Gastrointestinal infections with pathogenic bacteria y the subsequent clinical expression of disease occur frequently in young animals under current intensive production systems. Infections are responsible growth rates and consequently cause economic losses in animal production. Antibiotics modify the microflora of the gastrointestinal tract (GIT) and are the main available tool to prevent and treat digestive illness. The inclusion of antibiotics at low levels intro the feed for an extended period of time was a common practice in the poultry industry to control digestive disorders and proved to provide economic benefits to the broiler industry (Castanon, 2007). However, the indiscriminate use of in-feed growth promoters of antibiotic origin may result in selection for the survival o resistant bacterial species or strains. In addition, genes encoding for resistance to antibiotics also can be transferred to formally susceptible bacteria, posing a threat to both animal and human health. Consequently, the European Union (EU-27) banned the marketing of antibiotics as in-feed growth promoters. On the other hand, the use of animal proteins such as meat and bone meal are also banned in poultry feeds. Moreover, the use of fish meal and other animal protein sources is reduced to minimum because of cost and further legislative restriction. Consequently, the feeds currently produced by the European integrated poultry Industry are based exclusively on vegetable feedstuffs without any growth promoter of antibiotic origin. Under these circumstances, necrotic enteritis and related problems are frequently reported under field conditions. Therefore, producers are forced to introduce modifications in the diets to reduce the incidence of enteric diseases (Mateos et al., 2002). The manipulation of the ingredient composition and nutrient content of the diet together with changes in feed manufacture, technology together with management practices in the field, may improve health status of the GIT. Feeding highly digestible ingredients, enzyme supplementation, heat processing of the cereal and inclusion of moderate amounts of fiber in the diet have been some of the alternatives proposed to improve nutrient digestibility and growth performance in the absence of growth promoters (Mateos et al., 2002; González-Alvarado et al., 2007, 2008). Dietary fiber (DF) is a component of the diet that affects the development of the GIT and may modify the characteristics of the intestinal contents that promote the balanced growth of the native microbiota (Montagne et al., 2003; Mateos et al., 2012).
2. Dietary Fiber in Poultry
Tradicionally, DF has been considered an anti-nutritional factor and a diluent in non-ruminant diets. Also, many nutritionists have considered that the requirements of broiler for crude fiber (CF) are low and recommended to reduce its content in diets for broiler chick to less than 3.0-4.0%, depending on the age (Swennen et al., 2010). Janssen and Carré (1985) indicated that fibrous components of the food had negative effects on growth performance of the broiler chicks. In fact, these authors reported a strong negative correlation between CF of the diet and protein and ether extract digestibility. Also, Sklan et al. (2003) observed that increasing the CF content of the diet from 3 to 9% reduced growth performance and impaired nutrient retention in turkeys. However, in last years, the influence of CF content in the poultry diet on voluntary feed intake and digestibility of nutrients is subject to debate. Recent studies have defined in detail the beneficial effects of the fiber on growth performance and its influence on 1) the satiety and animal welfare, 2) gut health including non-specific colitis and other enteric disturbances, 3) changes in the intestinal microflora and 4) gizzard activity and motility of the TGI. Consequently, fiber fraction is not considered as anti-nutritional component o the diet. In fact, it has proposed that the inclusion of moderate amount of fiber in diets for broilers may have positive effects on gizzard activity improving the mixing of the digesta and motility of the GIT, gut health preventing the adhesion of certain pathogen bacterial population to the epithelial mucosa, and growth performance of non-ruminant animals (Mateos et al., 2002; Montagne et al., 2003; Mateos et al., 2012). Under practical conditions, the response of these variables to the incorporation of fiber in the diet depends on a great extent on the nutritional technologies and management techniques used, including type of housing (cage vs. floor pens), composition and physical structure of the basal diet (i.e. type of cereal), type and level of inclusion of fiber, feed form (mash vs. pellet or crumbles), health status (i.e. conditions of hygiene and incidence of diseases and digestive disorders), and age of the bird.
The controversy of the effects of the fiber on the broiler productivity might be because of the term of “dietary fiber” that is not clearly defined. Originally the main method used for analysis of fiber in feedstuffs was the CF, a method that is still widely accepted by the feed industry. Other methods provided are neutral detergent fiber, acid detergent fiber and lignin. All these analytical methods are more satisfactory alternative for defining and characterizing the fiber content of the ingredients. The term “dietary fiber” is, in most recent animal nutrition, defined as “edible parts of plants or analogous carbohydrates that are resistant to digestion and absorption in the human small intestine, with complete or partial fermentation in the large intestine” (AACC, 2001). Dietary fiber is predominantly found in plant cell walls and includes polysaccharides (resistant starch and soluble and insoluble nonstarch polysaccharides), oligosaccharides, lignin, and associated plant substances.
It is common to characterize DF based on its solubility in water. The soluble fiber corresponds to water extractable polysaccharides that precipitate in alcohol or acetone solutions, and includes among others β-glucans from barley and oats, arabinoxylans from wheat and rye, pectins from fruits and beet pulp and galactomanans from legumes. In contrast, insoluble fiber is composed of cellulose and hemicelluloses, and certain amounts of pectin substances, protein bound to the fiber and lignin. Dietary fiber exhibits a range of physical properties that act in concert with the chemical properties to determine the physiological effects in animals. Differences in structure, solubility, water holding capacity, viscosity, bulk and other physicochemical properties of fibrous ingredients may affect in different ways the structure of the digesta and passage rate through GIT (Fahey et al., 1992). Consequently, feed intake, development and epithelial morphology of the GIT, GIT motility, digestive juices secretion and nutrient digestion and absorption may vary depending on the source of fiber (Montagne et al., 2003; Svihus, 2011; Mateos et al., 2012). On the other hand, chemical composition and fermentative capability as well as the grade of lignification of the source of fiber may affect growth and distribution of the species and the total population of the resident microflora in the GIT.
