Underwater intrigue: exploring mycotoxins’ impact on fish

In brief:

  • The risk of mycotoxin contamination is never zero
  • A typical Tilapia diet comprises soybean meal, sunflower meal, yellow maize, rice bran and wheat middlings – all susceptible to mycotoxin contamination
  • Disease challenge is at an all-time high, which may mean mycotoxin risk is overlooked

Beneath the surface: subclinical impact of dietary imbalance

Typically, a producer’s key management concern centers around disease, environment, and cost of feed. Diseases are widespread in aquaculture and pose a high risk to profitability in fish. Environmental fluctuations and stressors add additional pressure. Feed price fluctuate based on global market supply and demand and are one of the biggest costs.

Like all living animals, fish and shrimp have a requirement for certain nutrients. This includes amino-acids, cholesterol, vitamins, and minerals. In commercial fish production, this feed is usually grain and oilseed based. This brings in a sometimes-overlooked challenge: mycotoxins, common contaminants in animal feed.

Clinical symptoms due to mycotoxin contamination levels are rarely observed in aquatic species. More frequently, animals are exposed to moderate levels of mycotoxins over a long time. This chronic exposure leads to unspecific effects typically observed as decreased performance.

Poor performance typically manifests as slow growth, increase in feed conversion ratio (FCR), higher susceptibility to disease, and increased medical costs. Nevertheless, these subtle effects often pass unnoticed or are not traced back to the presence of mycotoxins.

Balancing act: nutritional requirement and key feed ingredients

Dietary formulations vary, depending on raw material availability, price, and developmental stage. Production of salmon, trout, Tilapia, seabream and seabass through different developmental stages should include crude protein at 20 – 60% and crude lipid at 4-30% (1-5). For vitamin recommendations, dsm-firmenich has developed OVN Optimum Vitamin Nutrition® guidelines.

From a macro-ingredient perspective, fish feeds are following the global trend to reduce reliance on marine ingredients. This is typically delivered through increased usage of plant-based raw materials.

Plant proteins may be the largest protein contributor, but their increased inclusion is not without risk. Even when diets are nutritionally balanced to limit amino acids, any increase in plant ingredients means a greater chance of introducing unwanted contaminants. These include anti-nutritional factors (ANFs), including mycotoxins. Ultimately, this will impact health and performance.

Example of a typical Nile Tilapia diet in the Middle East:
Tilapia Raw materialTilapia Inclusion (%)
Soybean meal, 46% CP44
Poultry meal 55%7.15
Sunflower Meal 36% CP4.5
Yellow maize, 7.5%12.80
Fish premix, 0.5%0.5
Limestone (CaCO3)1.3
Rice bran, full fat11
Salt (NaCl)1.5
Wheat middlings - 14-1515
DL-Methionine0.14
Antioxidant0.05
Mono calcium phosphate (MCP)0.41
Soybean oil1.3
Mycotoxin binder, Mycofix®0.1
Fish oil0.5

Deep dive: impact of mycotoxins on salmonid performance

There has been quite some research done on effects of mycotoxins in salmonids. Most studies however are limited to rainbow trout (Oncorhynchus mykiss). Aflatoxins have been shown to lead to lesions in liver tissue at a high dosage of 80 ppm (6). Dose-dependent increase in liver tumor incidence was also observed at 4-64 ppb (7).

Although Aflatoxins are the most toxic mycotoxins, focus of research has been on the more frequently occurring Fusarium mycotoxins DON and ZEN, with less investigations for FUM (see table below).

Summary of observed detrimental effects of mycotoxins on liver, intestine and immune system, performance, and reproductive tract (selected studies):
 LiverIntestine and immune systemPerformanceelseReproductive Tract
DON

affected hepatosomatic index (1 200 ppb; 4 700 ppb)
(8) (9)

 

histopathological changes (1 200 – 2 800 ppb) (10), (11), (12), (13)

 

increased liver enzyme activities in serum (1 200-2700 ppb) (10)

 

increased relative liver weight (dose-dep., 500 -6000 ppb; Salmo salar) (14)

biomarkers of oxidative stress in liver, kidneys, and gill (1 960 ppb) (15)

 

Dose-dependent decrease in antibody response to Aeromonas salmonicidae vaccination. (500– 600 ppb; Salmo salar) (14)

