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World J Microbiol Biotechnol (2011) 27:341347 DOI 10.

1007/s11274-010-0464-x

ORIGINAL PAPER

Lupin as primary protein source in young broiler chicken diets: Effect of enzymes preparations catalyzing degradation of non-starch polysaccharides or phytates
Boguslaw Olkowski

Received: 10 December 2009 / Accepted: 24 May 2010 / Published online: 8 June 2010 Springer Science+Business Media B.V. 2010

Abstract This work examined the effects of three enzyme preparations (A,B,C) directed towards degradation of Non Starch Polysaccharides (NSP) and one targeting phytates (D) on performance traits in broilers fed maize meal basal diets containing 400 g/kg of yellow lupine seeds (LM). A soybean meal (SBM) based diet served as a reference control. Growth rate, coefcients of total tract apparent digestibility (CTTAD) of organic matter, protein and energy, as well as morphometric measurements of selected sections of gastrointestinal tract (GIT) were determined. In comparison to chickens fed the SBM diet, chickens fed the LM diet consumed less feed, had considerably lower body weight gain, as well as lower CTTAD of measured nutrients and energy. Also the GIT relative weight and length were increased within the group fed the LM diet. Addition of each NSP degrading enzymes (A,B,C) to the LM diet increased feed intake and decreased size of GIT organs (all p \ 0.05). Addition of enzymes A or B increased (p \ 0.05) growth rate of chicks, whereas only enzyme B increased fed efciency (p \ 0.05) and tended to slightly improve CTTAD of nutrients. The addition of enzyme D did not have any effect on feed intake, growth rate or CTTAD. This study indicates that a diet containing high levels of LM is detrimental to feed intake and condition of the digestive tract of young broilers, and thus affects their performance. However, when the LM diet is supplemented with suitable enzyme preparations, performance parameters are not different from those obtained with SBM.

Keywords Yellow lupine Broiler Enzyme Non starch polysaccharides Phytates

Introduction The use of lupine seed meal as a protein source for poultry has been a subject of various investigations for some time. Previous research provided divergent ndings on the tolerance of poultry to lupine based diets. For instance, Olver and Jonker (1997) indicated that the lupine meal may be used up to 400 g/kg in broiler diets, or even completely replace SBM. In contrast some authors (Brenes et al. 2002; Olkowski et al. 2005; Steenfeldt et al. 2003) argued that the inclusion of high levels of LM may have negative effects on chicken growth. Historically, the main problem limiting utilization of lupines in animal feeds was associated with the content in toxic alkaloids. Sparteine, lupinine, and ammodendrine are typical alkaloids for cultivars of yellow lupine, but there are some cultivars (called gramine cultivars) where gramine dominates. Typical alkaloids prole for yellow lupine is dominated by sparteine (up to 60%) and lupinine (up 40%), whereas in some cultivars gramine may constitute up to 80% of all alkaloids. Total alkaloids of yellow lupine seeds currently registered in Poland ranged from 0.0093 to 0.0254% (Manczak et al. 2007). There is a general consensus that levels of the toxic alkaloids in the modern varieties of lupines are negligible (Petterson 2000, Manczak et al. 2007), and from a nutritional toxicology stand point lupines are safe for chickens. However, the use of lupine seeds is still limited in poultry nutrition since it contains high quantities of non starch polysaccharides (Kluge et al 2002). The non starch

B. Olkowski (&) Faculty of Life Sciences, Institute of Bioengineering and Animal Breeding, University of Podlasie, ul. B. Prusa 14, 08-110 Siedlce, Poland e-mail: b.olkowski@ap.siedlce.pl

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World J Microbiol Biotechnol (2011) 27:341347 Table 1 Energy (MJ/kg), nutrients and anti-nutrients (g/kg) content in yellow lupine seeds (Dry matter based) Item Gross energy Metabolizable energy (AMEn) Crude protein Crude fat Crude ber Crude ash Cysteine Aspartic acid Methionine Threonine Serine Glutamic acid Proline Glycine Alanine Valine Isoleucine Leucine Phenylalanine Histidine Lysine Arginine Tyrosine Total alkaloids Lectins Total phytates Condensed tannins
a a