3. Dietary Fiber, Passage Rate and Development of the Gastrointestinal Tract
The effects of fiber inclusion on the transit time of the digesta and the development of the digestive organs vary depending on the physicochemical properties and level of fiber added (Bach Knudsen, 2001). In this respect, insoluble fibers such as that contained in oat hulls reduces length of the small intestine (González-Alvarado et al., 2007), stimulates gizzard activity and increases its contents (Jiménez-Moreno et al., 2009a; Hetland and Svihus, 2001) and decreases intestinal transit time which might indicate an improvement of the functioning of the GIT. A faster passage rate by feeding insoluble fiber may be related with the lack of physical structure such as microcrystalline cellulose (Cao et al., 1998) or fine grinding of the fiber (Hetland and Svihus, 2001). Coarse fiber particles are retained for a longer time in the gizzard than fine fiber particles. An accumulation of coarse fiber particles stimulates grinding activity of the gizzard, allowing for a better regulation of feed flow to the intestines and higher secretion of digestive juices.
Chicks adapt to fiber-rich diets by increasing the volume and weight of their digestive tract (Håkansson et al., 1978, González-Alvarado et al., 2008). The effect of the fiber on gutfill depends on type and level of inclusion of fiber and the segment of the GIT considered. An increase in the dietary fiber intake increases the amount of gutfill causing a physical distension of the walls of the digestive tract and a concomitant increase in size and gut capacity (Jørgensen et al., 1996; Jiménez-Moreno et al., 2009a, 2013a,b). An increase in size of the digestive organs might be indicative of a hypertrophy of gut tissues (Jørgensen et al., 1996). A hypertrophy of visceral organs such as the GIT makes precise higher energy expenditure than those associated to carcass yield (Anugwa et al., 1989). Also, the lack of fiber in the diet may cause a dilation and poor development of the walls of the proventriculus and gizzard (Svihus et al., 2011) that might affect theirs functionality. Damaged proventriculi are enlarged, swollen and filled with fluid and feed and often rupture during routine evisceration causing contamination of the carcass and important economic losses (Huff et al., 2001). On the hand, the inclusion of structural DF increases the size and holding capacity of the gizzard (Svihus, 2011; Jiménez-Moreno et al., 2013b). The gizzard is responsible for a complete grinding of feed and a well regulated feed flow as well as whole GIT motility. Duke (1992), Hetland et al. (2003) and Sacranie et al. (2012) have indicated that atrophy of the gizzard reduces the reflux of chyme from the intestines, impairing the digestive processes and reducing performance. In contrast, welldeveloped proventriculi and gizzards increase HCl secretion and intestinal refluxes that serve to reexpose the digesta to pepsin, facilitating the mixing of the feed with endogenous enzymes.
The magnitude of effects of the inclusion of the fiber on physiology and development of the digestive organs depends not only on the nature and particle size of the fiber source (Jiménez-Moreno et al., 2010) but the level of fiber (Jiménez-Moreno et al., 2011a; 2013b). Jiménez-Moreno et al (2013b) reported that the effects of fiber inclusion on the enlargement of GIT were more evident with sugar beet pulp than with oat hulls, a finding that could be related to the higher pectin content of sugar beet pulp. Soluble fiber particles such as those from sugar beet pulp, retain high amounts of water and swell when pass through GIT, increasing the bulk of the digesta and causing physical distension of the walls of the digestive tract and a concomitant increase in size. Jiménez-Moreno et al. (2009a) observed that chyme with a high pectin content may produce greater dilatation of the proventriculus increasing in size and its contents. The coarse fiber particles are selectively retained in the gizzard that ensures a complete grinding and a well-regulated feed flow and secretion of digestive juices. Jiménez-Moreno et al. (2010) reported that the inclusion of 3% of sugar beet pulp or oat hulls but not microcrystalline cellulose, increased gizzard weight in broilers fed similar type of diets. Cellulose inclusion resulted in similar relative size and digesta content of the gizzard than those of the control diet. Cellulose is a highly insoluble fiber source with a very a low particle size, water holding capacity, and swelling water capacity. Because of its lack of physical structure, cellulose particles did not accumulate and stimulate gizzard functioning. Consequently, cellulose inclusion did not produce any increase in size of digestive organs or to reduce gizzard pH. Oat hulls have high lignin content and therefore, oat hulls containing diets are more resistant to grinding than sugar beet pulp. Consequently, oat hulls particles could be retained for a longer time in agreement with the higher dry matter contents observed in the gizzard. An accumulation of oat hull particles stimulates the grinding activity of the gizzard, allowing for a better development of the muscular layers and causing an increase in organ size (González-Alvarado et al., 2008). Pectins from sugar beet pulp by its high solubility, water holding and swelling capacities, increased the bulk of the digesta which in turn might produce a physical dilation of the proventriculus walls and a concomitant increase in organ size. In addition, as swollen sugar beet pulp particles increased in size, they were retained for longer in the gizzard. Consequently, gizzard digesta content and size were increased and gizzard pH reduced in birds fed the sugar beet pulp diet. In a latter study, Jiménez-Moreno et al. (2011a) reported in 36 dold broilers reared in floor pens that the inclusion of 5% of oat hulls or sugar beet pulp increased the gizzard weight and its contents and reduced gizzard pH (Table 1). Also, these authors reported that the neutral and acid detergent fiber and lignin contents (based on dry matter) of the gizzard were higher in oat hulls containing- than in sugar beet pulp containing diets indicating that oat hulls particles were retained for a longer time that sugar beet pulp particles which in turn might lead to an increase in hydrochloric secretions from the proventriculus. Jiménez-Moreno et al. (2011b) reported an increased gizzard weight when pea hulls were increased up to 7.5% to a low fiber diet. However, gizzard pH was reduced with the inclusion of 2.5% of pea hulls but no further changes were observed with further pea hulls increases (Figure 1.a) in consistent with higher dry matter contents in this organ (Figure 1.b).
