Directory UMM :Data Elmu:jurnal:A:Animal Feed Science and Technology:Vol83.Issue2.Feb2000:
Animal Feed Science and Technology
83 (2000) 89±101
Effects of increasing amounts of Lupinus albus
seeds without or with whole egg powder in
the diet of growing pigs on performance
C. Van Nevela,c,*, M. Seynaeveb, G. Van De Voordec,
S. De Smetc, E. Van Driesschea, R. De Wildeb
a
Laboratory of Protein Chemistry, Institute for Molecular Biology and Biotechnology,
Vrije Universiteit Brussel, Paardenstraat, 65, B-1640 Sint-Genesius-Rode, Belgium
b
Laboratory of Animal Nutrition, Faculty of Veterinary Medicine, University of Ghent,
Heidestraat, 19, B-9820 Merelbeke, Belgium
c
Department of Animal Production, Faculty of Agricultural and Applied Biological Sciences,
University of Ghent, Proefhoevestraat, 10, B-9090 Melle, Belgium
Received 4 November 1998; received in revised form 30 March 1999; accepted 19 October 1999
Abstract
In a growth trial with pigs, the effect of the inclusion of 150 and 300 g of Lupinus albus seeds/kg
of feed in the diet was investigated. Parameters studied were: growth, feed utilization, digestibility of
nutrients, slaughter and carcass characteristics. Spray dried whole egg powder, a speci®c inhibitor of
lectins in L. albus seeds was also added (50 g/kg of feed), with the aim of verifying whether the
unfavourable effects of high levels of lupin seeds could be neutralized. Feeding the diet containing
300 g of lupin seeds/kg lowered the average daily gain from 727 to 674 g and feed intake from 2.32
to 2.05 kg, while feed conversion ratio remained unaltered. The presence of whole egg powder in the
lupin seed diets did not abolish the negative effects. Apparent faecal digestibility of most nutrients in
the diets was not in¯uenced by addition of lupin seeds or egg powder, except for the crude fat
fraction, whereas the digestibility coef®cient increased from 0.51 to 0.61. Crude ®bre digestibility
also increased, but only at the lowest lupin seed level. Carcass weight and dressing percentage were
lower in the groups fed the highest lupin seed level. Fatty acid pro®le of backfat was determined and
slightly higher proportions of C18:1 were observed when lupin seeds were fed. Possible reasons
accounting for the lower performance of animals receiving lupin seeds are discussed, but the exact
reason could not be derived from this experiment. # 2000 Elsevier Science B.V. All rights reserved.
Keywords: Pig growth; L. albus seeds; Antinutritional compounds; Egg powder
*
Corresponding author. Tel.: 32-9-2649014; fax: 32-9-2649099.
0377-8401/00/$ ± see front matter # 2000 Elsevier Science B.V. All rights reserved.
PII: S 0 3 7 7 - 8 4 0 1 ( 9 9 ) 0 0 1 2 5 - X
90
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
1. Introduction
In the search for alternative protein sources replacing the more traditional ingredients,
such as soyabean meal, meat meal or ®sh meal in pig diets, much attention has been paid
during the last decade to the use of lupin seeds, e.g. Lupinus angustifolius, L. albus and
L. luteus. Their potential use was made possible by genetic selection for cultivars with
low levels of alkaloids, which were thought to be the major antinutritional compounds in
lupin seeds (Petterson et al., 1986). Data concerning lectin content are very scarce.The
lack of detection of lectins in lupin seeds in earlier works was probably due to the fact
that, for the detection of lectins, the hemagglutination method was applied using nonprotease treated erythrocytes (Hill, 1977), and the test may not have been adequate.
Consequently, during the genetic selection process no attention was paid to the aspect of
lectin content. However, in earlier works using rabbit erythrocytes pretreated with
Pronase, hemagglutination activities of 41±82 units/mg of seed meal of L. albus and 5±20
units/mg of seed meal of L. angustifolius (Van Nevel et al., 1998) were determined.
Lectins in L. angustifolius seeds have also been found by Kim and Madhusudhan (1988)
and Rahman et al. (1997) using trypsinized red blood cells. A brief literature survey
showed that growth and feed intake of pigs decreased when the diet contained 150±430 g
of L. albus seeds/kg (Pearson and Carr, 1977; Batterham, 1979; Roth-Maier and
Kirchgessner, 1994; Zettl et al., 1995). Although it was generally thought that alkaloids
were the inhibitory compounds, it was put forward that other, yet unknown factors could
have been responsible for the negative effects on animal performance (Pearson and Carr,
1977). It is not inconceivable that the presence of lectins also played a role in the
unfavourable growth response when lupin seeds were fed to piglets or pigs. On the other
hand, in previous in vitro works studying the use of receptor-analogues, saturating the
sugar-binding site of lectins and thus inhibiting their activity in extracts of different
legume seeds, it was observed that whole egg powder was a very ef®cient inhibitor of
lectin activity in L. albus seeds (Van Nevel et al., 1998). Therefore, it was decided to
investigate in vivo, whether addition of whole egg powder (50 g/kg) was able to
neutralize the negative effect of lupin seed containing diets (0, 150 or 300 g/kg) on
performance of growing pigs. The following measurements were undertaken: daily gain,
feed intake, feed conversion ratio, apparent faecal digestibility, slaughter data and carcass
quality including fatty acid pro®le of backfat.
2. Materials and methods
2.1. Animals
Forty-two crossbred pigs (Belgian Negative PieÂtrain) of 23.8 2.1 kg (mean SD)
live weight (LW) were divided into seven homogenous (sex, LW, origin) groups and one
of the seven experimental diets was randomly assigned to each of the groups. The animals
were individually penned and had free access to feed and water. Every two weeks the
animals were weighed and their feed consumption determined. Three animals were
eliminated from the experiment: one barrow and one gilt (diet 2L30Ly) due to leg
weakness and one gilt (diet 2L30E) because of abnormal low-growth performance.
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C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
2.2. Diets
The experiment was divided into two periods and, for each period, diets with different
crude protein content were fed: 186 g/kg during a ®rst period (growth phase from 24 to
43 kg LW) and 170 g/kg during a second growth phase (43±102 kg LW). Seven diets
were formulated. Two diets acted as control without lupin seeds: a ®rst diet (G) without
egg powder, and a second diet (GE) containing 50 g of egg powder per kg of feed. Four
diets with lupin seeds were formulated containing, respectively, 150 and 300 g of lupin
seeds/kg of feed without (L15, respectively, L30) or with addition of 50 g of egg powder/
kg (respectively, L15E and L30E). A seventh diet (L30Ly) with extra supplementation of
lysine was included, because Batterham et al. (1986) found that when lupin seed meal
was fed, the ef®ciency of utilization of absorbed lysine was only 0.53. In this manner, it
could be demonstrated whether eventual negative effects of a diet containing 300 g of
lupin seeds/kg was due to lysine being limiting for growth. The composition of the
different diets is presented in Tables 1 and 2. Within each growth phase, diets were
balanced for total protein content, net energy value (9.43 and 9.18 MJ/kg for growth
phases 1 and 2, respectively ), Ca, P and some essential amino acids (based on small
intestinal digestibility). All ingredients were ground (mesh, 2.0 mm) and diets fed in the
dry form. Whole egg powder was provided by VEOS nv., Zwevezele, Belgium (VEPRO
Table 1
Composition (g/kg) of the diets (growth phase 24±43 kg)
Ingredients
Manioc
Wheat
Soyabean meala
Lupin seeds
Egg powder
Soyabean oil
Vitamins and mineralsb
Limestone
Dicalcium phosphate
Salt
L-Lysine
DL-Methionine
L-Threonine
L-Tryptophan
Stafoc
KHCO3
a
Diets
1G
1GE
1L15
1L15E
1L30
1L30E
1L30Ly
237.5
400.0
316.3
0.0
0.0
14.0
10.0
6.0
11.0
3.0
0.6
0.6
0.0
0.0
1.0
0.0
274.1
400.0
245.0
0.0
50.0
0.0
10.0
6.5
9.5
3.0
0.8
0.1
0.0
0.0
1.0
0.0
191.0
400.0
210.0
150.0
0.0
15.0
10.0
6.0
11.0
3.0
1.2
0.8
0.0
0.0
1.0
1.0
225.0
400.0
138.7
150.0
50.0
1.5
10.0
6.5
9.5
3.0
11.5
0.3
0.0
0.0
1.0
3.0
144.6
400.0
100.0
300.0
0.0
16.5
10.0
6.0
11.0
3.0
2.2
1.1
0.4
0.2
1.0
4.0
177.5
400.0
300.0
300.0
50.0
2.5
10.0
6.5
9.5
3.0
2.3
0.6
0.4
0.2
1.0
6.5
142.9
400.0
100.0
300.0
0.0
16.5
10.0
6.0
11.0
3.0
3.9
1.1
0.4
0.2
1.0
4.0
Solvent-extracted meal, containing 412 g of crude protein/kg.
