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October 14, 2020
Although common coproducts such as dried distillers grain with solubles (DDGS), wheat middlings, sugar beet pulp and soybean hulls are economically priced, the concentration of dietary fiber (DF) in these coproducts limits the ability of pigs to use energy and nutrients, thereby reducing caloric efficiency.
More recently, and because of this functional characteristic, feeding high-fiber diets has been used as a strategy to slow the growth of pigs to avoid oversupplying U.S. pork processing plants due to the COVID-19 pandemic.
As a result of the many diverse properties of DF, it has become a popular topic among scientists, nutritionists and pork producers.
Because our current knowledge on fiber classification, functionalities and sources is limited, our ability to predict the impacts of feeding fibrous coproducts on growth, physiological responses and intestinal function of pigs is still in its infancy.
Because chemical structures and functions of fibers are not identical, the term DF is used to describe the total content of carbohydrates in a feed ingredient that is indigestible in the small intestine. Based on the chemical structure of plant carbohydrates, DF is the sum of nonstarch polysaccharides plus lignin (Choct, 2015).
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Therefore, total dietary fiber, which is the sum of soluble and insoluble fiber, is the most suitable analytical assay that fits the functional definition compared with other common measurements such as crude fiber and neutral detergent fiber.
Traditionally, the fiber concentration obtained from chemical analysis has been monitored when formulating swine diets because of the inverse relationship between fiber content and nutrient digestibility in pigs (Moeser and Van Kempen, 2002).
However, these fiber measurements do not provide sufficient information on physiological effects of DF that may be used to improve the accuracy of estimating effects of fiber intake on energy digestibility, satiety and intestinal function and health status.
Saqui-Salces et al. (2017) and Vila et al. (2018) reported that pigs fed similar amounts of DF from different fiber sources exhibited different physiological responses, such as changes in intestinal nutrient sensors and transporters, mucin expression and immune responses.
These results suggest that determining the chemical composition of DF is insufficient for understanding its effects on physiological responses.
Indeed, fiber structure and physical-chemical properties impact physiological responses and nutrient metabolism that play a significant role in production performance (Guillon and Champ, 2000).
Among physical-chemical properties of DF, viscosity has a strong effect on digestive physiology.
Effects include but are not limited to the flow behavior of digesta (e.g., mean retention time; Schop et al., 2020); influence of digestibility and availability of nutrient and energy (Hooda et al., 2011); the capacity of mucin secretion (Piel et al., 2005); and modulation on hindgut fermentability and microbiome profile (Dikeman and Fahey, 2006; Capuano, 2017).
Additionally, viscosity is likely to influence intestinal health status through its effects on digesta retention time, nutrient digestibility and fermentation kinetic, thereby affecting microbial fermentation of undigested dietary components.
Therefore, the amount of DF and physical-chemical properties of DF contribute to various perspectives on the value of feeding fibrous coproducts.
However, our understanding of whether DF quantity or viscosity plays a greater role in affecting nutrient use, and whether these factors interact to affect intestinal function in growing pigs, needs to improve.
With this premise in mind, our hypothesis was that increased viscosity in high-fiber diets fed to pigs could cause a greater negative effect on nutrient digestibility when combined with other types of fiber.
In order to assess the exclusive role of viscosity on nutrient use and digestive physiology, carboxymethyl cellulose (CMC), a viscous, nonfermentable polysaccharide, was used since CMC has long been used as a viscosity modifier in food applications.
To evaluate the effect of DF quantity, we used DDGS, as it is a nutrient-dense source of fiber commonly used in swine diets in North America and globally.
Our Integrated Animal System Biology Team in the University of Minnesota conducted an experiment to test whether the quantity of DF that interacts with viscosity affected nutrient digestibility and intestinal physiology in growing pigs (Table 1).
