Chemical changes and influences of rapeseed
antinutritional factors on lamb physiology
and performance
1. Animal performance and thyroid histology
G. Derycke
a, N. Mabon
b, S.N.M. Mandiki
a,*, J.L. Bister
a,
J.-P. Wathelet
b, M. Marlier
b, R. Paquay
aaFaculteÂs Universitaires Notre-Dame de la Paix, Laboratoire de Physiologie Animale,
rue de Bruxelles 61, B-5000 Namur, Belgium
bFaculte Universitaire des Sciences Agronomiques, Unite de Chimie GeÂneÂrale et Organique,
Passage des deÂporteÂs 2, B-5030 Gembloux, Belgium
Received 7 July 1998; received in revised form 19 January 1999; accepted 19 May 1999
Abstract
Sixty six Texel, Suffolk or crossbred lambs allocated to three groups were used. From the end of their first month of age till slaughtering, they were fed ad libitum with concentrates containing 0% (Control) or 25% of rapeseed meal obtained from either Samourai (Samourai) or Honk (Honk) variety. The Samourai and Honk concentrates contained 1.95 and 4.22 mmoles/g DM of glucosinolates, respectively. Lambs were weaned at 888 days of age and 245 kg of live weight and were slaughtered when their fattening state was estimated to be optimal. Apart from low concentrate intake for suckling lambs at the beginning of the experiment in the Honk, no negative effect of low glucosinolates (LG)-rapeseed meal was noted concerning animal performance. The quality of perirenal fat was better for lambs which received rapeseed meal since lower (P< 0.5) proportions of saturated fatty acids (C10 : 0, C12 : 0, C14 : 0) and higher contents (P< 0.05) of some
unsaturated fatty acids (C18 : 1trans, C22 : 2) were determined. The thyroid weight was significantly
higher (P< 0.05) for the Honk (3.040.8 g) than in the Control (2.60.5 g) and the Samourai (2.70.6 g). Moreover, the percentages of small thyroid follicles were lower (P< 0.05) in the Honk than in the Control and Samourai groups. Conversely, the percentages of large thyroid follicles were higher (P< 0.05) in the Honk than in the two other groups. These results suggest that rapeseed meal can be used as the only protein supplement for fattening lambs despite the
81 (1999) 81±91
*Corresponding author. Tel.: +32-81724377; fax: +32-81724420
E-mail address: robert.mandiki@fundp.ac.be (S.N.M. Mandiki)
modification of thyroid histology by high glucosinolate content.#1999 Elsevier Science B.V. All rights reserved.
Keywords: Rapeseed meal; Sheep-lamb; Animal performance; Thyroid
1. Introduction
In comparison to soyabean meal, the nutritive value of rapeseed meal has been investigated mainly with regard to the effects of antinutritional factors on feed intake, zootechnical performance, morphological and physiological disturbances and quality of products. There are also reports on the changes in glucosinolates concentration during the technological processing, and in the digestive system (micro-organisms) as well as on the effects of breakdown products of glucosinolates (nitriles, isothiocyanates, thiocyanate ions, oxazolidinethione) in the animal.
The effects of antinutritional factors depend on their amount in the diet, thus, genetic improvement has been made in order to reduce the erucic acid and glucosinolate content in the rapeseed (varieties 00 or Canola). Up to now, rapeseed oil has been mainly used in human nutrition. However, new industrial applications are nowadays developing (fuel, cosmetic products, lubricant industry) and this may arise the interest in new varieties suitable for industrial purposes but which may contain more glucosinolates than the best current Canola varieties.
Moreover, studies on ruminants are still incomplete and most of them did not clarify the set of problems encountered with the rapeseed use in animal feeding. Indeed, some studies suggest that rapeseed meal might constitute the only source of protein for dairy cows and fattening cattle (Fiems and Buysse, 1985), but investigations are still needed to establish the maximal amount of rapeseed which may be included in the diet of ruminants, especially the young animals (Hill, 1991; Bell, 1993; Mawson et al., 1994a, b).