Providing per kg of feed: vitamins: A, 12 000 IU; D3, 2000 IU; E, 50 mg; K, 1 mg; B1, 0.6 mg; B2, 4 mg;
B3, 12.5 mg; B6, 1 mg; B12, 0.02 mg; niacin, 20 mg; folic acid, 1.5 mg; biotin, 0.10 mg; choline, 350 mg;
Minerals: iron, 150 mg; copper, 25 mg; manganese, 50 mg; cobalt, 1 mg; zinc, 100 mg; iodine, 2 mg; selenium,
0.4 mg; calcium, 870 mg; sodium, 0.2 mg; magnesium, 136 mg; Ethoxyquin, 1 mg; BHT, 1 mg.
c
Providing 10 ppm of Virginiamycin (P®zer Animal Health, Louvain la Neuve, Belgium).
b
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C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
Table 2
Composition (g/kg) of the diets (growth phase 43±102 kg)a
Ingredients
Manioc
Wheat
Soyabean meal
Lupin seeds
Egg powder
Wheat bran
Vitamins and minerals
Limestone
Dicalcium phosphate
Salt
L-Lysine
DL-Methionine
L-Threonine
L-Tryptophan
Stafo
KHCO3
a
Diets
2G
2GE
2L15
2L15E
2L30
2L30E
2L30Ly
300.0
387.1
270.0
0.0
0.0
20.0
10.0
3.0
6.0
3.0
0.2
0.2
0.0
0.0
0.5
0.0
300.0
343.0
185.0
0.0
50.0
100.0
10.0
4.5
3.5
3.0
0.5
0.0
0.0
0.0
0.5
0.0
300.0
338.5
177.5
150.0
0.0
10.0
10.0
3.0
6.0
3.0
1.0
0.5
0.0
0.0
0.5
0.0
300.0
296.0
93.5
150.0
50.0
85.0
10.0
4.5
3.5
3.0
1.0
0.0
0.0
0.0
0.5
3.0
300.0
287.0
85.0
300.0
0.0
0.0
10.0
3.0
6.0
3.0
1.1
0.7
0.1
0.1
0.5
3.5
300.0
251.0
0.0
300.0
50.0
70.0
10.0
4.5
3.5
3.0
1.5
0.2
0.2
0.1
0.5
5.5
300.0
285.3
85.0
300.0
0.0
0.0
10.0
3.0
6.0
3.0
2.8
0.7
0.1
0.1
0.5
3.5
See Footnotes of Table 1.
55EP). Lupin seeds (L. albus, cv. Lublanc) were imported from France (Groupe CANA,
44150 Ancenis).
2.3. Digestibility measurements
Faecal digestibility of nutrients was determined with three pigs per diet (barrows),
using 15 g of Celite 545 (VEL, Leuven, Belgium) as marker per kg of feed. Collection of
faecal material was undertaken during 5 days, after an adaptation period of at least 1
week during which the Celite containing diet was fed. Faecal material was stored at
ÿ228C until further processing. At the time of digestibility measurements, pigs weighed
70±80 kg, except for diet 2L30 where LW was 67 kg.
2.4. Slaughter and carcass characteristics
At an LW of 100±105 kg, animals were transported to the experimental slaughterhouse
of the Department of Animal Production, University of Ghent at Melle (Belgium). The
feed withdrawal period before slaughter was 20 h. The transportation time was 15 min
and the pigs did not receive sedatives. The following determinations were carried out:
dressing percentage, backfat thickness (measured at 3 locations: at the 1st, 7th and last
rib) and percentage of lean in carcass. The latter parameter was calculated by the
following regression model with the weight percentages of backfat (X1), loin (X2) and
leg (X3) as parameters, determined by a wholesale cut: percentage of lean
7.326 ÿ 1.334X1 1.511X2 0.794X3; R2 0.966, RSD 1.35 (Van De Voorde, to
be published). Backfat was sampled for determination of fatty acid pattern.
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
93
2.5. Chemical analysis
Approximate composition (Weende analysis) on feed and faecal material (homogenized and lyophilized) was undertaken following standard European Union procedures.
Celite was determined as 4 N HCl insoluble ash. Hemagglutinating activity (units/mg of
feed) as a measure of lectin presence in extracts of L. albus seed meal and diets was
determined using protease (Pronase, Boehringer, Mannheim, Germany) treated rabbit
erythrocytes as described previously (Van Nevel et al., 1998). Trypsin-inhibiting activity
was determined by Masterlab (Trouw Nutrition Nederland bv., Putten, The Netherlands)
using benzoyl-l-arginine-p-nitro-anilidide as substrate (Nederlands Normalisatie Instituut, 1993). Total and individual alkaloids in L. albus seeds were analyzed by Dr. M.
Muzquiz using a capillary GLC-MS procedure (Muzquiz et al., 1994). Fatty acid pattern
in diets and lupin seeds was determined as described by Sukhija and Palmquist (1988),
but C17:0 (heptadecanoic acid) was used as an internal standard. As seeds of L. albus
have a rather high lipid content (80±140 g/kg), containing 500±550 g/kg of oleic acid
(C18:1), 170±200 g/kg of linoleic acid (C18:2) and 90±100 g/kg of a-linolenic acid
(C18:3), fatty acid pattern in samples of backfat was also determined (Hill, 1977; Green
and Oram, 1983; Zettl et al., 1995). Lipids in backfat samples were extracted as described
by Folch et al. (1957). Transesteri®cation and extraction of fatty acid methyl esters was
done as outlined previously (Demeyer et al., 1978). C17:0 was used as internal standard
and individual fatty acids were determined by GC as reported by Van Nevel and Demeyer
(1996).
2.6. Statistics
The effect of lupin seeds and egg powder was tested in a 2 3 factorial model using
the data of diet one-to-six (General Linear Models procedure of SPSS, 1997). The least
squares means are given in the tables. Linear and quadratic polynomials were evaluated
for the effect of increasing lupin content of the diets. The effect of lysine supplementation
was separately tested by comparison of diet 7 (L30Ly) with diet 5 (L30) using a simple ttest.
3. Results
3.1. Diet composition
Approximate analysis of diets and some ingredients are shown in Table 3. Despite
accurate calculation and formulation, lupin seed containing diets fed during the ®rst
growth phase showed a somewhat higher crude protein content than both control diets
(1G and 1GE). Trypsin-inhibiting activity (TIA) and hemagglutinating activity (HA) in
extracts of diets and some ingredients are presented in Table 4. It is clear that TIA in lupin
seeds was very low in contrast to the whole egg powder, where very high values were
determined. Determination of HA revealed hemagglutination in L. albus seeds, in good
agreement with an earlier work (Van Nevel et al., 1998), but also in the diets, even when
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C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
Table 3
Chemical composition (Weende analysis) of diets, lupin seeds and whole egg powder
Diets
Nutrients (g/kg)a
DM
OM
CP
CL
CF
NFE
1G
1GE
1L15
1L15E
1L30
1L30E
1L30Ly
875
878
879
880
878
878
878
810
813
818
818
822
821
818
172
180
199
187
186
194
192
35
34
48
45
59
59
56
61
54
72
69
90
79
84
542
545
499
517
487
489
486
2G
2GE
2L15
2L15E
2L30
2L30E
2L30Ly
865
869
867
870
865
867
865
805
809
807
808
804
807
804
171
170
169
173
166
167
172
22
34
30
46
39
53
40
61
59
72
69
87
83
87
551
546
536
520
512
504
505
Lupin seeds
Egg powder
870
965
838
899
299
566
93
272
165
21
281
40
a
DM, OM, CP, CL, CF, NFE, respectively, dry matter, organic matter, crude protein, crude fat, crude ®bre,
nitrogen-free extractive.
lupin seeds were not incorporated. The reason for this was an unexpected very high HA in
extracted soyabean meal. In a further experiment, HA in extracts of soyabean meal, wheat
and manioc was measured using untreated erythrocytes and all results were negative.