Grinding of fibrous ingredients might modify the native structure of the fiber and in consequence, the physicochemical properties of the digesta, the passage rate and development of GIT (Amerah et al., 2007; Jiménez-Moreno et al., 2010). Coarsely ground oat hulls increase feed passage as compared to finely ground oat hulls (Hetland and Svihus, 2001). Stimulating effect of coarse insoluble on gizzard function, in particular more frequent and powerful contractions and the subsequent intraluminal pressure changes that they induce, leads to an increase in the occurrence of gastric refluxes (Hetland et al., 2003; Sacranie et al., 2012) improving nutrient digestibility. In contrast, fine ground fiber may impair gizzard function, reducing nutrient digestibility. In this respect, Jiménez-Moreno et al. (2010) studied the effects of type and particle size of dietary fiber on digestive traits and growth performance of broilers from 1 to 21 d of age. The control diet contained 3% sepiolite and had 1.54% CF. The other diets substituted (wt/wt) the sepiolite of the control diet by microcrystalline cellulose or by oat hulls or sugar beet pulp ground through a 0.5 or 2.0-mm screen. These authors observed that broiler fed fine oat hulls diet exhibited similar gizzard weight and pH suggesting that fine oat hulls particles were retained and partly induced the same response in agreement with findings of Sacranie et al. (2012). Contrary, broilers fed fine sugar beet pulp diet had lighter gizzards but higher contents indicating that grinding of sugar beet pulp resulted in a loss of mechanical abrasion of the gizzard walls. When these two fiber sources were finely ground, the sugar beet pulp lost its physical structure where the oat hulls maintained it.
The grade of lignification and elasticity y/or resistance to grinding of insoluble fiber sources might affect also, digestive characteristics and growth performance of broilers. Jiménez-Moreno et al. (unpublished data; Table 2) reported that diluting a control diet with increases of oat hulls, sunflower hulls or rice hulls (0 to 5%) increased gizzard weight and reduced gizzard pH; effects that were more evident for oat hulls than for rice hulls being sunflower hulls in intermediate position. Oat hulls particles are fusiform, more elastic and resistant to grinding whereas rice hulls and sunflower hulls particles are rectangular, more stiffness, and poorly resistant to breakage by pressure in aqueous medium. Therefore, it is expected that oat hulls particles will be retained in the gizzard for a longer time resulting in a higher mechanical abrasion of the gizzard walls and organ size. Contrary, rice hulls have high silica contents that caused an erosion of the Koilin layer of the gizzard when broilers ate high amounts of these hulls for a long term.
Pelleting reduces feed particle size and modifies the structure of the feed that affect digestive characteristics and growth performance of broilers. Pelleting may modify the functional properties (viscosity, binding, resistance) of the fiber fraction (Thomas et al., 1998) and in consequence, the response of broilers to fiber inclusion. In this respect, Jiménez-Moreno et al. (unpublished data) indicated that diluting broiler diets with increases of level of inclusion of insoluble fiber (0 to 5%) increased gizzard weight; an effect that was more evident in mash than in pelleted diets and in oat hulls containing- than in sunflower or rice hulls containing diets (Figure 2). Probably, the structure and functional properties of insoluble fiber may be altered after pelleting.
Changes in pH of the GIT, especially in the upper part may favors enzymatic activity and prevent the pathogen growth in the distal part of the GIT. Digesta pH of the GIT is related with the digesta content retained in the organ. A reduced proventriculus pH has been observed when a soluble fiber such as sugar beet pulp has been included in the diet (Jiménez-Moreno et al., 2009b,c, Jiménez-Moreno et al., 2013b). The proventriculus is characterized by having very distensible walls, fast rate of feed passage and limited storage capacity (Moran, 1982). Sugar beet pulp particles swell to retain water, which could increase its capacity favouring the passage of the feed from the proventriculus to the gizzard. The inclusion of structural fiber reduces gizzard pH that could be associated with the increased digesta contents (Jiménez-Moreno et al., 2009b,c, Sacranie et al., 2012, Jiménez-Moreno et al., 2013b). The reduction of gizzard pH by the inclusion of fiber probably results from higher HCl secretion from proventriculus, a consequence of the longer retention time of the digesta in the gizzard. Very little scientific literature exists that examines the effects of increasing the fiber content of the diet on intestinal digesta in birds. Jiménez-Moreno et al. (2009c) evaluated the changes of pH through GIT when 3% coarse oat hulls or sugar beet pulp or microcrystalline cellulose were added to a low fiber diet for broilers. These authors observed that the inclusion of fiber did not affect pH of the duodenum in contrast to the findings in the upper part of the GIT. Differences in pH observed among fiber sources in the upper part disappeared in this segment, suggesting that bile salts secretion was higher in chicks fed the oat hulls and sugar beet pulp diets than in chicks fed the cellulose and the control diets without fiber added (Figure 3). Digesta pH decreased from the duodenum to the ileum, a reduction that it was more pronounced with the cellulose than with the sugar beet pulp diet. However, in the ceca, the pH was reduced by sugar beet pulp probably because of the fiber of sugar beet pulp may be fermented by the resident anaerobic microflora of the ceca.
