Accepted Manuscript

Title: Starch Digestion in broiler chickens fed cereal diets

Author: F. Zaefarian M.R. Abdollahi V. Ravindran
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DOI:
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S0377-8401(15)00248-5
http://dx.doi.org/doi:10.1016/j.anifeedsci.2015.07.020
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Please cite this article as: Zaefarian, F., Abdollahi, M.R., Ravindran, V.,Starch Digestion
in broiler chickens fed cereal diets, Animal Feed Science and Technology (2015),
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Starch Digestion in broiler chickens fed cereal diets

F. Zaefariana,*, M.R. Abdollahia, V. Ravindrana

Bag 11 222, Palmerston North 4442, New Zealand

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Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Private

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Abbreviations: RS, resistant starch; DF, dietary fibre; SDF, soluble dietary fibre; IDF,

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insoluble dietary fibre; AME, apparent metabolisable energy; GIT, gastrointestinal tract;

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NSP, non-starch polysaccharides.

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E-mail address: F.Zaefarian@massey.ac.nz (F. Zaefarian).

Corresponding author: Tel.: +64 6 356 9099

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ABSTRACT

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Starch, comprising up to 70-80% of most cereal grains, is the primary source of energy in

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poultry diets. Although it is generally believed that starch is well digested by poultry, low

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total tract and ileal starch digestibility has been reported in some studies. The structure

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and composition of starch granules, their interaction with protein matrix, and their

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availability after feed processing play important roles in the digestion of starch. There is

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clear evidence that starch digestion is highly correlated with its structural location within

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feedstuffs and components associated with starch granule. Viscous non-starch

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polysaccharides and feed technology practices such as pelleting, whole grain feeding

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and inclusion

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digestibility. The aim of this review is to focus on factors affecting the digestion and

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absorption processes of starch in poultry. The effects of components associated with

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starch granule, soluble and insoluble dietary fibre, anti-nutrients and feed processing on

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starch digestion are also reviewed.

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Keywords: Starch; Digestion; Cereals; Feed processing; Broiler chickens.

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Key factor affecting starch digestibility is structural characteristics of starch.

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Presence of proteins and lipids on the granule surface limit the starch digestion.

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Pelleting has variable outcomes on starch digestibility depending on grain type.

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High levels of soluble NSP in grains may not be beneficial for starch digestion.

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Whole grains maintain gizzard stimulating effect and increase starch digestibility.

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1. Introduction

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Starch is the main source of energy in poultry diets, comprising approximately 40%

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of the diet and contributing to more than half the metabolisable energy intake (Svihus,

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2011). Variations in starch digestion therefore have a strong influence on the energy

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value of poultry diets. Despite this, starch digestion has not received much attention until

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recently because of starch digestion is seldom a problem in poultry fed maize-based diets.

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Several studies indicate that starch in maize is almost completely digested in broiler

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chickens (Table 1). Chickens are also able to increase the secretion of pancreatic -

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amylase with increasing amounts of starch ingestion (Moran, 1985). However, evidence

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is accumulating to suggest that starch is not fully digested in poultry and that there is

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considerable variation among cereal species and cultivars within species. Thus

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consideration of the factors that could lower total tract or ileal starch digestibility is of

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critical relevance in practical feed formulations. Factors contributing to the variability in

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starch digestibility, including starch granule structure, anti-nutritional factors and cell

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wall structure, are reviewed herein. The influence of feed technology practices such as

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pelleting and thermal treatments, whole grain feeding, inclusion of structural components

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in the diet and feed particle size are also discussed.

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2. Starch structure and classification

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Starch accumulates in granules in the endosperm and consists of two different glucose

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polymers, namely amylose and amylopectin. Structure of these polymers and differences

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between amylose and amylopectin has been described in many studies (Heijnen, 1997;

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Oates, 1997; French, 1984; Gallant et al., 1992; Hizukuri et al., 1997; Buleon et al., 1998;

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Imberty et al., 1991). The negative relationship between amylose to amylopectin ratio and

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starch digestion rate is well recognised (Topping et al., 1997; kerbeg et al., 1998;

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Bednar et al., 2001; Saito et al., 2001; Abdel-Aal et al., 2002). Raw starches high in

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amylopectin have been shown to be digested more quickly than those high in amylose

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(Svihus et al., 2005). The starch granules may vary in size and shape. The granule size

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distribution and shape are two important factors which affect the functional property of

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starch (Svihus et al., 2005). More details can be found in the comprehensive reviews by

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Morrison and Karkalas (1990) and Tester and Karkalas (2002).

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One of the most widely used methods to classify the starches in human nutrition was

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suggested by Englyst et al. (1992). According to these authors, starch may be categorised

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into three groups based on the in vitro simulation of stomach and intestinal conditions. i)

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Rapidly digestible starch: amount of glucose released after 20 minutes, which include

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gelatinised starch, ii) Slowly digestible starch: amount of glucose released between 20

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and 120 minutes, which include native starch granules from most cereals, iii) Resistant

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starch (RS): total starch minus the amount of glucose released within 120 minutes of in

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vitro digestion, which is resistant to digestion.

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From the human nutritional point of view, starch can be divided into glycogenic,

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which is absorbed in the small intestine, and RS, which is not absorbed in the small

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intestine of healthy individuals (Asp, 1992; Englyst et al., 1996; Berry, 1986). The RS

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category is considered to include four subcategories, namely RS1, RS2, RS3 and RS4

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(Brown, 1996). Extensive studies regarding RS subcategories have been published

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(Eerlingen et al. 1994; Bird et al., 2000; Leszczynski, 2004; Nugent, 2005; Sajilata et al.,

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2006). Briefly, the RS1 is defined as inaccessible starch granules in whole or partially

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ground starch-containing ingredients. The RS2 includes native starch granules in which

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the degree of resistance appears to be related to the granule structure and its susceptibility

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to gelatinisation. The RS3 reflects retrograded starch during processing (Brown, 1996).

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The last fraction is RS4, which is defined as chemically or physically modified starches.

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Types of modification include esterification, etherification, and cross bonding (Nugent,

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2005).

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3. Starch digestion and gelatinisation in poultry

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The starch hydrolysis process and enzymes involved in poultry has been described in

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details by Moran (1982) and Gray (1992), and will only be briefly outlined herein. Starch

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hydrolysis is mostly carried out by the action of pancreatic -amylase in the duodenum

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and jejunum, which hydrolyses most -(1-4) glycosidic linkages in amylose and

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amylopectin (Lehmann and Robin, 2007). During the hydrolysis, amylose is broken down

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to maltose and maltotriose. Amylopectin is degraded to maltose, maltotriose and -

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dextrins (Moran, 1982). These water-soluble molecules cannot pass the intestinal wall.

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They are further hydrolysed into glucose by the activities of maltase and isomaltase

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located at the brush-border membrane of enterocytes. Glucose is absorbed from the small

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intestine and transported across the intestinal wall by a specific glucose carrier which

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depends on the presence of Na+ in the lumen. The driving force behind this transport is

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Na-K pump which pumps the Na+ back again into the lumen (Gray, 1992). Part of the

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absorbed glucose is oxidised and serves as an energy source for the gut wall. The

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remainder is transported by the portal vein and supply energy to other tissues or stored as

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glycogen or fat for future energy demands (Weurding, 2002).

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Starch gelatinisation involves uptake of water into the granule, hydration and

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swelling, uptake of heat, loss of crystallinity (Hoover, 1995). Initially, the swelling is

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reversible, but when a certain temperature threshold is reached, the swelling becomes

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irreversible and the structure of the granule is significantly altered. Gelatinisation opens

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up the granular structure which enables digestive enzymes to enter the starch granules

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and increase the susceptibility for amylolytic degradation (Rooney and Pflugfelder, 1986;

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Kishida et al., 2001; Singh et al., 2007). The review of Svihus et al. (2005) is an excellent

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reference for starch gelatinisation.

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At high water contents, most starches will be gelatinised at temperatures between 50

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and 70 C (Donald, 2001). At limited water contents, on the other hand, the gelatinisation

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temperature will be higher (Camire et al., 1990; Donald, 2001; Parker and Ring, 2001). In

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the presence of limited amount of water, more heat is needed to complete the

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gelatinisation and gelatinisation takes place over a wider temperature range (Sun et al.,

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2002). In most feed processing techniques, high temperatures are needed to initiate starch

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gelatinisation, as low water content are generally used (Svihus et al., 2005). Starches

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from different cereals show different gelatinisation characteristics (Lund, 1984), with

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wheat starch having lower gelatinisation temperatures (52-65 C) compared to maize

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starch (65-70.6 C). Taylor and Dewar (2001) observed that sorghum starch have higher

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gelatinisation temperatures (68-78 C) compared to maize starch (62-72 C). Sorghum-

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based diets therefore require higher conditioning temperatures than wheat-based diets to

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achieve starch gelatinisation, with maize-based diets being intermediate.

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The effect of pelleting on starch gelatinisation of most cereals is low, ranging

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between 8 and 20%. Although part of this gelatinisation may occur during steam-

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conditioning, the majority of gelatinisation takes place during the pelleting process

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(Heffner and Pfost, 1973; Zimonja et al., 2008; Abdollahi et al., 2010, 2011), especially

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in the pellet die, due to the high friction heat. Abdollahi et al. (2010) investigated the

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effects of heat from die holes on the gelatinised starch content of maize- and sorghum-

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based broiler diets and reported a significant increase in gelatinised starch after the diets

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passed through the pellet die (conditioned and pelleted diets) compared to conditioned-

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only samples (not passed through the pellet die).

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4. Factors affecting starch digestibility in poultry

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4.1.

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Perhaps the most important factor affecting starch digestibility, at the total tract or

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ileal levels, is the accessibility of starch fraction by digestive enzymes. Accessibility is

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determined by several factors, including granule size, shape, surface area and amylose to

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amylopectin ratio (Singh et al., 2007). Briefly, the lower susceptibility of large granule

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starches to enzymatic hydrolysis has been attributed to their smaller granule specific

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surface area, which may decrease the extent of enzyme binding and ultimately result in

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less hydrolysis than small granules (Tester et al., 2006). The negative relationship

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between amylose to amylopectin ratio and starch digestion rate is well recognised

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(Topping et al., 1997; kerbeg et al., 1998; Bednar et al., 2001; Saito et al., 2001; Abdel-

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Aal et al., 2002; Svihus et al., 2005). The hydrogen bonds linking glucose chains in

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amylose starch make the amylose molecules less susceptible to amylase attack compared

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to amylopectin molecule, since the linear chains in amylopectin are much shorter.

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4.2.

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A review of components associated with starch granules can be found in Rooney and

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Pflugfelder (1986) and Svihus et al. (2005). In cereal grains, endosperm accounts for

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approximately 80% of the total kernel weight. Most of the starch is located in the

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endosperm. The effect of protein matrix on starch digestion has been reported by Rooney

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and Pflugfelder (1986) and Aura et al. (1999) in sorghum and rye, respectively.

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Components associated with the starch granule

Granules themselves contain very little protein (Abdel-Aal et al., 2002); however, the

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proportion of protein increases toward the surface of starch granules (Baldwin, 2001).

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Protein-starch interactions are common in cereal grains (Rooney and Pflugfelder, 1986).

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Hamaker and Bugusu (2003) reported that protein fractions such as albumin, globulins

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and glutenins help in gluing the protein bodies into a matrix surrounding starch granules,

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which may act as a barrier towards starch digestibility. Jenkins et al. (1987) studied the

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effect of starch-protein interaction on in vitro starch digestibility in wheat and suggested

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that the occurrence of a starch-protein interaction may account for the reduced rate of

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digestion. Greenwell and Schofield (1989) reported that starch granules in soft wheat

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contain high amount of friabilin, a water soluble protein, while this protein is low in hard

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wheat and absent in durum wheat. Friabilin is concentrated at starch-protein interface,

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which may impede the bonding properties between matrix protein and starch granules in

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soft wheat and can cause a soft endosperm that fracture easily with milling compared to

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hard wheat.