Barrows were surgically equipped with a T-cannula about 4 inches before the ileocecal valve to collect digesta for determining digestibility. After a recovery period, 36 barrows were allotted to six blocks of six pigs with similar initial body weight (BW). Pigs (n = 6/treatment; BW = 26.5 ± 3.9 kg) within each block were fed either corn-soybean meal (CSBM) or CSBM plus 30% DDGS basal diets with three levels of viscosity (low, medium and high) using cellulose, medium-viscous CMC and high-viscous CMC, respectively, for 29 days.
All six diets were formulated to meet nutrient requirements for growing pigs, containing the same amount of metabolizable energy at 3,300 kcal/kg diet. On days 27 and 28, ileal digesta were collected to calculate apparent ileal digestibility (AID).
In addition, pigs were euthanized on Day 29 to measure activity of digestive enzymes, and changes in intestinal morphology and gene expression of nutrient transporters. Here, only AID and growth performance will be presented and discussed.
Results from the study (Hung et al., unpublished) showed that increasing viscosity by adding CMC significantly increased (Table 1) viscosity of whole digesta and digesta supernatant liquid in the ileum, compared with low-viscosity treatment.
In contrast, increasing fiber quantity by adding DDGS to the diet had no impact on viscosity of whole digesta and digesta supernatant.
Our observations are similar to those from other studies that showed inclusion of viscous ingredients in the diet increases digesta viscosity. However, a novel observation in this study was that the inclusion of DDGS fiber had no impact on viscosity of whole digesta and digesta supernatant.
As digesta is a mixture that consists of solid particles and fluids that have differing flow behavior in the lumen, presenting viscosity of whole digesta and digesta supernatant is representative for the physiological state.
A second important observation of this experiment was that increased diet viscosity and quantity of fiber decreased nutrient digestibility in an independent manner (Figure 1).
The increased fiber quantity provided by adding DDGS to the diet reduced AID of DM by 13% and AID of crude protein (CP) by 4% compared with feeding the CSBM diets, indicating fiber content was the main cause of reduced nutrient use.
Furthermore, increasing viscosity by adding CMC significantly decreased AID of DM, ash, EE and CP compared with the low-viscosity treatment, indicating that viscosity has an adverse effect for energy, amino acid and mineral utilization. Interestingly, fiber quantity did not interact with viscosity to cause greater reduction on digestibility.
The current digestibility data were consistent with growth performance responses of pigs fed viscous diets, where the medium-viscosity and high-viscosity treatments significantly decreased average daily gain (ADG) compared with low-viscosity treatment.
This led to a decrease in final BW by 14% and 9%, respectively, compared with the low-viscosity treatment (Table 2).
Because these pigs were fed the same amount of feed with similar nutrient densities, the reduction of growth performance under the current experimental condition is likely due to decreased nutrient availability.
Digesta viscosity matters
The ultimate goal in precision feeding programs is to avoid overfeeding and underfeeding energy and nutrients during each stage of growth or reproduction. Therefore, if the digestibility value is overestimated, the amount of energy and nutrients will be insufficient to meet the requirements, and suboptimal performance will occur.
The reasons of observing suboptimal growth of pigs fed high-fiber diets is likely related to overestimated nutrient availability in diets containing viscous ingredients. To adjust better for the nutrient density of feeding fibrous diets, viscosity should be taken into consideration.
Hence, common chemical analysis for determining fiber quantity is not adequate for predicting nutrient utilization when feeding various high fiber coproducts.
The techniques for determining fiber quantity and viscosity are available, but nutritionists have previously not considered measuring and using viscosity in feed formulation.
Dusel et al. (1997) reported the extract viscosity of wheat is correlated with the viscosity of intestinal contents, suggesting that the measurement of diet viscosity could be used in commercial practice.
Viscometers and rheometers can measure viscosity, but each instrument has advantages and disadvantages (Dikeman and Fahey, 2006). To avoid misinterpretations on viscosity data among different studies, establishing a standardized method for viscosity measurement will be imperative.
Additionally, further studies, such as viscosity titration trials, are needed to expand on the findings of the magnitudes of viscosity's effect on nutrient use.
