Introduction
Mycotoxins are toxic secondary metabolites produced by fungi that can contaminate feed and pose a major threat in aquaculture. These toxic compounds can cause various health problems, including liver damage, immunosuppression, reduced growth, increased susceptibility to infectious diseases, and even death. Therefore, finding effective strategies to prevent or reduce the negative effects of mycotoxins in aquaculture is crucial for ensuring the health and productivity of farmed fish and shrimp.
Plant extracts have been found to exhibit various beneficial activities in aquaculture, such as anti-stress, growth promotion, appetite stimulation, tonicity enhancement, immunostimulation, culture species maturation, anti-pathogen, and aphrodisiac properties. These activities are attributed to the presence of active principles like terpenoids, alkaloids, tannins, saponins, flavonoids, phenolics, steroids, or essential oils (Chakraborty and Hancz, 2011; Citarasu, 2010). In addition to their beneficial effects, the use of plant extracts in aquaculture can also reduce treatment costs and be more environmentally friendly as they tend to be more biodegradable than synthetic molecules. Furthermore, their diverse chemical composition minimizes the likelihood of drug resistance development in parasites (Olusola et al., 2013).
Silymarin and curcumin are natural compounds known for their potential health benefits and therapeutic properties. Silymarin is a flavonoid complex derived from milk thistle (Silybum marianum) seeds. It is well-regarded for its hepatoprotective properties, meaning it supports and protects the liver, and for its capacity to protect mitochondria from ROS and lipid peroxidation. Silymarin is often used as a dietary supplement to promote liver health, especially in cases of liver diseases.
Curcumin, on the other hand, is a bioactive compound found in turmeric (Curcuma longa), a spice commonly used in Indian cuisine. Curcumin is recognized for its anti-inflammatory and antioxidant properties. Additionally, curcumin is known for its role in promoting digestive health and potentially reducing the risk of chronic diseases.
Therefore, both silymarin and curcumin have gained attention for their natural and holistic approaches to animal health.
Curcumin and its effects on aquaculture performance and health
As aforementioned, curcumin is a polyphenol compound found in the turmeric root, which has been shown to possess antioxidant, anti-inflammatory, and hepatoprotective properties. Therefore, it has been demonstrated that curcumin offers a wide range of health benefits in animal nutrition (Table 1).
Rainbow trout supplemented with curcumin for 8 weeks exhibited a significant increase in growth. Fish that consumed curcumin-enriched diets also demonstrated improved feed conversion ratios compared to those on a regular diet (Yonar et al., 2019). The addition of curcumin to tilapia fish diets led to enhancements in growth indices (WG, SGR, and DWG), feed efficiency (lower FCR), and protein efficiency ratio (Mahmoud et al., 2017). Similarly, other studies have indicated that Nile tilapia fed diets containing curcumin experienced improved growth indices and feed efficiency (Cui et al., 2017; El-Barbary, 2018). Furthermore, crucian carp that were fed dietary curcumin displayed enhanced growth indices (increased WG, improved feed efficiency, and increased hepatopancreas weight), increased activity of digestive enzymes (trypsin and lipase), elevated GIT antioxidant activities, and upregulated mRNA gene expression levels (trypsin, lipase, Na+, alkaline phosphatase, creatine kinase, K+-ATPase, gamma-glutamyl transpeptidase, SOD, CAT, GSH-Px, GST, and glucocorticoid receptor) (Jiang et al., 2016). Additionally, curcumin inclusion in Nile tilapia fish diets led to quadratic improvements in growth indices (Mohamed et al., 2020). These findings collectively suggest that curcumin can enhance fish growth performance, likely due to its digestion-enhancing properties, and can be safely incorporated into fish nutrition practices.
The fish’s immune system is an important indicator of their nutritional and health status, as well as their ability to adapt to their environment. The inclusion of curcumin in the diets of rainbow trout resulted in improved immune responses, as evidenced by increased antioxidant enzyme activities and decreased lipid peroxidation (MDA) (Yonar et al., 2019). Furthermore, researchers have observed significantly higher immune values in fish fed with curcumin-enriched diets compared to those on a normal diet. Supplementing Nile tilapia diets with curcumin improved antioxidant status (as indicated by increased catalase and GSH and decreased MDA) and immune response (including increased lysozyme activity and elevated levels of total immunoglobulins such as IgG and IgM) (Mahmoud et al., 2017). In common carp, the inclusion of curcumin resulted in a significant decrease in kidney and liver MDA values compared to the control group (Yonar, 2018).
