Amylose-inclusion complexes: Formation, identity and physico-chemical properties

Journal of Cereal Science 51 (2010) 238e247

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Review

Amylose-inclusion complexes: Formation, identity and physico-chemical properties J.A. Putseys*, L. Lamberts, J.A. Delcour Laboratory of Food Chemistry and Biochemistry and Leuven Food Science and Nutrition Research Centre (LFoRCe), Katholieke Universiteit Leuven, Kasteelpark Arenberg 20, B-3001 Heverlee, Belgium

a r t i c l e i n f o

a b s t r a c t

Article history: Received 16 October 2009 Received in revised form 22 January 2010 Accepted 22 January 2010

Many ligands can form inclusion complexes with amylose. Their presence induces a conformation change involving the transformation of amylose double helices to a single helix. The resulting so called Vamylose is compact and has a central hydrophobic cavity in which the hydrocarbon chain of the ligand can reside. We discuss the different ways of formation of amylose-inclusion complexes, with emphasis on amyloseelipid complexes. Both amorphous and semicrystalline amylose-inclusion complexes are considered. The influence of variables in the synthesis reactions on the physico-chemical characteristics of amyloseelipid complexes is highlighted and the hydrolysis and functionality of (in situ formed) amyloseelipid complexes, such as their possible role in starch-based systems, is reviewed. Ó 2010 Elsevier Ltd. All rights reserved.

Keywords: Starch Amylose Lipid Complexation Synthesis Hydrolysis

1. Introduction Starch is a mixture of two polymers, amylose which is a predominantly linear glucose polymer, and amylopectin which is a branched glucose polymer. In the presence of ligands such as iodine and linear alcohols, amylose undergoes a conformation change resulting in a single, left-handed helix that can complex the ligand (Fig. 1). In their unordered form, amylose-inclusion complexes are known as ‘type I’ complexes. When these amorphous complexes are organized in lamellae and give rise to the formation of crystallites, they are referred to as ‘type II’ amyloseinclusion complexes. Colin and de Claubry discovered the interaction of starch and iodine in 1814 (Saenger, 1984) and its helical nature was first demonstrated by Rundle and Baldwin (1943). In this form, amylose is also referred to as ‘V-amylose’ (Katz, 1937). Katz chose this name because he considered the observed pattern to be that of gelatinized starch, or ‘Verkleisterter Stärke’ in German, abbreviated as Vstarch. However, it turned out that the pattern resulted from the complexation of gelatinized starch with the alcohol used to dehydrate it. The name was nevertheless kept (Zobel, 1988).

Abbreviations: CLA, conjugated linoleic acid; DMSO, dimethyl sulfoxide; DP, degree of polymerization; DSC, Differential Scanning Calorimetry; GMP, glyceryl monopalmitate; RVA, rapid viscoanalyzer. * Corresponding author. Tel.: þ32 16321634; fax þ32 16321997. E-mail address: [email protected] (J.A. Putseys). 0733-5210/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jcs.2010.01.011

The mechanism by which lipids interact with starch is similar to that described for iodine and alcohols (Mikus et al., 1946). Amyloseelipid complexes can be naturally present in starch (Evans, 1986, Morrison et al., 1993) or formed upon gelatinization of starch in the presence of lipids. However, while the absence of the V-amylose pattern in native starch granules would imply that the endogenous amylose complexes lack crystalline order, the predominance of native starch crystals may well hide the presence of a V-amylose contribution. 2. Identity of amylose-inclusion complexes V-amylose structures are single, left-handed helices with an internal cavity where the complexed ligand can reside (Saenger, 1984), as shown in Fig. 1. Each ligand, however, imposes its own specific helix dimensions, as described for amylose complexation with e.g. iodine (Rundle and French, 1943), potassium hydroxide (Sarko and Biloski, 1980) and dimethyl sulfoxide (DMSO) (Simpson et al., 1972). Thus, helix diameter and dimensions are determined by the complexing agent and the amount of water bound to the glucose units, as proposed by Valletta et al. (1964). 2.1. Driving forces for complex formation The presence of a suitable ligand induces a compact helical conformation of amylose. This results in a helix with a hydrophobic

J.A. Putseys et al. / Journal of Cereal Science 51 (2010) 238e247

Fig. 1. A left-handed single amylose helix, complexed with a ligand of which the polar head is located outside the helix, whereas its aliphatic chain is situated in the helix cavity [based on Carlson et al. (1979)]. The pitch is the distance between identical points in sequential turns.

cavity which provides binding sites with a high affinity for the apolar (part of the) ligand (Rutschmann and Solms, 1990; Whittam et al., 1989). After this initial molecular association between amylose and the ligand, and depending on the reaction conditions, the obtained complexes might acquire a certain degree of order, resulting in the formation of crystals (Whittam et al., 1989). Helbert (1994) suggested that helix formation was induced by the lower energy of the ligand in the helix cavity and Heinemann et al. (2001) proposed the driving force for the creation of these complex structures to be the tendency of amylose to minimize its interaction with water. Complexation between amylose and an inclusion compound is a reversible process. Differential Scanning Calorimetry (DSC) of complexes reveals an endotherm during heating and an exotherm during cooling (Biliaderis et al., 1985). The necessity for heat to dissociate the complex between amylose and its ligand suggests that there are certain forces that steady the helix conformation. Intramolecular bonds, such as van der Waals forces and hydrogen bonding, occur between the turns along the helix, and stabilize a single chain helix (Banks and Greenwood, 1971; Karkalas et al., 1995; Rappenecker and Zugenmaier, 1981; Yamashita and Monobe, 1971). Intermolecular forces, on the other hand, stabilize the interaction between amylose and its ligand. The amylose helix is hydrophilic on the outside and hydrophobic inside its cavity (Immel and Lichtenthaler, 2000), favouring the formation of hydrophobic interactions (Winter and Sarko, 1974). However, van der Waals forces have also been described (Banks and Greenwood, 1971; Immel and Lichtenthaler, 2000). Karkalas et al. (1995) suggest that van der Waals interactions are possible only between methylene groups of the lipid and hydrogen of carbon five in glucose.