A large experiment on the optimal level of rapeseed meal in the diet of ruminants (cattle and sheep) during different physiological states (growth-fattening and gestation-lactation) was undertaken in order to study simultaneously several aspects, such as metabolism and target organs of glucosinolates, zootechnical performance, endocrine and metabolic modifications, morphology and physiology of some organs and quality of products. This series of articles summarizes a study on the effects of two rapeseed varieties with different levels of glucosinolates on the growth and fattening performance of lambs. We will successively present data concerning the animal performance and histological aspects (part 1), the plasma substances and thyroid activity (part 2) and the metabolism as well as the target organs of antinutritional substances (part 3).
2. Materials and methods
2.1. Animal and management
The experiment was carried out at the Ovine Research Centre of Faulx-les-Tombes (508250North and 5820East), Belgium. Sixty six Texel, Suffolk or crossbred lambs were
allocated to three groups according to their sex, body weight (8.92.8 kg) and age
(288 day). They received ad libitum water and hay plus concentrates containing 0%
(Control) or 25% of rapeseed meal obtained from either the rape varieties Samourai
(15mmoles of glucosinolates/g dry matter-DM in the oil seed, 1.95mmoles of
glucosinolates/g DM in the complete concentrate) or Honk (33 and 4.22mmoles of
glucosinolates/g, respectively). Rapeseed meal was the sole supplement for the two experimental concentrates. The two types of rapeseed meal were chosen among the varieties used in Belgium on the basis of total glucosinolates content and their distribution, especially the percentage of progoitrine, the major precursor of the 5-vinyl-1,3-oxazolidine-2-thione during metabolism. According to the criteria used to define the Canola rapeseed varieties (<30 mmoles of glucosinolates/g in the free-oil dry matter, Bell, 1993) the Samourai variety qualifies as Canola while the Honk variety does not qualify but the two rapeseed concentrates are considered as a low glucosinolates (LG)-rapeseed meal as reported previously by (<10 mmoles of glucosinolates/g DM in diet, Mawson et al., 1994a, b).
From weaning, at 888 days of age and 245 kg of live weight to slaughter weight (30±35 kg for female, 35±40 kg for males) concentrates were the major component of the diet apart from a small quantity of hay (0.4 kg/day).
Lambs were weighed at birth and afterwards fortnightly and just before slaughtering. Feed intake was also estimated fortnightly. After slaughtering, the carcasses were weighed and evaluated for conformation and fattening state. Thyroids were collected at slaughtering and immediately weighed. Samples of perirenal fat were also collected and stored frozen.
2.2. Methods
2.2.1. Diet composition and analysis
The experimental concentrates were presented as pellets of 4 mm diameter, their composition being shown in Table 1. The rapeseed meal was `Schilffers' obtained after oil extraction with an experimental pressing machine based on an Archimedian screw without heating and pounding units.
The chemical composition of seeds, rapeseed meal and concentrates was determined by official procedures (AOAC, 1980). The energy value and digestibility of organic matter were determined as described by De Boever et al. (1986). The fatty acids composition of diet and perirenal fat was determined by gas±liquid chromatography. High performance liquid chromatography (HPLC) by elution gradient was used for glucosinolate determination (ISO No. 9167-1). Details concerning glucosinolates and their breakdown products will be presented in the third article of the series.
2.2.2. Body weight and carcass evaluation
The animals and diets were weighed using an electronic scale (100 g). The carcass
conformation was estimated using the SEUROP system (S= highest score, P= lowest
score). To facilitate this estimation, numeric scoring was used (S= 6, P= 1). For the fattening state, a scoring scale of 1 (very lean) to 5 (very fat) was used.
2.2.3. Histology of thyroid
Just after slaughtering, the thyroids were weighed and stored in Bouin solution. After
paraplast inclusion, slices of 7mm were made and stained with HES (Hemalun±
Erythrosine±Safran) or Trichrome of Masson before being examined with a microscope.
After visual inspection, the slides were photographed at 1010 and 1032
magnification with a color film 800 ASA, 13536. The pictures were produced in a
digital form on disk by the Kodak Society and stored in JPEG format, they were analysed using a photosharp program running on a Macintosh personal computer. All the follicles observed on pictures taken with low magnification were classified by their diameter into three classes, ranging from 25, 50 and >75 pixels for small, medium and large follicles, respectively. The surface of the six larger follicles was measured. For each follicle, the mean height of the surrounding cells was estimated by measuring the height of six different cells at the circumference of this follicle.