The effect of fiber on epithelial morphology and cell turnover is variable and depends on the physicochemical characteristics of the DF, their level of inclusion, the duration of ingestion, age, and the site in the intestinal tract (van der Klis and A. van Voorst, 1993; Iji et al., 2001). Villus height to crypt depth ratio is a useful criterion for estimating the absorptive capacity of the small intestine (Montagne et al., 2003). A high villus height to crypt depth ratio is indicative of better function and maturity of the intestinal mucosa. Jiménez-Moreno et al. (2011a) reported the highest villus height to crypt depth ratio was observed with dietary pea hulls of 2.5% and that an increase to 7.5% of pea hulls impaired it. In a second study of these same authors (Jiménez-Moreno et al., 2013b) observed that diluting a control diet with increases of sugar beet pulp but not of oat hulls (0 to 7.5%) reduced villus height and crypth depth and tended to reduce villus height to crypt depth ratio of 12 d-old broilers (Table 3). Sarikhan et al. (2010) and Rezaei et al. (2011) observed that the inclusion of 0.25 to 0.75% of a micronized insoluble fiber constituted mostly by cellulose, increased villus height to crypt depth ratio in the ileum of 42 d-old broilers. An excess of DF, as reported by Jiménez-Moreno et al. (2011a, 2013b) when 7.5% of pea hulls or sugar beet pulp, were added to the diet, could have increased the abrasion of the mucosal surface of the small intestine shorting the villus and increasing mucus output. As a result, it reduced the absorptive villus surface and hindered nutrient retention.
4. Dietary fiber and digestive process
Tradicionally, fiber represents the indigestible component in poultry diets because do not digest cellulose. Janssen and Carré (1985) reported a strong negative correlation between CF content of the diet and protein and fat digestibility in broilers and concluded that low CF diets improve poultry performance. However, recent studies indicate that the inclusion of moderate amount of fiber might benefit digestive physiology (González-Alvarado et al., 2008; Jiménez-Moreno et al., 2011a, 2013a). In fact, Hetland et al. (2003) reported that the inclusion of 10% insoluble fiber in the diet increased the ileal digestibility of starch and stimulate gizzard activity. Recently, González-Alvarado et al. (2007) demonstrated that the inclusion of 3% of oat hulls or soy hulls improved nutrient digestibility and AMEn at 18 d of age; an effect that was more evident in diets based on rice than in those based on corn. Diets rich in structural fiber remain in the upper GIT longer and might be digested more completely because of increased gastrointestinal refluxes (Sacranie et al., 2012) and hydrochloric acid secretion (Jiménez-Moreno et al., 2010) and other digestive enzymes. Hetland et al. (2003) observed that the inclusion of oat hulls increased amylase activity and bile salt concentration in the chyme of broilers improving ileal starch digestibility (Table 4). The inclusion of structural fiber such as oat hulls, in the diet prolongs the exposure time of food to both the mechanical and chemical components of digestion and reduces the time available for microbial fermentation in the small intestine.
Differences in the physicochemical properties of fibrous ingredients such as solubility, water holding capacity, viscosity, bulk, fermentability and ability to bind bile acids, might affect in different ways the development of the GIT and the digestibility of nutrients in non-ruminants animals (Montagne et al., 2003). Coarse feed particles, such as oat hulls, retain longer in the upper part of the GIT stimulating the gizzard activity and increasing hydrochloric acid secretion. A low gizzard pH improves pepsin activity and nitrogen retention, and increases the solubility of the inorganic fraction of the feed (Guinotte et al., 1995) which in turn might favor its absorption. Hetland and Svihus (2001) found that apparent ileal digestibility of starch increased when oat hulls were included in the diet but that those of nitrogen, fat, and ash were not modified. Jiménez-Moreno et al. (2009b) reported that the inclusion of a moderate amount (3%) of sugar beet pulp to low fiber diet impaired the ileal digestibility of dry matter, organic matter, protein, and energy as well as AMEn as compared with the inclusion of 3% of oat hulls (Table 5). Sugar beet pulp has high content in pectin, and its particles have high water holding and swelling capacities that might be retained for longer in the GIT. An increase in chyme accumulation in the GIT with sugar beet pulp inclusion might result from an increase of the digesta viscosity (Sandhu et al., 1987). As a result, the accumulation of viscous material in the GIT might interfere with the diffusion of nutrients through the mucosal surface slowing down nutrient absorption (Forman and Schneeman, 1980). In addition, soluble fiber sources may increase the thickness of the unstirred water layers of the mucosa reducing nutrient dispersion and impairing absorption (Johnson and Gee, 1981).
The magnitude of the response of poultry to the inclusion of fiber in the diet might vary not only with the type of fiber but with the level of inclusion. Jiménez-Moreno et al. (2011b) reported that ileal crude protein and starch digestibility increased with increasing level of pea hulls, showing maximum values with pea hulls level between 2.5 and 5% (Table 6). Also, in a recent study, Jiménez-Moreno et al. (2013a) observed that diluting a control diet with increases of oat hulls in the diet but not of sugar beet pulp (0 to 7.5%), improved the ileal crude protein digestibility and starch. Similar results were observed by Pettersson and Razdan (1993) who found that the inclusion of 9.2% in the diet had no effect on crude protein digestibility. Rogel et al. (1987) reported in broilers that starch digestibility of raw potato increased as the level of oat hulls in the diet increased from 0 to 12%. Similarly, Amerah et al. (2009) observed a 9% increase in starch digestibility when the diet was diluted with 6% wood shavings but not when diluted with the same amount of microcrystalline cellulose. Jiménez-Moreno et al. (unpublished data) observed increases in AMEn of diets as the level of inclusion of oat hulls or sunflower hulls but not of rice hulls, increased from 2.5 to 5% in the diet. High DF diets might increase mucus output resulting in an increase in the ileal flow of nitrogen. Also, high DF diets enhance abrasion in the small intestine of birds increasing endogenous cell losses to the lumen. As a result, ileal digestibility of crude protein may be reduced.