2.2. Lipid organization inside the helix Theoretically 18e24 glucose units are required for the complexation of one lipid molecule (i.e. fatty acid or monoacyl glycerol with 14, 16, 18,. carbon atoms in its tail), organized in

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three turns, each containing six or eight glucose residues per pitch (Fig. 1). The pitch is the distance between identical points in two sequential turns. Some outer branches of amylopectin have average chain lengths of about 15 e 25 glucose units (Hizukuri, 1986; Mua and Jackson, 1997; Tester et al., 2004) and can therefore also partly participate in complex formation (Eliasson, 1994), as observed for amylose-free starches (Kaneda et al., 1996). Based on molar ratios of amylose and glycerol monopalmitate (GMP), Lagendijk and Pennings (1970) calculated that one long amylose chain (with a degree of polymerization, DP, of 900) can contain 10e12 helices, with each helix binding at least one, but often two GMP molecules. Godet et al. (1995a, 1996) suggested that the critical size of amylose for complex formation was the length required to accommodate two fatty acid molecules: 30e40 glucose residues were required for complexation of palmitic acid, while 20e30 appear to be sufficient for lauric acid.. According to Gelders et al. (2006), a semienzymically synthesized (cf. infra) amyloseelipid complex consists of two segments of helix, each with two complexed lipid molecules. Depending on the lipid chain length (cf. infra), this particular synthesis method results in complexes with amylose chains of 60e130 glucose units (Gelders et al., 2006). It is generally accepted that, for most amyloseelipid complexes, the lipid molecules are located with their aliphatic chain inside the helix cavity, with the methyl end groups facing each other. Godet et al. (1993b) suggested that the carboxyl groups were outside the helix due to steric and electrostatic repulsions. All other polar groups of a size exceeding that of a carboxyl group will thus, most probably, also be located outside the helix cavity (Snape et al., 1998). However, more recently, Shogren et al. (2006) described the carboxyl group of the lipids as being included in the central canal after all.

2.3. Dimensions of the crystal unit cell A general subdivision of V-amylose into different groups, depending on the dimensions of its unit cell and the position of the ligand, can be made. The hydrated form, Vh-amylose, also known as V6I, has been described most. This helix consists of six glucose units per turn with ligands residing only in the helix cavity (Rappenecker and Zugenmaier, 1981), as listed in Table 1. Vh-amylose is formed in the presence of, e.g., saturated lipids and linear alcohols. It has mostly been described as an orthorhombic structure (Germino and Valletta, 1964; Sarko and Biloski, 1980; Valletta et al., 1964; Yamashita et al., 1973; Zobel et al., 1967), with dimensions a ¼ 1.36e1.37 nm, b ¼ 2.37e2.58 nm and c ¼ 0.78e0.81 nm (Hinkle and Zobel, 1968; Rappenecker and Zugenmaier, 1981; Takeo and Kuge, 1971; Zobel et al., 1967). This results in a helix with an external diameter of 13.0e13.7  A and an internal cavity with a diameter of 5.0e5.4  A (Hinkle and Zobel, 1968; Immel and Lichtenthaler, 2000; Saenger, 1984; Takeo and Kuge, 1971). Upon drying of Vh-amylose, an anhydrous form, Va, is obtained. This helix has somewhat smaller unit dimensions: a ¼ 1.30e1.32 nm, b ¼ 2.25e2.70 nm and c ¼ 0.790e0.792 nm (Hinkle and Zobel, 1968; Zobel et al.,1967) with an external diameter of 13.0e13.3  A, as listed in Table 1 (Hinkle and Zobel, 1968; Mikus et al., 1946). In the Vbutanol form, also known as V6II, complexed ligands are not only located in the helix cavity, but also in the interstitial space between helices (Table 1). The unit cell dimensions are, thus, larger with a ¼ 2.74 nm and b ¼ 2.65 nm. The pitch, however, remains the same, with c ¼ 0.8 nm (Helbert and Chanzy, 1994). This helix conformation is formed in the presence of, e.g., short chain alcohols.

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Table 1 Overview of the unit cell dimensions and ligand locations of amylose-inclusion complexes with 6 glucose units per turn. Name

Location ligand

Vh

V6I

Va Vbutanol

V6II

Visopropanol

V6III

Unit cell dimensions

References

a (nm)

b (nm)

c (nm)

Helix cavity

1.36e1.37

2.37e2.58

0.78e0.81

Helix cavity Helix cavity (interstitial space) (helix cavity) Interstitial space

1.30e1.32 2.74

2.25e2.70 2.65

0.79 0.80

Hinkle and Zobel (1968), Rappenecker and Zugenmaier (1981), Takeo and Kuge (1971), Zobel et al. (1967) Hinkle and Zobel (1968), Zobel et al. (1967) Helbert and Chanzy (1994)

2.82

2.93

0.80

Buléon et al. (1990)