polysaccharides (NSP) of lupines are of major concern because they have a detrimental effect on gastrointestinal physiology and decrease utilization of nutrients and energy, which may signicantly affect performance parameters (Brenes et al. 2003; Hughes et al. 1999; Steenfeldt et al. 2003). Other compounds of anti-nutritional concern in lupine seeds are phytates. Phytate content in yellow lupine (Lupinus luteus L.) may be as high as 3040 g/kg (Birk 1994; Muzquiz et al. 1989). Phytates caused signicant reduction in chick performance (Shan and Davis 1994). Their major detrimental effects of phytates include reduction of the bioavailability of minerals, decreased activity of digestive enzymes, and the lowered availability of other dietary components (Ravindran et al. 2000; Sandberg 2002). The negative effects of NSP and phytates in broilers can be alleviated by adding dietary enzymes degrading those compounds (Choct 2006). Most trials with enzymes for lupine meal diets for poultry used Lupinus angustifolius L. and Lupinus albus L. (Annison et al. 1996; Brenes et al. 2002; Mieczkowska et al. 2004, 2005; Naveed et al. 1998, 1999; Steenfeldt et al. 2003). On the other hand, there is a paucity of information regarding supplementation of enzymes in the diet based on Lupinus luteus. Lupines usually contain considerably higher levels of NSP than SBM, other legumes, or cereals (Bach Knudsen 1997). In addition, in comparison to SBM lupine seeds contain the highest concentration of cellulose and verbascose and monosugars such as galactose, arabinose and xylose (Bach Knudsen 1997, van Barneveld 1999). Of note, among the three main cultivated lupine species (L. albus L., L. angustifolius L., L. luteus L.) yellow lupine has the highest content of protein and the lowest NSP content, with an amino acid prole nearly similar to SBM. Therefore, yellow lupine variety shows the strongest potential for wide use in broiler nutrition (Petterson 2000). Accordingly, the present study examined the effects of three commercial enzyme preparations with specic activity degrading NSP, and one with phytate degrading activity in diets containing yellow lupine as a main source of protein in broiler diets.

Content 19.9 9.9 467.9 41.6 141.3 46.7 9.8 46.5 3.4 15.0 22.2 105.7 19.1 17.9 14.9 16.8 16.4 35.8 17.8 14.6 21.6 54.1 13.5 0.7 1.0 21.6 ND

AMEn calculations were based on chemical analysis of feedstuffs using formula according to European Tables of Energy Values of Feeds for Poultry (WPSA 1989). ND not detectable

Materials and methods Feeds Seeds of sweet variety of yellow lupines (LM) were used as a primary protein source in substitution of soybean meal (SBM). Energy content and chemical composition of LM are shown in Tables 1 and 2. The experimental diets were based on maize meal and 365 g/kg of SBM, or 400 g/kg of LM. The test diets included LM without enzyme or

supplemented with four (A,B,C,D) commercial feed enzymes. The names, level and origin (manufacturer) of used enzymes, and their activities units per gram crude product according to the producers declaration were as follows: Enzyme A, 0.1 g/kg (Roxazyme G; F. Hoffmann La Roche AG, Basel, Switzerland) contained 8,000 units of cellulase, 18,000 units of b-glucanase, and 26,000 units of b-xylanase activities; Enzyme B, 1 g/kg; (Energex CT; Novo Nordisk A/S, Bagsvaerd, Denmark) contained 75 units of b-glucanase, 15,000 units of hemicellulase, 10,000 units of pectinase, and 400 units of endoglucanase; Enzyme C, 1 g/kg (Avizyme 1500; Finnfeeds International, Marlborough, England, Danisco Animal Nutrition) contained 8,000 units of protease, 2,000 units of a-amylase and 6,000 units of b-xylanase, Enzyme D, 0.25 g/kg (Phytase Nowo CT; Novo Nordisk A/S, Bagsvaerd, Denmark) contained phytase 2,500 FYT units.