Bile acid secretion might be the limiting step in fat digestion in young chicks and DF might increase bile acids secretion and facilitate the emulsification of the released dietary lipids. In fact, Hetland et al. (2003) reported that diluting by 10% a control diet with oat hulls increased the amount of bile acids present in the small intestine of broilers. An increase in bile acid concentration in the gizzard of birds suggests stronger gastroduodenal refluxes which might help to improve nutrient utilization. Jiménez- Moreno et al. (2009b) reported that the inclusion of 3% of oat hulls or sugar beet pulp in the diet increased ether extract digestibility in 21-d-old broilers, an improvement that was more evident with yellow grease, a saturated fat source, than with soy oil, a more unsaturated fat source. An increase in bile salts production with DF might improve more the digestibility of saturated supplemental fats because in young chicks saturated fats relies more on biliary salts presence for emulsion and micelle formation.
5. Dietary Fiber, Feed Intake and Growth Performance
Diets high in fiber usually contain a low energy density that may decrease feed intake and feed conversion ratio in broilers. However, different authors demonstrated that the inclusion of moderate amounts of insoluble DF does not affect voluntary feed intake in broilers (Jiménez-Moreno et al., 2010; Sacranie et al., 2012). In fact, González-Alvarado et al. (2007) studied the effects of the inclusion of 3% oat hulls or soy hull into a control diet based on corn that contained 2.5% CF or a control diet based on rice that contained 1.5% CF. From 1 to 4 d of age, the inclusion of hulls reduced feed intake but not had effect on body weight gain (BWG) indicating broilers fed the hull-containing diets wasted more feed that those fed the control diet. In the period from 1 to 21 d, the feed intake and BWG were increased and feed conversion ratio (FCR) improved by the inclusion of both fiber sources. Jiménez-Moreno et al. (2011a) studied the effects of diluting a broiler diet with increased levels of pea hulls (0 to 7.5%) on growth, energy efficiency and nutrient digestibility (Table 6) of broilers from 1 to 18 d of age. The inclusion of up to 5% pea hull improved most performance traits studied, as well as nutrient digestibility. When 7.5% pea hull was added to the diet, the benefits disappeared but still most traits were similar to those of the control diet. Probably, level and type of DF as well as age of the bird, modifies the response of broilers with respect to feed intake. For example, González-Alvarado et al. (2010) reported that the inclusion in the diet of 3% of sugar beet pulp, a source of soluble DF, reduced feed intake from 25 to 42 d of age as compared with a diet containing 3% of oat hulls (Table 7). However, no negative effects of sugar beet pulp inclusion were observed during the first 10 d of life. Sugar beet pulp has high pectin content and pectins are characterized by their high water holding capacity and swelling capacity (Serena and Bach Knudsen, 2007). A wetter and bulkier digesta, as occurs when sugar beet pulp is included in the diet, causes physical distension of the GIT which might affect the physiological mechanisms that regulate feed intake (Denbow, 1994). In this respect, Pettersson and Razdan (1993) observed that feed intake in 18 d-old chicks was reduced when the level of sugar beet pulp of the diet was increased from 2.3 to 9.2%. Also, Shakouri et al. (2006) observed that the inclusion of 3.0% of either carboxymetil-cellulose or a highly methylated citrus pectin reduced feed intake. Probably, lower feed intake may be attributed to an increase in digesta viscosity and a longer retention time of the digesta in the GIT.
Feed form affects organ development and growth performance of broilers. Pelleting reduced feed particle size and modified feed structure and thus, pelleting of the diet might modify the response of broilers to fiber inclusion. Jiménez-Moreno et al. (unpublished data) studied the effects of diluting a low fiber diet (1.6 CF and 3.7% NDF) based on rice-soy protein concentrate-lard with 0, 2.5, and 5% of 3 fiber sources (OH, rice hulls, and sunflower hulls) on performance of broilers kept on cages fed mash or pelleted diets from 0 to 21 d of age. Pelleting improved feed intake, body weight gain and feed conversion ratio (Table 2). The inclusion up to 5% of rice hulls but not of oat hulls and sunflower hulls reduced AMEn of the diet at 21 d of age; an effect that was more evident in pelleted than in mash diets (data not shown). Probably, the ingestion of high silica from rice hulls in pelleted diet may explain the differences observed among fiber sources. Modern broilers have a high capacity for feed consumption and they might accept higher dilutions of the diet. The pellet is rapidly dissolved in the upper part of the GIT after consumption; feed particles will not usually be retained in the gizzard reducing in size and in functioning. The lack of a properly functioning gizzard is related with a feed overconsumption. A well-functioning gizzard may hinder feed overconsumption simply because of the physical constraints in gizzard volume combined with limitations to feed passage from the gizzard to duodenum. Moreover, previous research indicate that bird eat litter to compensate for lack of structure in the diet (Hetland et al., 2005). Therefore, it is recommended the inclusion of a moderate amount of structural DF to broiler diets to avoid a overconsumption, without hindering growth of the birds.