Visopropanol, also referred to as V6III, has even more interstitial space than the V6II helices, allowing ligands to reside both within and between helices (Table 1). In this case, helix dimensions are even larger: a ¼ 2.82 nm, b ¼ 2.93 nm, although the pitch remained constant, c ¼ 0.8 nm (Buléon et al., 1990). These last two unit cell structures, V6II and V6III, can be converted into V6I upon drying (Helbert and Chanzy, 1994). In the presence of more voluminous ligands, larger helix diameters are obtained for helices with seven (14.7  A) or eight (16.2  A) glucose units per turn as is the case for, e.g. menthone or fenchone in the case of V7 and naphthol in the case of V8. The corresponding crystal structures have been described as consisting of orthorhombic unit cells (Nuessli et al., 1995; Takeo and Kuge, 1971; Takeo et al., 1973; Yamashita and Hirai, 1966; Yamashita and Monobe, 1971; Yamashita et al., 1973; Zaslow, 1963). However, recent investigations of the single crystals of V-amylose complexes with naphthol by Cardoso et al. (2007) pointed towards tetragonal units cells with a ¼ b ¼ 2.28 nm and c ¼ 0.78 nm. They also suggested two amylose chains to be present per unit cell. When drying V7-complexes, a Vh-amylose form is obtained, whereas this is not the case for V8 complexes. That is why it is often assumed that V7-helices are actually V6-helices with ligands predominantly located in the interstitial spaces (V6II and V6III) (Buléon et al., 1990; Nuessli et al., 2003; Rondeau-Mouro et al., 2004). 2.4. Towards a larger crystal Semicrystalline, i.e. type II, amylose-inclusion complexes are (lamellarly) ordered, as opposed to their randomly oriented type I counterparts. They have a higher dissociation temperature (than the type I complexes) and a characteristic X-ray diffraction pattern with peaks around 7.5 , 13 and 20 (2q). However, under low moisture and high temperature conditions, the peaks shift to lower angles (6.9 , 12.0 and 18.5 (2q)), resulting in a variant known as E-amylose (Buléon et al., 1998). The semicrystalline inclusion complexes have helical chain segments ordered in structures with dimensions up to 14.5 nm (Galloway et al., 1989). After complexation of the ligand, further aggregation of the helices into lamellae occurs. The observed birefringence and lamellar thickness of 7.5e10 nm suggest a chain folding in the same or in successive lamellae (Biliaderis et al., 1986a; Schoch, 1942; Whittam et al., 1989; Zobel et al., 1967). For lipid-complexed amylose, Godet et al. (1996) proposed either a fringed micellar organization or a U-shaped folding. In the latter case, the complexes of one amylose chain are forced to form a crystalline area. The former consists of one amylose chain passing sequentially through amorphous and crystalline regions, thus taking part in adjacent crystalline layers. Gelders et al. (2005b) concluded that such a fringed micellar organization also existed in short chain semienzymically synthesized amylose complexes. Most authors agree that amylose helices are oriented perpendicular to the plane of the lamellae (Buléon et al., 1984; Jane and

Robyt, 1984; Manley, 1964; Whittam et al., 1989; Yamashita, 1965; Yamashita and Monobe, 1971). However, how these lamellae are organized further, is not clear. Whether the crystals are oriented into 10 nm thick hexagonal platelets (Buléon et al., 1984; Jane and Robyt, 1984; Whittam et al., 1989; Zobel et al., 1967), or spherically or radially stacked (Godet et al., 1996; Shogren et al., 2006; Stute and Konieczny-Janda, 1983) is unclear. Heinemann et al. (2003, 2005) have even described three types of spherocrystals, each for different lactones. Different particle forms, depending on the number of glucose units per turn, have also been observed: one spherical/lobed for the V7-helices formed with bulkier ligands and another torus-shaped for the V6-amylose helices (Peterson et al., 2005). Lesmes et al. (2009) reported a rod-like or ellipsoid structural organization of V-amylose with a length of a few to several hundreds of nanometres and a thickness of a few nanometres, depending on the production method and the degree of unsaturation of the complexing ligand. 3. Formation of amylose-inclusion complexes Different methods for formation of amylose-inclusion complexes have been described. In general, these can be subdivided into three main categories, either (i) starting from starch and ligands, or (ii) starting from amylose and ligands, or (iii) synthesizing amylose in the presence of the ligands. Depending on the method used, the characteristics of the obtained amylose-inclusion complexes differ. The complexes are more pure and monodisperse when using methods [(ii) or] (iii). By adding ligands to a starch dispersion and heating, in situ complexation can occur as soon as starch gelatinizes. Amylose chains need to have acquired enough mobility to interact with ligands (Evans, 1986) which must also be in the right phase (Eliasson, 1994). For lipids, e.g., the liquid crystalline phase is suited best for amylose complexation (Krog, 1981; Krog and Jensen, 1970). The solvent used influences the solubility of both starch and additive. Small emulsifiers can enter the starch granule and complex internally with amylose (Ghiasi et al., 1982). However, complexation at the granule surface, with amylose leaching out during gelatinization, has also been described (Eliasson, 1985). Either way, amyloseelipid complexes are formed during the processing of starch-based systems such as during and after heating in an autoclave (Wulff et al., 2005), during extrusion (Medcalf et al., 1968), parboiling (Derycke et al., 2005; Lamberts et al., 2009) and bread making (Krog and Jensen, 1970; Stampfli and Nersten, 1995). Interestingly, Larsson and Miezis (1979) proposed that complexation of partially digested amylose molecules with monoacyl glycerols occurred in the small intestine. Purer amylose-inclusion complexes can be formed by dissolving amylose, extracted from starch, in DMSO or an alkaline solution,

