Choline supplementation prevents diet induced gut mucosa lipid accumulation in post-smolt Atlantic salmon (Salmo salar L.)

Abstract

Background Various intestinal morphological alterations have been reported in cultured fish fed diets with high contents of plant ingredients. Since 2000, salmon farmers have reported symptoms indicating an intestinal problem, which we suggest calling lipid malabsorption syndrome (LMS), characterized by pale and foamy appearance of the enterocytes of the pyloric caeca, the result of lipid accumulation. The objective of the present study was to investigate if insufficient dietary choline may be a key component in development of the LMS. Results The results showed that Atlantic salmon (Salmo salar), average weight 362 g, fed a plant based diet for 79 days developed signs of LMS. In fish fed a similar diet supplemented with 0.4% choline chloride no signs of LMS were seen. The relative weight of the pyloric caeca was 40% lower, reflecting 65% less triacylglycerol content and histologically normal gut mucosa. Choline supplementation further increased specific fish growth by 18%. The concomitant alterations in intestinal gene expression related to phosphatidylcholine synthesis (chk and pcyt1a), cholesterol transport (abcg5 and npc1l1), lipid metabolism and transport (mgat2a and fabp2) and lipoprotein formation (apoA1 and apoAIV) confirmed the importance of choline in lipid turnover in the intestine and its ability to prevent LMS. Another important observation was the apparent correlation between plin2 expression and degree of enterocyte hyper-vacuolation observed in the current study, which suggests that plin2 may serve as a marker for intestinal lipid accumulation and steatosis in fish. Future research should be conducted to strengthen the knowledge of choline’s critical role in lipid transport, phospholipid synthesis and lipoprotein secretion to improve formulations of plant based diets for larger fish and to prevent LMS. Conclusions Choline prevents excessive lipid accumulation in the proximal intestine and is essential for Atlantic salmon in seawater.

Dose–response relationship between dietary choline and lipid accumulation in pyloric enterocytes of Atlantic salmon (Salmo salar L.) in seawater

“…Dietary choline is rapidly transformed to phosphatidylcholine by the cytidine-diphospho (CDP)-choline pathway when entering the PI (4,5) . The present study confirmed the results from our previous study (3) , showing suppressed levels of chk and pcyt1a, which proteins catalyse the initial and second rate-limiting steps in the CDP-choline pathway for phosphatidylcholine synthesis, respectively. The concomitant decrease of both chk and pcyt1a by increasing choline levels could be a result of an increased production of phosphatidylcholine in the fish by increasing dietary choline doses and that phosphatidylcholine inhibits its own synthesis pathway through a negative feedback control.…”

“…Indicators of efficiency of lipid transport in the mucosa of the PI, supposedly the organ with the highest lipid turnover (60) , particular in rapidly growing fish fed high lipid diets, may be more suitable biomarkers for choline requirement. In our previous study (3) , we observed that the PI was the most sensitive tissue for studying the effects of variation in dietary choline. The present study confirms this observation, showing clear effects of choline level on the PI somatic index, macroscopically observed degree of whiteness and histologically observed lipid vacuolation in PI, whereas no significant effect on liver index was observed.…”

“…The likely explanation is limited lipid transport capacity. Our previous study (3) indicates that choline synthesis in post-smolt Atlantic salmon in seawater is insufficient to cover the requirement. One consequence of the shift from marine to plant-based diets is a lower content of choline, in the form of phosphatidylcholine in the raw materials (4) .…”

“…One consequence of the shift from marine to plant-based diets is a lower content of choline, in the form of phosphatidylcholine in the raw materials (4) . An exogenous supply of choline may therefore be essential for normal metabolism, transport and export of lipids across the mucosa of the pyloric caeca and for prevention of LMS in salmon, in the seawater phase (3) .…”

Choline and Bile Acids Mixture Improved Growth Performance and Intestinal Immunity via Altering Gut Microbiota and Bacterial Metabolites in the Colon of Weaned Piglets.

“…Previous studies demonstrated that dietary choline signi cantly improved the sh speci c growth rate [26,27]. To our knowledge, there was limited study on the choline effect on the swine growth performance.…”