2.2.4. Statistical analysis
Data are expressed as means with or withoutSD. They were analysed using GLM
procedures (SAS, 1985). The two-way analysis of variance was followed by the Fisher's protected LSD test when the main or interaction effects were significant (P< 0.05). All parameters expressed in percentages were ln-transformed before statistical analysis.
3. Results
3.1. Chemical composition of diets
The chemical composition of the three concentrates is presented in Table 2. Table 1
Composition of the Control, Samourai or Honk concentrates (%)
Control Samourai or Honk
Ovine minerals and vitamins mixture 1.0 1.0
Peas 5.9 ±
Maize gluten feed 15.0 ±
Full fat toasted soyabean 9.9 ±
Rapeseed meal (15% ether extract) ± 25.0
The protein content was 18.5 and 18.9% respectively, for the Samourai and Honk seeds and 26 and 26.8% for the rapeseed meal. Regarding the ether extract, high concentrations were obtained in the Samourai (41%) and Honk (41%) seeds as well as in the meal (21 and 22%) as an indication of a slight extraction of oil during the experimental process. Consequently, the fat content in the pellet concentrates (5±7% DM) was very high and thereby the net energy (8.1 MJ/kg DM). The fibre content expressed in NDF or ADF was slightly higher in the Control than in the two experimental concentrates with rapeseed meal.
As compared to the Control concentrate, very low proportions of saturated fatty acids (C12 : 0, C14 : 0) and a high proportion of unsaturated fatty acids, mainly the C18 : 1were
obtained in the concentrates with rapeseed meal. The Control diet also contained a high C18 : 2proportion.
3.2. Growth and carcass
From birth to slaughtering, no significant effects of rapeseed meal were observed. The daily weight gains before weaning varied between 241 and 255 g and increased after weaning to 262, 270 and 258 g respectively, for the Control, Samourai and Honk (Table 3). Consequently, the age at slaughtering was comparable among groups (between 130 and 135 days for the three groups).
Table 2
Chemical composition of concentrates (DM)
Control Samourai Honk
Net energy (MJ) 8.1 8.4 8.6
Crude protein (%) 18.3 16.4 15.9
Ether extract (%) 5.30 6.24 6.87
NDF (%) 35.4 26.6 26.1
ADF (%) 14.5 13.1 13.1
Starch (%) 17.19 22.73 22.52
Minerals (%) 9.97 9.16 8.66
Glucosinolates (mmoles/g DM) ± 1.95 4.22
Digestibility of organic matter (%) 90.9 90.8 91.2
Fatty acid composition (% of total fat)
C10 0.2 0.7 1.0
The slaughter data (carcass weight, dressing percentage, carcass classification and fat states, Table 4) did not differ significantly among groups. Only the quality of perirenal fat showed some modifications. The concentrates with rapeseed meal induced a significant (P< 0.05) decrease in some saturated acids (C10 : 0, C12 : 0 and C14 : 0). Moreover, an
increase (P< 0.01) in C22 : 2 was noted for the two experimental concentrates and this
was also apparent fortransC18 : 1 for the Honk group. The cholesterol concentrations
were respectively of 0.520.13; 0.540.08 and 0.660.13 mg/ml for the Samourai,
Honk and Control groups.
3.3. Feed intake and conversion
Before weaning, the concentrate intakes were low especially for the Honk group, at the start of feeding with rapeseed concentrates (Table 5). Indeed, lambs in the Honk group consumed only 7.4 kg DM of concentrates compared to 9.9 kg DM for those in the Samourai or Control groups. From weaning till the end of the fattening period values were similar among the three groups both for the concentrate (43.1, 41.3 and 41.4 for the Control, Samourai and Honk, respectively) and hay intake (400 g/lamb/d). The feed conversion was also similar among groups (3.41, 3.48 and 3.61 for the Control, Samourai and Honk, respectively)
3.4. Weight and histology of thyroid
Thyroid weights, expressed as absolute values or relative to body weight were comparable for the Control and the Samourai group (Table 6). In contrast, they were 15 or 18% higher (P< 0.05) in the Honk than in the Control.