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and mixing it with the desired ligand. In the DMSO-based synthesis procedure, amylose is dissolved in hot DMSO which is then diluted with boiling water. After equilibration of the suspension at the desired temperature, the ligand, dissolved in a hot alcoholic or aqueous suspension, is added dropwise. The mixture is kept at an elevated temperature for a certain time, after which it is left to cool slowly such that the resulting amylose-inclusion complexes precipitate (Biliaderis et al., 1985; Galloway et al., 1989; Jane and Robyt, 1984; Karkalas and Raphaelides, 1986; Raphaelides and Karkalas, 1988). In the alkaline synthesis method, the amylose is dissolved in 0.01 M potassium hydroxide with the subsequent addition of the ligand in the same solution. After neutralization, the mixture is cooled slowly overnight (Karkalas et al., 1995; Karkalas and Raphaelides, 1986; Kitahara et al., 1996; Raphaelides and Karkalas, 1988). The extracted or leached amylose chains that are formed by both methods are probably too long to form amylose complexes, and, as such, ‘loose ends’ may be present. Depending on the origin and properties of the amylose, both methods result in rather polydisperse amylose-inclusion complexes, i.e. they have widely varying DPs (Gelders et al., 2004). However, the literature on these two synthesis methods does not clarify whether, and to what extent, complex formation between a short amylose chain and a ligand occurs. Amylose-inclusion complexes can also be formed by in situ synthesis of amylose using potato phosphorylase. This enzyme elongates a short chain primer, such as maltohexaose or maltoheptaose, by transferring the glucose entity of glucose-1-phosphate to the non-reducing end of the primer. When this reaction occurs in the presence of a suitable ligand, the amylose chains that are formed, complex with the ligand, followed by precipitation (Gelders et al., 2005b; Kadokawa et al., 2001). For polyesters or single-wall carbon nanotubes, amylose is synthesized around the long ligand (Kadokawa et al., 2003; Yang et al., 2008). Kadokawa et al. (2003) believe this to happen in a ‘vine-twining’ way, i.e. complexation occurs during elongation of the primer. For shorter ligands, such as lipids, the precise interactions between amylose and the ligand are not yet clear. However, a hypothesis by Putseys et al. (2009) suggests polymerization to occur until an amylose chain is formed that is sufficiently long to complex a first lipid molecule. Afterwards, elongation of the extended primer continues, together with subsequent complexation of more lipid molecules. Once enough lipids have been complexed, the amyloseelipid complex becomes insoluble, precipitates and the enzymic elongation reaction ends. This semienzymic synthesis method results in short chain monodisperse amorphous type I amyloseelipid complexes. 4. Thermodynamic characteristics of amyloseelipid complexes Amylose complexes can be divided into two separable states: less ordered type I and semicrystalline type II amylose-inclusion complexes. Type I complexes are formed at or below 60  C and result in the formation of individual helical segments which are randomly oriented (Biliaderis and Seneviratne, 1990; Karkalas et al., 1995). Low temperatures result in a high nucleation rate, leading to helices freezing rapidly into their position, resulting in a low, if any, level of crystallinity (Biliaderis and Seneviratne, 1990). These complexes dissociate between 95 and 105  C (Galloway et al., 1989; Karkalas et al., 1995). Type II complexes, on the other hand, are obtained by heating the mixture of amylose and ligand at higher temperatures (at least 90  C) (Karkalas et al., 1995). Under these conditions, the nucleation rate is low, allowing sufficient propagation. This results in

241

structures with well defined crystalline regions (Biliaderis and Galloway, 1989). Type II complexes can be further subdivided into type IIa en type IIb complexes. The semicrystalline type IIa complexes melt around 115  C (Biliaderis et al., 1986b; Galloway et al., 1989). These complexes can be further annealed to form even more thermostable type IIb amylose complexes by partial melting and recrystallization (Karkalas et al., 1995). For the semienzymically synthesized complexes, the type I complexes that are obtained can be transformed into type II complexes by dissociation and crystallization of the former (Putseys et al., 2010). Kugimiya et al. (1980) first suggested the possibility of a transformation towards more crystalline complexes that dissociate at higher temperatures. This has been reported for complexes as two DSC-endotherms separated by an exotherm (Biliaderis et al., 1985). The exothermal transition indicates that, after dissociation of type I complexes, the helices acquire enough mobility to align around the remaining helices, acting as nuclei (Biliaderis et al., 1986a). This results in better ordered crystals. However, not all amylose and ligands can go through this crystal perfection. Amylose chains can be too short, or ligands too voluminous to form type II semicrystalline amyloseelipid complexes (Gelders et al., 2005a; Snape et al., 1998), to allow annealing of type I complexes into semicrystalline type II complexes. The endothermic enthalpies of both amylose complexes of types I and type II have been described as being very similar and rather independent of the lipid chain length (Biliaderis and Galloway, 1989; Godet et al., 1995a; Kowblansky, 1985; Putseys et al., 2010). However, one would logically assume that, apart from the energy needed to disrupt the forces between the amylose and the ligand, extra energy is necessary for melting of the crystal lattice in semicrystalline complexes. This energy is independent of the lipid chain length (Whittam et al., 1989). Godet et al. (1995a) explained the similarity in enthalpies for type I and type II complexes as resulting from the fact that the energy required for helix packing would be negligible compared to that necessary for dissociation and uncoiling of the helix. Kowblansky (1985) was one of the first to show the influence of the complexation conditions on complex crystallinity and also showed similar enthalpies for both types of complexes. She assumed that they were stabilized by the same forces, and attributed the similar endothermic enthalpies to a difference in entropy between the two types of amylose complexes. As the two complexes have similar melting or dissociation enthalpies and the melting temperature of type II complexes is much higher than the dissociation temperature of their amorphous type I counterparts, Biliaderis and Galloway (1989) deduced that the entropy of type II complexes must be much lower than that of type I complexes. It may seem suprising that the entropy change for type I complexes would be greater than for type II. However, upon melting of the crystalline type II complexes or dissociation of their randomly ordered type I counterparts, the two forms may not reach the same end state or less material may participate in the type II complexes than in the type I complexes. 5. Impact of amylose chain length, lipid characteristics and concentration on complex properties 5.1. Amylose chain length The DP of amylose impacts the properties of the complexes. Rutschmann et al. (1989) pointed out that, for complexation of menthone, the longer the amylose chains, the more stable the complexes that are formed. According to Godet et al. (1993a), long amylose chains can complex more lipid molecules and, hence, give

