no consistent responses except the prebiotic effect of the specific carbohydrate inulin, which encourages the growth of certain bacteria.

The lack of clarity on this issue is frustrating and expensive, because the relationship of dietary fiber to enteric disease is potentially valuable in maintenance of animal health.


CONCEPT 1: FERMENTABLE FIBER IS BENEFICIAL

The logic behind this concept is that fermentable fiber is an energy source for commensal bacteria living in the lower gut, that provision of more fiber supports growth of more commensal bacteria, and that the resulting large population of commensal bacteria inhibits the growth of pathogenic bacteria (Wenk, 2001).

There is considerable evidence that dietary fermentable fiber affects the microbial populations and activity in the digestive tract (e.g., Jensen and Jorgensen, 1994; Leser et al., 2000; Bikker et al., 2006), often reducing the number of coliforms. However, there is limited evidence that these effects on the microbiota are followed by protection from enteric diseases.

A complicating factor is that some fermentable fibers cause the contents of the digestive tract to become quite viscous (Hopwood et al., 2004; Dikeman et al., 2006), introducing a new series of problems.


CONCEPT 2: FERMENTABLE FIBER IS DETRIMENTAL

Of the three concepts, the one most firmly grounded in empirical data is the notion that fermentable fiber is detrimental. Several studies have shown that removing fermentable fiber from the diet provides protection against swine dysentery caused by Brachyspira hyodysenteriae (e.g., Siba et al., 1996; Pluske et al., 1998; note that the name of the organism has changed to Serpulina hyodysenteriae). Further studies have extended that observation to enteric disease caused by E. coli in young pigs (Hopwood et al., 2004; Montagne et al., 2004).


These experiments have shown a clear distinction between fermentable and nonfermentable fiber. Fermentable fiber was repeatedly detrimental, but these studies showed no harm ful effect of nonfermentable fiber on incidence or severity of enteric disease.


CONCEPT 3: NONFERMENTABLE FIBER IS BENEFICIAL

It has also been proposed (e.g., Whitney et al., 2006a,b,c) that the nonfermentable fiber found in DDGS may be beneficial. Recent interest in this issue in North America was heightened by suggestions from the industry that dietary DDGS helped to protect pigs against ileitis, a diarrheal disease caused by Lawsonia intracellularis.

The logic for the suggestion of benefits from nonfermentable fiber is based on several physiological effects that may impact microbial populations. First, it increases the secretion of saliva, gastric juice, pancreatic juice and bile, which contain bactericidal enzymes and antibacterial peptides. Second, it alters the secretory function of the epithelium, perhaps interfering with bacterial adhesion. Third, nonfermentable fiber (as opposed to fermentable fiber) reduces viscosity of the digesta and therefore provides a cleansing action. Fourth, it stimulates gut motility.

Finally, it increases the rate of enterocyte turnover, which may be particularly important in the case of Lawsonia, the intracellular pathogen that causes ileitis.

These concepts appear to have driven, at least partially, the use of barley (as a source of both fermentable and nonfermentable fiber) in diets for weanling pigs (Maribo, 2003; N. Kjeldsen, personal communication).

However, a series of Lawsonia challenge experiments (Whitney et al., 2006a,b,c) failed to show consistent benefits of DDGS. DDGS appeared to reduce the incidence and severity of intestinal lesions typical of ileitis in only one (Whitney et al., 2006b) of the three experiments, and there were no clear clinical benefits.

On the other hand, a large feeding trial (Cook et al., 2005) provides support for beneficial effects of DDGS. An experiment with 1,040 finishing pigs from 42 to 116 kg body weight (10 pens of 26 pigs/pen per treatment) showed that as the level of DDGS in the diet was increased from 0 to 10, 20 and 30%, the percent mortality of the pigs declined linearly (6.0, 2.8, 2.4, and 1.6%, respectively).

The notion that DDGS and barley help to keep pigs healthy persists in the industry.


Recent research at the University of Illinois

Our laboratory has engaged in studies related to effects of dietary fiber on resistance to enteric disease in pigs. Our approach was to compare the use of several cereals varying in fiber content as the base of the diet for weanling pigs. Conclusions about fiber must be drawn carefully because these cereals vary in characteristics other than fiber as well.

The cereals chosen were corn, barley (high in both soluble and insoluble fiber), oat groats (soluble fiber) and rice (very low fiber). We have completed experiments using an E. coli challenge in our disease containment chambers, plus a feeding trial on a commercial farm. We are currently measuring the impact of cereal choice on microbial ecology of the digestive tract. Key results to date are summarized in Table 1.