6. Dietary fiber and Microflora
Biochemical conditions in the digesta, as a result of feed composition or physiological responses from the host affect substrate availability and concentration and thus microbial product formation. The degree of solubility, the fermentative capability and viscosity are 3 key physicochemical properties of fiber fraction to modulate the growth and distribution of the species and the total population of the resident microflora in the GIT. Soluble fiber is highly fermentable that may alter microbial activities increasing toxin production and enhancing enteric disease (Bach Knudsen et al., 1991). An increase in the viscosity of lumen contents from soluble fiber not only decreases laminar flow and convective efficiency of villi for nutrient absorption, but gas exchange between wall and digesta also lessens. A lower partial pressure for oxygen with increased concentrations of nutrients can enhance development of transient microbes, particularly anaerobes. The inclusion of high methylated citruc pectin could change the intestinal microbial population and increased the microbial activity in the ileum especially those of Enterococci, Bacteroidaceae, Clostridia, and E. Coli and total counts of anaerobic bacteria in the small intestine (Shakouri et al., 2006). Jørgensen et al. (1996) observed an increased amount of short-chain fatty acids (mainly lactic acid and acetic acid) and H2 excretion as result of a higher degradation of FD (pea fiber, wheat bran or oat bran) from microbial fermentation. Contrary, insoluble fiber is poorly fermentable and increases fecal bulk in poultry. Therefore, the effects of insoluble fiber effects on the composition and quantity of the microflora might be relatively insignificant. However, the inclusion of an insoluble fiber sources, such as OH, in the diet, improved gizzard functionality and reduce gizzard pH and might activate mechanically mucosa surface, increasing GIT motility and reducing the chances of bacteria, such as Clostridium perfringens adhering to the mucosa surface in the distal part of the GIT. Jiménez-Moreno et al (2011b) observed that diluting a control diet with 5% of oat hulls but not with sugar beet pulp, reduced the count of Clostridium perfringens and Enterobacteriae (Table 8) in consistent with a higher amount of fibrous particles retained in the gizzard (Table 1). Therefore, an improved functionality of the gizzard, low gizzard pH and a more rapid passage rate from the inclusion of insoluble FD, is considered to potentially have a beneficial effect on gut health through the sterilizing properties and lower time available for microbial fermentation in the small intestine.
The effect of DF on the erosion of mucus and recovery of mucins in ileal digesta seems to depend on their physical properties, including solubility. The inclusion of insoluble DF has a more abrasive action, scraping mucin from the mucosa as they pass through the digestive tract. Soluble DF due to its high water holding capacity, the particles swell and enhance action on the small intestine of birds increasing mucus output resulting in an increase flow of crude mucus in the lumen (Montagne et al., 2003). The modification of the composition of the mucins following DF ingestion probably leads to modification of the composition of commensal bacteria fixed on the mucus layer, which in turn might alter the competition between commensal and pathogen bacteria. The inclusion of DF that leads to more acid mucins such as insoluble fiber, appears to increase the potential of mucus to resist attack by bacterial enzymes, which favours the elimination of pathogens. Kalmendal et al. (2011) reported that the inclusion in the diet of high levels of sunflower meal, an insoluble source of DF, was associated with significant decreases in colony counts of Clostridium spp. Moreover, a shortening of the villi from soluble fiber ingestion reduces to area of mucins in the crypts of the small intestine indicating that the birds fed with soluble fiber might be more susceptible to pathogenic bacteria.
The inclusion of moderate amount of structural fiber in diets low in fiber stimulates gizzard activity and improves nutrient retention and growth performance of young broilers. The effects of inclusion of DF on physiology and development of GIT, passage rate, microbial growth, nutrient digestibility and growth performance differ depending on the composition of the basal diet, feed form, type and level of DF, and age of the bird. The inclusion of up to 3% coarse insoluble fiber source such as oat hulls, to conventional diets stimulates the development of the GIT and improves nutrient digestibility and growth performance. Under commercial conditions, birds require a minimum and a maximum amount of fiber in the diet for optimal performance. Therefore, diets for broilers should be formulated with a minimum and a maximum level of DF.
1. Amerah, A.M., V. Ravindran, R.G. Lentle, and D. G. Thomas. 2007. Feed particle size: Implications on the digestion and performanceof poultry.World`s Poult. Sci. 63:439-455.
2. Amerah, A.M., V. Ravindran, and R. G. Lentle, 2009. Influence of insoluble fibre and whole wheat inclusion on the performance, digestive tract development and ileal microbiota profile of broiler chickens. Br. Poult. Sci. 50:366-375.
3. American Association of Cereal Chemists. 2001. The definition of dietary fiber: report of the Dietary Fiber Definition Committee to the Board of Directors of the American Association of Cereal Chemists. Cereal Foods World. 2001:46:112–26.
4. Anugwa, F. O. I., V. H. Varel, J. S. Dickson, W. G. Pond, and L. P. Krook. 1989. Effect of dietary fibre and protein concentration on growth, feed efficiency, visceral organ weights and large intestine microbial populations of swine. J. Nutr. 119:879-886.
5. Bach Knudsen, K. E., B. B. Jensen, and I. Hansen. 1991. Gastrointestinal implications in pigs of wheat and oat fractions. 2. Microbial activity in the gastrointestinal tract. Br. J. Nuttr. 65:233-248.
6. Bach Knudsen, K. E. 2001. The nutritional significance of “dietary fiber” analysis. Anim. Feed Sci. Technol. 90:3-20.
7. Cao, B., T. Kumaro, and Y. Karasawa. 1998. Effects of dietary cellulose levels on growth, nitrogen utilization and retention time of diets on intestine in chicks fed equal amounts of nutrients. Pages 402-403 in Proceedings of the 6th Asian Pacific Poultry Congress, Nagoya, Japan.