During a last trial using Pronase-treated erythrocytes, HA was again determined in
Table 4
Trypsin inhibiting activity (TIA) and hemagglutination activity (HA) of diets and some ingredients
Dieta
TIAb,c
HAd
1G
1GE
1L15
1L15E
1L30
1L30E
1L30Ly
0
2.0
0.09
2.09
0.18
2.18
0.18
41
20±41
20±41
20±41
20±41
10±41
20±41
Lupin seeds
Egg powder
Soyabean meal
0.59
40.0
n.d.e
20±41
nd
1024±2048
a
Growth phase 1 only.
Trypsin inhibited, in mg/g of feed.
c
Calculated from TIA in lupin seeds and egg powder, assuming that other ingredients contained no trypsin
inhibitors.
d
Determined in duplo and when not identical, both values are shown.
e
Not determined, but usually negligible (solvent extracted).
b
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
95
extracts of the same ingredients and again high values were observed for soyabean meal
(1024 to 2048 units/mg), very low values for wheat (2±4 units) and no HA in manioc
extracts. It thus seems that use of Pronase treated erythrocytes increased the sensitivity of
the HA method to a very considerable extent.
3.2. Animal performance
3.2.1. General
Statistical treatment indicated that for all parameters studied, no signi®cant differences
could be observed between the group receiving the diet containing 300 g of lupin seeds
(L30) and the group fed the same diet but with extra supplementation of lysine (L30Ly).
Therefore, data concerning the latter group were not mentioned in the following tables.
Furthermore, statistical analysis also showed that between both the treatments, namely
addition of egg powder and lupin seed inclusion, no signi®cant interaction could be
calculated, except for one parameter, i.e. faecal digestibility of crude fat (Table 6).
Consequently, results for both treatments could be discussed separately in the text, while
the aspect of crude fat digestibility was brie¯y treated in Section 3.2.3. For statistical
treatment of the data concerning daily gain and feed intake during Growth phase 2 and
the entire trial, ®nal body weight was included as a covariate. The same procedure was
undertaken for carcass weight (Table 7).
3.2.2. Growth, feed intake and feeding ef®ciency
Addition of egg powder to the diet had no effect on the parameters investigated
(Table 5). A trend to a lower average daily gain was observed for the groups fed 300 g of
lupin seeds/kg of feed. Feed conversion ratio was not in¯uenced.
3.2.3. Digestibility of nutrients
Digestibility of the crude fat fraction was higher in diets containing egg powder and
lupin seeds (Table 6). Statistical treatment revealed interaction between both treatments
due to the fact that digestibility coef®cients increased with increasing amounts of lupin
seed in the diet, but only in the presence of egg powder. Compared to the control group,
crude ®bre digestibility tended to be higher for lupin seed-containing diets. Digestibility
of the other nutrients was not altered by both the treatments.
3.2.4. Slaughtering performance and carcass characteristics
Carcass weight and dressing percentage of animals receiving lupin seeds was lower
than the other groups (Table 7). No statistically signi®cant differences were observed with
regard to percent lean in carcass and backfat thickness, although a tendency towards more
lean and less fat in carcass of animals receiving lupin seeds was observed. Fatty acid
pattern in lipids of diets, lupin seeds, egg powder and backfat is presented in Table 8. It is
clear that fatty acid composition of the diets was rather variable, being the resultant of
using different proportions of ingredients as listed in Table 2. On the other hand, fatty
acid pro®le of backfat was fairly constant for the different treatments, as only for the
proportion of C18:1, slightly higher values were found in animals fed lupin seeds. C18:3,
C20:0 and C20:1 could not be detected in backfat samples.
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C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
Table 5
Reponse of growing pigs to diets containing L.albus seeds fed without or with egg powder
Parametera
SEMc
Treatment
egg powder(g/kg)
b
lupin seeds (g/kg)
0(18)
50(18)
0(12)
150(12)
300(12)
Phase 1
LW1 (kg)
LW2 (kg)
ADG (g)d
Feed intake (kg/d)e
FCR
23.9
43.1
534
1.31
2.49
23.7
42.8
552
1.38
2.53
23.9
43.5
598
1.47
2.54
23.8
42.5
528
1.35
2.57
23.5
42.9
504
1.21
2.42
0.37
0.29
15
0.03
0.04
Phase 2
LW1
LW2
ADG
Feed intakef
FCR
43.1
102.1
767
2.62
3.45
42.8
101.8
791
2.66
3.38
43.5
102.8
792
2.71
3.44
42.5
102.6
800
2.78
3.48
42.9
100.4
744
2.44
3.34
0.29
0.53
13
0.05
0.08
Total trial
ADGf
Feed intakef
FCR
689
2.20
3.21
715
2.25
3.17
727
2.32
3.20
706
230
3.27
674
2.05
3.10
10
0.04
0.07
a
LW1, LW2, respectively, initial body weight and weight at end of growth phase; ADG. average daily gain;
FCR, feed conversion ratio (kg of feed/kg of gain).
b
Number of observations in parentheses.
c
Standard of the mean, calculated from pooled values (n 36).
d
Trend for linear effect of lupin seeds (p < 0.1).
e
Linear effect of lupin seeds (p < 0.01).
f
Linear effect of lupin seeds (p < 0.05).
Table 6
Apparent faecal digestibility coef®cients of nutrients
Nutrient
SEMb
Treatment
egg powder(g/kg)
a
Dry matter
Organic matter
Crude protein
Crude fatc
Crude ®bred
NFEe
a
lupin seeds (g/kg)
0(9)
50(9)
0(6)
150(6)
300(6)
0.79
0.84
0.73
0.46
0.50
0.93
0.81
0.85
0.80
0.67
0.51
0.92
0.80
0.84
0.77
0.51
0.44
0.92
0.81
0.85
0.80
0.57
0.57
0.93
0.79
0.83
0.78
0.61
0.51
0.93
0.005
0.005
0.010
0.011
0.016
0.003
Number of observations in parentheses.
Standard error of the mean, calculated from pooled values (n 18).
c
Linear and quadratic effect of lupin seeds (p < 0.01). An interaction effect between the treatments egg
powder and lupin seeds was noted.
d
Trend for linear effect of lupin seeds (p < 0.1).
e
Nitrogen-free extractives.
b
97
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
Table 7
Slaughter and carcass characteristics
Parameter
SEMf
Treatment
egg powder(g/kg)
a
b
LW (kg)
Carcass weight (kg)c
Dressing %d
% Lean
Backfat thicknesse (mm)
lupin seeds (g/kg)
0(18)
50(18)
0(12)
150(12)
300(12)
101.1
84.9
84.0
60.2
80.7
101.1
84.9
84.0
60.3
77.8
102.3
86.1
85.0
59.1
83.7
101.3
85.1
84.1
60.2
83.3
99.6
83.5
82.8
61.6
70.7
0.5
0.3
0.3
0.9
2.9
a
Number of observations between parentheses.
