High Lipid Content of Prey Fish and n−3 PUFA Peroxidation Impair the Thiamine Status of Feeding-Migrating Atlantic Salmon (Salmo salar) and Is Reflected in Hepatic Biochemical Indices

Abstract

Signs of impaired thiamine (vitamin B1) status in feeding-migrating Atlantic salmon (Salmo salar) were studied in three Baltic Sea areas, which differ in the proportion and nutritional composition of prey fish sprat (Sprattus sprattus) and herring (Clupea harengus). The concentration of n−3 polyunsaturated fatty acids (n−3 PUFAs) increased in salmon with dietary lipids and n−3 PUFAs, and the hepatic peroxidation product malondialdehyde (MDA) concentration increased exponentially with increasing n−3 PUFA and docosahexaenoic acid (DHA, 22:6n−3) concentration, whereas hepatic total thiamine concentration, a sensitive indicator of thiamine status, decreased with the increase in both body lipid and n−3 PUFA or DHA concentration. The hepatic glucose 6-phosphate dehydrogenase activity was suppressed by high dietary lipids. In salmon muscle and in prey fish, the proportion of thiamine pyrophosphate increased, and that of free thiamine decreased, with increasing body lipid content or PUFAs, or merely DHA. The thiamine status of salmon was impaired mainly due to the peroxidation of n−3 PUFAs, whereas lipids as a source of metabolic energy had less effect. Organochlorines or general oxidative stress did not affect the thiamine status. The amount of lipids, and, specifically, their long-chain n−3 PUFAs, are thus responsible for generating thiamine deficiency, and not a prey fish species per se.

Seasonal and genetic effects on lipid profiles of juvenile Atlantic salmon

“…High lipid content in the liver can suggest physiological issues resembling non-alcoholic fatty liver in humans and involving lipid peroxidation and oxidative stress. However, we are currently just beginning to understand these mechanisms in salmon (Espe et al, 2019; Keinänen et al, 2022).…”

“…In contrast, the TG species accumulated during summer and detected in the autumn samples had a lower degree of unsaturation, which, during higher summer and autumn water temperature and physiological activity, may protect juvenile salmon against oxidative stress (Gray, 1978; Kjær et al, 2008). Adult female salmon with the largest reserves of polyunsaturated lipid are known to suffer from oxidative stress during spawning and fail to breed (Keinänen et al, 2022; Vuorinen et al, 2020). Therefore, the lipid species profiles of the juvenile salmon of this study suggest that distributing highly unsaturated fatty acids into phospholipids may reduce the rates of polyunsaturated fatty acid peroxidation and thereby reduce oxidative stress..…”

A Comprehensive Review of the Impacts of Climate Change on Salmon: Strengths and Weaknesses of the Literature by Life Stage

“…Conversely, other Forage and groundfish are important as salmon prey when they are small, then competitors and predators as they grow, depending on their spatial and temporal overlap with salmon. However, in California, the excess consumption of anchovy due to lack of other prey in recent years has led to a thiamine deficiency, causing reproductive failure in critically endangered winter-run Chinook salmon [178]. Large schools of forage fish also attract predators, which might then increase or decrease predation on salmon [179,180].…”

Thiamine Deficiency M74 Developed in Salmon (Salmo salar) Stocks in Two Baltic Sea Areas after the Hatching of Large Year-Classes of Two Clupeid Species—Detected by Fatty Acid Signature Analysis

“…Fatty fish that feed on fatty marine prey fish are prone to suffer from thiamine deficiency [1,13] because the requirement for thiamine increases with the increase in the diet's energy content [14] and because thiamine is depleted as a consequence of lipid peroxidation [14][15][16]. n−3 PUFAs are abundant in marine fish lipids [9], and docosahexaenoic acid (DHA, 22:6n−3) is the most common PUFA in Baltic clupeids and salmon [13,17]. All PUFAs are susceptible to peroxidation initiated by the free radicals normally generated in metabolism [18], but DHA is most susceptible due to its large number of double bonds [19].…”

“…All PUFAs are susceptible to peroxidation initiated by the free radicals normally generated in metabolism [18], but DHA is most susceptible due to its large number of double bonds [19]. Peroxidation was manifested as an increase in the concentration of malondialdehyde (MDA), the main peroxidation product of n−3 PUFAs, as the concentration of DHA increased in the tissues of Baltic salmon [13,20]. The unphosphorylated form of thiamine, i.e., free thiamine (THIAM), serves as an antioxidant for lipid peroxidation in tissues and is destroyed in such reactions [10,16,21], as described in salmon by Keinänen et al [1,13] and Vuorinen et al [8,22].…”