Gut health impacts
Several review papers suggest that functional properties of DF are associated with intestinal health in young pigs (Molist et al., 2014; Agyekum and Nyachoti, 2017; Jha et al., 2019).
It does this because DF increases the production of volatile fatty acids in the large intestine, and volatile fatty acids provide many useful functions such as growth of beneficial microbes, intestinal barrier integrity and immune responses.
Furthermore, hindgut fermentation in monogastric animals generates butyrate as an energy source for colonocytes though β-oxidation, which will use oxygen and maintain a hypoxia environment that is unfavorable for facultative anaerobic pathogens, such as E. coli and salmonella (Jha et al., 2019).
Byproducts with a high content of soluble DF have greater fermentability and cause greater production of volatile fatty acids than byproducts with a high content of insoluble DF.
On the other hand, some sources of insoluble DF are proposed to have beneficial effects against pathogen colonization, or the impact of the pathogen on macroscopic and microscopic lesions.
For example, feeding 10% DDGS decreased intestinal lesions in the ileum and colon of pigs experimentally inoculated with Lawsonia intracellularis (Whitney et al., 2006).
We speculate that this effect is due to the fact that insoluble DF in DDGS does not induce changes in viscosity in the ileal digesta, thereby decreasing digesta retention time and limiting the time for pathogen proliferation in the intestine (Kim et al., 2012).
A positive linear relationship between soluble DF intake and digesta viscosity has been observed in pigs (Figure 2) (Hopwood et al., 2004), and excess viscosity is potentially harmful for gut homeostasis.
Viscosity-induced decrease in nutrient digestibility increases nutrient fermentation by microbes in the large intestine. Although protein fermentation can produce volatile fatty acids, toxic metabolites are also generated, such as ammonia and biogenic amines that are detrimental to intestinal homeostasis and may increase the incidence of diarrhea (Jha and Berrocoso, 2016).
Furthermore, a variety of metabolites from microbial fermentation might lead to inflammation, increased intestinal permeability (leaky gut), and dysbiosis. In fact, the association between digesta viscosity and increased E. coli colonization in pigs fed soluble DF has been shown in previous studies.
Compared with a diet based on cooked rice, pigs fed 50% viscous pearl barley diets raised digesta viscosity and aggravated the magnitude of colibacillosis induced by orally challenged with enterotoxigenic hemolytic E. coli (ETEC) in postweaning pigs (Hopwood et al., 2004).
Kim et al. (2012) suggested that 15 to 45 g/kg of soluble dietary nonstarch polysaccharides (NSP) may stimulate colonization of ETEC in the small intestine.
A summary of several studies has shown that dietary NSP inclusion, including viscous, nonfermentable fiber, exhibits a positive relationship with the count of ETEC in the small intestine (Figure 3) (Hopwood et al., 2006).
Moreover, increasing digesta viscosity by adding low-viscous and high-viscous CMC was associated with increased shedding of ETEC and incidence of diarrhea in nursery pigs (McDonald et al., 2001), suggesting viscosity per se may affect gut health.
These results suggested excess viscosity induced by soluble DF might be detrimental to intestinal health status, especially in young pigs.
Therefore, coproducts containing a significant amount of viscous, soluble DF should be used judiciously in swine diets to preserve healthy hindgut fermentation.
Additionally, the inclusion of moderate amounts of insoluble or slowly fermentable fiber might benefit gut health in terms of maintaining intestinal homeostasis, reducing retention time, and limiting proliferation of pathogens (Figure 3).
In the near future, measuring viscosity can be a useful tool to adjust nutrient density in diet formulation for pigs, especially in feeding diets containing fibrous coproducts.
Thus, knowing fiber quantity and viscosity are critical for optimizing fiber utilization and maintaining expected growth performance and gut health of pigs fed agro-industrial byproducts and coproducts.
Hung and Zhu are research assistants, Shurson is a professor in swine nutrition, Saqui-Salces is an assistant professor in gastrointestinal physiology and Urriola is a research associate professor in Veterinary Population Medicine, all with the University of Minnesota Department of Animal Science.
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