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Lipids are also one of the important non-starch components in starch granules and

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usually consist of free fatty acids (mostly palmitic and linoleic acids) and phospholipids

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(mostly lysophospholipids). Tester and Karkalas (2002) reported that lipids are present

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only in cereal starches, represent 1.5% of the granule and are associated with amylose.

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Most of the lipids are found on the surface of starch granules (Baldwin et al., 1997). The

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interaction between amylose and fatty acids and the reduction in enzymatic starch

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digestion has been reported (Cui and Oates, 1999; Crowe et al., 2000). Lipid-starch

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complexes may decrease the contact between enzymes and starch, and also prevent the

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swelling of starch granule due to hydrophobicity (Vasanthan and Bhatty, 1996). Raeker et

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al. (1998) found that small granules have higher lipid contents than large granules, which

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may be due to the higher surface to volume ratio in small starch granules.

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Mineral fractions are negligible in cereal starches, but other sources of starch such as

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those in potato are known to contain high amounts of phosphate, which are mainly

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associated with starch in the amorphous region of granules. The presence of phosphate on

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the surface of starch granules may prevent its swelling and consequently the digestion of

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starch (Blennow et al., 2000).

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It can therefore be concluded that the presence of non-starchy components such as

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proteins, lipids and phosphate over the granule surface may limit the rate of starch

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digestion by reducing the contact between digestive enzymes and starch granule, and

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through reduced swelling of starch granules and interacting with gelatinisation properties

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during feed processing (Oates, 1997; Svihus et al., 2005).

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4.3.

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Dietary fibre (DF) is divided in two categories, namely water soluble and insoluble

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dietary fibre (SDF and IDF, respectively). Soluble dietary fibres with high molecular

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weight are found mainly in cereal grains (rye > barley > triticale > wheat > maize >

Dietary fibre

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sorghum) and are able to increase the viscosity of intestinal contents (Classen, 1996;

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Carr, 2004) altering the digesta passage rate, microbiota, metabolites, and efficacy of

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digestion (Bach Knudsen, 2001). The SDF fraction, including -glucans (mostly barley

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and oats) and arabinoxylans (wheat, maize, sorghum, rye and triticale), can lower the

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digestibility of nutrients, including starch (Choct and Annison, 1992a,b; Maisonnier et

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al., 2001). Rogel et al. (1987a) evaluating 38 wheat samples, observed large variations in

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total tract starch digestibility (0.818-0.999) and attributed to the soluble non-starch

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polysaccharides (NSP) contents. However, among major nutrients, the extent of

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digestibility reduction due to viscosity is lowest for starch (Choct and Annison, 1992a,b;

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Smits et al., 1997; Maisonnier et al., 2001). In fact, starch digestibility does not show

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much sensitivity to viscosity variations. Maisonnier et al. (2001) showed that the addition

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of guar gum NSP resulted in a decrease of only 2% total tract starch digestibility. Carr et

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al. (2002) also reported that the viscosity cannot be proposed as a major factor for low

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total tract starch digestibility in wheat-based broiler diets.

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Supplementation of exogenous xylanase or -glucanase to wheat- and barley-based

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diets is known to increase starch digestibility, especially in young birds (Ankrah et al.,

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1999; Choct et al., 1999; Marron et al., 2001). Viscosity decreases, induced by

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supplemental enzymes was attributed as the reason for this improvement. Ankrah et al.

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(1999) reported a large reduction in ileal viscosity and improvement in ileal and total

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tract starch digestion with -glucanase addition in birds fed barley-based diets. However,

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the reduction in ileal viscosity is sometimes very small in wheat-based diets and cannot

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explain the large magnitude of improvement seen in starch digestibility (Marron et al.,

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2001). Wheat-based diets are reported to have higher viscosity in pelleted than in mash

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diet (Cowieson et al., 2005; Zimonja et al., 2008; de Vries et al., 2012). Cowieson et al.

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(2005) attributed the increased diet viscosity in pelleted wheat-based diets to increased

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solubility of NSP. Zimonja et al. (2008) also reported a two-fold increase in intestinal

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digesta viscosity in broiler chickens when wheat-based diets were steam-pelleted at 90

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C.

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Insoluble fibre in monogastric diets is generally considered as a diluent of nutrients

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(Edwards, 1995). Since IDF is not digested in the birds digestive tract, it tends to reduce

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the apparent metabolisable energy (AME) of the whole diet. On the other hand, IDF has

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been reported to improve gut health, gut microbial profile and digestive organ

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development which consequently may increase the digestibility of non-fibre components

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(Rogel et al., 1987a; Hetland et al., 2003, 2005; Hetland and Svihus, 2007; Amerah et al.,

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2009; Gonzlez-Alvarado et al., 2010; Svihus, 2011). Therefore, the AME of the whole

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diet depends on the balance between negative and positive effects of IDF on AME. If the

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balance is positive, feed intake is reduced in order to adjust to the ME intake requirement.

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Hill and Dansky (1954) reported that the birds fed IDF tended to increase feed

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consumption as a way to compensate for the reduced nutrient concentration in the feed. In

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contrast, Mateos et al. (2012) observed negative effects of IDF on feed intake.

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Dietary IDF may decrease nutrient digestion, as it encapsulates nutrients within the

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cell wall, which can reduce the contact with digestive enzymes (Mateos et al., 2012).

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Some fibre sources may cause pancreatic hypertrophy, leading to an increase in

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pancreatic secretions (Kratzer et al., 1967). However, low to moderate inclusion of IDF

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has been reported to have some beneficial effects on nutrient digestibility (Rogel et al.,

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1987a,b). It has been suggested that as long as only moderate concentrations of IDF is

Page 11 of 53

included, performance of birds will not be affected despite the fact that the nutrient

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concentration of the diet is reduced (Hetland and Svihus, 2001; Hetland et al., 2002). The

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effect of IDF on total tract or ileal starch digestibility have also been evaluated in some

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studies (Rogel et al., 1987b; Svihus and Hetland, 2001; Hetland et al., 2003; Amerah et

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al., 2009; Jimnez-Moreno et al., 2011). Rogel et al. (1987b), examining the effect of oat

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hulls on total tract digestibility of raw potato starch in poultry, observed that the starch

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digestibility coefficients increased from 0.55 to 0.93. Amerah et al. (2009) reported a

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significant increase in ileal starch digestibility from 0.85 to 0.94 when 6% wood shavings

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was included in a wheat-based diet, but observed that the inclusion of 6% cellulose had

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no effect compared with the control diet (0.85 vs 0.87, respectively). In contrast, Svihus

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and Hetland (2001) reported that diluting wheat-based diets with 10% fine cellulose

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increased the ileal starch digestibility from 0.79 to 0.93. Hetland et al. (2003) reported

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that oat hull inclusion either in ground or whole wheat pelleted diets resulted in a higher

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ileal starch digestibility (0.99 vs. 0.97) and amylase production (146 vs. 255 U/g jejunal

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dry matter) in broiler chickens compared to the control diet. In the same study, it was also

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found that layers benefitted nutritionally from the inclusion of wood shavings in both

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ground wheat and 40% whole wheat diets. They reported that wood shaving addition to

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ground wheat-basal diets increased the ileal starch digestibility from 0.96 to 0.98. In diets

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with 40% whole wheat, starch digestibility was increased from 0.95 to 0.98. They found

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that bile acid concentration in the gizzard was increased with the addition of wood

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shavings, indicating stimulation of digestive process and gastro-duodenal reflux. The

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beneficial effects of IDF on nutrient digestibility are generally attributed to its effects on

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gizzard development and the associated increase in the secretion of HCl and digestive

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enzymes. Svihus (2006) hypothesised that the modern broiler strains tend to over-

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consume feed, which results in the overloading of the digestive system and reduced

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nutrients digestibility. Amerah et al. (2009) observed ileal starch digestibility

275

improvements with the added wood shavings and attributed this to the larger gizzard size

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and better gut motility. Svihus and Hetland (2001) observed that wheat starch

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concentration in the intestinal chyme was inversely correlated to ileal starch digestibility

278

and hypothesised that gizzard may be the main site for the prevention of starch overload

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in the gastrointestinal tract (GIT).

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The solubility, fermentation capacity, particle size, and degree of lignification of fibre

281

(Jorgensen et al., 1996; Shakouri et al., 2006; Jimnez-Moreno et al., 2011) as well as the

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inclusion level, cereal type used in basal diet (Jimnez-Moreno et al., 2009), feed form

283

(Jimnez-Moreno et al., 2007), type and age of the birds, rearing conditions and access of

284

birds to the litter can affect bird responses to IDF (Gonzlez-Alvarado et al., 2010).

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Although the IDF is not digested and may reduce the AME of the whole diet,

286

moderate concentration of IDF can improve upper gut functionality and consequently

287

may improve nutrient digestibility. The presence of IDF, especially of insoluble and

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lignified coarsely ground fibre, in the gizzard increases the grinding function of the

289

gizzard and anti-peristaltic refluxes of the GIT, resulting in better mixing of digesta with

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digestive juices. This process may explain the positive effects of IDF on the digestibility

291

of starch (Li and Owyang, 1993; Ferket, 2000; Svihus et al., 2004).

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4.4.

Other anti-nutrients

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In addition to dietary fibre, anti-nutrients such as phytic acid (Thorne et al., 1983),

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lectins (Maenz et al., 1999; Fasina et al., 2004), condensed tannin (Longstaff and McNab,

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1991a,b; Trevino et al., 1992, Grosjean et al., 1999) and -amylase inhibitors (Saunders,

297

1975; Granum and Eskeland, 1981; Rogel et al., 1987a ) in feedstuffs may also influence

298

starch digestibility. Phytic acid can affect starch digestion through interaction with

299

amylase protein or binding with calcium which is a co-factor for amylase activity (Yoon,

300

1983). A study by Camden et al. (2001) provides indirect evidence for the role of phytic

301

acid in starch digestion. In this study, a small but significant increase in ileal starch

302

digestibility was observed following the addition of exogenous phytase enzyme to maize-

303

based diets. Small amounts of anti-nutritional factors such as enzyme inhibitors, lectins,

304

phytate and tannins, have also been suggested to produce hypoglycaemia (Jenkins et al.,

305

1982). Some feed ingredients (beans, rye, wheat, triticale, sorghum and oats) contain

306

varying concentrations of -amylase inhibitors (Saunders, 1975). -Amylase inhibitors

307

form complexes with amylase and reduce starch digestion. It has been reported that wheat

308

-amylase inhibitors are sensitive to pepsin hydrolysis (Macri et al., 1977; Rogel et al.,

309

1987a). However a portion of -amylase inhibitors may escape pepsin hydrolysis and

310

cause a negative response. Chickens have also been shown to be able to adapt to -

311

amylase inhibitors (Macri et al., 1977), probably by increasing the pancreatic size and

312

pancreatic -amylase secretion. Carr (2004) suggested that pepsin hydrolysis combined

313

with this adaptation process results in only a negligible effect of -amylase inhibitors on

314

starch digestibility in chickens. However, in diets, which are not heat-treated and in

315

modern broiler strains that over-consume feed, -amylase inhibitors could become a

316

factor limiting starch digestion.

