Hostname: page-component-7b9c58cd5d-nzzs5 Total loading time: 0 Render date: 2025-03-15T08:33:05.050Z Has data issue: false hasContentIssue false
  • English
  • Français

Dietary low-glucosinolate rapeseed meal affects thyroid status and nutrient utilization in rainbow trout (Oncorhynchus mykiss)

Published online by Cambridge University Press:  09 March 2007

Christine Burel ,
Thierry Boujard ,
Anne-Marie Escaffre ,
Sadasivam J. Kaushik ,
Gilles Boeuf ,
Koen A. Mol ,
Serge Van der Geyten  and
Eduard R. Kühn
Christine Burel
Affiliation:
Laboratoire de Nutrition des Poissons, Unité mixte INRA-IFREMER, Station d'Hydrobiologie, BP 3, 64310 Saint Pée-sur-Nivelle, France
Thierry Boujard*
Affiliation:
Laboratoire de Nutrition des Poissons, Unité mixte INRA-IFREMER, Station d'Hydrobiologie, BP 3, 64310 Saint Pée-sur-Nivelle, France
Anne-Marie Escaffre
Affiliation:
Laboratoire de Nutrition des Poissons, Unité mixte INRA-IFREMER, Station d'Hydrobiologie, BP 3, 64310 Saint Pée-sur-Nivelle, France
Sadasivam J. Kaushik
Affiliation:
Laboratoire de Nutrition des Poissons, Unité mixte INRA-IFREMER, Station d'Hydrobiologie, BP 3, 64310 Saint Pée-sur-Nivelle, France
Gilles Boeuf
Affiliation:
Laboratoire de Physiologie des Poissons, IFREMER, Station de Brest, BP 70, 29280 Plouzané, France
Koen A. Mol
Affiliation:
Laboratory of Comparative Endocrinology, Catholic University of Leuven, Naamsestraat 59, 3000 Leuven, Belgium
Serge Van der Geyten
Affiliation:
Laboratory of Comparative Endocrinology, Catholic University of Leuven, Naamsestraat 59, 3000 Leuven, Belgium
Eduard R. Kühn
Affiliation:
Laboratory of Comparative Endocrinology, Catholic University of Leuven, Naamsestraat 59, 3000 Leuven, Belgium
*
*Corresponding author: Dr Thierry Boujard, fax +33 (0) 5 59 54 51 52, email boujard@st-pee.inra.fr
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Two rapeseed (Brassica napus) meals, RM1 and RM2, with two levels of glucosinolates (GLS; 5 and 41 μmol/g DM respectively) were incorporated at the levels of 300 and 500 g/kg of the diets of juvenile rainbow trout (Oncorhynchus mykiss) in replacement of fish meal, and compared with a fish-meal-based diet. A decrease in the digestibility of the DM, protein, gross energy and P was observed with high-rapeseed meal (RM) incorporation. In trout fed on RM-based diets, growth performance was reduced even after only 3 weeks of feeding. Feed efficiency was adversely affected by RM and GLS intake. Protein and energy retention coefficients were significantly lower in fish fed on the diet containing the higher level of GLS. P retention was significantly lower with all the RM-based diets than with the fish-meal diet. Irrespective of the degree of growth inhibition, fish fed on RM-based diets exhibited similar typical features of hypothyroid condition due to GLS intake, expressed by lower plasma levels of triiodothyronine and especially thyroxine and a hyperactivity of the thyroid follicles. This hypothyroidal condition led to a strong adjustment of the deiodinase activities in the liver, the kidney and the brain. A significant increase of the outer ring deiodinase activities (deiodinases type I and II respectively) and a decrease of the inner ring deiodinase activity (deiodinase type III) were observed. It is concluded that the observed growth depression could be attributed to the concomitant presence of GLS, depressing the thyroid function, and of other antinutritional factors affecting digestibility and the metabolic utilization of dietary nutrients and energy.

Keywords

Rainbow troutRapeseedGrowthGlucosinolatesThyroid function
Type
Research Article
Information
British Journal of Nutrition , Volume 83 , Issue 6 , June 2000 , pp. 653 - 664
Copyright
Copyright © The Nutrition Society 2000