Body weight at slaughter.
c
Linear effect of lupin seeds (p < 0.01).
d
Linear effect of lupin seeds (p < 0.05).
e
Sum of measurements at three locations: 1st, 7th and last rib.
f
Standard error of the mean, calculated from pooled values (n 36).
b
Table 8
Fatty acid pro®le (g/kg) of lipid in diets, egg powder, lupin seeds and backfat
Diet
Fatty acid
C16:0
C16:1
C18:0
C18:1
C18:2
C18:3
2G
2GE
2L15
2L15E
2L30
2L30E
2L30Ly
223
211
195
197
172
137
191
0
12
17
20
26
21
0
67
57
44
57
27
32
53
331
297
314
346
369
455
371
308
310
319
245
289
223
312
26
25
38
30
42
52
46
0
0
0
0
0
0
0
0
0
0
13
0
18
0
55EPa
L. albus seeds
265
92
28
10
98
20
463
550
125
140
6
67
0
11
0
41
Backfat
Fatty acid
Treatment
egg powder (g/kg)
b
C16:0
C16:1
C18:0
C18:1d
C18:2
a
lupin seeds (g/kg)
0(18)
50(18)
0(12)
150(12)
300(12)
SEMc
250
7
157
518
68
248
13
149
522
68
252
11
158
505
75
254
11
154
517
64
242
8
146
538
66
2
2
3
5
3
Egg powder (from Cotterill et al., 1978).
Number of observations in parentheses.
c
Standard of the mean, calculated from pooled values (n 36).
d
Linear effect of lupin seeds (p < 0.05).
b
C20:0
C20:1
98
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
4. Discussion
4.1. Diet composition and digestibility of nutrients
In agreement with literature data (Hill, 1977), TIA of L. albus seeds was very low, as
opposed to whole egg powder. Ovomucoid (100 g/kg egg protein) is one of the most
important trypsin-inhibiting substances (Kato and Matsuda, 1997). Hartmann (1995) also
found very high concentrations of trypsin and cathepsin D inhibitors in egg white and
yolk. The present experiment showed that TIA in the diets fed was too low to have
caused growth inhibition of the animals. The fact that in extracts of solvent extracted
soyabean meal considerable HA as a measure of lectin activity was found, was due to the
use of protease-treated erythrocytes making the method much more sensitive. Very
recently, small but substantial amounts of carbohydrate-binding lectin could be
determined in several samples of conventionally processed soyabean meal (Maenz
et al., 1999). It is certainly not known to what extent these residual lectins can affect
performance of pigs or other animals. However, this phenomenon cannot account for
the lower performance of the groups fed lupin seed diets in this experiment, as the
proportion of solvent-extracted soyabean meal in these diets was much lower than in
the control diet (Tables 1 and 2).
Apparent faecal digestibility coef®cients of the different nutrients were within
the normal range observed with similar diets (Zettl et al., 1995; Flis et al., 1996).
Higher digestibility of crude fat in diets containing egg powder are related to
somewhat higher lipid content of these rations (Table 3, Growth phase 2) and this
fraction must have been highly digestible. Digestibility of the crude-®bre fraction
was higher in the present experiment, but in the literature this value was found to be
rather variable and also dependent on the other ingredients in the ration. Additionally,
Aguilera et al. (1985) determined a digestibility coef®cient of 0.83 for crude ®bre
in L. albus, cv. Multolupa.
4.2. Growth, feed intake and feeding ef®ciency
Daily gain and feed conversion ratios observed were comparable with results of other
studies feeding similar diets (Pearson and Carr, 1977; Batterham, 1979; Zettl et al., 1995).
Supplementing the L30 diet with lysine (L30Ly) had no effect on performance, which
agrees with Batterham et al. (1986), who investigated the effect of mixing seeds of L.
angustifolius in pig diets. The possibility of the presence of factors in the seeds also
decreasing utilization of the lysine supplement, a phenomenon thought to be speci®c to
pigs, was also considered. In experiments with rats receiving L. angustifolius seeds,
Rahman et al. (1997) concluded that a low utilization of absorbed N was caused by an
increased N-excretion in urine, indicating disturbances in the systemic N-metabolism. Nutilization was also negatively in¯uenced by the presence of important amounts of nonstarch polysaccharides (NSP).
Literature data show that the in¯uence of lupin seeds on daily gain and feed
consumption of fattening pigs was not very consistent. The effect of adding extra lysine
or methionine to diets containing lupin seeds has also been variable. Overall results
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
99
showed that feeding diets containing >200 g of lupin seeds/kg of feed caused a lowered
daily gain and feed intake, especially during a ®rst growth phase, although differences
were not always statistically signi®cant (Pearson and Carr, 1977; Batterham, 1979; Zettl
et al., 1995). Feed conversion ratio was not in¯uenced. Several mechanisms explaining
these observations have been proposed. Seeds of L. albus can contain very high amounts
of Mn (467±3750 ppm) and it has been suggested that such high concentrations can
possibly result in depressed growth in pigs (National Research Council, 1998). On the
other hand, the presence of quinolizidine alkaloids decrease palatability of the diet
causing lower feed intake. Analysis of alkaloids in the lupin seeds fed in the present
experiment showed a total amount of 0.0123 mg/100 mg of seeds with the following
pattern: 0.0011 mg of angustifoline, 0.0090 mg of lupanine and 0.0022 mg of 13-OH
lupanine. Taking into account the available literature data, it can be concluded that
alkaloids in the current diets were not responsible for the lowered feed intake or growth
performance because their concentration was very low (Godfrey et al., 1985;
Buraczewska et al., 1993; Wasilewko et al., 1997). It was also clearly established by
Pearson and Carr (1977) that an eventual high amount of manganese in lupin seeds was
not responsible for unfavourable effects; the authors suggested that besides an eventual
high content of alkaloids, other factors were probably responsible for lower feed intake of
lupin seed-containing diets. As it has been shown that lysine in lupin seeds and also lysine
supplemented to diets containing lupin seed was only utilized with an abnormally low
ef®ciency, it cannot be completely excluded that poorer performances of the animals
observed in the current experiment were due to an inadequate provision of this essential
amino acid (Batterham et al., 1986).
Addition of whole egg powder (50 g/kg) to the different diets had no effect on growth
performance and feed intake, which was completely different from the effect of egg
powder in piglet and chicks diets, where growth inhibition has been observed (Peo et al.,
1969; Watkins and Veum, 1986; Kratzer et al., 1988). It also ruled out the possibility of
biotin de®ciency caused by the presence of avidin in the egg powder in the current trial
(Kratzer et al., 1988).
4.3. Carcass characteristics and fatty acid pro®le of backfat
The lower carcass weight and dressing percentage of animals receiving the highest
amount of lupin seeds is probably due to a larger gut ®ll caused by the higher ®bre
content of this diet (Batterham, 1979), while the tendency towards more lean and
less fat in their carcass is probably the result of slower growth rates related to lower
fat deposit.
Fatty acid pattern of lipid in lupin seeds used in this experiment agrees well
with the range reported in literature, although the proportion of a-linolenic acid
(C18:3) was somewhat lower (Green and Oram, 1983; Roth-Maier and Kirchgessner,
1993; Zettl et al., 1995; Zdunczyk et al., 1996). Fatty acid pattern of backfat was
rather constant and did not re¯ect the changes in fatty acid proportion determined in
the diets, which was also found by Zettl et al. (1995). Therefore, it can be concluded
that consistency and stability of backfat was not in¯uenced by addition of lupin seed
or egg powder.
100
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
5. Conclusions
It can be stated with certainty that the presence of lectins did not play a role in the
problems observed when lupin seeds were fed, as their concentration was very low, and
the fact that adding whole egg powder had no effect on parameters studied supports this
statement. On the other hand, the exact reasons for the negative effects on feeding lupin
seeds remain unknown and could not be determined from this experiment.
Acknowledgements
The research was ®nancially supported by the Ministry of Agriculture, DG6,
Brussels and VEOS nv. Zwevezele, Belgium. Technical help from S. Galle, E. Maes,
Daisy Bayens, H. De Rycke, N. Vanrolleghem and Jenny Martens is gratefully
acknowledged.