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Page 14 of 53

Condensed tannins are found in seeds with dark-coloured coats (peas, faba beans and

318

sorghum). According to available data, the effect of low levels of condensed tannins on

319

starch digestibility is negligible (Trevino et al., 1992, Igbasan and Guenter, 1996;

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Grosjean et al., 1999). However, high dietary levels of condensed tannins will have

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significant negative effects (Longstaff and McNab, 1991a,b; Flores et al., 1994a,b).

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4.5.

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Feed manufacture involves number of processing steps including grinding, pelleting,

325

steam flaking, extrusion and expanding. These processing methods may affect total or

326

ileal starch digestibility by altering starch properties or by interacting with other

327

components in the feed (Svihus et al., 2005). Rate and extent of starch digestion can also

328

be altered by means of feed processing. Processing methods involving heat, moisture and

329

shear force generally reduce the particle size and change the crystalline structure of the

330

starch. These effects may make starch more accessible to digestive enzymes (Weurding,

331

2002). Therefore, starch may be digested more rapidly, leading to shifting of the site of

332

starch digestion (Weurding et al., 2001). Since gelatinisation increases the access of

333

starch granules to enzymatic degradation, starch digestibility may be expected to be

334

increased in processed feeds. The extent of starch gelatinisation during pelleting is

335

generally small and is of minor importance (Svihus et al., 2004; Zimonja et al., 2008).

336

Svihus et al. (2005) reported that steam conditioning and pelleting will not have marked

337

effects on cereal starch digestibility. However, during expander and extrusion processing,

338

high amount of water is added per kg of feed (water addition: extrusion > expander >

339

pellet) and the feed is subjected to temperatures above 100 C under pressure

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Feed processing

Page 15 of 53

(temperature involved: extrusion > expander > pellet). These two factors have been

341

reported to increase the digestibility of starch (Murray et al., 2001). During steam

342

conditioning and pelleting, only between 8 and 20% total starch is usually gelatinised, but

343

expander processing results in an extent of gelatinisation between 22 to 35% starch

344

(Cramer et al., 2003). Extruder processing, on the other hand, results in a more complete

345

gelatinisation and disintegration of starch granules (Skoch et al., 1983a,b; Colonna et al.,

346

1989).

us

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340

Dehulling, soaking and germination of cereals may increase starch digestibility due to

348

the loss of phytic acid, tannins and polyphenols which inhibit the activity of -amylase. It

349

has also been suggested that the removal of tannins and phytic acid creates a space within

350

the matrix, which increases the susceptibility to enzymatic attack, consequently

351

improving starch digestion (Rehman and Shah, 2005).

an

347

Feed processing may also denature -amylase inhibitors and thus increase starch

353

digestibility. Saunders (1975) reported that pelleting reduced -amylase inhibitor levels

354

in wheat bran. On the other hand, Jacobs and Delcour (1998) and Asp and Bjorck (1989)

355

showed that processing may increase the formation of amylose-lipid complexes and

356

reduce the digestibility of starch.

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357

The positive effect of pelleting on starch digestibility of legumes was first proposed

358

by Moran et al. (1968) who observed improvements in the metabolisable energy (ME) of

359

peas with pelleting. This thesis was later confirmed in broiler chickens and adult

360

cockerels in studies evaluating the effect of pelleting on peas and faba beans (Carr et al.,

361

1987; Conan et al., 1992; Grosjean et al., 1999). This effect of pelleting could be

362

attributed partly to the damage by high shear force to starch in the cell wall matrix. The

Page 16 of 53

363

results of Carr et al. (1987) showed that pelleting of feedstuffs with low starch

364

digestibility (e.g. pea and faba bean) improves total tract starch digestion.
The effect of pelleting on the starch digestibility of different cereals has been studied

366

extensively (Table 2). Early work showed that grinding and pelleting resulted in the

367

rupture of aleurone cells and improved the availability of nutrients of wheat grains

368

(Saunders et al., 1968). However, cereal starch is located mainly in the endosperm and

369

not in aleurone cells (Carr, 2004). Svihus (2001) reported that high ileal starch

370

digestibility in wheat-based diets usually coincides with mash feeding, whereas low

371

starch digestibility is associated with feeding cold-pelleted diets. Ileal starch digestibility

372

coefficients of 0.79 and 0.95 were reported for pelleted and mash diets, respectively.

373

Svihus and Hetland (2001) speculated that an overload of starch in the small intestine of

374

birds fed pelleted wheat-based diets, due to feed over-consumption, is the major cause of

375

low ileal starch digestibility. Later studies indicated that the over-consumption was linked

376

to an under-developed gizzard (Svihus, 2010). Abdollahi et al. (2011) also reported

377

significant decreases in the ileal starch digestibility of wheat-based diets, from 0.96 in

378

mash diets to 0.84 and 0.83 in diets pelleted at 60 and 90 C, respectively, in broilers.

379

Abdollahi et al. (2013a,b) showed that the effect of feed form on ileal starch digestion

380

depends on cereal type. While pelleting had no effect on the ileal digestibility of starch in

381

maize-based diets (0.98 vs 0.98), it decreased the digestibility in wheat-based diets (0.92

382

vs 0.97).

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383

Only limited studies have investigated the effect of feed form on starch digestibility in

384

sorghum-based diets. Selle et al. (2012) found that pelleting had no effect on the ileal

385

starch digestibility of sorghum-based diets. However, Selle et al. (2013) reported inferior

Page 17 of 53

ileal starch digestibility in red sorghum-based pelleted diets (0.74) compared to the mash

387

diets (0.82) and reground pellets (0.81). Similar results have been reported by Abdollahi

388

et al. (2014), who observed that ileal starch digestion in birds fed red sorghum-based

389

pelleted diets was lower (0.93) compared to those fed mash diets (0.96). Formation of

390

Kafirin protein complexes may account for the low starch digestibility in pelleted

391

sorghum-based diets (Selle et al., 2013). In the endosperm of sorghum grain, Kafirin

392

proteins surround starch granules with both embedded in the glutelin protein matrix (Liu

393

et al., 2013). There is the possibility that kafirin-glutelin-starch interact in the sorghum

394

endosperm during steam pelleting and this can increase the polymerisation of kafirin

395

protein into high molecular weight polymers that may impede starch digestion. Published

396

data regarding the effect of pelleting of maize-based diets on starch digestion are scant.

397

Abdollahi et al. (2013b) stated that, in maize-based diets, pelleting had no effect on the

398

ileal digestibility of starch compared to mash diets possibly because of the already high

399

starch digestibility which may not leave any room for pelleting to further improve the

400

digestibility.

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386

401

Overall, these results suggest that pelleting may not be beneficial for ileal starch

402

digestibility in cereals especially in wheat and sorghum and may even decrease ileal

403

starch digestibility in cereals under some circumstances as a result of high feed intake.

404

405

4.6.

406

It is generally believed that the classical grinding process can overcome the

407

accessibility limitations in grains and coarse particles and increase starch digestibility, at

408

least in legume seeds (Longstaff and McNab, 1987; Carr, 2004). In legume seeds, coarse

Particle size

Page 18 of 53

grinding compared to fine grinding has been shown to decrease energy utilisation and the

410

digestibility of starch (Carr, 2004). Fine grinding of peas was reported to improve the

411

total tract digestibility of starch and protein when fed as mash diets (Carr et al., 1998;

412

Daveby et al., 1998; Carr, 2000). Such differences between fine and coarse grindings

413

were not observed in wheat (Uddin et al., 1996). In pelleted diets, fine grinding of peas is

414

not required to improve the starch digestibility (Conan et al., 1992). Kilburn and Edwards

415

(2001) reported that fine grinding of maize increased the true metabolisable energy

416

values in mash diets, but the opposite effect was observed in pelleted diets. Amerah et al.

417

(2008) reported that coarse grinding tended to improve the AME in pelleted wheat-based

418

diets, but not in maize-based diets. In contrast, Svihus et al. (2004) found no effect of

419

wheat particle size on the AME. Pron et al. (2005) found that fine grinding of hard

420

wheat improved total tract starch digestibility (0.93 vs. 0.85) and the AME (13.03 vs.

421

12.37 MJ/kg DM) compared to coarse grinding in pelleted diets. A negative relationship

422

between wheat hardness and the digestibility of starch in pelleted diets has been reported

423

by Carr et al. (2002, 2005). This negative effect may be related to the larger particle

424

size, which can reduce the surface area and the accessibility of digestive enzymes (Carr

425

et al., 2005; Pron et al., 2005). Pelleting tends to even out the differences in particle size

426

distribution, due to the grinding effect caused by the narrow gap between pellet rollers

427

and the pellet die and the frictional force inside the die hole (Abdollahi et al., 2013a).

428

Several studies have shown that pelleting reduces the feed particle size and equalises the

429

differences between coarsely and finely ground particles (Pron et al., 2005; Svihus et al.,

430

2004; Amerah et al., 2007; Abdollahi et al., 2011). Kilburn and Edwards (2004) stated

431

that coarser particles are retained longer in the digestive tract allowing more time for

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409

Page 19 of 53

digestion and absorption. These benefits were reduced when the diet was fed in pelleted

433

or crumbled form, presumably as a result of concomitant diminution of larger particles

434

during the pelleting process. Amerah et al. (2007) suggested that pelleting decreases the

435

grinding requirement by the gizzard so that gizzard function is reduced to that of a transit

436

organ. It is well documented that birds fed mash diets with coarsely ground particles have

437

well developed gizzards and longer retention time in the gizzard (Nir et al., 1994; Carr,

438

2000; Hetland and Svihus, 2001; Engberg et al., 2002). As pelleting may result in further

439

reductions in particle size and, subsequently suboptimal gizzard development and

440

reduced nutrient digestibility, strategies which can overcome the particle size reduction

441

by pelleting may be considered. Abdollahi et al. (2012) reported that water added during

442

conditioning may reduce this problem and attributed this to the lubrication of pellet die.

443

Another processing adjustment to reduce this problem could be the addition of structural

444

components which are resistant to crushing during the pelleting process. Fibrous and

445

hardy components such as oat hulls and wood shavings have been shown to maintain

446

their gizzard-stimulating effect after pelleting and thus may stimulate gizzard

447

development even at rather low inclusion levels (Svihus, 2011).

cr

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448

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432

449

4.7.

450

Whole grain feeding in broiler diets is being increasingly accepted world-wide.

451

Adverse effects of finely ground, pelleted diets on digestive tract development can be

452

effectively overcome by whole grain feeding (Singh et al., 2014). Whole grains practice

453

must be introduced early in life (prior to 7 days of age) with low inclusion levels and

Whole grain feeding

Page 20 of 53

gradually increasing to a maximum. The most widely used whole grain is wheat. Singh et

455

al. (2014) suggested 300 g/kg as upper level of whole wheat inclusion for older birds.

456

Among cereals, the inclusion of whole wheat has become more common practice. Many

457

studies have shown that replacement of ground wheat with whole wheat improved starch

458

digestibility (Svihus and Hetland, 2001; Hetland et al., 2002; 2003; Svihus et al., 2004;

459

Wu et al., 2004). Hetland et al. (2002) showed that starch digestibility was improved by

460

replacing ground barley with whole barley. Svihus et al. (2004) reported that post

461

pelleting inclusion of 37.5 % whole wheat increased the digestibility of starch by 3.1 and

462

6.6% at both total tract and ileal levels, respectively. However, they reported that 500

463

g/kg pre-pelleting replacement of ground wheat with whole wheat failed to show any

464

improvement in starch digestibility (0.95 vs 0.98). A reduced feed intake due to the grain

465

cereal feeding has been reported in some studies (Jensen, 1994; Yo et al., 1997; Hetland

466

et al., 2002). Amerah and Ravindran (2008) reported a three-fold increase in gizzard

467

contents of birds offered whole wheat as compared to those offered ground wheat. As

468

noted previously, Svihus (2006) hypothesised that modern broiler chickens fed pelleted

469

diets, over-consume, leading to intestinal starch overload and reduced starch digestibility.