References

Abdou Dade, BAguirre, P, Blanc, D and Kaushik, SJ (1990) Incorporation du colza 00 sous forme de tourteau ou d'amande dans les aliments de la truite arc-en-ciel (Oncorhynchus mykiss): performance zootechnique et digestibilité (Incorporation of rapeseed 00, in the form of cattle cake, or almond in diets for rainbow trout (Oncorhynchus mykiss): zootechnical performance and digestibility) Bulletin Francais de la Pêche et de la Pisciculture 317, 50–57.CrossRefGoogle Scholar
Bell, JM (1993) Factors affecting the nutritional value of canola meal: a review Canadian Journal of Animal Science 73, 679–697.CrossRefGoogle Scholar
Bille, NEggum, BOJacobsen, IOlsen, O and Sorensen, H (1983) Antinutritional and toxic effects in rats of individual glucosinolates (+/- myrosinases) added to a standard diet Zeitschrift fur Tierphysiologie, Tierernahrung und Futtermittelkunde 49, 195–210.CrossRefGoogle ScholarPubMed
Boeuf, G and Prunet, P (1985) Measurements of gill (Na+-K+)ATPase activity and plasma thyroid hormones during smoltification in Atlantic salmon (Salmo salar L.) Aquaculture 45, 111–119.CrossRefGoogle Scholar
Bolin, DWKing, RP and Klosterman, EW (1952) A simplified method for the determination of chromic oxide (Cr2O3) when used as an index substance Science 116, 634–635.CrossRefGoogle Scholar
Bourdon, D and Aumaître, A (1990) Low-glucosinolate rapeseeds and rapeseed meals: effect of technological treatments on chemical composition, digestible energy content and feeding value for growing pigs Animal Feed Science and Technology 30, 175–191.CrossRefGoogle Scholar
Boyages, SCCollins, JKMaberly, GF, Jupp, JJMorris, J and Eastman, CJ (1989) Iodine deficiency impairs intellectual and neuromotor development in apparently normal persons: a study of rural inhabitants of north-central China Medical Journal of Australia 150, 676–682.CrossRefGoogle Scholar
Bunting, ES (editor) (1981) Production and Utilization of Protein in Oilseed Crops. The Hague: Martinus Nijhoff.CrossRefGoogle Scholar
Choubert, G (1999) La digestibilité des nutriments chez les poissons: aspects de méthodologie. (Digestibility of nutrients by fish: methodological considerations) Cybium 23(Suppl.), 113-125.Google Scholar
Choubert, GDe la Noue, J and Luquet, P (1982) Digestibility in fish: improved device for the automatic collection of feces Aquaculture 29, 185–189.CrossRefGoogle Scholar
Davies, NT and Reid, H (1979) An evaluation of the phytate, zinc, copper, iron and manganese contents of, and Zn availability from, soya-based textured-vegetable-protein meat-substitutes or meat-extenders British Journal of Nutrition 41, 579–589.CrossRefGoogle ScholarPubMed
Eelkman Rooda, SJOtten, MH, Van Loon, MACKaptein, E and Visser, TJ (1989) Metabolism of triiodothyronine in rat hepatocytes Endocrinology 125, 2187–2197.CrossRefGoogle Scholar
Farchi-Pisanty, OHackett, PBJ and Moav, B (1995) Regulation of fish growth hormone transcription Molecular Marine Biology and Biotechnology 4, 215–223.Google ScholarPubMed
Fenwick, GR (1982) The assessment of a new protein source — rapeseed Proceedings of the Nutrition Society 41, 277–288.CrossRefGoogle ScholarPubMed
Gabe, M (1968) Techniques Histologiques (Techniques in Histology). Paris: Masson.Google Scholar
Gardner, WS and Miller, WH (1980) Reverse-phase liquid chromatography of amino acids after reaction with ophthalaldehyde Analytical Biochemistry 101, 61–70.CrossRefGoogle ScholarPubMed
Gomes, EFCorraze, G and Kaushik, S (1993) Effects of dietary incorporation of a co-extruded plant protein (rapeseed and peas) on growth, nutrient utilization and muscle fatty acid composition of rainbow trout (Oncorhynchus mykiss) Aquaculture 113, 339–353.CrossRefGoogle Scholar
Gomes, EF & Kaushik, SJ (1989) Incorporation of lupin seed meal, colzapro or triticale as protein/energy substitutes in rainbow trout diets. In Proceedings of Third International Symposium on Feeding and Nutrition in Fish, pp. 315–324 [Takeda, M and Watanabe, T, editors]. Toba, Japan, August 28–September 1, 1989.Google Scholar