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83 (2000) 89±101
Effects of increasing amounts of Lupinus albus
seeds without or with whole egg powder in
the diet of growing pigs on performance
C. Van Nevela,c,*, M. Seynaeveb, G. Van De Voordec,
S. De Smetc, E. Van Driesschea, R. De Wildeb
a
Laboratory of Protein Chemistry, Institute for Molecular Biology and Biotechnology,
Vrije Universiteit Brussel, Paardenstraat, 65, B-1640 Sint-Genesius-Rode, Belgium
b
Laboratory of Animal Nutrition, Faculty of Veterinary Medicine, University of Ghent,
Heidestraat, 19, B-9820 Merelbeke, Belgium
c
Department of Animal Production, Faculty of Agricultural and Applied Biological Sciences,
University of Ghent, Proefhoevestraat, 10, B-9090 Melle, Belgium
Received 4 November 1998; received in revised form 30 March 1999; accepted 19 October 1999
Abstract
In a growth trial with pigs, the effect of the inclusion of 150 and 300 g of Lupinus albus seeds/kg
of feed in the diet was investigated. Parameters studied were: growth, feed utilization, digestibility of
nutrients, slaughter and carcass characteristics. Spray dried whole egg powder, a speci®c inhibitor of
lectins in L. albus seeds was also added (50 g/kg of feed), with the aim of verifying whether the
unfavourable effects of high levels of lupin seeds could be neutralized. Feeding the diet containing
300 g of lupin seeds/kg lowered the average daily gain from 727 to 674 g and feed intake from 2.32
to 2.05 kg, while feed conversion ratio remained unaltered. The presence of whole egg powder in the
lupin seed diets did not abolish the negative effects. Apparent faecal digestibility of most nutrients in
the diets was not in¯uenced by addition of lupin seeds or egg powder, except for the crude fat
fraction, whereas the digestibility coef®cient increased from 0.51 to 0.61. Crude ®bre digestibility
also increased, but only at the lowest lupin seed level. Carcass weight and dressing percentage were
lower in the groups fed the highest lupin seed level. Fatty acid pro®le of backfat was determined and
slightly higher proportions of C18:1 were observed when lupin seeds were fed. Possible reasons
accounting for the lower performance of animals receiving lupin seeds are discussed, but the exact
reason could not be derived from this experiment. # 2000 Elsevier Science B.V. All rights reserved.
Keywords: Pig growth; L. albus seeds; Antinutritional compounds; Egg powder
*
Corresponding author. Tel.: 32-9-2649014; fax: 32-9-2649099.
0377-8401/00/$ ± see front matter # 2000 Elsevier Science B.V. All rights reserved.
PII: S 0 3 7 7 - 8 4 0 1 ( 9 9 ) 0 0 1 2 5 - X
90
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
1. Introduction
In the search for alternative protein sources replacing the more traditional ingredients,
such as soyabean meal, meat meal or ®sh meal in pig diets, much attention has been paid
during the last decade to the use of lupin seeds, e.g. Lupinus angustifolius, L. albus and
L. luteus. Their potential use was made possible by genetic selection for cultivars with
low levels of alkaloids, which were thought to be the major antinutritional compounds in
lupin seeds (Petterson et al., 1986). Data concerning lectin content are very scarce.The
lack of detection of lectins in lupin seeds in earlier works was probably due to the fact
that, for the detection of lectins, the hemagglutination method was applied using nonprotease treated erythrocytes (Hill, 1977), and the test may not have been adequate.
Consequently, during the genetic selection process no attention was paid to the aspect of
lectin content. However, in earlier works using rabbit erythrocytes pretreated with
Pronase, hemagglutination activities of 41±82 units/mg of seed meal of L. albus and 5±20
units/mg of seed meal of L. angustifolius (Van Nevel et al., 1998) were determined.
Lectins in L. angustifolius seeds have also been found by Kim and Madhusudhan (1988)
and Rahman et al. (1997) using trypsinized red blood cells. A brief literature survey
showed that growth and feed intake of pigs decreased when the diet contained 150±430 g
of L. albus seeds/kg (Pearson and Carr, 1977; Batterham, 1979; Roth-Maier and
Kirchgessner, 1994; Zettl et al., 1995). Although it was generally thought that alkaloids
were the inhibitory compounds, it was put forward that other, yet unknown factors could
have been responsible for the negative effects on animal performance (Pearson and Carr,
1977). It is not inconceivable that the presence of lectins also played a role in the
unfavourable growth response when lupin seeds were fed to piglets or pigs. On the other
hand, in previous in vitro works studying the use of receptor-analogues, saturating the
sugar-binding site of lectins and thus inhibiting their activity in extracts of different
legume seeds, it was observed that whole egg powder was a very ef®cient inhibitor of
lectin activity in L. albus seeds (Van Nevel et al., 1998). Therefore, it was decided to
investigate in vivo, whether addition of whole egg powder (50 g/kg) was able to
neutralize the negative effect of lupin seed containing diets (0, 150 or 300 g/kg) on
performance of growing pigs. The following measurements were undertaken: daily gain,
feed intake, feed conversion ratio, apparent faecal digestibility, slaughter data and carcass
quality including fatty acid pro®le of backfat.
2. Materials and methods
2.1. Animals
Forty-two crossbred pigs (Belgian Negative PieÂtrain) of 23.8 2.1 kg (mean SD)
live weight (LW) were divided into seven homogenous (sex, LW, origin) groups and one
of the seven experimental diets was randomly assigned to each of the groups. The animals
were individually penned and had free access to feed and water. Every two weeks the
animals were weighed and their feed consumption determined. Three animals were
eliminated from the experiment: one barrow and one gilt (diet 2L30Ly) due to leg
weakness and one gilt (diet 2L30E) because of abnormal low-growth performance.
91
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
2.2. Diets
The experiment was divided into two periods and, for each period, diets with different
crude protein content were fed: 186 g/kg during a ®rst period (growth phase from 24 to
43 kg LW) and 170 g/kg during a second growth phase (43±102 kg LW). Seven diets
were formulated. Two diets acted as control without lupin seeds: a ®rst diet (G) without
egg powder, and a second diet (GE) containing 50 g of egg powder per kg of feed. Four
diets with lupin seeds were formulated containing, respectively, 150 and 300 g of lupin
seeds/kg of feed without (L15, respectively, L30) or with addition of 50 g of egg powder/
kg (respectively, L15E and L30E). A seventh diet (L30Ly) with extra supplementation of
lysine was included, because Batterham et al. (1986) found that when lupin seed meal
was fed, the ef®ciency of utilization of absorbed lysine was only 0.53. In this manner, it
could be demonstrated whether eventual negative effects of a diet containing 300 g of
lupin seeds/kg was due to lysine being limiting for growth. The composition of the
different diets is presented in Tables 1 and 2. Within each growth phase, diets were
balanced for total protein content, net energy value (9.43 and 9.18 MJ/kg for growth
phases 1 and 2, respectively ), Ca, P and some essential amino acids (based on small
intestinal digestibility). All ingredients were ground (mesh, 2.0 mm) and diets fed in the
dry form. Whole egg powder was provided by VEOS nv., Zwevezele, Belgium (VEPRO
Table 1
Composition (g/kg) of the diets (growth phase 24±43 kg)
Ingredients
Manioc
Wheat
Soyabean meala
Lupin seeds
Egg powder
Soyabean oil
Vitamins and mineralsb
Limestone
Dicalcium phosphate
Salt
L-Lysine
DL-Methionine
L-Threonine
L-Tryptophan
Stafoc
KHCO3
a
Diets
1G
1GE
1L15
1L15E
1L30
1L30E
1L30Ly
237.5
400.0
316.3
0.0
0.0
14.0
10.0
6.0
11.0
3.0
0.6
0.6
0.0
0.0
1.0
0.0
274.1
400.0
245.0
0.0
50.0
0.0
10.0
6.5
9.5
3.0
0.8
0.1
0.0
0.0
1.0
0.0
191.0
400.0
210.0
150.0
0.0
15.0
10.0
6.0
11.0
3.0
1.2
0.8
0.0
0.0
1.0
1.0
225.0
400.0
138.7
150.0
50.0
1.5
10.0
6.5
9.5
3.0
11.5
0.3
0.0
0.0
1.0
3.0
144.6
400.0
100.0
300.0
0.0
16.5
10.0
6.0
11.0
3.0
2.2
1.1
0.4
0.2
1.0
4.0
177.5
400.0
300.0
300.0
50.0
2.5
10.0
6.5
9.5
3.0
2.3
0.6
0.4
0.2
1.0
6.5
142.9
400.0
100.0
300.0
0.0
16.5
10.0
6.0
11.0
3.0
3.9
1.1
0.4
0.2
1.0
4.0
Solvent-extracted meal, containing 412 g of crude protein/kg.