Feeding silver catfish dietary curcumin resulted in 100% disease resistance against Streptococcus agalactiae (Baldissera et al., 2018). Rainbow trout fed a diet containing curcumin exhibited the highest survival percentage (76.67%) compared to the control group (36.67%) when infected with Aeromonas salmonicida, suggesting that curcumin treatment may improve cellular and humoral immune variables, leading to decreased mortality and increased disease resistance (Yonar et al., 2019). Previous studies have demonstrated that curcumin inclusion in the diet can improve disease resistance in various fish species, such as Labeo rohita and Oreochromis niloticus, against A. hydrophila challenge (Behera et al., 2011; Mahmoud et al., 2017). Studies on this topic have been conducted worldwide, and dietary curcumin inclusion has been shown to improve disease resistance against Vibrio alginolyticus in Nile tilapia fish (Cui et al., 2017; El-Barbary, 2016). Dietary curcumin and salicylcurcumin have defensive roles against lipid oxidation and DNA injury, and can enhance survival rate and disease resistance in freshwater climbing perch fish (Manju et al., 2013). Curcumin’s pleiotropic effects against diseases stem from its ability to interact with various molecular targets, triggering cellular signaling pathways such as apoptosis and inflammation.
Effects of curcumin on toxins and pollutants (Hepatoprotective Effect)
Curcumin could have a synergistic effect with garlic in enhancing the performance of Nile tilapia exposed to aflatoxicosis (El-Barbary, 2016). In addition, dietary curcumin inclusion has been shown to improve liver function and health status in various fish species. Also, curcumin can protect against the detrimental effects of chromium and copper by enhancing antioxidant capacity and decreasing cytokine gene expression.
Adding curcumin to the diet of Jian carp can protect their liver from damage caused by carbon tetrachloride (Cao et al., 2015). This was evident from the decrease in aspartate transaminase, alanine transaminase, and hepatocyte degeneration, as well as the reduction of MDA levels in the liver. The enhanced antioxidant activities (SOD, antioxidant capacity, and GSH in the liver) and the inhibition of cytokine expressions (TNF-α and IL-1 via the NF-kB signaling pathway) were also observed. Additionally, curcumin can suppress the production of pro-inflammatory cytokines including TNFα, IL-1, IL-2, IL-6, IL-8, and IL-12, as well as chemokines, by inhibiting the activity of NF-κB, (Zhou et al., 2011). Hence, curcumin’s bioactive components have immunomodulatory properties that can counteract the harmful effects of toxins of pesticides and mycotoxins on fish.
Table 1. Effects of curcumin on aquatic species in challenging mycotoxin and other contaminants.