 

histopathological changes intestine (2 800 ppb) (13)

 

decreased mucosal fold width and enterocyte width in the midgut (1 329 ppb) (9)

Decreased body weight (370 ppb) (10), (>4 700 ppb) (8), plus ZEN (16), (9), (12), (13)

 

Decreased weight gain (>4 700 ppb) (8), (start 300 ppb) (17), (2 100 ppb) (20), (11), (18), (9), (12), (13)

 

Decreased feed intake (>4 700 ppb) (8), (2 700 ppb) (10), plus ZEN (16), (11), (18)

 

Increased feed intake (370 ppb) (10), (2 100 ppb) (20),

 

Decreased feed efficiency (370 ppb) (10), plus ZEN (19), (start 300 ppb) (17), (2 100 ppb) (20), (11), (18), (9), (12), (13)

 

Decreased crude protein content, retained nitrogen (retention) (start 300 ppb) (17), (2 100 ppb) (20), (11), (18)

altered body composition (8), (2 100 ppb; 10), (20)


abnormal body confirmation and anal papilla (2 700 ppb) (10)

 

decreased blood levels of hemoglobin, glucose, cholesterol, ammonia, histopathological changes in the caudal kidney (1 960 ppb) (25)

 

increase in whole body water content (start 300 ppb) (18)

 
ZENhistopathological changes (1 800 ppb) (21)

Effects on immunological parameters and oxidative stress biomarkers in serum and intestines (300-600 ppb) (22)

 

affected hematological parameters (e.g., decreased B lymphocyte concentration) and cytokine expression in different organs (2 000 ppb) (23)

reduced feed intake and weight gain (500 ppb + 3 300 ppb DON) (500 ppb + 4 100 ppb DON) (16) (19)

 

reduced final body weight, weight gain, specific growth rate, increased FCR (300-600 ppb) (22)

 

increased growth, decreased FCR (23)

Effects on digestive enzymes (300-600 ppb) 

 (22)

 

inflammation of the trunk kidney (2000 ppb) (23)

advanced ovarian development (1 800 ppb) (21)

 

increased mortality of offspring, morphological anomalies in gonads, increased vitellogenin concentration in plasma of male fish (2 000 ppb) (24)

FUMhistopathological changes, affected hepatosomatic index (~8 800 ppb) (13)histopathological changes in intestines (~8 800 ppb) (13)inhibited growth, reduced final body weight and feed conversion ratio (~8 800 ppb) (13)  
DON = deoxynivalenol; ZEN = zearalenone; FUM = fumonisins

Research shows that negative effects on the liver can not only be the result of a contamination with Aflatoxin, but also with DON, ZEN and FUM. These mycotoxins show a negative effect on performance of salmonids, as reduced final body weight, reduced feed intake and increased FCR. First studies highlight the negative impact of the estrogenic mycotoxin ZEN on the reproductive tract in rainbow trout with a concentration at EU guidance value of 2,000 ppb.

An impact on the immune system and intestine of salmonids is indicated as well. The immune system of fish is quite complex, and similar to the immune systems of mammals, including innate and adaptive immunity (35). Important for the fish immune system are also specialized organs and cell types as the thyme, head kidney and spleen, as well as the mucosa-associated lymphoid tissue; skin, gill, and gut-associated (35).

Several detrimental effects were described on the intestine and immune system. Studies found histopathological lesions in the intestine, a negative effect on gut mucosa, hematological parameters, oxidative stress biomarkers in the liver, kidneys, and gill. Conversely, some studies describe no increased mortality in the presence of mycotoxins and challenge to Yersinia ruckeri and Flavobacterium psychrophilum (10, 19, 36).

Decreased antibody response to vaccination to Aeromonas salmonicidae was described in Salmo salar. Fish are constantly challenged by pathogens due to their environment, so a negative impact of mycotoxins on different parts of the immune system would add further challenge.

For OTA research results are limited. A high dose intra-peritoneal study at 2,000 ppb resulted in degeneration and necrosis of liver and kidney, swollen liver as well as pale kidney and increased mortality (26).