470

Whole grain feeding can increase the gizzard size and its grinding activity, which can

471

prevent this overload of starch by reducing the feed intake in birds (Svihus and Hetland,

472

2001). Svihus (2011) suggested that, at least 20% grain particles in diets should be larger

473

than 1.5-2.0 mm in size to stimulate gizzard development.

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474
475

4.8.

Grain hardness

Page 21 of 53

Hardness of wheat grain is determined either by the continuity and the strength of

477

protein matrix surrounding the starch granules in the endosperm cells or by the amount of

478

adhesion between the protein matrix and the starch granules (Stenvert and Kingswood,

479

1977; Dobraszczyk et al., 2002). Turnbull and Rahman (2002) defined the relative

480

hardness or softness of a grain as the relative resistance to deformation or crushing when

481

an external force is applied. A number of factors affect wheat harness, including genetics

482

(Sourdille et al., 1996; Turnbull and Rahman, 2002), environmental conditions (Stenvert

483

and Kingswood, 1977; Dobraszczyk et al., 2002), protein content (Cornell and Hoveling,

484

1998; Turnbull and Rahman, 2002) and, quantity and quality of pentosans and moisture

485

content (Turnbull and Rahman, 2002). It has been reported that protein content and

486

soluble and insoluble pentosan contents are positively correlated with wheat hardness,

487

while moisture content was negatively correlated. Soft wheat is reported to contain higher

488

moisture levels compared to hard wheat (Turnbull and Rahman, 2002). Grain hardness is

489

related largely to the interaction between protein matrix and starch granule (Glenn and

490

Saunders, 1990; Kim et al., 2004). Major proteins that are involved in this interaction are

491

puroindolines a and b (Giroux and Morris, 1998) and glutenins and gliadins (Galande et

492

al., 2001; Turner et al., 2004).

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476

493

Published data on the effect of wheat endosperm harness on starch digestibility are

494

limited and equivocal. It is widely thought that a harder wheat produces larger particles,

495

which may account for the better development of gizzard. However, as hydration pattern

496

of any substrate is crucial to enzyme action and subsequent digestion, it is possible that

497

the soft wheat, with a better hydration pattern, may be more digestible than hard wheat

498

(Wiseman, 2006). The positive effect of soft wheat on starch digestibility was reported in

Page 22 of 53

some studies (Carr et al. 2002, 2005; Pron et al., 2006). Pron et al. (2006) reported a

500

negative relationship between wheat hardness and total tract digestibility of starch in

501

pelleted diets. Low starch digestibility in hard wheat can be related to accessibility

502

problems, as milling of hard wheat produces more coarse particles compared to soft

503

wheat (Pron et al., 2006). Carr et al. (2005) examined the variation in total tract starch

504

digestibility in 14 wheat samples differing in hardness and reported that the variation in

505

grain hardness was responsible for 7% variation (between 0.89 to 0.96) in starch

506

digestibility. It was also stated that the inclusion of soft wheat in pelleted diets has

507

advantages over hard wheat in terms of starch digestibility. Lower surface area of the

508

hard wheat particles and poor accessibility to digestive enzymes were stated as reasons

509

for lower starch digestibility in hard wheat diets. Guerrieri et al. (1997) and Pron et al.

510

(2006) suggested that the interaction between starch granules and the surrounding protein

511

matrix may act to impede enzyme hydrolysis of starch in hard wheat. Pron et al. (2005)

512

found that fine grinding of hard wheat in pelleted diets increased total tract starch

513

digestibility. When physical stress is applied, starch granules in soft wheat compared to

514

hard wheat are readily expelled from the matrix (Glenn and Saunders, 1990; Turnbull and

515

Rahman, 2002; Kim et al., 2004). In contrast, Uddin et al. (1996) found that the AME of

516

pelleted wheat diets was not affected by endosperm hardness. In mash diets, the lack of

517

relationship between wheat hardness and AME and starch digestibility has been reported

518

(Rogel et al., 1987a, Rose et al., 2001; Pirgozliev et al., 2003). Pron et al. (2006)

519

reported that, depending on wheat hardness, the grinding activity of gizzard may result in

520

the production of variable amounts of free starch, regardless of feed particles. It was

521

stated that, in birds fed soft wheat diets, increased action of the gizzard is not required to

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499

Page 23 of 53

522

expel free starch granules and make them accessible to digestive enzyme. In contrast, in

523

birds fed hard wheat diets, higher activity of gizzards is required for starch digestion.

524
525

4.9.

526

Bird genetics may be another factor causing the variability in nutrient digestibility. It

527

has been reported that the relative gizzard weight depends on either the genetic origin of

528

the birds (Pron et al., 2006; Rougire and Carr, 2010; de Verdal et al., 2011) or diet

529

physical characteristics (Hetland et al., 2003; Amerah et al., 2007; Rougire and Carr,

530

2010). Mignon-Grasteau et al. (2004) reported significant differences in all digestibility

531

parameters (AMEn and, digestibility of lipids, starch and proteins) at the first generation

532

of selection with two selected divergent lines D+ (high digestive efficiency) and D - (low

533

digestive efficiency). Anatomical differences in digestive system between these two lines

534

are greater gizzard relative size in D+ compared with D- (Pron et al. 2006; Rougire et al,

535

2009; Rougire and Carr, 2010). Pron et al. (2006) showed that D+ birds had higher

536

values than D- for total tract digestibility of starch, protein and lipids. It was stated that

537

part of the difference in total tract starch digestibility between the lines was related to the

538

increased proventriculus and gizzard weights in D+ line. de Verdal et al. (2011) reported

539

that in D+ lines, the genetic correlation between digestion efficiency and relative gizzard

540

weight was high. Pron et al. (2006) reported that the rapid transit time in D - birds fed

541

soft wheat may cause lower digestibility of proteins and lipids. However, these negative

542

effects on digestibility were not observed in D+ birds, because of the more developed

543

digestive tract. Rougire and Carr (2010) observed that in D - birds, a standard diet

544

resulted in a lower gizzard retention time, which is possibly associated with the lower

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Bird genetics

Page 24 of 53

muscular activity of this organ. In a follow-up study, Rougire et al. (2012) reported that

546

the lack of reaction of gizzard to environmental stimuli (meal distribution after fasting

547

and switching the light after dark) in D - birds was due mainly to the lack of relaxation

548

during the rest period. It was suggested that the ability of gizzard to relax is decreased in

549

D- compared with D+ birds, which can be a reason for the shorter digesta retention time in

550

the gizzard of D- birds.

cr

ip
t

545

Type of bird is another factor contributing to the variability in starch digestibility.

552

Despite the fact that chickens are well adapted to starch-based diets, it is still possible that

553

the high feed intake of modern fast-growing broiler chickens results in physiological

554

limitations to starch digestion. Nir et al. (1993) determined the activities of pancreatic

555

digestive enzymes from hatching to 14 d of age in meat- and egg-type birds. It was found

556

that in meat and egg-type chickens, pancreatic enzyme activities were similar, but

557

activities in the small intestinal contents were lower in meat-type compared to egg-type

558

chickens. Uni et al. (1995) reported that enzyme secretion per gram of feed intake in the

559

duodenum on day 4 after hatching was higher in a heavy broiler strain (Arbor Acres) than

560

in a light strain (Lohmann), but no differences were found thereafter. Starch digestion

561

during days 4 to 14 in heavy-strain and light-strain birds ranged from 90 to 95% and 80 to

562

93%, respectively. Interestingly, results from a study by Zelenka and Ceresnakova (2005)

563

showed that total tract starch digestibility was slightly lower in fast growing broilers than

564

in slow growing layer-type chickens fed identical diets. These authors also found that

565

starch digestibility decreased linearly with advancing age in fast-growing broilers, but

566

similar in layer type birds. Retention time in duodenum and jejunum was estimated by

567

Rougire and Carr (2010) to be around 1 h, highlighting the limited time available for

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551

Page 25 of 53

568

starch digestion in broiler chickens. This estimate supports the conclusion by Svihus

569

(2014) that the short time available for digestion may be one of the causes for the

570

impaired starch digestion under some circumstances.

5. Conclusions

572

In general, starch digestibility in cereals for chickens is relatively high. However,

573

because starch is the major energy component in poultry diets, any strategy capable of

574

reducing

575

performance. Multiple inter-related factors can lower total tract or ileal starch

576

digestibility in poultry. The major factors are structural characteristics of starch,

577

components associated with starch granule, dietary concentrations of SDF and IDF and

578

genetic origin of the birds. Feed processing techniques such as pelleting have variable

579

outcomes on starch digestibility, depending on the grain type. Pelleting may not be

580

beneficial for starch digestion in cereals containing high levels of soluble NSP and may

581

even decrease starch digestibility as a result of high feed intake. Pelleting also may result

582

in further reductions in particle size and subsequently lead to suboptimal gizzard

583

development and reduced nutrient digestibility. Feed technology practices which increase

584

gizzard development and feed retention time may be used as strategies to overcome the

585

negative effects of pelleting and fine particle size on cereal starch digestibility. Whole

586

grain feeding and low level inclusion of structural components, such as oat hull and wood

587

shavings, may also maintain the gizzard-stimulating effect.

starch

would

cr

undigested

be advantageous

to

overall

bird

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the

ip
t

571

588
589

References

Page 26 of 53

590

Abdel-Aal, E.S.M., Hucl, P., Chibbar, R.N., Han, H.L., Demeke, T., 2002.

591

Physicochemical and structural characteristics of flours and starches from waxy and

592

non-waxy wheats. Cereal Chem. 79, 458-464.

Abdollahi, M.R., Ravindran, V., Wester, T.J., Ravindran, G., Thomas, D.V., 2010.

594

Influence of conditioning temperature on performance, apparent metabolisable energy,

595

ileal digestibility of starch and nitrogen and the quality of pellets, in broiler starters fed

596

maize- and sorghum-based diets. Anim. Feed Sci. Technol. 162, 106-115.

us

cr

ip
t

593

Abdollahi, M.R., Ravindran, V., Wester, T.J., Ravindran, G., Thomas, D.V., 2011.

598

Influence of feed form and conditioning temperature on performance, apparent

599

metabolisable energy and ileal digestibility of starch and nitrogen in broiler starters fed

600

wheat-based diet. Anim. Feed Sci. Technol. 168, 88-99.

an

597

Abdollahi, M.R., Ravindran, V., Wester, T.J., Ravindran, G., Thomas, D.V., 2012. Effect

602

of improved pellet quality from the addition of a pellet binder and/or moisture to a

603

wheat-based diet conditioned at two different temperatures on performance, apparent

604

metabolisable energy and ileal digestibility of starch and nitrogen in broilers. Anim.

605

Feed Sci. Technol. 175, 150-157.

Ac
ce
p

te

601

606

Abdollahi, M.R., Ravindran, V., Wester, T.J., Ravindran, G., Thomas, D.V., 2013a.

607

Influence of pellet diameter and length on the quality of pellets and, performance,

608

nutrient utilisation and digestive tract development of broilers fed wheat-based diets.

609

Br. Poult. Sci. 54, 337-345.

610

Abdollahi, M.R., Ravindran, V., Wester, T.J., Ravindran, G., Thomas, D.V., 2013b. The

611

effect of manipulation of pellet size (diameter and length) on pellet quality and

Page 27 of 53

612

performance, apparent metabolisable energy and ileal nutrient digestibility in broilers

613

fed maize-based diets. Anim. Prod. Sci. 53, 114-120.