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rise to crystals with higher melting temperatures. The melting temperature, stability, crystallite size and level of organization of amyloseelipid complexes increase generally with the length of the amylose chain (Gelders et al., 2004; Godet et al., 1995a, 1996). However, if the amylose chains are too long, this leads to conformational disorders, resulting in faults in the crystal structure (Gelders et al., 2004). On the other hand, if too short, they can disturb the crystal formation. Godet et al. (1995a) stated that amylose chains of DP 20 are too short to complex with a lipid and Gelders et al. (2004) observed that amylose of DP 60 cannot be arranged into more ordered type II amyloseelipid complexes. 5.2. Lipid type, chain length and unsaturation Not only the amylose fraction, but also the lipid chain length, degree of unsaturation and identity of the polar head impact the complex properties. Several authors have described dissociation temperatures of amyloseelipid complexes to increase with the length of the aliphatic chain of the lipid (Eliasson and Krog, 1985; Gelders et al., 2004, 2006; Godet et al., 1995a, 1996; Raphaelides and Papavergou, 1991; Stute and Konieczny-Janda, 1983; Tufvesson et al., 2003a, b). They attributed this to the lower hydrophilicity of longer lipid chains, and the resulting stronger preference to reside within the hydrophobic helix cavity. The longer hydrocarbon chain allows more hydrophobic interactions with the interior of the helix, requiring higher temperatures to break these bonds (Raphaelides and Karkalas, 1988). Lipids with chain lengths of 10 or less carbon atoms appear to be too short to induce complex formation (Godet et al., 1995b; Karkalas and Raphaelides, 1986; Lebail et al., 2000; Tufvesson et al., 2003b), presumably because they are too soluble in the aqueous environment to be retained properly in the hydrophobic helix cavity. There is, however, disagreement on the identity of the best complexing lipid. Some suggest that a lipid chain length with 14 carbon atoms is best for complex formation (Bhatnagar and Hanna, 1994a; Hoover and Hadziyev, 1981; Krog, 1971) while others have found 16 or 18 carbon atoms to be the preferred lipid chain length (Krog, 1971; Lagendijk and Pennings, 1970). The number of double bonds in the aliphatic lipid chain also has a distinct influence on the thermal properties of the amyloseelipid complexes. The higher the degree of unsaturation, the lower the thermal stability of the resulting complex (Eliasson and Krog, 1985; Karkalas et al., 1995; Krog, 1971; Lagendijk and Pennings, 1970; Raphaelides and Karkalas, 1988; Raphaelides and Papavergou, 1991; Stute and Konieczny-Janda, 1983; Yamada et al., 1998; Zabar et al., 2009). However, the quasi-linear trans-unsaturated lipids can be complexed rather well in the helix cavity. cis-Unsaturated lipids, on the other hand, have a kink in their lipid chain and are, thus, subject to steric hindrance inside the helix cavity (Lagendijk and Pennings, 1970). Yamada et al. (1998) suggested this to result in only partial inclusion in the helix. However, this seems rather doubtful since the carbon atoms adjacent to the double bond can still rotate freely, resulting in a more or less linearly oriented chain (Karkalas et al., 1995; Karkalas and Raphaelides, 1986; Raphaelides and Karkalas, 1988). It thus seems more probable that less linear ligands require a larger helix cavity (as is the case for V6II or V6III), as suggested by Karkalas et al. (1995) and Putseys et al. (2009). The type of lipid also affects the characteristics of the complex. Fatty acids, mono and diacyl glycerols can complex with amylose, whereas triacyl lipids cannot (Eliasson, 1994). Tufvesson et al. (2003a, b) compared the complex forming ability of fatty acids and monoacyl glycerols and reported that complexes with fatty acids were more heat stable than those with monoacyl glycerols. This has been confirmed by Gelders et al. (2005b) who attributed this to the ability of fatty acids to protrude deeper into the helix