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World J Microbiol Biotechnol (2011) 27:341347 Table 2 The content (g/kg) of soluble and insoluble fractions of mono sugars, uronic acids and total non starch polysaccharides (NSP) in yellow lupine seeds (Dry matter based) Item Form of sugars Soybean meal Soluble Rhamnose Fucose Arabinose Xylose Mannose Galactose Glucose Uronic acids Total NSP 0.4 0.2 10.0 5.8 2.0 21.2 19.8 15.8 75.1 Insoluble 0.7 0.7 24.7 20.4 1.5 31.0 65.2 21.0 165.1 Total 1.1 0.9 34.8 26.3 3.5 52.2 85.0 36.7 240.2 Yellow lupine meal Soybean oil Dicalcium phosphate Limestone Premixb L-Lysine HCL DL-methionine Salt Maize meal Nutritional value of diets Metabolisable energy (AMEn)c 12.2 207.6 27.3 9.5 4.4 21.0 12.2 8.8 92.5 9.6 12.3 206.6 66.3 10.0 4.2 30.0 12.2 9.0 129.1 13.9 Crude protein Crude ber Calcium Available phosphorus Linoleic acid Lysine Methionine?Cystine Non starch polysaccharides Phytates
a

343 Table 3 Composition and nutritional details of soya bean (SBM) and lupine basal (LM) diets (g /kg, energy MJ/kg) Item SBM 365.0 40.0 11.8 21.6 5.0 2.0 2.4 3.0 Up to 1,000 LMa 400.0 60.0 12.1 20.9 5.0 3.5 2.5 3.0 Up to 1,000

All diets were balanced for metabolizable energy (AMEn), crude protein, and methionine and lysine (using synthetic amino acids), Ca, P and were supplemented with mineral-vitamin premix for broilers. The level of AMEn in diets was equilibrated with soya oil. AMEn calculations in feedstuffs were based on chemical analysis using formula according to European Tables of Energy Values of Feeds for Poultry (WPSA 1989). Composition, nutritional value, and the content of NSP and phytates in diets are listed in Table 3. It is noteworthy that substitution of SBM with LM in diet resulted in higher levels of NSP and phytates in LM based diets in comparison to SBM diet. Birds and measurements One day old male commercial broiler chickens (Hybro G) were randomly assigned to 6 groups consisting of 20 chickens (4 replicates, 5 chickens per replicate). The chickens were reared in metal battery cages in an environmentally controlled room. Water and feeds were offered ad libitum. On day 22, eight chickens from each group were left in cages, fasted for 16 h to be used in the digestibility balance trial. These birds were fed their respective diets for 72 h and then fasted for 16 h. The excreta were collected in plastic containers twice a day. After removal of all contaminants (feathers, scales), samples were dried at 60C, chilled, and ground prior to analysis. Coefcients of total tract apparent digestibility (CATTD) of the organic matter, protein and energy were calculated as the difference between concentration of nutrient ingested and excreted, divided per concentration of ingested nutrient. In case of protein CATTD separation of the N content of excreta into N of urinary and fecal origin was done by a chemical method (Terpstra and De Hart 1974). From the pool of broilers that were not used for the digestibility study, 6 chicks randomly selected from each group were weighed and euthanized. Following dissection,

Four LM test diets were supplemented with enzyme (A,B,C,D) preparation (for details see Material and methods)

The minerals and vitamins were supplemented as follows (mg): Fe 60.0; Zn 50.0; Mn 100.0; Cu 8.0; I 0.8; Se 0.2; Co 0.4; Vit.E 30.0; Vit. K3 3.0; Vit. K3 2.0; Vit. B1 2.0; Vit. B2 6.0; Vit. B6 3.5; Vit. B12 0.02; Biotine 0.2; Folic acid 1.5; Nicotinic acid 30.0; Calcium pantothenate 15.0; Choline 600.0 or (IU): Vit. A 12,500; Vit. D3 3,000 As in Table 1

the entire gastrointestinal tract was excised and subjected to post mortem examination. Liver, voided small intestine and ceca were used for morphometric (weight and length) measurements. The experiment was conducted in agreement with the Polish regulations regarding the protection of experimental animals (Animals Protection Act 1997). Chemical analysis Lupine seeds were subjected to proximate analysis, as well as energy, amino acids, non starch polysaccharides, phytates, total alkaloids, and condensed tannins analyses. Proximate analyses were carried out according to standard methods listed by AOAC (1990). Gross energy was determined using an adiabatic bomb calorimeter (type Kl-6, Bydgoszcz, Poland). Amino acids (except tryptophanenot measured) were analyzed using Amino Acid Analyzer system (Beckman Gold 126AA) as described by Llames and Fontaine (1994).