Grob, K and Matile, P (1979) Vacuolar location of glucosinolate in horseradish root cells Plant Scientific Letters 14, 327–335.CrossRefGoogle Scholar
Hardy, RW and Sullivan, CV (1983) Canola meal in rainbow trout (Salmo gairdneri) production diets Canadian Journal of Fisheries and Aquatic Sciences 40, 281–286.CrossRefGoogle Scholar
Harvey, SScanes, CG and Klandorf, H (1988) Thyrotrophin-releasing hormone induces growth hormone secretion in adult hypothyroid fowl General and Comparative Endocrinology 69, 233–237.CrossRefGoogle ScholarPubMed
Hetzel, BS (1994) S.O.S. for a billion — the nature and magnitude of the iodine deficiency disorders. In S.O.S. for a Billion: The Conquest of Iodine Deficiency Disorders, pp. 1–26 [Hetzel, BS and Pandav, CS, editors]. Oxford University Press: Delhi.Google Scholar
Higgs, DA, Dosanjh, BS, Beames, RM, Prendergast, AF, Mwachireya, SA & Deacon, G (1996) Nutritive value of rapeseed/canola protein products for salmonids. In Eastern Nutrition Conference, pp. 187–196 [Kent, N and Anderson, D, editors]. Dartmouth/Halifax, Canada, May 15–17, 1996.Google Scholar
Higgs, DAMcBride, JR, Markert, JRDosanjh, BS, Plotnikoff, MD and Clarke, WC (1982) Evaluation of Tower and Candle rapeseed (Canola) meal and Bronowski rapeseed protein concentrate as protein supplements in practical dry diets for juvenile chinook salmon (Oncorhynchus tshawytscha) Aquaculture 29, 1–31.CrossRefGoogle Scholar
Hilton, JW and Slinger, SJ (1986) Digestibility and utilization of canola meal in practical-type diets for rainbow trout (Salmo gairdneri) Canadian Journal of Fisheries and Aquatic Sciences 43, 1149–1155.CrossRefGoogle Scholar
Hodin, RAChamberlain, SM and Upton, MP (1992) Thyroid hormone differentially regulates rat intestinal brush border enzyme gene expression Gastroenterology 103, 1529–1536.CrossRefGoogle ScholarPubMed
Hossain, MA and Jauncey, K (1988) Toxic effects of glucosinolate (allyl isothiocyanate) (synthetic and from mustard oilcake) on growth and food utilization in common carp Indian Journal of Fisheries 35, 186–196.Google Scholar
Kuhn, ER, Mol, KA and Darras, VM (1993) Control strategies of thyroid hormone monodeiodination in vertebrates Zoological Science 10, 873–885.Google Scholar
Leatherland, JF (1994) Reflections on the thyroidology of fishes: from molecules to humankind Guelph Ichthyology Reviews 2, 1–67.Google Scholar
Leatherland, JFHilton, JW and Slinger, SJ (1987) Effects of thyroid hormone supplementation of canola meal-based diets on growth, and interrenal and thyroid gland physiology of rainbow trout (Salmo gairdneri) Fish Physiology and Biochemistry 3, 73–82.CrossRefGoogle ScholarPubMed
Leonard, JL & Visser, TJ (1986) Biochemistry of deiodination. In Thyroid Hormone Metabolism, pp. 189–229 [Henneman, G, editor]. New York, NY: Marcel Dekker Inc.Google Scholar
Luo, D and McKeown, BA (1991) The effect of thyroid hormone and glucocorticoids on carp growth hormone-releasing factor (GRF)-induced growth hormone (GH) release in rainbow trout (Oncorhynchus mykiss) Comparative Biochemistry and Physiology 99, 621–626.CrossRefGoogle ScholarPubMed
McCurdy, SM and March, BE (1992) Processing of canola meal for incorporation in trout and salmon diets Journal of the American Oil Chemists Society 69, 213–220.CrossRefGoogle Scholar
Martinez, IDreyer, BArgersborg, A, Le Roux, A and Boeuf, G (1995) Effect of triiodothyronine and rearing temperature on growth and skeletal myosin heavy chain isoform transition during early development in salmonid (Salvelinus alpinus L.) Comparative Biochemistry and Physiology 112, 717–725.CrossRefGoogle Scholar
Mawson, RHeaney, RKZdunczyk, Z and Kozlowska, H (1993) Rapeseed meal-glucosinolates and their antinutritional effects. Part 1. Rapeseed production and chemistry of glucosinolates Nahrung 37, 131–140.CrossRefGoogle ScholarPubMed
Mawson, RHeaney, RZZdunczyk, Z and Kozlowska, H (1994) Rapeseed meal-glucosinolates and their antinutritional effects. Part 3. Animal growth and performance Nahrung 38, 167–177.CrossRefGoogle ScholarPubMed