Table 1. Effects of dietary fiber sources on pigs affected by enteric disease: Summary.


¹Buckingham et al. (2006)
²Perez-Mendoza et al. (2006)



The treatment effects in these experiments were not completely consistent, but they favor the rice treatment, which is very low in fiber. That is consistent with reports from Australia (Hopwood et al., 2004; Montagne et al., 2004). However, some of our results also favor barley. We interpret these results to support the notion that the impact of cereal choice on resistance to enteric disease deserves more investigation, and by extension that fiber deserves more investigation.

References

Bikker, P., A. Dirkzwager, J. Fledderus, P. Trevisi, I. Le Huërou-Luron, J.P. Lallès and A.A. Awati. 2006. The effect of dietary protein and fermentable carbohydrates levels in newly weaned pigs on performance and intestinal characteristics. Proceedings from the 10th International Symposium on Digestive Physiology in Pigs, Vejle, Denmark.

Buckingham, J., F. Ji, P. Laski and J.E. Pettigrew. 2006. Impact of various dietary cereals on clinical response to E. coli. J. Anim. Sci. 84(Suppl. 1):43-44.

Cook, D., N. Paton and M. Gibson. 2005. Effect of dietary level of distillers dried grains with solubles (DDGS) on growth performance, mortality and carcass characteristics of grow-finish barrows and gilts. J. Anim. Sci. 83(Suppl. 1):335.

Dikeman, C.L., M.R. Murphy and G.C. Fahey, Jr. 2006. Dietary fibers affect viscosity of solutions and simulated human gastric and small intestinal digesta. J. Nutr. 136(4):913-919.

Hopwood, D.E., D.W. Pethick, J.R. Pluske and D.J. Hampson. 2004. Addition of pearl barley to a rice-based diet for newly weaned piglets increases the viscosity of the intestinal contents, reduces starch digestibility and exacerbates post-weaning colibacillosis. Br. J. Nutr. 92:419-427.

Jensen, B.B. and H. Jørgensen. 1994. Effect of dietary fiber on microbial activity and microbial gas production in various regions of the gastrointestinal tract of pigs. Appl. Environ. Microbiol. 60(6):897-1904.

Leser, T.D., R. H. Lindecrona, T.K. Jensen, B.B. Jensen and K. Møller. 2000. Changes in bacterial community structure in the colon of pigs fed different experimental diets and after infection with Brachyspira hyodysenteriae. Appl. Environ. Microbiol. 66(8):3290-3296.

Maribo, H.. 2003. Weaning pigs without antibiotic growth promoters: strategies to improve health and performance. In: Nutritional Biotechnology in the Feed and Food Industries, Proceedings of Alltech’s 19th Annual Symposium (T.P. Lyons and K.A. Jacques, eds). Nottingham University Press, UK, pp. 179-184.

Montagne, L., F.S. Cavaney, D.J. Hampson, J.P. Lallès and J.R. Pluske. 2004. Effect of diet composition on postweaning colibacillosis in piglets. J. Anim. Sci. 82:2364- 2374.

Perez-Mendoza, V.G., M.U. Steidinger, G.R. Hollis and J.E. Pettigrew. 2006. Growth performance of nursery pigs fed different cereal grains on a commercial farm. J. Anim. Sci. 84(Suppl. 1):44-45.

Pluske, J.R., Z. Durmic, D.W. Pethick, B.P. Mullan and D.J. Hampson. 1998. Confirmation of the role of rapidly fermentable carbohydrates in the expression of swine dysentery in pigs after experimental infection. J. Nutr. 128(10):1737-1744.

Siba, P.M., D.W. Pethick and D.J. Hampson. 1996. Pigs experimentally infected with Serpulina hyodysenteriae can be protected from developing swine dysentery by feeding them a highly digestible diet. Epidemiol. Infect. 116:207-216.

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Whitney, M.H., G.C. Shurson and R.C. Guedes. 2006a. Effect of dietary inclusion of distillers dried grains with solubles on the ability of growing pigs to resist a Lawsonia intracellularis challenge. J. Anim. Sci. 84:1860-1869.

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Whitney, M.H., G.C. Shurson and R.C. Guedes. 2006c. Effect of dietary inclusion of distillers dried grains with solubles, soybean hulls, or a polyclonal antibody product on the ability of growing pigs to resist a Lawsonia intracellularis challenge. J. Anim. Sci. 84:1880-1889.