Providing per kg of feed: vitamins: A, 12 000 IU; D3, 2000 IU; E, 50 mg; K, 1 mg; B1, 0.6 mg; B2, 4 mg;
B3, 12.5 mg; B6, 1 mg; B12, 0.02 mg; niacin, 20 mg; folic acid, 1.5 mg; biotin, 0.10 mg; choline, 350 mg;
Minerals: iron, 150 mg; copper, 25 mg; manganese, 50 mg; cobalt, 1 mg; zinc, 100 mg; iodine, 2 mg; selenium,
0.4 mg; calcium, 870 mg; sodium, 0.2 mg; magnesium, 136 mg; Ethoxyquin, 1 mg; BHT, 1 mg.
c
Providing 10 ppm of Virginiamycin (P®zer Animal Health, Louvain la Neuve, Belgium).
b
92
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
Table 2
Composition (g/kg) of the diets (growth phase 43±102 kg)a
Ingredients
Manioc
Wheat
Soyabean meal
Lupin seeds
Egg powder
Wheat bran
Vitamins and minerals
Limestone
Dicalcium phosphate
Salt
L-Lysine
DL-Methionine
L-Threonine
L-Tryptophan
Stafo
KHCO3
a
Diets
2G
2GE
2L15
2L15E
2L30
2L30E
2L30Ly
300.0
387.1
270.0
0.0
0.0
20.0
10.0
3.0
6.0
3.0
0.2
0.2
0.0
0.0
0.5
0.0
300.0
343.0
185.0
0.0
50.0
100.0
10.0
4.5
3.5
3.0
0.5
0.0
0.0
0.0
0.5
0.0
300.0
338.5
177.5
150.0
0.0
10.0
10.0
3.0
6.0
3.0
1.0
0.5
0.0
0.0
0.5
0.0
300.0
296.0
93.5
150.0
50.0
85.0
10.0
4.5
3.5
3.0
1.0
0.0
0.0
0.0
0.5
3.0
300.0
287.0
85.0
300.0
0.0
0.0
10.0
3.0
6.0
3.0
1.1
0.7
0.1
0.1
0.5
3.5
300.0
251.0
0.0
300.0
50.0
70.0
10.0
4.5
3.5
3.0
1.5
0.2
0.2
0.1
0.5
5.5
300.0
285.3
85.0
300.0
0.0
0.0
10.0
3.0
6.0
3.0
2.8
0.7
0.1
0.1
0.5
3.5
See Footnotes of Table 1.
55EP). Lupin seeds (L. albus, cv. Lublanc) were imported from France (Groupe CANA,
44150 Ancenis).
2.3. Digestibility measurements
Faecal digestibility of nutrients was determined with three pigs per diet (barrows),
using 15 g of Celite 545 (VEL, Leuven, Belgium) as marker per kg of feed. Collection of
faecal material was undertaken during 5 days, after an adaptation period of at least 1
week during which the Celite containing diet was fed. Faecal material was stored at
ÿ228C until further processing. At the time of digestibility measurements, pigs weighed
70±80 kg, except for diet 2L30 where LW was 67 kg.
2.4. Slaughter and carcass characteristics
At an LW of 100±105 kg, animals were transported to the experimental slaughterhouse
of the Department of Animal Production, University of Ghent at Melle (Belgium). The
feed withdrawal period before slaughter was 20 h. The transportation time was 15 min
and the pigs did not receive sedatives. The following determinations were carried out:
dressing percentage, backfat thickness (measured at 3 locations: at the 1st, 7th and last
rib) and percentage of lean in carcass. The latter parameter was calculated by the
following regression model with the weight percentages of backfat (X1), loin (X2) and
leg (X3) as parameters, determined by a wholesale cut: percentage of lean
7.326 ÿ 1.334X1 1.511X2 0.794X3; R2 0.966, RSD 1.35 (Van De Voorde, to
be published). Backfat was sampled for determination of fatty acid pattern.
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
93
2.5. Chemical analysis
Approximate composition (Weende analysis) on feed and faecal material (homogenized and lyophilized) was undertaken following standard European Union procedures.
Celite was determined as 4 N HCl insoluble ash. Hemagglutinating activity (units/mg of
feed) as a measure of lectin presence in extracts of L. albus seed meal and diets was
determined using protease (Pronase, Boehringer, Mannheim, Germany) treated rabbit
erythrocytes as described previously (Van Nevel et al., 1998). Trypsin-inhibiting activity
was determined by Masterlab (Trouw Nutrition Nederland bv., Putten, The Netherlands)
using benzoyl-l-arginine-p-nitro-anilidide as substrate (Nederlands Normalisatie Instituut, 1993). Total and individual alkaloids in L. albus seeds were analyzed by Dr. M.
Muzquiz using a capillary GLC-MS procedure (Muzquiz et al., 1994). Fatty acid pattern
in diets and lupin seeds was determined as described by Sukhija and Palmquist (1988),
but C17:0 (heptadecanoic acid) was used as an internal standard. As seeds of L. albus
have a rather high lipid content (80±140 g/kg), containing 500±550 g/kg of oleic acid
(C18:1), 170±200 g/kg of linoleic acid (C18:2) and 90±100 g/kg of a-linolenic acid
(C18:3), fatty acid pattern in samples of backfat was also determined (Hill, 1977; Green
and Oram, 1983; Zettl et al., 1995). Lipids in backfat samples were extracted as described
by Folch et al. (1957). Transesteri®cation and extraction of fatty acid methyl esters was
done as outlined previously (Demeyer et al., 1978). C17:0 was used as internal standard
and individual fatty acids were determined by GC as reported by Van Nevel and Demeyer
(1996).
2.6. Statistics
The effect of lupin seeds and egg powder was tested in a 2 3 factorial model using
the data of diet one-to-six (General Linear Models procedure of SPSS, 1997). The least
squares means are given in the tables. Linear and quadratic polynomials were evaluated
for the effect of increasing lupin content of the diets. The effect of lysine supplementation
was separately tested by comparison of diet 7 (L30Ly) with diet 5 (L30) using a simple ttest.
3. Results
3.1. Diet composition
Approximate analysis of diets and some ingredients are shown in Table 3. Despite
accurate calculation and formulation, lupin seed containing diets fed during the ®rst
growth phase showed a somewhat higher crude protein content than both control diets
(1G and 1GE). Trypsin-inhibiting activity (TIA) and hemagglutinating activity (HA) in
extracts of diets and some ingredients are presented in Table 4. It is clear that TIA in lupin
seeds was very low in contrast to the whole egg powder, where very high values were
determined. Determination of HA revealed hemagglutination in L. albus seeds, in good
agreement with an earlier work (Van Nevel et al., 1998), but also in the diets, even when
94
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
Table 3
Chemical composition (Weende analysis) of diets, lupin seeds and whole egg powder
Diets
Nutrients (g/kg)a
DM
OM
CP
CL
CF
NFE
1G
1GE
1L15
1L15E
1L30
1L30E
1L30Ly
875
878
879
880
878
878
878
810
813
818
818
822
821
818
172
180
199
187
186
194
192
35
34
48
45
59
59
56
61
54
72
69
90
79
84
542
545
499
517
487
489
486
2G
2GE
2L15
2L15E
2L30
2L30E
2L30Ly
865
869
867
870
865
867
865
805
809
807
808
804
807
804
171
170
169
173
166
167
172
22
34
30
46
39
53
40
61
59
72
69
87
83
87
551
546
536
520
512
504
505
Lupin seeds
Egg powder
870
965
838
899
299
566
93
272
165
21
281
40
a
DM, OM, CP, CL, CF, NFE, respectively, dry matter, organic matter, crude protein, crude fat, crude ®bre,
nitrogen-free extractive.
lupin seeds were not incorporated. The reason for this was an unexpected very high HA in
extracted soyabean meal. In a further experiment, HA in extracts of soyabean meal, wheat
and manioc was measured using untreated erythrocytes and all results were negative.