| Target species | Challenge | Curcumin Doses | Effects | References |
|---|---|---|---|---|
| Nile tilapia | 0, 50, 100,150, and 200 ppm CUR | → alteration in growth, nutrient efficiency, digestive enzymes efficiency, biometric indices, survival rates, and hematological components. ↑ lysozyme and bactericidal activities | El Basuini et al., 2023 in press | |
| Tilapia | 0.5% and 1% CUR | ↑ growth and feeding efficiency, ↑ α-amylase, protease activities, and lipase enzymes in the gut. Regulate leptin gene and its receptor thereby modulating energy homeostasis. | Sruthia et al., 2018 | |
| Nile tilapia | 0, 50, 100, 150 or 200 mg CUR kg−1 diet | ↑ final weight, daily weight gain, and specific growth rate. ↑ effects on growth performance, feed utilization, immune functions, antioxidant status, and disease resistance. | Mahmoud et al., 2017 | |
| Gift tilapia | 0, 50, 100, 150 and 200 mg CUR/kg ration | ↑ weight gain, final body weight, specific growth rate; ↓ feed conversion, MDA in 150 mg/kg CUR fed ration; ↑ serum total protein, liver HSP70 . | Cui et al., 2017 | |
| Nile tilapia | V. alginolyticus | 0%, and 2% CUR | ↑ serum protein, peroxidase, serum bactericidal activity; 100% survivability in CUR fed ration challenged with V. alginolyticus. | Elgendy et al., 2016 |
| Nile tilapia | injected aflatoXin B1 at a rate of 6 mg/kg B.W. | 5, 10, 20 g/kg CUR | ↑ growth indices and feed efficiency. | El-Barbary, 2016, 2018 |
| Nile tilapia | Fish were exposed to Cr (VI) (4.57 mg/L) | 200 mg/kg | ↑quadratically improved growth indices. | Mohamed et al., 2020 |
| Rainbow trout | Aeromonas salmonicida subsp.Achromogenes | 1% (E1), 2% (E2), 4% (E3) CUR | ↑ weight gain, SGR, survival; ↓ FCR, RBC, Hb, ↑ SOD, CAT, GSH-Px but ↓ MDA in the liver, head kidney, and spleen; ↑ immune response and antioxidant status. | Yonar et al., 2019 |
| Silver catfish | infected fish Streptococcus agalactiae | 150 mg/kg CUR | ↓ disease sign, erratic swimming, corneal opacity, skin lesions in fin and tail, ↑ 100% disease resistance against Streptococcus agalactiae, and ↑ appetite. | Baldissera et al., 2018 |
| Juvenile grass carp | Fish were challenged by 1.2 mg/kg ochratoxin A | 400 mg/kg CUR | ↓ myoblast differentiation and myofibrillar development-related proteins, ↓muscle toxicity, ↑ growth performance, ↑ weight gain percentage, and final body weight. | Zhao et al., 2024a |
| Juvenile grass carp | Fish were challenged by 1.2 mg/kg ochratoxin A | 400 mg/kg CUR | ↓ OTA residues, ↓ gill injuries, ↓ intestinal damage, ↑antioxidant defenses. | Zhao et al., 2024b |
| Red Tilapia | Aspergillus flavus infection | 50–60 mg/kg nano-curcumin | ↑BW, ADG, FI, fish survival, and protein content, ↓ FCR and lipid content. | Eissa et al., 2023 |
| Pacific white shrimp | 2.5, 5, and 10 g TUR 0.075, 0.150 and 0.300 g CUR 0.075, 0.150 and 0.300 g NMC per kg of diet | ↑ final weight, WG (%), specific growth rate, and FCR. ↑ Survival rate ↑ biomass gain. ↓serum alanine transaminase and aspartate transaminase ↑ acid phosphatase, total antioxidant capacity, GSH, CAT, and SOD, ↓ MDA. | Houriyeh Moghadam et al., 2021 | |
| Pacific white shrimp | exposed to low and high salinity stress at 5 and 55 g L−1 | 2.5, 5, and 10 g TUR 0.075, 0.150 and 0.300 g CUR 0.075, 0.150 and 0.300 g NMC per kg of diet | ↑antioxidant and immunity responses. ↑overall performance and ↑resistance to salinity stress. ↓TRIG, CHO, GLU, and CORT ↑TP in haemolymph before and after the salinity stress. ↑ survival rate increased under salinity stress. ↓ haemolymph triglycerides, cholesterol. | Houriyeh Moghadam et al., 2022 |
| Pacific white shrimp | aflatoxin B1 (AFB1) 500 μg/kg | 100 mg/kg Zn-CM 200 mg/kg Zn-CM | ↑ recovery of growth performances. ↓ AFB1-induced toxic effect on growth performance. ↑ alleviate or repair the impact of AFB1 on hepatopancreas damage. ↑ recovery of lipid peroxide levels and activity of GSH. ↑ameliorates the toxicity of AFB1, immunological capacity and hepatoprotective. ↑ Powerful detoxifier for toxicity induced by AFB1 in shrimp. | Yu et al., 2018 |
Weight gain (WG), specific growth rate (SGR), feed conversion ratio (FCR), superoxide dismutase (SOD), catalase activity (CAT), malondialdehyde (MDA), glutathione (GSH), ochratoxin A (OTA), aflatoxin (AF), curcumin (CUR), turmeric (TUR), Zinc (Zn).