Abdollahi, M.R., Ravindran, V., Svihus, B., 2014. Influence of feed form on growth

615

performance, ileal nutrient digestibility, and energy utilisation in broiler starters fed a

616

sorghum-based diet. Livestock Sci. 165, 80-86.

ip
t

614

kerberg, A., Liljeberg, H., Bjrck, I., 1998. Effects of amylose/amylopectin ratio and

618

baking conditions on resistant starch formation and glycaemic indices. J. Cereal Sci.

619

28, 71-80.

us

cr

617

Amerah, A.M., Ravindran, V., 2008. Influence of method of whole-wheat feeding on

621

performance, digestive tract development and carcass traits of broiler chickens. Anim.

622

Feed Sci. Technol. 147, 326-339.

an

620

Amerah, A.M., Ravindran, V., Lentle, R.G., Thomas, D.G., 2008. Influence of feed

624

particle size on the performance, energy utilisation, digestive tract development, and

625

digesta parameters of broiler starters fed wheat- and corn-based diets. Poult. Sci. 87,

626

2320-2328.

Ac
ce
p

te

623

627

Amerah, A.M., Ravindran, V., Lentle, R.G., 2009. Influence of insoluble fibre and whole

628

wheat inclusion on the performance, digestive tract development and ileal microbiota

629

profile of broiler chickens. Br. Poult. Sci. 50, 366-375.

630

Amerah, A.M., Ravindran, V., Lentle, R.G., Thomas, D.G., 2007. Influence of feed

631

particle size on the performance, energy utilization, digestive tract development and

632

digestive parameter of broiler starters. Poult. Sci. 86, 2615-2623.

Page 28 of 53

633

Ankrah, N.O., Campbell, G.L., Tyler, R.T., Rossnagel, B.G., Sokhansanj, S.R.T., 1999.

634

Hydrothermal and -glucanase effects on the nutritional and physical properties of

635

starch in normal and waxy hull-less barley. Anim. Feed Sci. Technol. 81, 205-219.
Asp, N.G., 1992. Resistant Starch- Proceedings from the second plenary meeting of

637

EURESTA: European FLAIR Concerted Action No. 11 on physiological implications

638

of the consumption of resistant starch in man. Eur. J. Clin. Nutr. 46, S1.

cr

ip
t

636

Asp, N.G., Bjorck, I., 1989. Nutritional properties of extruded foods. In: Mercier, C.,

640

Linko, P., Harper, J.M. (Eds.), Extrusion Cooking. American Association of Cereal

641

Chemists, St Paul, MN, pp 399-434.

an

us

639

Aura, A.M., Harkonen, H., Fabritius, M., Poutanen, K., 1999. Development of an in vitro

643

enzymic digestion method for removal of starch and protein and assessment of its

644

performance using rye and wheat breads. J. Cereal Sci. 29, 139-152.

647
648

te

646

Bach Knudsen, K.E., 2001. The nutritional significance of dietary fibre analysis. Anim.
Feed Sci. Technol. 90, 3-20.

Baldwin, P.M., 2001. Starch granule-associated proteins and polypeptides: a review.

Ac
ce
p

645

642

Starch-Starke 53, 475-503.

649

Baldwin, P.M., Melia, C.D., Davies, M.C., 1997. The surface chemistry of starch

650

granules studied by time-of-flight secondary ion mass spectrometry. J. Cereal Sci. 26,

651

329-346.

652

Bednar, G.E., Patil, A.R., Murray, S.M., Grieshop, C.M., Merchen, N.R., Fahey Jr., G.C.,

653

2001. Starch and fibre fractions in selected food and feed ingredients affect their small

654

intestinal digestibility and fermentability and their large bowel fermentability in vitro

655

in a canine model. J. Nutr. 131, 27-286.

Page 29 of 53

656

Blennow, A., Bay-Smith, A.M., Oslen, C.E., Moller, B.L., 2000. The distribution

657

covalently bound phosphate in the starch granule in relation to starch crytallinity. Int.

658

J. Biol. Macromol. 27, 211-218.

Berry, C.S., 1986. Resistant starch formation and measurement of starch that survives

660

exhaustive digestion with amylolytic enzymes during the determination of dietary

661

fibre. J. Cereal Sci. 4, 301-314.

665
666
667

cr

us

Bolton, W., 1960. The digestibility of mash and pellets by chicks. J. Agric. Sci. 55, 141-

an

664

microflora and human health. Current Issues in Int. Microbiol. 1, 25-37.

142.

Buleon, A., Colonna, P., Planchot, V., Ball, S., 1998. Starch granules: structure and

663

Bird, A.R., Brown, I.L., Topping, D.L., 2000. Starches, resistant starches, the gut

biosynthesis. Int. J. Biol. Macromol. 23, 85-112.

662

ip
t

659

Brown, I., 1996. Complex carbohydrates and resistant starch. Nutr. Rev. 54, 115-119.

669

Cabrera, M.R., 1994. Effect of sorghum genotype and particle size on milling

670

characteristics and performance of fishing pigs, broiler chicks and layer hens. Masters

671

Thesis, Kansas State University. Manhattan, KS.

Ac
ce
p

te

668

672

Camden, B.J., Morel, P.C.H., Thomas, D.V., Ravindran, V., Bedford, M.R., 2001.

673

Effectiveness of exogenous microbial phytase in improving the bioavailabilities of

674

phosphorus and other nutrients in maize-soya-bean meal diets for broilers. Anim. Sci.

675

73, 289-297.

676
677

Camire, M.E., Camire, A., Krumhar, K., 1990. Chemical and nutritional changes in foods
during extrusion. Crit. Rev. Food Sci. Nutr. 29, 35-57.

Page 30 of 53

679
680
681

Carr, B., 2000. Effets de la taille des particules alimentaires sur les processus digestifs
chez les oiseaux d'levage. Anim. 13, 131-136.
Carr, B., 2004. Causes for variation in digestibility of starch among feedstuffs. Worlds
Poult. Sci. J. 60, 76-89.

ip
t

678

Carre, B., Escartin, R., Melcion, J.P., Champ, M., Roux, G., Leclercq, B., 1987. Effect

683

of pelleting and associations with maize or wheat on the nutritive value of smooth pea

684

(Pisum sativum) seeds in adult cockerels. Br. Poult. Sci. 28, 219-229.

us

cr

682

Carr, B., Melcion, J.P., Widiez, J.L., Biot, P., 1998. Effects of various processes of

686

fractionation, grinding and storage of peas on the digestibility of pea starch in

687

chickens. Anim. Feed Sci. Technol. 71, 19-33.

an

685

Carr, B., Idi, A., Maisonnier, S., Melcion, J.P., Oury, F.X., Gomez, J., Pluchard, P.,

689

2002. Relationships between digestibilities of food components and characteristics of

690

wheats (Triticum aestivum) introduced as the only cereal source in a broiler chicken

691

diet. Br. Poult. Sci. 43, 404-415.

Ac
ce
p

te

688

692

Carr, B., Muley, N., Gomez, J., Oury, F.X., Laffitte, E., Guillou, D., Signoret, C., 2005.

693

Soft wheat instead of hard wheat in pelleted diets results in high starch digestibility in

694

broiler chickens. Br. Poult. Sci. 46, 66-74.

695
696
697
698

Choct, M., Annison, G., 1992a. Anti-nutritive effect of wheat pentosans in broiler
chickens: roles of viscosity and gut microflora. Br. Poult. Sci. 33, 821-834.
Choct, M., Annison, G., 1992b. The inhibition of nutrient digestion by wheat pentosans.
Br. J. Nutr. 67, 123-132.

Page 31 of 53

699

Choct, M., Hughes, R.J., Bedford, M.R., 1999. Effects of a xylanase on individual bird

700

variation, starch digestion throughout the intestine, and ileal and caecal volatile fatty

701

acid production in chickens fed wheat. Br. Poult. Sci. 40, 419-422.

703

Classen, H.L., 1996. Cereal grain starch and exogenous enzymes in poultry diets. Anim.

ip
t

702

Feed Sci. Technol. 62, 21-27.

Colonna, P., Tayeb, J., Mercier, C., 1989. Extrusion cooking of starch and starchy

705

products. In: Mercier, C., Linko, P., Harper, J.M. (Eds.), Extrusion Cooking. American

706

Association of Cereal Chemists, St Paul, MN, pp 247-319.

us

cr

704

Conan, L., Barrier-Guillot, B., Widiez, J.L., Lucbert, J., 1992. Effect of grinding and

708

pelleting on the nutritional value of smooth pea seed (Pisum staivum) in adult

709

cockerel. In: Proceedings of the 1st European Conference on Grain Legumes. Paris, pp

710

479-480.

712

Cornell, H.J., Hoveling, A.W., 1998. Wheat; Chemistry and utilisation. Technomic,
Lancaster, PA, pp 8.

te

711

an

707

Cowieson, A.J., Hruby, M., Faurschou, Isaksen, M., 2005. The effect of conditioning

714

temperature and exogenous xylanase addition on the viscosity of wheat-based diets

715

and the performance of broiler chickens. Br. Poult. Sci. 46, 717-724.

Ac
ce
p

713

716

Cramer, K.R., Wilson, K.J., Moritz, J.S., Beyer, R.S., 2003. Effect of sorghum-based

717

diets subjected to various manufacturing procedures on broiler performance. J. Appl.

718

Poult. Res. 12, 404-410.

719

Crowe, T.C., Seligman, S.A., Copeland, L., 2000. Inhibition of enzymic digestion of

720

amylose by free fatty acids in vitro contributes to resistant starch formation. J. Nutr.

721

130, 2006-2008.

Page 32 of 53

722
723

Cui, R., Oates, C.G., 1999. The effect of amylose-lipid complex formation on enzyme
susceptibility of sago starch. Food Chem. 65, 417-425.
Daveby, Y.D., Razdan, A., Aman, P., 1998. Effect of particle size and enzyme

725

supplementation of diets based on dehulled peas on the nutritive value for broiler

726

chickens. Anim. Feed Sci. Technol. 74, 229-239.

ip
t

724

de Verdal, H., Narcy, A., Bastianelli, D., Chapuis, H., Meme, N., Urvoix, S., Le Bihan-

728

Duval, E., Mignon-Grasteau, S., 2011. Improving the efficiency of feed utilization in

729

poultry by selection. 1. Genetic parameters of anatomy of the gastrointestinal tract and

730

digestive efficiency. BMC Genet. 12, 59.

an

us

cr

727

de Vries, S., Pustjens, A.M., Schols, H.A., Hendriks, W.H., Gerrits, W.J.J., 2012.

732

Improving digestive utilization of fiber-rich feedstuffs in pigs and poultry by

733

processing and enzyme technologies: A review. Anim. Feed Sci. Technol. 178, 123-

734

138.

te

731

Dobraszczyk, B.J., Whitworth, M.B., Vincent, J.F.V., Khan, A.A., 2002. Single kernel

736

wheat hardness and fracture properties in relation to density and the modelling of

737

fracture in wheat endosperm. J. Cereal Sci. 35, 245-263.

738
739

Ac
ce
p

735

Donald, A.M., 2001. Review. Plasticization and self-assembly in the starch granule.
Cereal Chem. 78, 307-314.

740

Edwards, C.A., 1995. The physiological effect of dietary fibre. In: Kritchewsky, D. and

741

Bonfield, C. (eds) Dietary fibre in health and disease. Eagan Press, St. Paul,

742

Minnesota, USA, pp 58-71.