Mawson, RHeaney, RKZdunczyk, Z and Kozlowska, H (1994) Rapeseed meal-glucosinolates and their antinutritional effects. Part 4. Goitrogenicity and internal organs abnormalities in animals Nahrung 38, 178–191.CrossRefGoogle ScholarPubMed
Maynard, LA & Loosly, JK (1979) Animal Nutrition, 6th ed. New York, NY: McGraw-Hill Book Co.Google Scholar
Melamed, PEliahu, NLevavi-Sivan, B, Ofir, MFarchi-Pisanty, O, Rentier-Delrue, FSmal, J, Yaron, Z and Naor, Z (1995) Hypothalamic and thyroidal regulation of growth hormone in tilapia General and Comparative Endocrinology 97, 13–30.CrossRefGoogle ScholarPubMed
Mol, KAVan der Geyten, SBurel, C, Kuhn, ER, Boujard, T and Darras, VM (1998) Comparative study of iodothyronine outer ring and inner ring deiodinase activities in five teleostean fishes Fish Physiology and Biochemistry 18, 253–266.CrossRefGoogle Scholar
National Research Council (1993) Nutrient Requirements of Fish. Washington, D.C.: National Academic Press.Google Scholar
Nugon-Baudon, L and Rabot, S (1994) Glucosinolates and glucosinolate derivatives: implications for protection against chemical carcinogenesis Nutrition Research Reviews 7, 205–231.CrossRefGoogle ScholarPubMed
Rabot, SNugon-Baudon, L and Szylit, O (1993) Alterations of the hepatic xenobiotic-metabolizing enzymes by a glucosinolate-rich diet in germ-free rats: influence of a pre-induction with phenobarbital British Journal of Nutrition 70, 347–354.CrossRefGoogle ScholarPubMed
Roland, NRabot, S and Nugon-Baudon, L (1996) Modulation of the biological effects of glucosinolates by inulin and oat fibre in gnotobiotic rats inoculated with a human whole faecal flora Food and Chemical Toxicology 34, 671–677.CrossRefGoogle ScholarPubMed
Spinelli, JHoule, CR and Wekell, JC (1983) The effect of phytates on the growth of rainbow trout (Salmo gairdneri) fed purified diets containing varying quantities of calcium and magnesium Aquaculture 30, 71–83.CrossRefGoogle Scholar
Teskeredzic, ZHiggs, DADosanjh, BS, McBride, JR, Hardy, RWBeames, RM, Jones, JDSimell, MVaara, T and Bridges, RB (1995) Assessment of undephytinized and dephytinized rapeseed protein concentrate as sources of dietary protein concentrate as sources of dietary protein for juvenile rainbow trout (Oncorhynchus mykiss) Aquaculture 131, 261–277.CrossRefGoogle Scholar
Thivend, P, Mercier, C & Guilbot, A (1972) Determination of starch with glucoamylase. In Methods in Carbohydrate Chemistry, vol. IV, pp. 100–105 [Whistler, RL and Bemiller, JN, editors]. New York, London: Academic Press.Google Scholar
VanEtten, CH & Tookey, HL (1983) Glucosinolates. In Handbook of Naturally Occuring Food Toxicants, p. 15 [Rechcigl, M, editor]. Boca Raton, FL: CRC Press.Google Scholar
Vermorel, M and Baudet, JJ (1987) Valorization of rapeseed meal. 2. Nutritive value of high or low-glucosinolate varieties and effect of dehulling Reproduction, Nutrition, Développment 27, 45–55.CrossRefGoogle ScholarPubMed
Vemorel, MHeaney, RK and Fenwick, GR (1986) Nutritive value of rapeseed meal: effects of individual glucosinolates Journal of Sciences of Food and Agriculture 37, 1197–1202.CrossRefGoogle Scholar
Webster, CDTiu, LGTidwell, JH and Grizzle, JM (1997) Growth and body composition of channel catfish (Ictalurus punctatus) fed diets containing various percentages of canola meal Aquaculture 150, 103–112.CrossRefGoogle Scholar
Williamson, GWang, H and Griffiths, S (1996) Glucosinolates as bioactive components of Brassica vegetables: induction of cytochrome P450 1A1 in Hep G2 cells as assessed using transient transfection Biochemical Society Transactions 24, 383S.CrossRefGoogle ScholarPubMed
Woo, NYSChung, ASB and Ng, TB (1991) Influence of oral administration of 3,5,3′-triiodo-L-thyronine on growth, digestion, food conversion and metabolism in the underyearling red sea bream, Chrysophrys major (Temminck & Schlegel) Journal of Fish Biology 39, 459–468.CrossRefGoogle Scholar
Yurkowski, MBailey, JK Evans RE, Tabachek J-AL and Burton Ayles, G (1978) Acceptability of rapeseed proteins in diets of rainbow trout (Salmo gairdneri) Journal of the Fisheries Research Board of Canada 35, 951–962.CrossRefGoogle Scholar