Moreover, the proportion of small follicles was significantly lower (P< 0.05) in the Honk group compared to the Control group but the difference between Honk and Samourai groups was not significant. The proportions of large thyroid follicles were significantly higher (P< 0.05) in the Honk than in the Samourai and Control. Values were Table 3
Table 4
Slaughter performance of lambsa
Control Samourai Honk
Carcass weight (kg) 17.01.6 17.41.6 17.21.2
Dressing percentage 48.43.0 49.42.3 48.63.0
Carcass classification (score 1±6) 3.70.8 3.70.9 3.60.8
Fat state (score 1±5) 2.20.4 2.30.4 2.40.4
Fatty acid (mass %) composition of perirenal fat
C10 : 0 0.32 a 0.25 b 0.20 b
aValues carrying a and b are significantly different means (P< 0.05).
Table 5
Diet intake and feed conversion
Control Samourai Honk
Concentrate intake (dry matter)
Intake before weaning (kg) 9.91 9.92 7.41
Intake after weaning (kg) 43.21 41.35 41.39
Total intake (kg) 53.12 51.27 48.80
Daily intake before weaning (g/d) 163 164 124
Daily intake after weaning (g/d) 847 915 849
Daily intake after weaning (g/kg LW0.75/d) 67 70 66
Hay intake
Intake after weaning (g/d) 354 356 361
Dry matter intake
Intake after weaning (g/d) 1.1 1.0
Feed conversion
After weaning (kg/kg) 3.41 3.48 3.61
comparable among the three groups for medium follicles. No significant difference was calculated between groups concerning the surfaces of the largest thyroid follicles. The height of follicular cells was relatively constant and did not significantly differ between treatments.
4. Discussion
4.1. Diets
The current experiment showed the effects of massive incorporation of a low glucosinolates (LG) rapeseed meal obtained from either a high glucosinolates or double low-rapeseed varieties in the diet of young lambs. The concentrates were offered ad libitum from the end of their first month of age and were the major component of the diet from weaning to the end of the experiment. Moreover, the LG-rapeseed meal was almost the sole protein supplement for the two experimental concentrates.
Diets with rapeseed meal contained slightly low contents of fiber in relation to differences in proportions of ingredients (e.g. lucerne, etc.). As a consequence of an elevated residual concentration of fat (21 and 22%) in the rapeseed meal, the experimental diet had a very high concentration of ether extract (5±7%), and thereby a high energy value (e.g. 8.1 and 8.4 MJ/ kg DM versus 7.9 MJ/kg DM of net energy for the barley).
The incorporation of LG-rapeseed meal in the pellets decreased the proportions of saturated fatty acids and increased the contents of unsaturated fatty acids such as C18 : 1transcontent in the ether extract as previously reported by Vanbelle and Tychon
(1986) and Emanuelson et al. (1991).
4.2. Animal performance
Whatever the zootechnical parameter considered (live weight, gains, food intake, feed conversion, carcass weight, dressing percentage, carcass classification, fat state), the Table 6
Weight and some histological characteristics of the thyroida
Control Samourai Honk
Weight (g) 2.60.5 2.70.6 3.00.8 b
Ratiob 73
12 a 7716 8626 b
Height of follicular cells (p)c 27.8
4.6 28.32.0 293.5
Surface of follicles (p)d 27.8
16 24.15 27.97
Proportions of follicles (%)d
Small follicles (25 p in diameter) 4227 a 2913 b 2415 b
Medium follicles (50 p in diameter) 4520 557 5112
Large follicles (>75 p in diameter) 1214 a 1410 a 2718 b
aValues carrying a and b are significantly different means (P<0.05). bThyroid weight in milligram per final body weight in kilogram. cp: Pixel.
dPercentages of follicles per unit of thyroid tissue.
incorporation of LG-rapeseed meal in the diet had no significant negative effect. After weaning, the growth rate (250±270 g/day) and the feed efficiency were satisfactory in all treatments despite a slightly low level of concentrate intake (1 kg/animal) and in agreement with the available results in the literature (Mawson et al., 1994a).