Page 33 of 53

743

Eerlingen, R.C., Jacobs, H., Delcour, J.A., 1994. Enzyme- resistant starch. 5. Effect of

744

retrogradation of waxy maize starch on enzyme susceptibility. Cereal Chem. 71, 351-

745

355.
Engberg, R.M., Hedemann, M.S., Jensen, B.B., 2002. The influence of grinding and

747

pelleting of feed on the microbial composition and activity in the digestive tract of

748

broiler chickens. Br. Poult. Sci. 43, 569-579.

751
752

starch in vitro and in vivo. Br. J. Nutr. 75, 749-55.

cr

us

750

Englyst, H.N., Kingman S., Hudson, G., Cummings, J., 1996. Measurement of resistant

Englyst, K.N., Kingman, S.M., Cummings, J.H., 1992. Classification and measurement of

an

749

ip
t

746

nutritionally important starch fractions. Eur. J. Clin. Nutr. 46, S33-S50.

Fasina, Y.O., Garlich, J.D., Classen, H.L., Ferket, P.R., Havenstein, G.B., Grimes, J.L.

754

Qureshi, M.A., Christensen, V.L., 2004. Response of turkey poults to soybean lectin

755

levels typically encountered in commercial diets. 1. Effect on growth and nutrient

756

digestibility. Poult. Sci. 83, 1559-1571.

758

te

Ferket, P., 2000. Feeding whole grains to poultry improves gut health. Feedstuffs, 72, 12-

Ac
ce
p

757

753

14.

759

Flores, M.P., Castanon, J.I.R., Mcnab, J.M., 1994a. Effects of tannins on starch

760

digestibility and TMEn of triticale and semipurified starches from triticale and field

761

beans. Br. Poult. Sci. 35, 281-286.

762
763
764
765

Flores, M.P., Castanon, J.I.R., Mcnab, J.M., 1994b. Nutritive value of triticale fed to
cockerels and chicks. Br. Poult. Sci. 35, 527-536.
French, D., 1984. Organization of starch granules. In Starch: Chemistry and Technology,
ed. RL Whistler, IN Bemiller, EF Pashall, Academic Press, NY, pp 183-245.

Page 34 of 53

Galande, A.A., Tiwari, R., Ammiraju, J.S.S., Santra, D.K., Lagu, M.D., Rao, V.S., Gupta,

767

V.S., Misra, B.K., Nagarajan, S., Ranjekar, P.K. 2001. Genetic analysis of kernel

768

hardness in bread wheat using PCR-based markers. Theor. Appl. Genet. 103, 601-606.

769

Gallant, D.J., Boucet, B., Buleon, A., Perez, S., 1992. physical characteristics of starch

770

granules and susceptibility to enzymatic degradation, Eur. J. Clin. Nutr. 46 (Suppl. 2)

771

S3-S16.

cr

ip
t

766

Giroux, M.J., Morris, C.F., 1998. Wheat grain hardness results from highly conserved

773

mutations in the friabilin components puroindoline a and b. Proceeding of National

774

Academy of Sciences, USA 95, 6262-6266.

an

776

Glenn, G.M., Saunders, R.M., 1990. Physical and structural properties of wheat
endosperm associated with grain texture. Cereal Chem. 67,176-182.

775

us

772

Gonzlez-Alvarado, J.M., Jimnez-Moreno, E., Gonzlez-Snchez, D., Lzaro, R.,

778

Mateos, G.G., 2010. Effect of inclusion of oat hulls and sugar beet pulp in the diet on

779

productive performance and digestive traits of broilers from 1 to 42 days of age. Anim.

780

Feed Sci. Technol. 162, 37-46.

782
783
784

te

Ac
ce
p

781

777

Gracia, M.I., Aranibar, M.J., Lazaro, R., Medel, P., Mateos, G.G., 2003. -Amylase
supplementation of broiler diets based on corn. Poult. Sci. 82, 436-442.
Granum, P.E., Eskeland, B., 1981. Nutritional significance of a-amylase inhibitors from
wheat. Nutr. Rep. Inter. 23, 155-162.

785

Gray, G.M., 1992. Starch digestion and absorption in nonruminant. J. Nutr. 122, 172-177.

786

Greenwell, P., Schofield, J.D., 1989. The chemical basis of grain hardness and softness.

787

In: H. Salovaara (Ed). Wheat End-Use Properties, Proceedings from the ICC 89

Page 35 of 53

788

Symposium, University of Helsinki Lahti Research and Training Centre, Lahti,

789

Finland, pp. 59-72.

Grosjean, F., Barrier-Guillot, B., Bastianelli, D., Rudeaux, F., Bourdillon A., Peyronnet

791

C., 1999. Feeding value of three categories of pea (Pisum sativum, L.) for poultry.

792

Anim. Sci. 69, 591-599.

cr

794

Guerrieri, N., Eynard, L., Lavelli, V., Cerletti, P., 1997. Interactions of protein and starch
studied through amyloglucosidase action. Cereal Chem. 74, 846-850.

us

793

ip
t

790

Hamaker, B.R., Bugusu, B.A., 2003. Overview: sorghum proteins and food quality.

796

Pretoria, South Africa: Paper presented at the Workshop on the proteins of sorghum

797

and millets: enhancing nutritional and functional properties for Africa.

an

795

Heffner, L.E., Pfost, H.B., 1973. Gelatinisation during pelleting. Feedstuffs, 45, 32-33.

799

Heijnen, M.L.A., 1997. Physical effects of consumption of resistant starch. PhD. Thesis,

802
803
804
805
806

te

801

Wageningen Agricultural University, Wageningen, the Netherlands.

Hetland, H., Svihus, B., 2001. Effect of oat hulls on performance, gut capacity and feed
passing time in broiler chickens. Br. Poult. Sci. 42, 354-361.

Ac
ce
p

800

798

Hetland, H., Svihus B., 2007. Inclusion of dust bathing materials affects nutrient
digestion and gut physiology of layers. J. Appl. Poult. Res. 16, 22-26.
Hetland, H., Svihus, B., Choct, M., 2005. Role of insoluble fiber on gizzard activity in
layers. J. Appl. Poult. Res. 14, 38-46.

807

Hetland, H., Svihus, B., Krogdahl, A., 2003. Effects of oat hulls and wood shavings on

808

digestion in broilers and layers fed diets based on whole or ground wheat. Br. Poult.

809

Sci. 44, 275-282.

Page 36 of 53

810

Hetland, H., Svihus B., Olaisen, V., 2002. Effect of feeding whole cereals on

811

performance, starch digestibility and duodenal particle size distribution in broiler

812

chickens. Br. Poult. Sci. 43, 416-423.

814

Hill, F.W., Dansky, L.M., 1954. Studies of the energy requirements of chickens. Poult.

ip
t

813

Sci. 33,112-119.

Hizukuri, S., Takeda, J., Abe, I., Hanashiro, G., Matsunobu, G., Kiyota, H., 1997.

816

Analytical developments: molecular and microstructural characterization. In: Frazier,

817

P.J., Donald, A.M., Richmond, P. (Eds.), Starch: Structure and Functionality. The

818

Royal Society of Chemistry, London, UK, pp 121-128.

an

us

cr

815

Hoover, R., 1995. Starch retrogradation. Food Rev. Inter. 11, 331-346.

820

Igbasan, F.A., Guenter, W., 1996. The enhancement of the nutritive value of peas for

821

broiler chickens: an evaluation of micronization and dehulling processes. Poult. Sci.

822

75, 1243-1252.

825
826

d
te

824

Imberty, A., Buleon, A., Tran, V., Perez, S., 1991. Recent advances in knowledge of
starch structure. Starch 43 (10), 375-384.

Ac
ce
p

823

819

Jacobs, H., Delcour, J.A., 1998. Hydrothermal modifications of granular starch, with
retention of the granular structure: A review. J. Agric. Food Chem. 46, 2895-2905.

827

Jenkins, D.J.A., Thorne, M.J., Camelon, K., Jenkins, A., Rao, A.V., Taylor, R.H.,

828

Thompson, L.U., Kalmusky, J., Reichert, R., Francis, T., 1982. Effect of processing on

829

digestibility and the blood glucose response: a study of lentils. Am. J. Clin. Nutr. 36,

830

1093-1101.

Page 37 of 53

831

Jenkins, D.J.A., Thorne, M.J., Wolever, T.M.S., Jenkins, A.L., Rao, A.V., Thompson,

832

L.U., 1987. The effect of starch-protein interaction in wheat on the glycemic response

833

and rate of in vitro digestion. Am. J. Clin. Nutr. 45, 946-951.

Jensen, J.F., 1994. Choice feeding in practice. In Proceedings, 9th European poultry

835

conference II. (UK Branch of Worlds Poultry Science Association: Glasgow, UK), pp.

836

223-236.

cr

ip
t

834

Jimnez-Moreno, E., Gonzlez-Alvarado, J.M., Bonilla, A.P., Lzaro, R., Mateos, G.G.,

838

2007. Influence of feed form and fibre inclusion in the diet on performance of broilers

839

from one to twenty one days of age. Poult. Sci. 86 (Suppl. 1), 68.

an

us

837

Jimnez-Moreno, E., Gonzlez-Alvarado, J.M., Gonzlez-Serrano, A., Lzaro, R.,

841

Mateos, G.G., 2009. Effect of dietary fibre and fat on performance and digestive traits

842

of broilers from one to twenty-one days of age. Poult. Sci. 88, 2562-2574.

840

Jimnez-Moreno, E., Chamorro, S., Frikha, M., Safaa, H.M., Lzaro, R., Mateos, G.G.,

844

2011. Effects of increasing levels of pea hulls in the diet on productive performance

845

and digestive traits of broilers from one to eighteen days of age. Anim. Feed Sci.

846

Technol. 168, 100-112.

Ac
ce
p

te

843

847

Jorgensen, H., Zhoa, X.Q., Knudsen, K.E., Eggum, B.O., 1996. The influence of dietary

848

fibre source and level on the development of the gastrointestinal tract, digestibility and

849

energy metabolism in broiler chickens. Br. J. Nutr. 75, 379-395.

850

Kilburn, J., Edwards, H.M., 2001. The response of broilers to the feeding of mash or

851

pelleted diets containing maize of varying particle sizes. Br. Poult. Sci. 42, 484-492.

852

Kilburn, J., Edwards, H.M., 2004. The effect of particle size of commercial soybean meal

853

on performance and nutrient utilization of broiler chicks. Poult. Sci. 83, 428-432.

Page 38 of 53

854
855

Kim, W., Choi, S.G., Kerr, W.L., Johnson, J.W., Gaines, C.S., 2004. Effect of heating on
particle size distribution in hard and soft wheat flour. J. Cereal Sci. 40, 9-16.
Kishida, T., Nogami, H., Himeno, S., Ebihara, K., 2001. Heat moisture treatment of high

857

amylose corn starch increases its resistant starch content but not its physiological

858

effects in rats. J. Nutr. 131, 2716-2721.

cr

860

Kotarski, S.F., Waniska, R.D., Thurn, K.K., 1992. Starch hydrolysis by ruminal
microflora. J. Nutr. 122, 178-190.

us

859

ip
t

856

Kratzer, F.H., Rajagura R.W.A.S.B., Vohra, P., 1967. The effect of polysaccharides on

862

energy utilization, nitrogen retention and fat absorption in chickens. Poult. Sci. 46,

863

1489-1493.

867
868
869
870
871
872
873

866

implications: a review. Tre. Food Sci. and Technol. 18, 346-355.

Leszczynski, W., 2004. Resistant Starch - Classification, Strucutre, Production. Polish J.

te

865

Lehmann, U., Robin, F., 2007. Slowly digestible starch- its structure and health

Food Nutr. Sci. 13, 37-50.