8. Castanon, J. I. R. 2007. History of the use of antibiotic as growth promoters in European Poultry Feeds. Poult. Sci. 86:2466- 2471.
9. Denbow, D. M. 1994. Peripheral regulation of food intake in poultry. J. Nutr. 124:1349S-1354S.
10. Duke, G. E. 1992. Recent studies on regulation of gastric motility in turkeys. Poult. Sci. 71:1-8.
11. Fahey, G. C. Jr., N. R. Merchen, J. E. Corbin, A. K. Hamilton, L. L. Bauer, E. C. Titgemeyer and D. A. Hirakawa. 1992. Dietary fiber for dogs: III. Effects of beet pulp and oat fiber additions to dog diets on nutrient intake, digestibility, metabolizable energy, and digesta mean retention time. J. Anim. Sci. 70:1169-1174.
12. Forman, L. P., and B. O. Schneeman. 1980. Effects of dietary pectin and fat on the small intestinal contents and exocrine pancreas of rats. J. Nutr. 110:1992-1999.
13. González-Alvarado, J. M., E. Jiménez-Moreno, R. Lázaro, and G. G. Mateos. 2007. Effects of type of cereal, heat processing of the cereal, and inclusion of fiber in the diet on productive performance and digestive traits of broilers. Poult. Sci. 86:1705- 1715.
14. González-Alvarado, J. M., E. Jiménez-Moreno, D. G. Valencia, R. Lázaro, and G. G. Mateos. 2008. Effects of fiber source and heat processing of the cereal on the development and pH of the gastrointestinal tract of broilers fed diets based on corn or rice. Poult. Sci. 87:1779-1795.
15. González-Alvarado, J. M., E. Jiménez-Moreno, D. González-Sánchez, R. Lázaro, and G. G. Mateos. 2010. Effect of inclusion of oat hulls and sugar beet pulp in the diet on productive performance and digestive traits of broilers from 1 to 42 days of age. Anim. Feed Sci. Technol. 162:37-46.
16. Guinotte, F., J. Gautron, and Y. Nys. 1995. Calcium solubilization and retention in the gastrointestinal tract in chicks (Gallus domesticus) as a function of gastric acid secretion inhibition and of calcium carbonate particle size. Br. J. Nutr. 73:125-139.
17. Håkansson, J., S. Eriksson, A. Svensson., 1978. The influence of feed energy level on feed consumption, growth and development of different organs of chicks. Report No. 59, Swedish University of Agricultural Sciences, Department of Animal Husbandry, Uppsala, Sweden
18. Hetland, H., and B. Svihus. 2001. Effect of oat hulls on performance, gut capacity and feed passage time in broiler chickens. Br. Poult. Sci. 42:354-361.
19. Hetland, H., B. Svihus, and Å. Krögdahl. 2003. Effects of oat hulls and wood shavings on digestion in broilers and layers fed diets based on whole or ground wheat. Br. Poult. Sci. 44:275-282.
20. Huff, G. R., Q. Zheng, L. A. Newberry, W. E. Huff, J. M. Balog, N. C. Rath, K. S. Kim, E. M. Mrtin, S.C. Goeke, and J. K. Skeeles. 2001. Viral and bacterial agents associated with experimental transmission of infectious proventriculus of broiler chickens. Avian Dis. 45:828-843.
21. Iji, P.A., A. A. Saki, D.R. Tivey. 2001. Intestinal development and body growth of broiler chicks on diets supplemented with non-starch polysaccharides. Anim. Feed Sci. Technol. 89:175-188.
22. Janssen, W. M. M. A., and B. Carré. 1985. Influence of fiber on digestibility of broiler feeds. Pages 78-93 in Recent Advances in Animal nutrition. D. J. A. Cole and W. Haresign, eds. Butterworths, London, UK.
23. Jiménez-Moreno, E., J. M. González-Alvarado, R. Lázaro, and G. G. Mateos. 2009a. Effects of type of cereal, heat processing of the cereal, and fiber inclusion in the diet on gizzard pH and nutrient utilization in broilers at different ages. Poult. Sci. 88:1925-1933.
24. Jiménez-Moreno, E., J. M. González-Alvarado, A. González-Serrano, R. Lázaro, and G. G. Mateos. 2009b. Effect of dietary fiber and fat on performance and digestive traits of broilers from one to twenty-one days of age. Poult. Sci. 88:2562-2574.
25. Jiménez-Moreno, E., J. M. González-Alvarado, A. de Coca-Sinova, R. Lázaro, and G. G. Mateos. 2009c. Effects of source of fibre on the development and pH of the gastrointestinal tract of broilers. Anim. Feed Sci. Technol. 154:93-101.
26. Jiménez-Moreno, E., J. M. González-Alvarado, D. González-Sánchez, R. Lázaro, and G. G. Mateos. 2010. Effects of type and particle size of dietary fiber on growth performance and digestive traits of broilers from 1 to 21 days of age. Poult. Sci. 89:2197-2212.
27. Jiménez-Moreno, E., S. Chamorro, M. Frikha, H. M. Safaa, R. Lázaro, and G. G. Mateos. 2011a. Effects of increasing levels of pea hulls in the diet on productive performance and digestive traits of broilers from one to eighteen days of age. Anim. Feed Sci. Technol. 168:100-112.