Effects of curcumin on mycotoxins in aquaculture
In studies conducted on Nile tilapia, it was found that injecting aflatoxin B1 at a rate of 6 mg/kg body weight and supplementing with varying concentrations of 5, 10, and 20 g/kg led to an increase in growth indices and feed efficiency (El-Barbary, 2016 and 2018). Similarly, in Pacific white shrimp exposed to aflatoxin B1 (AFB1) at 500 μg/kg, adding 100 mg/kg and 200 mg/kg of Zn-CM demonstrated an upward trend in the recovery of growth performances. Furthermore, the treatment helped mitigate the toxic effects of AFB1 on growth performance, alleviate or repair the damage to the hepatopancreas, and recover lipid peroxide levels and the activity of glutathione (GSH). This study, conducted by Yua et al. in 2018, suggested that the addition of Zn-CM acted as a powerful detoxifier, alleviating the toxicity of AFB1 by modulating antioxidation, enhancing immunological capacity, and providing hepatoprotective effects in shrimp.
Silymarin and its effects on aquatic species performance and health
How can silymarin mitigate the effects of mycotoxins on fish by its antioxidant and hepatoprotective effect?
The relationship between silymarin and mycotoxins lies in the protective effects of silymarin against oxidative stress and inflammation induced by mycotoxins. Mycotoxins are toxic compounds produced by fungi that can contaminate food and feed. Silymarin, extracted from milk thistle, acts as a potent antioxidant by neutralizing free radicals and inhibiting enzymes involved in reactive oxygen species (ROS) production (Surai et al. 2015). This antioxidant property serves as a defense mechanism against the oxidative stress caused by mycotoxins, preventing cellular damage in fish.
According to silymarin properties, this antioxidant compound has been tested against mycotoxins’ effects due to its capacity to inhibit lipid peroxidation linked to the enzymes related to oxidative stress catalase, superoxide dismutase, glutathione (GSH) peroxidase, GST and glutathione reductase, and additionally, can protect some organs from injury by activating PI3K-Akt cell survival pathway preventing apoptosis (Ghosh et al., 2016). Accordingly, in a preclinical study, silymarin was able to relieve the hepatic damage induced by FB1 toxicity attributed to its antioxidant activity linked to the reduction of the vascular endothelial growth factor (VEGF) and fibroblast growth factor-2 (FGF-2) expressions and the apoptotic rate, thereby, conferring a hepatoprotective effect (Sozmen et al., 2014). Moreover, mycotoxins often trigger inflammatory responses in the body. Silymarin, through its anti-inflammatory properties, inhibits the NF-κB signaling pathway and reduces inflammation-related gene expression. This dual action of antioxidation and anti-inflammation contributes to an overall protective effect against the harmful impact of mycotoxins on the fish’s health, as highlighted by Esmaeil et al. (2017) and Ahmadi et al. (2012).
Additionally, silymarin enhances the fish immune system, positively affecting immune cells like phagocytes and lymphocytes and increasing antibody production. This immune enhancement complements its antioxidant capabilities, providing a comprehensive defense mechanism against mycotoxins. The studies mentioned, such as those by Xiao et al. (2017), Wei et al. (2020), and Wang et al. (2019), showcase how silymarin benefits fish growth, intestinal health, and overall immune function in the presence of mycotoxin-related challenges.
When fish and shrimp exposure to environmental or pathological factors leads to liver damage or oxidative stress, silymarin supplementation works as an antioxidant and hepatoprotective compound. Several studies emphasize the protective effects of silymarin on the liver, immune response, and overall health of fish and shrimp under various conditions, and the counteracting effects of silymarin on performance parameters in aquaculture species. The effects of exposure to polluted water with harmful particles on aquaculture species were diminished by the supplementation of sylimarin (Khalil et al., 2022 ; Veisi et al., 2021). Similar positive effects were observed with the supplementation of silymarin when aquaculture species were exposed to bacteria (Owatari et al., 2018; El-Houseiny et al., 2022; Hasanthi et al., 2024).