Closer look: mycotoxin impact on tilapia performance

Fewer studies are available for research on the effects of mycotoxins in Tilapia. High focus rests on aflatoxins, confirming their toxic effects in animals especially on the liver. Contamination with Aflatoxin amongst others, also increased mortality of Tilapia in several studies. Aflatoxin also impacted kidney and spleen as well as fish carcass. Although residues in the liver have been described at high contamination levels, one study indicated residues in the whole body. Negative effects on liver health have been also observed in the presence of DON, and one study suggests a co-contamination of Aflatoxin with FUM might promote liver tumors. For all toxins described in the table below, an impairment of performance can be observed. A study with co-contamination of DON and ZEN showed a dose-dependent decrease of performance and an increase in mortality.

Summary of observed detrimental effects of mycotoxins on liver, intestine and immune system, performance, and reproductive tract (selected studies):
 LiverPerformanceelseReproductive Tract
Afla

Chronic liver manifestations (yellowing, enlargement, necrosis, inflammation, cellular swelling) (5-39 ppb) (43)

 

Hepatic disorder (245 ppb) (28)

 

Hepatosomatic index (150-245 ppb) (28) (27)

 

Residues in liver (200 ppb) (29), (28)

 

Histopathological changes (200 ppb) (29)

Decreased growth rate and increased FCR (40 – 20 000 ppb) (40), (34), (41), (42), (37), (39), (27), (28), (29)

Increased mortality (5-200 ppb) (34) (29) (43)

 

No significant effect on mortality (30 000 ppb) (40), (37)

 

Kidney-somatic index (150 ppb) (27)

 

Impaired spleen (27) (29)

 

blood parameters (27)

 

fish carcass (27)

 

residues (whole body) (27)

Gonads-somatic index (27)
DON

Histopathological changes (1 600 + ZEN 340 ppb, 1 000 ppb FUM)) (30)

 

Increased hepatosomatic index (1 600 + ZEN 340 ppb, 1 000 ppb FUM) (30)

Reduced weight gain, feed intake and efficiency 

(dose-dependent effect with ZEN (310 ppb and 90 ppb) (33)

 

Decreased biomass gain 

(1 600 + ZEN 340 ppb, 1 000 ppb FUM) (30)

No effect (100 – 1 100 ppb) (17)

Increase in mortality (dose-dependent effect with ZEN (310 ppb and 90 ppb) (33) 
ZEN 

Reduced weight gain, feed intake and feed efficiency 

(dose-dependent effect with ZEN (start 70 ppb and 10 ppb) (33)

Increase in mortality (dose-dependent effect with ZEN (310 ppb and 90 ppb) (33) 
FUMMay promote liver tumors when co-contamination with Afla (32)Weight gain, feed efficiency (50 000 ppb) (31)

mRNA expression reduced (growth hormone receptor, insulin growth) (50 000 ppb) (31)

 

decreased hematocrit (38)

 
Afla = aflatoxins; DON = deoxynivalenol; ZEN = zearalenone; FUM = fumonisins

What’s next?

The risk of mycotoxin contamination is never zero. Even with the best quality control procedures, mycotoxins are a constant threat. So how do producers manage this, alongside the demands of disease challenge? A robust mycotoxin risk management program is essential. Part of the toolbox is using mycotoxin deactivator in the feed formulation. Mycofix® is a state-of-the-art mycotoxin deactivator comprising three modes of action for the ultimate insurance policy against a wide range of known, and emerging mycotoxins. Adsorption to bind adsorbable mycotoxins, biotransformation to detoxify non-adsorbable mycotoxins and bioprotection, natural ingredients supporting liver and hepatopancreas, immune system and intestinal barrier.

A proper mycotoxin risk management is key to protect fish from the adverse effects of mycotoxins, thus supporting business profitability.

References

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  31. Claudino-Silva 2018. Fumonisin affects performance and modulates the gene expression of IGF-1 and GHR in Nile tilapia fingerlings and juveniles. https://doi.org/10.1016/j.aquaculture.2019.04.027
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Published on

11 June 2024

Tags

  • Aquaculture
  • Fish
  • Mycotoxins

About the Author

Anneliese Müller - Product Manager Mycotoxin Risk Management, Animal Nutrition & Health at dsm-firmenich

Anneliese Müller is a Global Product Manager for Mycotoxin Risk Management. She studied biology at the University of Vienna and did her PhD in survival mechanisms of foodborne pathogens  at the University of Veterinary Medicine Vienna. She is regularly working with and publishing the results of the global dsm-firmenich Mycotoxin Survey.

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