During a last trial using Pronase-treated erythrocytes, HA was again determined in
Table 4
Trypsin inhibiting activity (TIA) and hemagglutination activity (HA) of diets and some ingredients
Dieta
TIAb,c
HAd
1G
1GE
1L15
1L15E
1L30
1L30E
1L30Ly
0
2.0
0.09
2.09
0.18
2.18
0.18
41
20±41
20±41
20±41
20±41
10±41
20±41
Lupin seeds
Egg powder
Soyabean meal
0.59
40.0
n.d.e
20±41
nd
1024±2048
a
Growth phase 1 only.
Trypsin inhibited, in mg/g of feed.
c
Calculated from TIA in lupin seeds and egg powder, assuming that other ingredients contained no trypsin
inhibitors.
d
Determined in duplo and when not identical, both values are shown.
e
Not determined, but usually negligible (solvent extracted).
b
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
95
extracts of the same ingredients and again high values were observed for soyabean meal
(1024 to 2048 units/mg), very low values for wheat (2±4 units) and no HA in manioc
extracts. It thus seems that use of Pronase treated erythrocytes increased the sensitivity of
the HA method to a very considerable extent.
3.2. Animal performance
3.2.1. General
Statistical treatment indicated that for all parameters studied, no signi®cant differences
could be observed between the group receiving the diet containing 300 g of lupin seeds
(L30) and the group fed the same diet but with extra supplementation of lysine (L30Ly).
Therefore, data concerning the latter group were not mentioned in the following tables.
Furthermore, statistical analysis also showed that between both the treatments, namely
addition of egg powder and lupin seed inclusion, no signi®cant interaction could be
calculated, except for one parameter, i.e. faecal digestibility of crude fat (Table 6).
Consequently, results for both treatments could be discussed separately in the text, while
the aspect of crude fat digestibility was brie¯y treated in Section 3.2.3. For statistical
treatment of the data concerning daily gain and feed intake during Growth phase 2 and
the entire trial, ®nal body weight was included as a covariate. The same procedure was
undertaken for carcass weight (Table 7).
3.2.2. Growth, feed intake and feeding ef®ciency
Addition of egg powder to the diet had no effect on the parameters investigated
(Table 5). A trend to a lower average daily gain was observed for the groups fed 300 g of
lupin seeds/kg of feed. Feed conversion ratio was not in¯uenced.
3.2.3. Digestibility of nutrients
Digestibility of the crude fat fraction was higher in diets containing egg powder and
lupin seeds (Table 6). Statistical treatment revealed interaction between both treatments
due to the fact that digestibility coef®cients increased with increasing amounts of lupin
seed in the diet, but only in the presence of egg powder. Compared to the control group,
crude ®bre digestibility tended to be higher for lupin seed-containing diets. Digestibility
of the other nutrients was not altered by both the treatments.
3.2.4. Slaughtering performance and carcass characteristics
Carcass weight and dressing percentage of animals receiving lupin seeds was lower
than the other groups (Table 7). No statistically signi®cant differences were observed with
regard to percent lean in carcass and backfat thickness, although a tendency towards more
lean and less fat in carcass of animals receiving lupin seeds was observed. Fatty acid
pattern in lipids of diets, lupin seeds, egg powder and backfat is presented in Table 8. It is
clear that fatty acid composition of the diets was rather variable, being the resultant of
using different proportions of ingredients as listed in Table 2. On the other hand, fatty
acid pro®le of backfat was fairly constant for the different treatments, as only for the
proportion of C18:1, slightly higher values were found in animals fed lupin seeds. C18:3,
C20:0 and C20:1 could not be detected in backfat samples.
96
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
Table 5
Reponse of growing pigs to diets containing L.albus seeds fed without or with egg powder
Parametera
SEMc
Treatment
egg powder(g/kg)
b
lupin seeds (g/kg)
0(18)
50(18)
0(12)
150(12)
300(12)
Phase 1
LW1 (kg)
LW2 (kg)
ADG (g)d
Feed intake (kg/d)e
FCR
23.9
43.1
534
1.31
2.49
23.7
42.8
552
1.38
2.53
23.9
43.5
598
1.47
2.54
23.8
42.5
528
1.35
2.57
23.5
42.9
504
1.21
2.42
0.37
0.29
15
0.03
0.04
Phase 2
LW1
LW2
ADG
Feed intakef
FCR
43.1
102.1
767
2.62
3.45
42.8
101.8
791
2.66
3.38
43.5
102.8
792
2.71
3.44
42.5
102.6
800
2.78
3.48
42.9
100.4
744
2.44
3.34
0.29
0.53
13
0.05
0.08
Total trial
ADGf
Feed intakef
FCR
689
2.20
3.21
715
2.25
3.17
727
2.32
3.20
706
230
3.27
674
2.05
3.10
10
0.04
0.07
a
LW1, LW2, respectively, initial body weight and weight at end of growth phase; ADG. average daily gain;
FCR, feed conversion ratio (kg of feed/kg of gain).
b
Number of observations in parentheses.
c
Standard of the mean, calculated from pooled values (n 36).
d
Trend for linear effect of lupin seeds (p < 0.1).
e
Linear effect of lupin seeds (p < 0.01).
f
Linear effect of lupin seeds (p < 0.05).
Table 6
Apparent faecal digestibility coef®cients of nutrients
Nutrient
SEMb
Treatment
egg powder(g/kg)
a
Dry matter
Organic matter
Crude protein
Crude fatc
Crude ®bred
NFEe
a
lupin seeds (g/kg)
0(9)
50(9)
0(6)
150(6)
300(6)
0.79
0.84
0.73
0.46
0.50
0.93
0.81
0.85
0.80
0.67
0.51
0.92
0.80
0.84
0.77
0.51
0.44
0.92
0.81
0.85
0.80
0.57
0.57
0.93
0.79
0.83
0.78
0.61
0.51
0.93
0.005
0.005
0.010
0.011
0.016
0.003
Number of observations in parentheses.
Standard error of the mean, calculated from pooled values (n 18).
c
Linear and quadratic effect of lupin seeds (p < 0.01). An interaction effect between the treatments egg
powder and lupin seeds was noted.
d
Trend for linear effect of lupin seeds (p < 0.1).
e
Nitrogen-free extractives.
b
97
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
Table 7
Slaughter and carcass characteristics
Parameter
SEMf
Treatment
egg powder(g/kg)
a
b
LW (kg)
Carcass weight (kg)c
Dressing %d
% Lean
Backfat thicknesse (mm)
lupin seeds (g/kg)
0(18)
50(18)
0(12)
150(12)
300(12)
101.1
84.9
84.0
60.2
80.7
101.1
84.9
84.0
60.3
77.8
102.3
86.1
85.0
59.1
83.7
101.3
85.1
84.1
60.2
83.3
99.6
83.5
82.8
61.6
70.7
0.5
0.3
0.3
0.9
2.9
a
Number of observations between parentheses.