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The NSP and their constituent sugars were analyzed using the Englyst procedure (Englyst 1989). Phytates were analyzed as phytic acid using the HPLC method (Newkirk and Classen 1998). Total alkaloids were determined according to the methods described by Skolik and Wiewiorowski (1959), condensed tannins as described by Butler et al. (1982). Lectins with specicity to galactose were measured by afnity chromatography according to Maenz et al. (1999). Samples of the diets and excreta were analyzed for nutrients and energy according to methods mentioned for LM. All analyses were performed in duplicate. Statistical analysis Statistical analyses were carried out by ANOVA from the computer package NCSS (Hintze 1995). The means were compared using Tukeys test. Statistical signicance was assumed to exist when the probability was less than 0.05.

Results Gross energy appeared high, but the proportion of metabolizable energy was merely 50% (Table 1). The protein content was 468 g/kg and the amino acid composition showed that the content of lysine was 21.6 g/kg, whereas the content of methionine was only 3.4 g/kg. It is noteworthy that LM contained 54 g/kg of arginine. The total alkaloids content in LM was 0.7 g/kg, and the total phytic acid content being 21.6 g/kg (Table 2). Most of phytates were present as IP-6. The LM also contained 1 g/kg specic to galactose lectins, whereas condensed tannins were not detectable. Total NSP content in LM was 240 g/kg and

the majority of sugars constituting the NSP were insoluble (Table 2). Among monosaccharides, glucose (35%) and galactose (22%) were dominant, followed by uronates (15%), arabinose (14%) and xylose (11%). Feed intake (FI) and body weight gain (BWG) were (13 and 20%, respectively) lower (p \ 0.05) in broilers fed LM diet in comparison to broilers fed SBM diet (Fig. 1). Supplementation of all enzymes degrading NSP improved (p \ 0.05) FI and BWG. The FI of LM diet supplemented with enzyme A was highest, being approximately 10% higher in comparison to SBM diet. Interestingly broilers fed LM supplemented with enzyme B had considerably higher BWG (p \ 0.05) than birds fed SBM diet. Feed conversion efceincy (FCE) calculated as BWG/FI was signicantly increased (p \ 0.05) by addition of enzyme B. Supplementation with enzyme D did not improve FI or BWG. Coefcients of total tract apparent digestibility (CTTAD) of organic matter, protein and energy were signicantly lower (p \ 0.05) in chicks fed LM diet than in those fed SBM diet (Fig. 2). The enzyme supplement B slighty(p \ 0.05) improved CTTAD of organic matter and protein. It is worth mentioning that the addition of enzyme B to LM diet tended to improve CTTAD of energy close to the value obtained for SBM diet, but the difference was statistically not signicant (p [ 0.05). In comparison to the SBM based diet, dietary LM increased (p \ 0.05) all morphometric variables evaluated in the present study (Figs. 3 and 4). The effect of enzymes on morphometric parameters were variable. With the exception of enzyme D, enzyme preparations with activity directed towards NSP (enzyme A, B, C) signicantly decreased (p \ 0.05) weight of the liver and gizzard, as well as the length of all segements of small intestine and ceca, whereas phytase (enzyme D) decreased only intestinal parameters.

FI,BWG[g]; FCE[g/kg]

Fig. 1 Feed intake (FI) and Body weight gain (BWG) and Fed conversion efciency (FCE; calculated as BWG/FI) of broilers. The data represent means of each treatment group, bars SE. Means with a similar letter did not differ, p \ 0.05

SBM
900 800 700 600 500 400 300 200 100 0

LM

LM+A

LM+B

LM+C

LM+D

b bc a

bc a

bc c

ab a

bc ab

ab c

FI

BWG

FCE

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World J Microbiol Biotechnol (2011) 27:341347 Fig. 2 Coefcients of Total Tract Apparent Digestibility (CTTAD) of energy, organic matter and protein. The data represent means of each treatment group, bars SE. Means with a similar letter did not differ, p \ 0.05
CTTAD

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SBM
0,90 0,80 0,70 0,60 0,50 0,40 0,30 0,20 0,10 0,00

LM

LM+A

LM+B

LM+C

LM+D

c ab ab b

c a ab b

d ab ab c

a a

Energy

Organic Matter

Protein

[g/100g]

Fig. 3 Weight of liver and gizzard. The presented values are normalized for body weight (per 100 g). The data represent means of each treatment group, bars SE. Means with a similar letter did not differ, p \ 0.05

