Lactic acid fermentation eliminates indigestible carbohydrates and antinutritional factors in soybean meal for Atlantic salmon (Salmo salar)
Introduction
Soybeans contain approximately 30% indigestible carbohydrates (Bach-Knudsen, 1997) and numerous antinutritional factors (Rackis, 1974, Rumsey et al., 1994, Anderson and Wolf, 1995). Heat labile ANFs like proteinase inhibitors and agglutinating lectins are largely deactivated by the toasting step when producing solvent extracted (de-oiled) soybean meal (Vohra and Kratzer, 1991, Maenz et al., 1999). However, several of the ANFs in soy are heat stable. Among the most critical are still unidentified factor(s) that causes pathomorphological changes in the distal intestine of salmonid fish (Ingh et al., 1991, Ingh et al., 1996, Rumsey et al., 1994, Baeverfjord and Krogdahl, 1996, Burrells et al., 1999, Krogdahl et al., 2000). This condition is commonly known as soybean meal-induced enteritis. The precise causative agent is not known, but one or more of the alcohol soluble components of soy are suspected of being involved (Ingh et al., 1991, Ingh et al., 1996, Krogdahl et al., 2000).
Inclusion of solvent extracted soybean meal in the diet reduces the overall digestibility of lipid by Atlantic salmon (Refstie et al., 1998, Refstie et al., 1999, Refstie et al., 2000, Refstie et al., 2001, Storebakken et al., 1998). The reason for this is still unclear. Refstie et al. (1999) suggested a negative effect of soy polysaccharides on nutrient absorption both in Atlantic salmon and broiler chickens. The soy polysaccharide fraction is in the form of indigestible non-starch polysaccharides (NSP), of which a large fraction is soluble in water (Bach-Knudsen, 1997). Furthermore, indigestible soy oligosaccharides (α-galactosyl homologues of sucrose) may affect the osmotic conditions in the intestine and facilitate microbial fermentation (Wiggins, 1984). Soybean meal-induced enteritis also corresponds with reduced absorptive capacity for nutrients by the distal intestine of salmonids (Nordrum et al., 2000). How much the latter actually contributes to the reduced absorption of nutrients seen in soybean meal fed salmonids is unclear, as the distal intestine is not recognised as a major absorptive site in fish (reviewed by Buddington et al., 1997).
The factor(s) in soybean meal that induces enteritis in salmonid fish is removed by alcohol washing used in the production of soy protein concentrates (Ingh et al., 1991, Ingh et al., 1996, Rumsey et al., 1994, Krogdahl et al., 2000, Refstie et al., 2001). This process also removes sugars and soluble polysaccharides. However, this is an elaborate treatment to produce a high-priced product. Fermentation has been suggested as an alternative means to improve the nutritional value of vegetable protein sources for fish feeds. Shimeno et al. (1994) examined fermentation of solvent extracted soybean meal by yellow mould (Aspergillus usamii). Unfortunately, the physical properties of the resulting fermented soy were too poor to allow proper evaluation by a fish trial. Fermentation by lactic acid bacteria (Lactobacillus acidophilus) did, however, significantly improve the nutritional value of sesame seed meal to the Indian rohu carp (Mukhopadhyay and Ray, 1999).
Fermentation by a Lactobacillus sp. has also been used with success to reduce the levels of non-starch carbohydrates in wheat and barley whole meals (Skrede et al., 2001, Skrede et al., 2002, Skrede et al., 2003). This lactic acid fermentation was particularly efficient in eliminating soluble mixed-linked (1-3)(1-4)-β-glucans, but also sucrose and raffinose (Gal (α1-6) Glc (β1-2) Fru). Substitution of unfermented cereals by lactic acid fermented cereals in extruded diets resulted in a significant increase in the overall apparent digestibilities of starch, lipid, and energy by Atlantic salmon (Skrede et al., 2002). Similar but slighter responses were observed in mink (Skrede et al., 2001).
Lactic acid fermentation has also been shown to give a significant reduction in phytic acid in cereal (Marklinder et al., 1996, Skrede et al., 2002) and sesame seed (Mukhopadhyay and Ray, 1999) whole meals. However, as the cereals and sesame seed meals were not heated before fermentation, it has been unclear whether this hydrolysis of phytic acid resulted from microbial Lactobacilli activity, or phytase endogenous to the grains. Plant seeds express high phytase activity, but these phytases are largely inactivated by thermal treatments of feedstuffs and feeds (Jongbloed and Kemme, 1990).
The objectives of the present work were 1) to investigate how lactic acid fermentation alters the composition of extracted (de-oiled) soybean white flakes, 2) to evaluate lactic acid fermentation as a means to improve the nutritive value of soybean meal white flakes to Atlantic salmon, and 3) to compare the nutritional value of fermented white flakes to that of commercial biotechnologically processed extracted soybean meal in Atlantic salmon.
Section snippets
Dietary protein ingredients
Three soy products were obtained from commercial suppliers: Extracted soybean meal with hulls (SBM; Denosoy, Denofa, Fredrikstad, Norway), extracted soybean meal without hulls (white flakes; ADM, Hamburg, Germany), and biotechnologically processed extracted soybean meal (BPSBM; HP300, Hamlet Protein, Horsens, Denmark). BPSBM results from a proprietary process that reduces the oligosaccharide content, increases the protein concentration, and eliminates antinutritional factors in soybean meal.