Body weight at slaughter.
c
Linear effect of lupin seeds (p < 0.01).
d
Linear effect of lupin seeds (p < 0.05).
e
Sum of measurements at three locations: 1st, 7th and last rib.
f
Standard error of the mean, calculated from pooled values (n 36).
b
Table 8
Fatty acid pro®le (g/kg) of lipid in diets, egg powder, lupin seeds and backfat
Diet
Fatty acid
C16:0
C16:1
C18:0
C18:1
C18:2
C18:3
2G
2GE
2L15
2L15E
2L30
2L30E
2L30Ly
223
211
195
197
172
137
191
0
12
17
20
26
21
0
67
57
44
57
27
32
53
331
297
314
346
369
455
371
308
310
319
245
289
223
312
26
25
38
30
42
52
46
0
0
0
0
0
0
0
0
0
0
13
0
18
0
55EPa
L. albus seeds
265
92
28
10
98
20
463
550
125
140
6
67
0
11
0
41
Backfat
Fatty acid
Treatment
egg powder (g/kg)
b
C16:0
C16:1
C18:0
C18:1d
C18:2
a
lupin seeds (g/kg)
0(18)
50(18)
0(12)
150(12)
300(12)
SEMc
250
7
157
518
68
248
13
149
522
68
252
11
158
505
75
254
11
154
517
64
242
8
146
538
66
2
2
3
5
3
Egg powder (from Cotterill et al., 1978).
Number of observations in parentheses.
c
Standard of the mean, calculated from pooled values (n 36).
d
Linear effect of lupin seeds (p < 0.05).
b
C20:0
C20:1
98
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
4. Discussion
4.1. Diet composition and digestibility of nutrients
In agreement with literature data (Hill, 1977), TIA of L. albus seeds was very low, as
opposed to whole egg powder. Ovomucoid (100 g/kg egg protein) is one of the most
important trypsin-inhibiting substances (Kato and Matsuda, 1997). Hartmann (1995) also
found very high concentrations of trypsin and cathepsin D inhibitors in egg white and
yolk. The present experiment showed that TIA in the diets fed was too low to have
caused growth inhibition of the animals. The fact that in extracts of solvent extracted
soyabean meal considerable HA as a measure of lectin activity was found, was due to the
use of protease-treated erythrocytes making the method much more sensitive. Very
recently, small but substantial amounts of carbohydrate-binding lectin could be
determined in several samples of conventionally processed soyabean meal (Maenz
et al., 1999). It is certainly not known to what extent these residual lectins can affect
performance of pigs or other animals. However, this phenomenon cannot account for
the lower performance of the groups fed lupin seed diets in this experiment, as the
proportion of solvent-extracted soyabean meal in these diets was much lower than in
the control diet (Tables 1 and 2).
Apparent faecal digestibility coef®cients of the different nutrients were within
the normal range observed with similar diets (Zettl et al., 1995; Flis et al., 1996).
Higher digestibility of crude fat in diets containing egg powder are related to
somewhat higher lipid content of these rations (Table 3, Growth phase 2) and this
fraction must have been highly digestible. Digestibility of the crude-®bre fraction
was higher in the present experiment, but in the literature this value was found to be
rather variable and also dependent on the other ingredients in the ration. Additionally,
Aguilera et al. (1985) determined a digestibility coef®cient of 0.83 for crude ®bre
in L. albus, cv. Multolupa.
4.2. Growth, feed intake and feeding ef®ciency
Daily gain and feed conversion ratios observed were comparable with results of other
studies feeding similar diets (Pearson and Carr, 1977; Batterham, 1979; Zettl et al., 1995).
Supplementing the L30 diet with lysine (L30Ly) had no effect on performance, which
agrees with Batterham et al. (1986), who investigated the effect of mixing seeds of L.
angustifolius in pig diets. The possibility of the presence of factors in the seeds also
decreasing utilization of the lysine supplement, a phenomenon thought to be speci®c to
pigs, was also considered. In experiments with rats receiving L. angustifolius seeds,
Rahman et al. (1997) concluded that a low utilization of absorbed N was caused by an
increased N-excretion in urine, indicating disturbances in the systemic N-metabolism. Nutilization was also negatively in¯uenced by the presence of important amounts of nonstarch polysaccharides (NSP).
Literature data show that the in¯uence of lupin seeds on daily gain and feed
consumption of fattening pigs was not very consistent. The effect of adding extra lysine
or methionine to diets containing lupin seeds has also been variable. Overall results
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
99
showed that feeding diets containing >200 g of lupin seeds/kg of feed caused a lowered
daily gain and feed intake, especially during a ®rst growth phase, although differences
were not always statistically signi®cant (Pearson and Carr, 1977; Batterham, 1979; Zettl
et al., 1995). Feed conversion ratio was not in¯uenced. Several mechanisms explaining
these observations have been proposed. Seeds of L. albus can contain very high amounts
of Mn (467±3750 ppm) and it has been suggested that such high concentrations can
possibly result in depressed growth in pigs (National Research Council, 1998). On the
other hand, the presence of quinolizidine alkaloids decrease palatability of the diet
causing lower feed intake. Analysis of alkaloids in the lupin seeds fed in the present
experiment showed a total amount of 0.0123 mg/100 mg of seeds with the following
pattern: 0.0011 mg of angustifoline, 0.0090 mg of lupanine and 0.0022 mg of 13-OH
lupanine. Taking into account the available literature data, it can be concluded that
alkaloids in the current diets were not responsible for the lowered feed intake or growth
performance because their concentration was very low (Godfrey et al., 1985;
Buraczewska et al., 1993; Wasilewko et al., 1997). It was also clearly established by
Pearson and Carr (1977) that an eventual high amount of manganese in lupin seeds was
not responsible for unfavourable effects; the authors suggested that besides an eventual
high content of alkaloids, other factors were probably responsible for lower feed intake of
lupin seed-containing diets. As it has been shown that lysine in lupin seeds and also lysine
supplemented to diets containing lupin seed was only utilized with an abnormally low
ef®ciency, it cannot be completely excluded that poorer performances of the animals
observed in the current experiment were due to an inadequate provision of this essential
amino acid (Batterham et al., 1986).
Addition of whole egg powder (50 g/kg) to the different diets had no effect on growth
performance and feed intake, which was completely different from the effect of egg
powder in piglet and chicks diets, where growth inhibition has been observed (Peo et al.,
1969; Watkins and Veum, 1986; Kratzer et al., 1988). It also ruled out the possibility of
biotin de®ciency caused by the presence of avidin in the egg powder in the current trial
(Kratzer et al., 1988).
4.3. Carcass characteristics and fatty acid pro®le of backfat
The lower carcass weight and dressing percentage of animals receiving the highest
amount of lupin seeds is probably due to a larger gut ®ll caused by the higher ®bre
content of this diet (Batterham, 1979), while the tendency towards more lean and
less fat in their carcass is probably the result of slower growth rates related to lower
fat deposit.
Fatty acid pattern of lipid in lupin seeds used in this experiment agrees well
with the range reported in literature, although the proportion of a-linolenic acid
(C18:3) was somewhat lower (Green and Oram, 1983; Roth-Maier and Kirchgessner,
1993; Zettl et al., 1995; Zdunczyk et al., 1996). Fatty acid pattern of backfat was
rather constant and did not re¯ect the changes in fatty acid proportion determined in
the diets, which was also found by Zettl et al. (1995). Therefore, it can be concluded
that consistency and stability of backfat was not in¯uenced by addition of lupin seed
or egg powder.
100
C. Van Nevel et al. / Animal Feed Science and Technology 83 (2000) 89±101
5. Conclusions
It can be stated with certainty that the presence of lectins did not play a role in the
problems observed when lupin seeds were fed, as their concentration was very low, and
the fact that adding whole egg powder had no effect on parameters studied supports this
statement. On the other hand, the exact reasons for the negative effects on feeding lupin
seeds remain unknown and could not be determined from this experiment.
Acknowledgements
The research was ®nancially supported by the Ministry of Agriculture, DG6,
Brussels and VEOS nv. Zwevezele, Belgium. Technical help from S. Galle, E. Maes,
Daisy Bayens, H. De Rycke, N. Vanrolleghem and Jenny Martens is gratefully
acknowledged.
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