Ac
ce
p

864

an

861

Li, Y., Owyang, C., 1993. Vagal afferent pathway mediates physiological action of
cholecystokinin on pancreatic-enzyme secretion. J. Clin. Invest. 92, 418-424
Liu, S.Y., Selle, P.H., Cowieson, A.J., 2013. Strategies to enhance the performance of
pigs and poultry on sorghum-based diets. Anim. Feed Sci. Technol. 181, 1-14.
Longstaff, M., Mcnab, J.M., 1987. Digestion of starch and fibre carbohydrates in peas by
adult cockerels. Br. Poult. Sci. 28, 261-285.

874

Longstaff, M., Mcnab, J.M., 1991a. The inhibitory effects of hull polysaccharides and

875

tannins of field beans (Vicia faba L.) on the digestion of amino acids, starch and lipid

876

and on digestive enzyme activities in young chicks. Br. J. Nutr. 65, 199-216.

Page 39 of 53

Longstaff, M., Mcnab, J.M., 1991b. The effect of concentration of tannin-rich bean hulls

878

(Vicia faba L.) on activities of lipase (EC 3.1.1.3) and amylase (EC 3.2.I.I) in digesta

879

and pancreas and on the digestion of lipid and starch by young chicks. Br. J. Nutr. 66,

880

139-147.

882

Lund, D., 1984. Influence of time, temperature, moisture, ingredients, and processing
conditions on starch gelatinisation. Crit. Rev. Food Sci. Nutr. 20, 249-273.

cr

881

ip
t

877

Lundblad, K.K., Issa, S., Hancock, J.D., Behnke, K.C., McKinney, L.J., Alavi, S.,

884

Prestlkken, E., Fledderus, J., Srensen, M., 2011. Effect of steam conditioning at low

885

and high temperature, expander conditioning and extruder processing prior to pelleting

886

on growth performance and nutrient digestibility in nursery pigs and broiler chickens.

887

Anim. Feed Sci. Technol. 169, 208-217.

an

us

883

Macri, A., Parlamenti, R., Silano, V., Valfre, F., 1977. Adaptation of the domestic

889

chicken, Callus Domesticus, to continuous feeding of albumin amylase inhibitors from

890

wheat flour as gastro-resistant microgranules. Poult. Sci. 56, 434-441.

te

888

Maenz D.D., Irish G.G., Classen H.L., 1999. Carbohydrate- binding and agglutinating

892

lectins in raw and processed soybean meals. Anim. Feed Sci. Technol. 76, 335-343

893

Maisonnier, S., Gomez, J., Carr, B., 2001. Nutrient digestibility and intestinal viscosities

894

in broiler chickens fed on wheat-based diets, as compared to guar gum added maize-

895

diets. Br. Poult. Sci. 42, 102-110.

Ac
ce
p

891

896

Marron, L., Bedford, M.R., Mccracken, K.J., 2001. The effects of adding xylanase,

897

vitamin C and copper sulphate to wheat-based diets on broiler performance. Br. Poult.

898

Sci. 42, 493-500.

Page 40 of 53

899

Mateos, G.G., Jimnez-Moreno, E., Serrano, M.P., Lzaro, V., 2012. Poultry response to

900

high levels of dietary fibre sources varying in physical and chemical characteristics. J.

901

Appl. Poult. Res. 21, 156-174.

Moran, E.T., 1982. Starch digestion in fowl. Poult. Sci. 61, 1257-1267.

903

Moran, E.T., 1985. Digestion and absorption of carbohydrates in fowl and events through
perinatal development. J. Nutr. 115, 665-674.

cr

904

ip
t

902

Moran, E.T., Summers, J.D., Jones, G.E., 1968. Field peas as a major dietary protein

906

source for the growing chick and laying hens with emphasis on high-temperature

907

steam pelleting as a practical mean of improving nutritional value. Can. J. Anim. Sci.

908

48, 47-55.

an

910

Morrison, W.R., Karkalas, J., 1990. Starch, in: Methods in Plant Biochemistry (P.M.
Dey, ed.), Volume 2, London: Academic Press, pp 323-352.

909

us

905

Murray, S.M., Flickinger, E.A., Patil, A.R., Merchen, N.R., Brent, J.L., Fahey, G.C.,

912

2001. In vitro fermentation characteristics of native and processed cereal grains and

913

potato starch using ileal chyme from dogs. J. Anim. Sci. 79, 435-444.

Ac
ce
p

te

911

914

Naderinejad, S., Zaefarian, F., Abdollahi, M.R., Hassanabadi, A., Kermanshahi, H.,

915

Ravindran, V., 2015. Influence of feed form and particle size on the performance and

916

nutrient utilisation of broiler starters fed maize-based diets. Proceedings of the

917

Australian Poultry Science Symposium, 26, 141-144.

918

Nir, I., Nitsan, Z., Mahagna, M., 1993. Comparative growth and development of the

919

digestive organs and of some enzymes in broiler and egg type chicks after hatching.

920

Br. Poult. Sci. 34, 523-532.

Page 41 of 53

921

Nir, I., Twina, Y., Grossman, E. and Nitsan, Z., 1994. Quantitative effects of pelleting on

922

performance, gastrointestinal tract and behaviour of meat-type chickens. Br. Poult.

923

Sci. 35, 589-602.

927
928
929

ip
t

Oates, C.G., 1997. Towards an understanding of granule structure and hydrolysis. Tre.

cr

926

27-54.

Food Sci. and Technol. 8, 375-382.

us

925

Nugent, A.P., 2005. Health properties of resistant starch. Br. Nut. Found. Nutri. Bulle. 30,

Parker, R., Ring, S.G., 2001. Aspects of the physical chemistry of starch. J. Cereal Sci.

an

924

34, 1-17.

Pron, A., Bastianelli, D., Oury, F.X., Gomez, J., Carr, B., 2005. Effects of food

931

deprivation and particle size of ground wheat on digestibility of food components in

932

broilers fed on a pelleted diet. Br. Poult. Sci. 46, 223-230.

930

Pron, A., Gomez, J., Mignon-Grasteau, S., Sellier, N., Besnard, J., Derouet, M., Juin, H.,

934

Carr, B., 2006. Effects of wheat quality on digestion differ between the D + and D-

935

chicken lines selected for divergent digestion capacity. Poult. Sci. 85, 462-469.

Ac
ce
p

te

933

936

Pirgozliev, V.R., Birch, C.L., Rose, S.P., Kettlewell, P.S., Bedford, M.R., 2003.

937

Chemical composition and the nutritive quality of different wheat cultivars for broiler

938

chickens. Br. Poult. Sci. 44, 464-475.

939

Raeker, M.O., Gaines, C.S., Finney, P.L., Donelson, T., 1998. Granule size distribution

940

and chemical composition of starches from 12 soft wheat cultivars. Cereal Chem. 75,

941

721-728.

942
943

Rehman, Z.U., Shah, W.R., 2005. Thermal heat processing effects on antinutrients,
protein and starch digestibility of food legumes. Food Chem. 91, 327-331.

Page 42 of 53

944
945

Rogel, A.M., Annison, E.F., Bryden, W.L., Balnave, D., 1987a. The digestion of wheat
starch in broiler chickens. Aust. J. Agric. Res. 38, 639-649.
Rogel, A.M., Balnave, D., Bryden, W.L., Annison, E.F., 1987b. Improvement of raw

947

potato starch digestion in chickens by feeding oat hulls and other fibrous feedstuffs.

948

Aust. J. Agric. Res 38, 629-637.

951
952

cr

emphasis on sorghum and corn. J. Anim. Sci. 63, 1607-1623.

us

950

Rooney, L.W., Pflugfelder, R.L., 1986. Factors affecting starch digestibility with special

Rose, S.P., Tucker, L.A., Kettlewell, P.S., Collier, J.D.A., 2001. Rapid tests of wheat
nutritive value for growing chickens. J. Cereal Sci. 34, 181-190.

an

949

ip
t

946

Rougire, N., Carr, B., 2010. Comparison of gastrointestinal transit times between

954

chickens from D+ and D- genetic lines selected for divergent digestion efficiency.

955

Anim. 4, 1861-1872.

953

Rougire, N., Gomez, J., Mignon-Grasteau, S., Carr, B., 2009. Effects of diet particle

957

size on digestive parameters in D+ and D- genetic chicken lines selected for divergent

958

digestion efficiency. Poult. Sci. 88, 1206-1215.

Ac
ce
p

te

956

959

Rougire, N., Malbert, C.H., Rideau, N., Cognie, J., Carr, B., 2012. Comparison of

960

gizzard activity between chickens from genetic D+ and D- lines selected for divergent

961

digestion efficiency. Poult. Sci. 91, 460-467.

962

Saito, K., Ito, T., Kuribayashi, T., Mochida, T., Nakakuki, T., Shibata, M., Sugawara, M.,

963

2001. Effect of raw and heat-moisture treated high-amylose corn starch on

964

fermentation by the rat cecal bacteria. Starch, 53, 424-430.

965
966

Sajilata, M.G., Singhal, R.S., Kulkarni, P.R., 2006. Resistant Starch - A Review.
Comprehensive Reviews in Food Science and Food Safety, 5, 1-17.

Page 43 of 53

968
969
970

Saunders, R.M., 1975. -Amylase inhibitors in wheat and other cereals. Cereal Foods
World, 20, 282-285.
Saunders, R.M., Walker, H.G., Kohler, G.O., 1968. The digestibility of steam-pelleted
wheat bran. Poult. Sci. 47, 1636-1637.

ip
t

967

Selle, P.H., Liu, S.Y., Cai, J., Cowieson, A.J., 2012. Steam-pelleting and feed form of

972

broiler diets based on three coarsely ground sorghums influences growth performance,

973

nutrient utilisation, starch and nitrogen digestibility. Anim. Prod. Sci. 52, 842-852.

us

cr

971

Selle, P.H., Liu, S.Y., Cai, J., Cowieson, A.J., 2013. Steam-pelleting temperatures, grain

975

variety, feed form and protease supplementation of mediumly ground, sorghum-based

976

broiler diets: influences on growth performance, relative gizzard weights, nutrient

977

utilisation, starch and nitrogen digestibility. Anim. Prod. Sci. 53, 378-387.

an

974

Selle, P.H., Liu, S.Y., Cai, J., Cowieson, A.J., 2014. Steam-pelleting temperatures and

979

grain variety of finely-ground, sorghum-based broiler diets. I. Influence on growth

980

performance, relative gizzard weights, nutrient utilisation, starch and nitrogen

981

digestibility. Anim. Prod. Sci. 54, 339-346.

Ac
ce
p

te

978

982

Shakouri, M.D., Kermanshahi, H., Mohsenzadeh, M., 2006. Effect of different non starch

983

polysaccharides in semi purified diets on performance and intestinal microflora of

984

young broiler chickens. Inter. J. Poult. Sci. 5, 557-561.

985

Singh, Y., Amerah, A.M., Ravindran, V., 2014. Whole grain feeding: Methodologies and

986

effects on performance, digestive tract development and nutrient utilisation of poultry.

987

Anim. Feed Sci. Technol. 190, 1-18.

Page 44 of 53

988

Singh, J., Kaur, L., Mccarthy, O.J., 2007. Factors influencing the physico-chemical,

989

morphological, thermal and rheological properties of some chemically modified

990

starches for food applications: a review. Food Hydrocolloids, 21, 1-22.

Skoch, E.R., Binder, S.F., Deyoe, C.W., Allee, G.L., Behnke, K.C., 1983a. Effects of

992

pelleting conditions on performance of pigs fed a corn-soybean meal diet. J. Anim.