SBM
4,5 4 3,5 3 2,5 2 1,5 1 0,5 0
b

LM

LM+A

LM+B

LM+C

LM+D

Liver

Gizzard

Discussion In comparison to SBM diet, LM based diet had detrimental effects on all performance parameters. Lower growth rate of broilers fed a lupine based diet was most likely associated with lower availability of dietary components from the gastrointestinal tract, as evidenced by lowered feed intake and digestibility. Addition of enzymes degrading NSPs, and in particular enzyme preparation B considerably reduced the negative effects of LM on FI and BWG. Since addition of enzymes signicantly improved FI, it can be inferred that the negative effect of LM was, in part, due to poor palatability of the diet, likely associated with specic taste of LM. Increased FI associated with addition of enzymes degrading NSP to LM based diet is in agreement with the studies of Brenes et al. (2002, 2005). Also the benecial effect of these enzymes on growth rate of chickens seen in the present study is in agreement with results reported by others (Brenes et al. 2005; Roth-Maier and Kirchgessner 1995). Decreased digestibility in broilers fed the LM based diets in the present study was evident, which is generally consistent with observations of other workers (Annison et al. 1996; Froidmont et al. 2004;

Hughes et al. 1999). However, it should be noted that the effectiveness of NSP degrading enzyme supplementation to LM diets may be slight or non-existent (Kocher et al. 2000) and may depend on the type of enzyme and the species or variety of lupines (Alloui et al. 1994). Meng and Slominski (2005) reported improved protein digestibility by multicarbohydrase cocktail addition to the corn-SBM diet but decreased digestibility for the corn-canola meal diet. The effects of LM on enlargement of GI, and partial alleviation of these effects resulting from addition of NSP degrading enzymes were evident in the present study, and these observations are consistent with ndings of others (Brenes et al. 1993, 2002; Rubio et al. 2003), but the patho-physiological relevance of these changes in the context of the changes in performance parameters cannot be explained at present. The content of phytic acid in LM was considerably lower than reported by Muzguiz et al. (1989) and, mostly represented in the form of IP6. Phytates have been reported to decrease chicken growth and feed consumption, and reduced availability of energy and nutrients (Ravindran et al. 2000; Sandberg 2002; Shan and Davis 1994), but lack of benecial effects by microbial phytase on broiler

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346 Fig. 4 Length of small intestine parts and ceca. The presented values are normalized for body weight (per 100 g). The data represent means of each treatment group, bars SE. Means with a similar letter did not differ, p \ 0.05

World J Microbiol Biotechnol (2011) 27:341347

SBM
12 10 8 6 4 2 0
b

LM

LM+A

LM+B

LM+C

LM+D

[cm/100g]

a b

d cd a ab b

c bc ab b

Doudeum

Jejunum

Illeum

Ceca

performance was also reported (Selle et al. 1999). Bryden and Li (2004) did not found any effect of phytase addition to lupine diet on the average apparent ileal digestibility coefcients of amino acids. In the present study, phytase supplementation to LM diet did not result in improvement of FI, BWG, or nutrient digestibility, which suggests that the level of phytates in LM diets was not high enough to inuence any performance parameters. Presence of lectins in LM observed in the present study appears to be in contrast with the general assumption that lupines do not show lectin activity (Petterson 2000). Generally, assessment of lectin contents in lupines was based on detection of haemaglutinating activity, and according to this assay lectins appear to exist only in trace amounts in lupines (Falcon et al. 2000). However, lack of haemaglutinating activity does not necessarily preclude the presence of lectins (Falcon et al. 2000; Maenz et al. 1999). It is well established that plant lectins can be detrimental to animals (Vasconcelos and Oliveira 2004). Lectin-like protein in LM has negligible in vitro haemaglutinating properties, but is toxic in vivo, and exerts toxicity by interfering with protein synthesis in the liver in rats (Rahman 2000). Lupines lectins with specicity for galactose measured by afnity chromatography can be detected at levels up to 2.2 g/kg (Olkowski, unpublished observation) and this approach to study potential anti-nutritional effects of lupine lectins deserves more consideration in future research.

seeds, when supplemented with suitable enzymes, can be used to fully substitute SBM in diets for young broilers.
Conict of interest statement I declare that I have no conict of interest in the subject matter or materials discussed in the manuscript.

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Conclusions In summary, the present study showed that yellow lupine seeds, when added to the diet in large quantities, may have negative effects on broiler production parameters and morphology of the gastrointestinal tract. These detrimental effects possibly appear to be alleviated by addition of an appropriate combination of enzyme preparations with activity towards degrading NSP compounds. Yellow lupine

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