Metabolic Hepatic Disorders Caused by Ciguatoxins in Goldfish (Carassius auratus)

Abstract

Ciguatera poisoning (CP) is a foodborne disease known for centuries; however, little research has been conducted on the effects of ciguatoxins (CTXs) on fish metabolism. The main objective of this study was to assess different hepatic compounds observed in goldfish (Carassius auratus) fed C-CTX1 using nuclear magnetic resonance (NMR)-based metabolomics. Thirteen goldfish were treated with C-CTX1-enriched flesh and sampled on days 1, 8, 15, 29, 36, and 43. On day 43, two individuals, referred to as ‘Detox’, were isolated until days 102 and 121 to evaluate the possible recovery after returning to a commercial feed. At each sampling, hepatic tissue was weighed to calculate the hepatosomatic index (HSI) and analyzed for the metabolomics study; animals fed toxic flesh showed a higher HSI, even greater in the ‘Detox’ individuals. Furthermore, altered concentrations of alanine, lactate, taurine, glucose, and glycogen were observed in animals with the toxic diet. These disturbances could be related to an increase in ammonium ion (NH4+) production. An increase in ammonia (NH3) concentration in water was observed in the aquarium where the fish ingested toxic meat compared to the non-toxic aquarium. All these changes may be rationalized by the relationship between CTXs and the glucose–alanine cycle.

Effects on Biochemical Parameters and Animal Welfare of Dusky Grouper (Epinephelus marginatus, Lowe 1834) by Feeding CTX Toxic Flesh

“…Moreover, the variations in HSI and GSI between feeding periods suggest temporal dynamics in response to different diets ( Table 4 ). Ramos-Sosa et al [ 20 ] fed 11 goldfish toxic flesh for 43 days and observed a greater HSI in the toxic fish than in the control group without finding significant differences. Featuring another analyzed marine species of the Serranidae family of the grouper, such as Serranus cabrilla , Anadon et al [ 26 ] fed seven fish with a concentration of 117.01 mg of Gambierdiscus spp.…”

“…This result may suggest a stress factor due to the time of exposure to the toxic diet. In the study performed by Ramos-Sosa et al [ 20 ], in which the authors analyzed the hepatic metabolism of glucose, lactate, and other metabolites such as alanine and taurine after feeding flesh with CTX to goldfish, they observed that the glucose–alanine cycle was altered; they also found an increase in hepatic glycogen in fish with toxic feeding, which suggested a greater HSI and glycogen reserves in the liver, which supports our results, where we found a greater HSI in the last weeks of feeding and an increase in lactate levels.…”

“…As CTXs move up the food chain, they may undergo biotransformation and accumulate to hazardous levels for human consumption [ 3 , 4 , 11 , 15 ]. The transfer of CTXs from the prey to the predator has been demonstrated by feeding experiments, even when using flesh from a high-order carnivorous to feed omnivorous fish [ 16 , 17 , 18 , 19 , 20 ]. Research indicates that fish metabolism plays a role in increasing the toxicity of CTXs.…”

“…There are several studies of dietary exposure to ciguatoxins that try to determine the effects of these powerful toxins in fish, how they bioaccumulate in tissues, and the molecular transformation of the toxins after ingestion of fish [ 21 , 22 , 23 , 24 , 25 , 26 ]. However, experimental models have been developed that try to imitate exposure to CTXs in the environment with some species that are not within the ciguatoxin cycle, resulting in the development of symptoms in some cases [ 18 , 20 , 23 , 24 ]. Erratic swimming, lethargy, and lack of appetite have been reported in goldfish ( Carassius auratus ) exposed to CTXs [ 18 , 20 ], and in marine medaka ( Oryzias melastigma ), it has been observed how the toxins affect reproductive and embryonic development, negatively affecting the growth of fish in their first stage of life [ 23 , 27 , 28 ].…”

“…However, experimental models have been developed that try to imitate exposure to CTXs in the environment with some species that are not within the ciguatoxin cycle, resulting in the development of symptoms in some cases [ 18 , 20 , 23 , 24 ]. Erratic swimming, lethargy, and lack of appetite have been reported in goldfish ( Carassius auratus ) exposed to CTXs [ 18 , 20 ], and in marine medaka ( Oryzias melastigma ), it has been observed how the toxins affect reproductive and embryonic development, negatively affecting the growth of fish in their first stage of life [ 23 , 27 , 28 ]. Other experimental models have studied the damage from the toxins over the months at a hepatotoxic level, applying histology to the possibly damaged tissues [ 26 , 29 ].…”