Concerning the intake, Hill (1991) reported that `it would be reasonable to assume low glucosinolates rapeseed meal could be included as the sole protein supplement in `starter' concentrates but that this should be demonstrated by experiments'. Using rapeseed meal, Theriez et al. (1971) noted intake to be less than with linseed meal. The latter authors did not give a value for glucosinolates concentration, which would be elevated in rapeseed varieties used at that time. In contrast to this, Hill et al. (1990) did not find any effect on feed intake of using concentrates made from rapeseed meal with low glucosinolate content (0±17.5mmol/g DM).
Regarding liveweight gain, it was reported that in early weaned lambs, the rate of weight gain from a concentrate feed containing high-glucosinolate rapeseed meal was less than that obtained using low-glucosinolate rapeseed meal or soyabean meal but remained acceptable (Hill, 1991; Mawson et al., 1994a). Other authors (Hopkins et al., 1995) found that lambs reared on rapeseed pasture were heavier than those grazing on irrigated perennial pasture. The negative influence of high-glucosinolate rapeseed meal on growth rate may be related to a drastic endocrine disturbance-induced antinutritional factors as reported by Ahlin et al. (1994). But, as we found, other authors (Theriez et al., 1971; Hill et al., 1990) did not observe any negatvie effect.
The results of the current study show that rapeseed meal has no negative effect on carcass quality. Few data are available in the literature concerning the slaughter performance of lambs fed with rapeseed meal. Hill (1991) note that `no published information is available to indicate that rapeseed meal has any adverse effect on carcass flavour' in lambs. On the same regard, Hopkins et al. (1995) reported that `based on objective assessments, the meat of lambs which grazed on rapeseed pasture will be of quality similar to that from lambs finished on perennial pasture, but that from subjective assessment of quality, some Australian consumers may detect a stronger, less acceptable flavour from the meat of rapeseed feed lambs'. In the current study, the use of rapeseed meals induced a significant decrease in the proportions of some saturated fatty acids (C12 : 0, C14 : 0) and an increase in unsaturated fatty acids of perirenal fat, mainly C22 : 2
and to less extenttransC18 : 1in Honk group. This modification is related to the chemical
composition of rapeseed meal and agrees with previous report (Emanuelson et al., 1991; Mawson et al., 1994a) that the incorporation of a high proportion of rapeseed meal in the diet of dairy cows increased the percentage of poly-unsaturated fatty acids in milk.
4.3. Thyroid weight and histology
Numerous studies have demonstrated that in non-ruminant animals, rapeseed meal has various effects on the development of the thyroid (hypertrophy), liver and kidney and modifies the histology of these organs. These changes have been described by Mawson et al. (1994b). The available results in the literature on ruminants seem conflicting and may vary according to the age of animal, with the youngest being more susceptible.
In the current study, we observed that the Samourai rapeseed meal, which had a low glucosinolate content, had no effect on the thyroid, whereas the Honk variety of high glucosinolate content modified the weight and the histology of this organ. These results agree with the previous finding by Hill et al. (1990) suggesting that the thyroid weight is positively correlated to the glucosinolate concentration in the diet for lambs during the rapid growth phase.
The differences between monogastric animals and ruminants as well as between young and adult ruminants in the effects of rapeseed meal, are due to the action of micro-organisms in the digestive system of ruminants which induce a transformation of glucosinolates and metabolites (Fiems and Buysse, 1985; Mawson et al., 1994b). This topic as well as the effect of hyperthyroidism on other parameters will be presented in the following parts of this series.
These results suggest that rapeseed meal can be used as the sole protein supplement for fattening lambs despite the modification of thyroid histology by a high intake of glucosinolates.
Acknowledgements
This work was supported by the General Office of Research and Development of the Belgian Agricultural Ministry and by the General Direction of Technologies, Research and Energy of Ministery of `Region Wallonne' in Belgium. The authors are grateful to M. A. Bouckoms-Vandermeir, the staff of Ovine Research Centre, the laboratory of Faulx-les-Tombes (Namur) and to M. Hardenne of the Department of General and Organic Chemistry of Gembloux for their technical assistance.
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