cavity, and thus be stabilized to a greater extent than monoacyl glycerols. However, only monoacyl glycerols with a short aliphatic chain (10e12 carbon atoms) can form semicrystalline complexes easily, whereas fatty acids cannot (Tufvesson et al., 2003a, b). 5.3. Ligand concentration and solubility Both ligand concentration and solubility determine the degree of complex formation (Tang and Copeland, 2007). Several authors state that a complex only precipitates when its amylose chain is saturated (Eliasson, 1994; Raphaelides and Karkalas, 1988). The ratio of ligand to amylose is, thus, a decisive factor influencing the characteristics of the amylose-inclusion complex. Lebail et al. (2000) reported that 10% lipid was sufficient for complexing all amylose molecules. However, this is not always possible due to steric hindrance. In this case, the uncomplexed lipid molecules can be trapped in the interstitial space between the helices. At lower ligand concentrations, amylose can also adopt a double helix conformation, leading to competition with the single helix conformation required for inclusion complexes. Under specified reaction conditions, Medcalf et al. (1968) reported that 0.3% (w/w) glycerol monostearate was sufficient to induce a V-amylose conformation. Rutschmann et al. (1989) investigated the influence of menthone concentration on complexation. They observed that longer amylose chains are the first to complex menthone at low ligand concentration. At higher ligand concentrations, shorter amylose chains also participate in complex formation. Such high concentrations lead to less specific binding, with amylopectin also able to participate in inclusion complex formation (Rutschmann and Solms, 1990). For complexation of ionic ligands, such as dodecyltrimethyl ammonium bromide, higher concentrations of the ligand lead to more difficult packing, and thus, to complexes with lower dissociation temperatures due to repulsion of the ionic charges (Villwock et al., 1999). The ligand needs to be in solution to interact with amylose. Therefore, its solubility is a decisive factor in the complexation with amylose. The presence of flavour compounds with a relatively high solubility may therefore be sufficient to induce complex formation, resulting in V7-amylose. For flavour molecules of low solubility, however, a stable complexation only takes place in the presence of lipids, inducing a V6-conformation for the ternary complex (Tapanapunnitikul et al., 2008). 6. Hydrolysis In general, the hydrolysis of amylose-inclusion complexes can be regarded as a two-step process. First, a rapid hydrolysis of the amorphous areas, i.e. the amylose linkers between the helices, occurs (Galloway et al.,1989; Jane and Robyt,1984). The second stage is slower and involves degradation of the amylose-inclusion complexes (Godet et al., 1996). Hydrolysis of complexes is influenced by both the amylose and lipid chain length. Resistance to both enzyme (e.g. pancreatic a-amylase) and acid hydrolysis increases with amylose DP and lipid chain length (Gelders et al., 2005a). The rate of in vitro amylose hydrolysis also depends on the enzyme activity. For low activities, e.g. in the case of salivary enzymes, only amorphous material is degraded. Thereafter, the remaining complexes can aggregate, resulting in more perfectly organized crystallites (Heinemann et al., 2005). In the gastrointestinal tract, enzymes are more active and present in higher concentrations than in the oral cavity. They can hydrolyze predominantly type I amylose-inclusion complexes to a greater extent, also due to the longer reaction times (Heinemann et al., 2005; Seneviratne and Biliaderis, 1991). In the digestive tract, pancreatin can release included compounds. Complexes can, thus,

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be used as a tool for slow release of desired compounds in the gastro-intestinal system (Conde-Petit et al., 2006). However, not all enzymes can degrade amylose-inclusion complexes and complexation renders amylose resistant to both b-amylase (Kim and Robinson, 1979) and glucoamylase (Kitahara et al., 1996). Although significant hydrolysis of amyloseelipid complexes by a-amylases has been reported (Nebesny et al., 2004), amyloseinclusion complexes are considered to be generally less enzyme degradable than amorphous amylose. The decrease in in vitro susceptibility towards a-amylases can be explained by the low solubility of the complexes and the steric hindrance they exert (Holm et al., 1983). However, in the presence of thermostable enzymes and at high temperatures, the complexes are hydrolysed fully and in vivo experiments also indicate complete, but somewhat slower, hydrolysis (Holm et al., 1983; Kwasniewska-Karolak et al., 2008). Apart from the restriction of granule swelling (cf. infra), which also lowers starch susceptibility towards enzymes, the inclusion complexes formed are more resistant to enzyme digestion than non-complexed amylose (Hanna and Lelievre, 1975; Siswoyo and Morita, 2003). This is in line with Vasanthan and Hoover (1992) who observed that defatting increases the accessibility of amylose towards enzymic attack. Lipid properties influence the digestibility of amyloseelipid complexes, since their hydrolysis depends on lipid chain lengths and degree of unsaturation (Eliasson and Krog, 1985; Guraya et al., 1997; Holm et al., 1983; Raphaelides and Papavergou, 1991; Stute and Konieczny-Janda, 1983). The structural characteristics of the complexes also strongly influence their degradability, with more highly crystalline amylose-inclusion complexes having lower digestibilities (Kwasniewska-Karolak et al., 2008; Seneviratne and Biliaderis, 1991). Type IIa and IIb complexes are sometimes even considered as part of the resistant starch fraction (Seneviratne and Biliaderis, 1991). The single helix conformation lowers the amylose hydrolysis rate, with glucose units being absorbed more slowly, resulting in a lower blood insulin response. These lower digestibility rates suggest amylose complexes to be well suited for the diet of diabetic patients (Murray et al., 1998; Takase et al., 1994). 7. Functionality 7.1. In situ amyloseelipid complex formation Starchelipid interactions decrease starch swelling capacity (Biliaderis and Tonogai, 1991; Lauro et al., 2000; Mira et al., 2007; Tester and Morrison, 1990), solubility and granule disruption (Bhatnagar and Hanna, 1994b; Eliasson et al., 1981b; Galloway et al., 1989; Ghiasi et al., 1982; Larsson, 1980). It also increases the gelatinization temperature (Eliasson et al., 1981a; Melvin, 1979). Additional exogenous pure lipids can form an insoluble layer around the granules, preventing the entry of water (van Lonkhuysen and Blankestijn, 1976). However, in situ complexation between amylose and these lipids, either at the surface or inside the granule, also contributes to these phenomena, mostly by preventing leaching of soluble carbohydrates (Hoover and Hadziyev, 1981; Lauro et al., 2000). The longer the lipid chain length and the higher its concentration, the more the pasting and gelatinization of the starch suspension are delayed (Eliasson et al., 1981a; Raphaelides and Georgiadis, 2006). The impact of amylose complexing ligands on starch gel formation depends on ligand chain length and concentration, on the amylose content of starch and on the water content of the system (Conde-Petit and Escher, 1995; Mitchell and Zillmann, 1951; Nuessli et al., 1995; Richardson et al., 2003). Different effects of ligand addition on starch viscosity and gelation have been