28. Jiménez-Moreno, E., C. Romero, J. D. Berrocoso, M. Frikha, and G. G. Mateos. 2011b. Effects of the inclusion of oat hulls or sugar beet pulp in the diet on gizzard characteristics, apparent ileal digestibility of nutrients, and microbial count in the ceca in 36-day-old broilers reared on floor. Poult. Sci. 90 (Suppl. 1):153 (Abst.).
29. Jiménez-Moreno, E., M. Frikha, A. de Coca-Sinova, J. García, and G. G. Mateos. 2013a. Oat hulls and sugar beet pulp in diets for broilers 1. Effects on growth performance and nutrient digestibility. Anim. Feed Sci. Technol. (In press)
30. Jiménez-Moreno, E., M. Frikha, A. de Coca-Sinova, R. Lazaro, and G. G. Mateos. 2013b. Oat hulls and sugar beet pulp in diets for broilers 2. Effects on the development of the gastrointestinal tract and on the structure of the jejuna mucosa. Anim. Feed Sci. Technol. (In press)
31. Johnson, I.T., and J. M. Gee. 1981. Effect of gel-forming gums on the intestinal unstirred layer and sugar transport in vitro. Gut 22:398-403.
32. Jørgensen, H., X. Q. Zhao, K. E. B. Knudsen, and B. O. Eggum. 1996. The influence of dietary fibre source and level on the development of the gastrointestinal tract, digestibility and energy metabolism in broiler chickens. Br. J. Nutr. 15:379-395.
33. Kalmendal, R., K. Elwinger, L. Holm, and R. Tauson. 2011. High-fibre sunflower cake affects small intestinal digestion and health in broiler chickens. Br. Poult. Sci. 52:86-96.
34. Mateos, G. G., R. Lázaro, and M. I. Gracia. 2002. The feasilibity of using nutritional modifications to replace drugs in poultry feeds. J. Appl. Poult. Res. 11:437-452.
35. Mateos, G. G., E. Jiménez-Moreno, M. P. Serrano, and R. Lázaro. 2012. Poultry response to high levels of dietary fiber sources varying in physical and chemical characteristics. J. Appl. Poult. Res. 21:156-174.
36. Montagne, L., J. R. Pluske, and D. J. Hampson. 2003. A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals. Anim. Feed Sci. Technol. 108:95-117.
37. Moran Jr., E.T., 1982. Comparative Nutrition of the Fowl and Swine. The Gastrointestinal Systems. University of Guelph, Guelph, ON, Canada.
38. Pettersson, D., and A. Razdan. 1993. Effects of increasing levels of sugar-beet pulp in broiler chicken diets on nutrient digestion and serum lipids. Br. J. Nutr. 70:127-137.
39. Rogel, A. M., D. Balnave, W. L. Bryden, E. F. Annison. 1987. Improvement of raw potato starch digestion in chickens by feeding oat hulls and other fibrous feedstuffs. Aust. J. Agric. Res. 38:629-637.
40. Rezaei, M., M. A.Karimi Torshizi, Y. Rouzbehan. 2011. The influence of different levels of micronized insoluble fiber on broiler performance and litter moisture. Poult. Sci. 90:2008-2012.
41. Sacranie, A., B. Svihus, V. Denstadli, B. Moen, P. A. Iji, and M. Chock. 2012. The effect of insoluble fiber and intermittent feeding on gizzard development, gut motility, and performance of broiler chickens. Poult. Sci. 91:693-700.
42. Sarikhan, M., H.A. Shartyar, B. Gholizadeh, M. H. Hosseinzadeh, B. Beheshti, A. Mahmoodnejad, 2010. Effects of insoluble fiber on growth performance, carcass traits and ileum morphological parameters on broiler chick males. Int. J. Agric. Biol. 12:531-536.
43. Serena, A., and K. E. Bach Knudsen. 2007. Chemical and physicochemical characterization of co-products from the vegetable food and agro industries. Anim. Feed Sci. Technol. 139:109-124.
44. Shakouri, M. D., H. Kermanshahi, and M. Mohsenzadeh. 2006. Effect of different non starch polysaccharides in semi purified diets on performance and intestinal microflora of young broiler chickens. Int. J. Poult. Sci. 5:557-561.
45. Shandhu, K. S., M. M. El Samahi, I. Mena, C. P. Dooley, and J. E. Valenzuela. 1987. Effect of pectin on gastric emptying and gastroduodenal motility in normal subjects. Gastroenterology 92:127-137.
46. Sklan, D., A. Smirnov, and I. Plavnik. 2003. The effect of dietary fiber on the small intestines and apparent digestion in the turkey. Br. Poult. Sci. 44:735-740.
47. Svihus, B. 2011. The gizzard: function, influence of diet structure and effects on nutrient availability. World’s Poult. Sci. 67:207- 224.
48. Swennen, Q., Everaert, N., Debonne, M., Verbaeys, I., Careghi, C., Tona, K., Janssens, G.P.J., Decuypere, E., Bruggeman, V., Buyse, J., 2010. Effect of macronutrient ratio of the prestarter diet on broiler performance and intermediary metabolism. J. Anim. Physiol. Anim. Nutr. 94:375-384.
49. Thomas, M., T. van Vliet, A. F. B. van der Poel., 1998. Physical quality of pelleted animal feed 3. Contribution of feedstuff components. Anim. Feed Sci. Tecnol. 70:59-78.
50. Van der Klis, J. D., and A. Van Voorst. 1993. The effect of caboxymethyllcellulose (a soluble polysaccharide) on the rate of marker excretion from the gastrointestinal tract of broilers. Poult. Sci. 72:503-512.
This paper was presented at the 6th annual meeting AECACEM, Querétaro, México, February 2013