993

Sci. 57, 922-928.

cr

ip
t

991

Skoch, E.R., Binder, S.F., Deyoe, C.W., Allee, G.L., Behnke, K.C., 1983b. Effects of

995

steam pelleting conditions and extrusion cooking on a swine diet containing wheat

996

middlings. J. Anim. Sci. 57, 929-935.

an

us

994

Smits, C.H.M., Veldman, A., Verstegen, M.W.A., Beynen, A.C., 1997. Dietary

998

carboxymethylcellulose with high instead of low viscosity reduces macronutrient

999

digestion in broiler chickens. J. Nutr. 127, 483-487.

997

Sourdille, P., Perretant, M.R., Gharmet, G., Leroy, P., Gautier, M.F., Joudrier, P., Nelson,

1001

J.C., Sorrells, M.E., Bernard, M., 1996. Linkage between RFLP markers and genes

1002

affecting kernel hardness in wheat. Theor. Appl. Genet. 93, 580-586.

1004
1005
1006

Ac
ce
p

1003

te

1000

Stenvert N.L., Kingswood, K., 1977. The influence of the physical structure of the
protein matrix on wheat hardness. J. Sci. Food Agric. 28, 11-19.
Sun, Z., Yang, W., Siebenmorgen, T., Stelwagen, A., Cnossen, A., 2002.
Thermomechanical transitions of rice kernels. Cereal Chem. 79, 349-353.

1007

Svihus, B., 2001. Research note: A consistent low starch digestibility observed in pelleted

1008

broiler chicken diets containing high levels of different wheat varieties. Anim. Feed

1009

Sci. Technol. 92, 45-49.

1010

Svihus, B., 2006. The role of feed processing on gastrointestinal function and health in

Page 45 of 53

1011

poultry. In: Perry, G.C. (Ed.), Avian Gut Function in Health and Disease.CAB

1012

International, Wallingford, UK, pp 183-194.

Svihus, B., 2010. Diet composition and processing adjustments to cover the birds need

1014

for structural components. Proceedings of the 8th Annual Mid-Atlantic Nutrition

1015

Conference, University of Maryland, College Park, MD. pp 99-107.

cr

1017

Svihus, B., 2011. Limitation to wheat starch digestion in growing broiler chickens: a brief
review. Anim. Prod. Sci. 51, 583-589.

us

1016

ip
t

1013

Svihus, B., 2014. Starch digestion capacity of poultry. Poult. Sci. 93, 2394-2399.

1019

Svihus, B., Choct, M., Classen, H.L., 2013. Fuction and nutritional roles of the avian

1020

an

1018

caeca: a review. Worlds Poult. Sci. J. 69, 249-263.

Svihus, B., Hetland, H., 2001. Ileal starch digestibility in growing broiler chickens fed on

1022

a wheat-based diet is improved by mash feeding, dilution with cellulose or whole

1023

wheat inclusion. Br. Poult. Sci. 42, 633-637.

te

1021

Svihus, B., Juvik, E., Hetland, H., Krogdahl, A., 2004. Causes for improvement in

1025

nutritive value of broiler chicken diets with whole wheat instead of ground wheat. Br.

1026

Poult. Sci. 45, 55-60.

Ac
ce
p

1024

1027

Svihus, B., Uhlen, A.K., Harstad, O.M., 2005. Review: effect of starch granule structure,

1028

associated components and processing on nutritive value of cereal starch. Anim. Feed

1029

Sci. Technol. 122, 303-320.

1030
1031
1032
1033

Taylor, J.R.N., Dewar, J., 2001. Developments in sorghum food technologies. Advan.
Food Nutr. Res. 43, 217-264.
Tester, R.F., Qi, X., Karkalas, J., 2006. Hydrolysis of native starches with amylases.
Anim. Feed Sci. Technol. 130, 39-54.

Page 46 of 53

Tester, R.F., Karkalas, J., 2002. Starch, in: Biopolymers, Polysaccharides II:

1035

Polysaccharides from Eukaryotes, (A. Steinbiichel series ed.; E. J. Vandamme, S. De

1036

Baets and A. Steinbiichel volume eds), Volume 6, Weinheim: Wiley-VCH. pp 381-

1037

438.

ip
t

1034

Thorne, M.J., Thompson, L.U., Jenkins, D.J.A., 1983. Factors affecting starch

1039

digestibility and the glycemic response with special reference to legumes. Am. J. Clin.

1040

Nutr. 38, 481-488.

us

cr

1038

Topping, D.L., Gooden, J.M., Brown, I.L., Biebrick, D.A., Mcgrath, L., Trimble, R.P.,

1042

Choct, M., Illman, R.J., 1997. A high amylose (amylomaize) starch raises proximal

1043

large bowel starch and increases colon length in pigs. J. Nutr. 127, 615-622.

an

1041

Trevino, J., Ortiz, L., Centeno, C., 1992. Effect of tannins from faba beans (Vicia faba)

1045

on the digestion of starch by growing chicks. Anim. Feed Sci. Technol. 37, 345-349.

1046

Turnbull, K.M., Rahman, S., 2002. Endosperm texture in wheat. J. Cereal Sci. 36, 327-

337.

te

1047

1044

Turner, A.S., Bradburne, R.P., Fish,L., Snape, J.W., 2004. New quantitative trait loci

1049

influencing grain texture and protein content in bread wheat. J. Cereal Sci. 40, 51-60.

1050

Uddin, M.S., Rose, S.P., Hiscock, T.A., Bonnet, S., 1996. A comparison of the energy

1051

availability for chickens of ground and whole grain samples of two wheat varieties.

1052

Br. Poult. Sci. 37, 347-357.

1053
1054

Ac
ce
p

1048

Uni, Z., Noy, Y., Sklan, D., 1995. Posthatch changes in morphology and function of the
small intestines in heavy-strain and light-strain chicks. Poult. Sci. 74, 1622-1629.

1055

Vasanthan, T., Bhatty, R.S., 1996. Physicochemical properties of small- and large-

1056

granule starches ofwaxy, regular and high amylose barleys. Cereal Chem. 73, 199-207.

Page 47 of 53

1058
1059
1060

Yo, T., Vilarino, M., Faure, J.M., Picard, M., 1997. Feed pecking in young chickens: new
techniques of evaluation. Physiol. Behav. 61, 803-810.
Yoon, J.H., 1983. The effect of phytic acid on in vitro rate of starch digestibility and
blood glucose response. Am. J. Clin. Nutr. 38, 835-842.

ip
t

1057

Yutste, P., Longstaff, M.A., Mcnab, J.M., Mccorquodale, C., 1991. The digestibility of

1062

semipurified starches from wheat, cassava, pea, bean and potato by adult cockerels and

1063

young chicks. Anim. Feed Sci. Technol. 35, 289-300.

us

cr

1061

Weurding, R.E., Veldman, A., Veen, W.A.G., Van Der Aar, P.J., Verstegen, M.W.A.,

1065

2001. Starch digestion rate in the small intestine of broiler chickens differs between

1066

feedstuffs. J. Nutr. 131, 2329-2335.

1069
1070

PhD. Thesis, Wageningen Agricultural University, Wageningen, the Netherlands.

1068

Weurding, R.E., 2002. Kenetics of starch digestion and performance of broiler chickens,

Wiseman, J., 2006. Variations in starch digestibility in non-ruminants. Anim. Feed Sci.
Technol. 130, 66-77.

te

1067

an

1064

Wu, Y., Ravindran, V., Thomas, D.G., Birtles, M.J., Hendriks, W.H., 2004. Influence of

1072

method of whole wheat inclusion and xylanase supplementation on the performance,

1073

apparent metabolisable energy, digestive tract measurements and gut morphology of

1074

broilers. Br. Poult. Sci. 45, 385-394.

1075
1076

Ac
ce
p

1071

Zelenka, J., Ceresnakova Z., 2005. Effect of age on digestibility of starch in chickens
with different growth rate. Czech J. Anim. Sci. 50, 411-415.

1077

Zimonja, O., Svihus, B., 2009. Effects of processing of wheat or oats starch on physical

1078

pellet quality and nutritional value for broilers. Anim. Feed Sci. Technol. 149, 287-

1079

297.

Page 48 of 53

1080

Zimonja, O., Hetland, H., Lazarevic, N., Edvardsen, D.H., Svihus, B., 2008. Effects of

1081

fibre content in pelleted wheat and oat diets on technical pellet quality and nutritional

1082

value for broiler chickens. Can. J. Anim. Sci. 88, 613-622.

ip
t

1083
1084

cr

1085

us

1086

Table 1

an

Starch digestibility of cereals in poultry

Grain type

Starch digestibility
Age

Ileal

14

Yutste et al. (1991)

0.97

Camden et al. (2001)

0.94-0.96

Maisonnier et al. (2001)

29

0.97

0.97

Weurding et al. (2001)

21

0.98-0.99

Abdollahi et al. (2013b)

0.931

Rogel et al. (1987a)

Ac
ce
p

24

Wheat

Reference

35

0.98

te

Maize

(day)

Total tract

42
14

0.98

Yutste et al. (1991)

24

0.82-0.87

Maisonnier et al. (2001)

21

0.79

Svihus (2001)

21

0.79

Svihus and Hetland (2001)

Page 49 of 53

0.94

Weurding et al. (2001)

24

0.97

Hetland et al. (2002)

38

0.94

Hetland et al. (2002)

33

0.97

Hetland et al. (2003)

24

0.94-0.97

Svihus et al. (2004)

25

0.95-0.98

Svihus et al. (2004)

24

0.89-0.96

Carr et al. (2005)

21

0.81-0.83

21

0.81-0.98

21

0.92-0.98

29

cr

us

an

Zimonja and Svihus (2009)

Abdollahi et al. (2011)

Abdollahi et al. (2013a)

0.95

Weurding et al. (2001)

0.87-0.91

Selle et al. (2012)

0.93-0.96

Abdollahi et al. (2014)

28

0.86-0.892

Selle et al. (2014)

28

0.84-0.913

Selle et al. (2014)

19

0.894

Hesselman and Aman

0.95

Ac
ce
p

21

27

Barley

ip
t

0.94

te

Sorghum

29

(1986)
19

0.855

Hesselman and Aman

(1986)

21

0.96

Svihus (2001)

Page 50 of 53

0.98

0.98

Weurding et al. (2001)

21

0.99

Svihus (2001)

21

0.96-0.97

Zimonja and Svihus (2009)

ip
t

Oat

29

Mean total starch digestibility of 38 wheat varieties grown in Australia

White sorghum, 3 Red sorghum, 4 Low viscous barley; 5 High viscous barley

Ac
ce
p

te

an

us

cr

Page 51 of 53

Table 2
Effect of feed form on starch digestibility in broiler chickens
Grain type

Feed form

Starch digestibility
Ileal

Maize-wheat-

Reference

Total tract

Mash

0.751

Pellet

0.731

Bolton (1960)

Pellet

0.98

Re-ground pellet

0.99

Mash

0.98

Pellet

0.97

Abdollahi et al. (2013b)

an

0.98

Mash

Naderinejad et al. (2015)

Mash

Ac
ce
p

Wheat

te

Maize

us

cr

ip
t

barley

0.772 (0.95)3

Rogel et al. (1987a)

0.982 (0.94)3

Pellet

Cold-pelleted

0.79

Svihus and Hetland (2001)

Re-ground pellet

0.95

Cold-pellet

0.83

0.97

Steam-pellet at 75 C

0.81

0.98

Extruded

0.95

0.99

Mash

0.92

Pellet at 47 C

0.94

Pellet at 90 C

0.96

Zimonja and Svihus (2009)

Lundblad et al. (2011)

Page 52 of 53

Page 53 of 53

te

Ac
ce
p
us

an

cr

ip
t