Therefore, silymarin’s antioxidant, anti-inflammatory, and immune-enhancing properties make it a valuable supplement in mitigating the adverse effects of mycotoxin exposure in aquatic organisms (see Table 2).
Table 2. Effects of silymarin on some aquatic species.
| Target species | Challenge | Sylimarin Doses | Effects | References |
|---|---|---|---|---|
| Nile tilapia | Cesafiados por Streptococcus agalactiae serotipo Ib | 0.1% HeptarineS® (16% fosfátido de silimarina) | ↑ Marco inmunomodulador con efectos hepatoprotectores, antes y después de la provocación con Streptococcus agalactiae sin efectos deletéreos. ↑ Efecto hepatoprotector e inmunomodulador. | Owatari et al., 2018 |
| Nile tilapia | Bentonite and Silymarin | 0 (control), 2.5, 5, 7.5 and 10 g kg−1 diet | ↑ WG, SGR, PER and apparent protein utilization APU. ↑ Serum protein concentration, albumin and globulin protein.↓ aspartate and alanine. ↑antioxidant enzyme activity of SOD and CAT, transcripts accumulation of growth hormone.↑ expression of immunoglobulin M-2 (IGM-2) in liver. | Hassaan et al., 2019 |
| Nile Tilapia | Exposed to silver nanoparticles (0.05, 0.1, and 0.5 mg L−1) | 50 and 200 mg/kg | ↑growth performance, ↓ MDA, ↑GPx and ↓ glucose | Veisi et al., 2021 |
| Nile Tilapia | reared in nickel (Ni)-polluted water 3.6 mg Ni /L water | 10 g MTP/kg , 40 mg CoQ10/kg, or MTP + CoQ10 | Best neurobehavioral performance and brain oxidative status. ↑Protective effect against Ni-induced neurobehavioral disturbances and neurotoxic impacts. | Khalil et al., 2022 |
| Pacific white shrimp | Low salinity | 0, 0.1, 0.2 and 0.4 g/kg | ↑ WG and ↓ feed coefficient at low salinity. ↑ activities of digestive enzymes. ↑ alleviated the oxidative damage caused by low salinity and ↑ improved the antioxidant capacity. ↓ The relative abundance of Bacteroides and Gracilibacteri. The structure of the hepatopancreas of shrimp becomes more complete with Silymarin. | Huifeng et al., 2021 |
| Pacific white shrimp | challenge test with V. parahaemolyticus (1 × 106 CFU/mL) | 0.5–1.0 g/kg dietary Micelle silymarin (MS) | ↑ growth performance immune response, antioxidant capacity, and gut morphology, ↓inflammation and lipid peroxidation | Hasanthi et al., 2024 |
| African catfish | challenged by Aeromonas sobria | 10 g/kg sylimarin | ↑ growth performance, ↓ hepatic and renal function | El-Houseiny et al., 2022 |
| Turbot | Plant protein-based diet. | 100, 200, and 400 mg/kg | ↑ growth performance,→ feed utilization. ↑ antioxidant capacity in the liver by not only inducing the activities of SOD and CAT.↑mRNA expression levels of SOD, ↑ glutathione peroxidase, and peroxiredoxin 6. ↑ enhanced the heights of villi and enterocytes. ↓ mRNA expression of interleukin-8 and tumor necrosis factor-α but induced the expression of transforming growth factor-β (TGF-β) in the intestine. | Wang et al., 2017 |
Weight gain (WG), specific growth rate (SGR), protein efficiency ratio (PER) and apparent protein utilization (APU), superoxide dismutase (SOD), and catalase activity (CAT) The message RNA (mRNA).
Conclusion
In conclusion, the potential of curcumin and silymarin to revolutionize aquaculture practices is evident. These natural compounds not only address the challenges posed by mycotoxins but also contribute to enhanced growth, immunity, and overall health of aquatic organisms. The diverse benefits, including antioxidant, anti-inflammatory, and hepatoprotective properties, position curcumin and silymarin as valuable additions to aquaculture nutrition practices. The combined action of curcumin and silymarin offers a synergistic approach to combat mycotoxin contamination and environmental challenges, paving the way for a prosperous future in aquaculture.