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described. On the one hand, the addition of inclusion components can restrict granule swelling and subsequently decrease peak and final viscosities (Evans, 1986; Medcalf et al., 1968; Osman and Dix, 1960; Ozcan and Jackson, 2002; Senior and Hamori, 1973; Zhou et al., 2007). The extent of this change depends on the chain length and polarity of the ligand (Osman and Dix, 1960). On the other hand, amylose-inclusion complexes may act as intergranular junction zones that induce gelation and, thus, lead to a viscosity increase (Conde-Petit and Escher, 1992; Evans, 1986; Heinemann et al., 2001, 2003; Nuessli et al., 1995, 2000; Richardson et al., 2003). Amylopectin outer branches can also complex with the lipid, increasing the rigidity of the granule remnants and, hence, the viscosity of the starchelipid gel (Biliaderis and Tonogai, 1991; Conde-Petit and Escher, 1992). It is, however, not clear whether the increase in viscosity upon addition of a starch-complexing ligand is observed solely during the cooling phase or also for the final viscosity. Osman and Dix (1960) noted a viscosity peak during cooling of a starch gel, which disappeared if the starch was defatted prior to heating and cooling, and suggested this increase to be due to complex formation between amylose and lipids. This was confirmed by Takahashi and Seib (1988). These authors observed a strong increase in viscosity during cooling after addition of 2.0% (w/w) wheat starch lipids prior to heating the aqueous starchadditive mixture. This effect was less pronounced when lipids were only added after gelatinization of the starch suspension. Conde-Petit and Escher (1995) attributed this discrepancy to the concentration of the starch gel. At low starch concentration, addition of emulsifiers or flavour components and their subsequent complexation with amylose induces gelation. The intergranular network, composed of amylose-inclusion complexes, provides physical cross-links between granule remnants, hence increasing gelation and viscosity. In concentrated starch gels, however, complexation of amylose, either by emulsifiers or flavour components, restricts crystallization during cooling, resulting in weaker starch gels when ligands are present. Complex formation restricts the solubility and mobility of amylose. This, in combination with steric hindrance brought about by complexation, prevents amylose double helix formation and crystallization (Gudmundsson and Eliasson, 1990; Lebail et al., 2000; Zhou et al., 2007). Amylose double helices might function as nuclei for retrogradation by cocrystallizing with amylopectin (Gudmundsson and Eliasson, 1990). Retrogradation is here defined as recrystallization of the amylopectin side chains (Delcour and Hoseney, 2010). The addition of lipid may impact this process in two ways. Firstly, amyloseelipid complexation can prevent the cocrystallization with amylopectin. Secondly, lipids can also complex with the outer branches of amylopectin and, as such, inhibit retrogradation in a more direct way (Eliasson and Ljunger, 1988; Gudmundsson and Eliasson, 1990; Huang and White, 1993; Nakazawa and Wang, 2004). The impact of surfactants and/or emulsifiers on bread firming has been discussed frequently. There is, however, no agreement on whether these additives decrease the initial crumb hardness or lower bread firming rate. The latter view is supported by several authors (Krog, 1971; Kulp and Ponte, 1981; Lagendijk and Pennings, 1970; Stauffer, 1996). Pisesookbunterng and D'Appolonia (1983) also observed that, although initial bread firmness was unaltered, these surfactants influenced the firming rate negatively. Others, however, have reported a lower initial crumb hardness for bread supplemented with emulsifiers (Delcour and Hoseney, 2009; Schoch, 1965), considering the firming rate to be similar to that of breads without any additive. Valjakka et al. (1994), on the other hand, claim that both effects are responsible for the improvement of the bread crumb quality upon addition of emulsifiers.