A
Characteristics of the protein ingredients
The compositions of the tested fishmeal and soy products are given in Table 1, Table 2, Table 3. The white flakes (WF) and Denosoy (SBM), which both were extracted (de-oiled) soybean meals, did not differ markedly in terms of composition. As a consequence of the dehulling step, the WF did, however, contain slightly more protein and slightly less neutral non-starch polysaccharides (NNSP). The total contents of protein, lipid, starch, ash, sucrose, raffinose, and NNSP accounted for 998 and 978 g
Discussion
The major finding of this experiment is that lactic acid fermentation of de-oiled soybean meal (extracted white flakes) partly eliminates and/or inactivates soy factor(s) that restrict the absorption of lipid by Atlantic salmon. This leads to higher digestibility of total dietary energy, and subsequently an improved feed efficiency. Lactic acid fermentation also reduces the antigenicity of soybean meal in salmon, resulting in less pronounced pathological changes in the distal intestine.
Conclusions
To conclude, lactic acid fermentation of white flakes eliminated sucrose, reduced the levels of raffinose, and lowered the trypsin inhibitor activity in the fermented white flakes. Lactic acid fermentation also improved the nutritional value of the white flakes by partly eliminating soy factor(s) that restrict the overall digestibility of lipid by Atlantic salmon and induce intestinal pathology. With regard to improved lipid digestibility, lactic acid fermentation was not as efficient as the
Acknowledgements
The authors want to acknowledge the skilful assistance of G. Vik and A.B. Fjermedal at EWOS Innovation, and A.B. Bævre at Matforsk. Financial support for this experiment was provided by a grant “Biotechnological Means to Improve the Nutritional Value of Vegetable Feed Ingredients” funded by the Research Council of Norway (grant # 132221/112) and EWOS Innovation.
References (59)
- et al.
Compositional changes in trypsin inhibitors, phytic acid, saponins and isoflavones related to soybean processing
J. Nutr.
(1995) Digestibility determination in fish using chromic oxide marking and analysis of contents from different segments of the gastrointestinal tract
Aquaculture
(1978)- et al.
Growth rate estimates for cultured Atlantic salmon and rainbow trout
Aquaculture
(1987) - et al.
Evaluation of selected trivalent metal oxides as inert markers used to estimate apparent digestibility in salmonids
Aquaculture
(2000) - et al.
Immunological, physiological and pathological responses of rainbow trout (Oncorhynchus mykiss) to increasing dietary concentrations of soybean proteins
Vet. Immunol. Immunopathol.
(1999) Predicting the dietary energy value of poultry feeds
Feeding systems for rainbow trout and other salmonids with reference to current estimates of energy and protein requirements
Aquaculture
(1992)Characterisation of feedstuffs for ruminants using some physical parameters
Anim. Feed Sci. Technol.
(2000)- et al.
Intrinsic buffering capacity of feedstuffs
Anim. Feed Sci. Technol.
(2002) - et al.
Influence of oligosaccharides on the digestibility of lupin meals when fed to rainbow trout, Oncorhynchus mykiss
Aquaculture
(2003)
Effect of pelleting mixed feeds on phytase activity and the apparent absorbability of phosphorus and calcium in pig feeds
Anim. Feed Sci. Technol.
Carbohydrate-binding and agglutinating lectins in raw and processed soybean meals
Anim. Feed Sci. Technol.
Influences of lactic acid bacteria on technological, nutritional, and sensory properties of barley sour dough bred
Food Qual. Prefer.
Effects of soybean meal and salinity on intestinal transport of nutrients in atlantic salmon (Salmo salar L.) and rainbow trout (Oncorhynchus mykiss)
Comp. Biochem. Physiol.
Potato protein concentrate with low content of solanidine glycoalkaloids in diets for Atlantic salmon (Salmo salar)
Aquaculture
Adaptation to soybean meal in diets for rainbow trout, Oncorhynchus mykiss
Aquaculture
Feed consumption and conversion in Atlantic salmon (Salmo salar) fed diets with fish meal, extracted soybean meal or soybean meal with reduced content of oligosaccharides, trypsin inhibitors, lectins and soya antigens
Aquaculture
Non-starch polysaccharides in soybean meals and effects on the absorption of nutrients in farmed Atlantic salmon and broiler chickens
Anim. Feed Sci. Technol.
Differing nutritional responses to dietary defatted soybean meal in rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar)
Aquaculture
Long-term protein and lipid growth of Atlantic salmon (Salmo salar) fed diets with partial replacement of fish meal by soy protein products at medium or high lipid level
Aquaculture
Effect of soybean protein on serological response, non-specific defence mechanisms, growth, and protein utilization in rainbow trout
Vet. Immunol. Immunopathol.
Effect of lactic acid fermentation of wheat and barley whole meal flour on carbohydrate composition and digestibility in mink (Mustela vison)
Anim. Feed Sci. Technol.
Lactic acid fermentation of wheat and barley whole meal flours improves digestibility of nutrients and energy in Atlantic salmon (Salmo salar L.) diets
Aquaculture
Effects of lactic acid fermentation on wheat and barley carbohydrate composition and production performance in the chicken
Anim. Feed Sci. Technol.
Binders in fish feeds: I. Effect of alginate and guar gum on growth, digestibility, feed intake and passage through the gastrointestinal tract of rainbow trout
Aquaculture
Binders in fish feeds: II. Effect of different alginates on the digestibility of macronutrients in rainbow trout
Aquaculture
The apparent digestibility of diets containing fish meal, soybean meal or bacterial meal fed to Atlantic salmon (Salmo salar): evaluation of different faecal collection methods
Aquaculture
Soybean carbohydrates appear to restrict the utilization of nutrients by Atlantic salmon (Salmo salar L.)
Polysaccharides of soybeans: VI. Neutral polysaccharides from cotyledon meal
Can. J. Chem.
Cited by (210)
Carbohydrate-active enzymes in animal feed
2023, Biotechnology Advances