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The addition of lipids to a system containing starch invokes a competition between amyloseelipid complexation, on the one hand, and amylose crystallization, on the other (Czuchajowska et al., 1991; Eerlingen et al., 1994; Eliasson and Wahlgren, 2000; Szczodrak and Pomeranz, 1992; Tufvesson et al., 2001). The crystalline amylose consists of double helices and is often the predominant resistant starch fraction after heating and cooling a starch sample. Most of the ligands suitable for complexation induce amylose single helix formation and complexation. However, hydroxylated lysolecithin stimulates amylose crystallization, as pointed out by Czuchajowska et al. (1991). The amylose-inclusion complexes that are formed are less easily degraded by enzymes, and can be regarded as part of the resistant starch fraction (Crowe et al., 2000; Cui and Oates, 1999; van Lonkhuysen and Blankestijn, 1976; Seneviratne and Biliaderis, 1991; Tufvesson et al., 2001). Fresh starch samples containing complexing ligands are, thus, hydrolysed to a lesser extent than the samples without additive. When the samples are left to retrograde for some days, the additive containing samples are hydrolysed to a greater extent, since, in this case, less resistant starch has been formed (Cui and Oates, 1999). In conclusion, even though less resistant starch is formed upon addition of an amylose complexing ligand, the complexes formed are themselves more slowly degradable than amorphous amylose and even sometimes considered as dietary fibre (Larsson, 1979). 7.2. Amylose complexes 7.2.1. Addition of complexes Amyloseelipid complexes have only very sporadically been used as additives. According to Eliasson et al. (1994), however, they only influence retrogradation positively after prior heating, i.e. after they have been heated and, thus, dissociated, prior to addition to the starch containing system. The lipid should, thus, be made available for interaction to impact starch containing systems. Gudmundsson (1992) added amyloseecetyltrimethylammonium bromide complexes to starch and amylopectin systems and noticed that the complexes did not decrease retrogradation significantly, but mainly diluted the starch system. Some sterical hindrance, caused by the complex, may result in slower crystallization of the amylopectin outer branches, but this effect was minor when compared to that of the uncomplexed ligand. Gelders et al. (2006) used a combination of pure lipid and amyloseelipid complexes as additives in starch gels. As opposed to only pure emulsifiers, these additives resulted in gels with a stable hot and cold paste viscosity. The authors attributed this effect to the liberation of the complexed ligand during heating. In contrast to these authors, Putseys et al. (2010) used defatted amyloseelipid complexes. In this way, the non-complexed lipid molecules were removed. The addition increased final viscosity in a Rapid Viscoanalyzer (RVA) heating and cooling cycle. The latter authors attributed this to the short amylose chains liberated from the amyloseelipid complexes, which subsequently induced amylose double helix interactions. In this way, the resulting network was strengthened. A possible role for amyloseelipid complexes as a tool for controlled release of both lipids and short amylose chains has, thus, been suggested. 7.2.2. Protection against oxidation and impact on flavour perception and release The flavour of starch containing products can be influenced negatively by oxidation (Nebesny et al., 2002). Amylose complexation can protect oxygen-sensitive molecules, such as unsaturated fatty acids, e.g. conjugated linoleic acid (CLA) (Lalush et al., 2005; Szejtli and Bankyelod, 1975), or vitamins (Heinemann

et al., 2005) against oxidation. Encapsulation into amylose complexes can also be used to stabilize volatile flavour compounds, such as aromatic molecules, thereby increasing their retention (Arvisenet et al., 2002a, b; Wulff et al., 2005). This way, however, also the perception of the aroma compound is influenced (Heinemann et al., 2005). Lalush et al. (2005) pointed out that complexation of CLA not only stabilises the ligand against oxidation, but, as such, also creates a vehicle for controlled release of the ligand in the intestine (instead of, e.g., the stomach). Further elaboration on this flavour complexing aspect can be found in an excellent review by Conde-Petit et al. (2006). 8. Conclusions Synthesis methods of amylose-inclusion complexes either start from starch or amylose, mixed with the desired ligand, or from synthesis of amylose chains in the ligand's presence. The temperature at which the synthesis is performed defines the type of complex: at low temperature, less ordered type I complexes are formed, whereas, at higher temperature, semicrystalline type II complexes are obtained. Lipid characteristics, such as the length of its aliphatic chain, its degree of unsaturation or the nature of its polar head, are important in all complexes synthesized with any of the three methods, whereas amylose characteristics only impact complexes formed with the methods starting from either starch suspensions or dissolved amylose [as in synthesis categories (i) and (ii), respectively]. The dimensions of the resulting amyloseinclusion complexes vary depending on the ligand properties, but general categories can be made, depending on the amount of glucose units per turn and the location of the ligand. When ligands, and more specifically lipids, are added to a starch system, complexes can be formed in situ impacting starch properties, such as gelatinization, viscosity, gelation, retrogradation and hydrolysis strongly. Acknowledgements This publication is in part financially supported by the European Commission in the Communities 6th Framework Programme, Project HEALTHGRAIN (FOOD-CT-2005-514008). It reflects the author's views and the Community is not liable for any use that may be made of the information contained in this publication. This research was also conducted in the framework of research project G.0427.07, financed by the Fund for Scientific Research e Flanders (FWO), Brussels, Belgium and is part of the Methusalem programme “Food for the Future” at the K.U.Leuven. The authors thank Professor Bart Goderis (Katholieke Universiteit Leuven, Belgium) and Professor Costas Biliaderis (Aristotle University, Thessaloniki, Greece) for helpful discussions. References Arvisenet, G., Le Bail, P., Voilley, A., Cayot, N., 2002a. Influence of physicochemical interactions between amylose and aroma compounds on the retention of aroma in food-like matrices. Journal of Agricultural and Food Chemistry 50, 7088e7093. Arvisenet, G., Voilley, A., Cayot, N., 2002b. Retention of aroma compounds in starch matrices: Competitions between aroma compounds toward amylose and amylopectin. Journal of Agricultural and Food Chemistry 50, 7345e7349. Banks, W., Greenwood, C.T., 1971. Amylose: a non-helical biopolymer in aqueous solution. Polymer 12, 141e145. Bhatnagar, S., Hanna, M.A., 1994a. Amylose lipid complex-formation during singlescrew extrusion of various corn starches. Cereal Chemistry 71, 582e587. Bhatnagar, S., Hanna, M.A., 1994b. Extrusion processing conditions for amyloseelipid complexing. Cereal Chemistry 71, 587e593. Biliaderis, C.G., Galloway, G., 1989. Crystallization behavior of amylose-V complexes - Structure property relationships. Carbohydrate Research 189, 31e48. Biliaderis, C.G., Page, C.M., Maurice, T.J., 1986a. Nonequilibrium melting of amyloseV complexes. Carbohydrate Polymers 6, 269e288.

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