1 Introduction

Aquaculture with an average annual growth rate of 8.9% since the early 1970s compared to 1.2% for capture fisheries and 2.8% for terrestrial farmed meat production systems over the same period has become the fastest growing food production sector world-wide (FAO, 2014). One of the key factors sustaining this growth has been the use of plant-based proteins in feeds designed for use in aquaculture (Francis et al., 2001; Tiamiyu and Solomon, 2011). This is due to their lower costs when compared with fish meal based feeds, whose production has been reported to be experiencing a global decline (Spring and Fegan, 2005; Santos et al., 2010; Encarnacao, 2011). The use of plant based ingredients in fish feed formulations poses a threat to fish health as these plant product may be veritable sources of mycotoxins in the compounded feeds (Santos et al., 2010); the introduction of mycotoxins contaminated plant products in aquaculture feeds has therefore become a major concern (Binder et al., 2007; Griesler and Encarnacao, 2009; Encarnacao, 2011). Fumonisins, especially Fumonisin B1 (FB₁) produced by fungi of the genus Fusarium (Fusarium verticiloides and F. proliferatum) has been reported to be frequent contaminant of maize and products made from maize (Walter and Marasas, 2001). Animal and human health problems related to this mycotoxin are almost exclusively associated with the consumption of contaminated maize or maize products (Bucci et al., 1998; Marasas, 2001).

Serum biochemical determinations in fish blood are recognized as indispensable tools for the assessment of fish nutrition and health (Tacon, 1992; Anderson et al., 1995). Mycotoxins have been noted to cause serum biochemical alterations in exposed fishes as well as in other aquatic species (Boonyanratpalin et al., 2001). Heterobranchus longifilis a Clariid fish cultured in the West African sub region, is generally fed with feed produced from maize (Ayinla, 2007; Tiamiyu and Solomon, 2011) thereby, inadvertently imposing the risk of dietary FB₁ exposures. There is a paucity of information on the effects of dietary FB₁ in H. longifilis, this study was therefore designed to profile the effects of dietary FB₁ on the serum biochemistry and serum lipids of H. longifilis catfish juveniles following dietary exposure.

2 Materials and Methods

A total of 450 H. longifilis catfish juveniles (with an average initial weight of 120 ± 9.16 g) were randomly distributed into fifteen 1 000 L plastic tanks at a stock density of 30 fish per tank. Prior to the commencement of the study, the fish were acclimatized to the experimental conditions for 15 days. Water was replaced daily and water quality parameters were monitored throughout the duration of the study.

2.1 Production of the Basal and Fumonisin B1 amended diets

The basal diet and the Fumonisisn B1amended diets were produced according to Ayinla (2007) with slight adjustments as described by Adeyemo et al. (2016). Briefly, 1 gram crystalline fumonisin B1 procured from Sigma Aldrich was dissolved in 1 000 µL acetonitrile-water (Vol:Vol), resulting in a 1 mg: 1 µL stock solution of fumonisin B1. From this FB₁ stock solution, micro-volumes of solutions needed to produce the experimental diets for the various FB₁ inclusions (namely: diet F0 = 0.0 mg FB₁/Kg; diet F1 = 10.0 mg FB₁/Kg; diet F2 = 20.0 mg FB₁/Kg; diet F3 = 40.0 mg FB₁/Kg and diet F4 = 80.0 mg FB₁/Kg) were pipetted into 1 000 mL beakers into which had been placed 200 mL distilled water. After careful stirring, weighted portions of the starch binders were added, followed by the addition of the weighed portions of the basal diets. The dough produced were then pelletized using a bench extruder fitted with a 3 mm dais, oven dried at 65°C for 30 minutes, allowed to cool to ambient temperature, and thereafter, subjected to proximate and fumonisin B1 content analyses before being packed in cellophane bags and then stored at 4°C until used.

2.2 Extraction of Serum and Determination of Lipids and Biochemical parameters

At time points 7, 28 and Day 56, post dietary exposure to the fumonisin B1 amended diets, blood was collected from the caudal vein using a 5 ml syringe fitted with a 23 gauge needle. The aspirated blood was carefully dispensed into clean narrow bored glass test tube and allowed to clot for 5 minutes. The separated serum were then eluted from the clotted blood by the use of clean tuberculin syringes after which, they were dispensed into Ependorph tubes and stored at 0.0°C until used.

2.2.1 Determination of Biochemical parameters

The serum assays were done using commercial test kits (Spectrum Laboratory, Egypt) and adhering strictly to manufacturer’s instructions. Serum total protein was determined by the biuret test (Campbell, 2012), Albumin was determined by the Bromocresol-green method and globulin calculated mathematically by subtracting the value obtained for albumin from the values obtained for total protein (Coz-Rakovac et al., 2005; Campbell, 2012). Serum urea nitrogen and serum creatinine were determined by the modified Berthrlot-Searcy and Modified Jaffe method respectively (Campbell, 2012). Serum activity of aspartate aminotransferase and alanine aminotransferase were determined following the Rietman-Frankel colorimetric method (Schumann et al., 2002). Serum alkaline phosphatase activity was determined using the phenolphthalein monophosphate method (Campbell, 2012).

2.2.2 Determination of Lipid profile

Total serum cholesterol was estimated using automatic serum chemistry auto analyser and kit (AUTOPAK supplied by Beyer Diagnostics India) by the enzymatic (Cholesterol Esterase, Cholesterol Oxidase and Peroxidase method of Allain et al. (1974). Results obtained were expressed as mg dL^-1 of serum. Serum Triglycerides estimation was carried out with the use of the automatic serum analyser and kit (AUTOPAK, Bayer Diagnostics India) by the enzymatic Lipoprotein lipase, Glycerol kinase, Glycerol-3-Phosphate Oxidase method of McGowan et al. (1983) and the results expressed as mg dL^-1 of serum. The serum high density lipid was estimated using the automatic serum analyser and kits (AUTOPAK, Bayer Diagnostics India) following the phosphotungstate method. Results obtained were expressed as mg dL^-1 of serum. Serum Very Low Density Lipoprotein-Cholesterol (VLVD) was estimated using the Friedewald formula (Friedewald et al., 1972; Allain et al., 1974).

VLVD-Chol = Serum triglycerides /5

And results obtained expressed as mg dL^-1 of serum.

The serum Low Density Lipoproteins was estimated mathematically as the difference between the serum total cholesterol and the sum of the Very Low Density Lipid cholesterol and the High Density Lipid cholesterol according to the Friedwald formula (Friedewald et al., 1972)

LDL-Chol (mg/dL serum) = Total Chol – (VLDL-Chol + HDL-Chol).

3 Statistical Analysis

Data obtained from the study were subjected to one-way analysis of variance (ANOVA) using SPSS version 20.0 (SPSS Inc., Chicago, IL, USA). Significant differences among groups were identified by Duncan’s multiple test (P < 0.05). Data are presented as mean ± SD.

4 Results

The physico-chemical properties of the culture water are presented in Table 1. It revealed that water temperature, salinity, pH, dissolved oxygen and unionized ammonia are within the optimum ranges for rearing Clariid fishes (Boyd and Tucker, 1992).

Table 2 shows values obtained for the proximate and fumonisin B1 analysis of the experimental diets. It shows the experimental diets had higher concentrations of FB₁ than as was introduced at the time of production namely, the formulated diets had fumomnisin B1 concentrations of 2.37; 14.68; 24.74; 43.04 and 82.77 mg. kg ^-1 FB₁ for diets F0, F1, F2, F3 and F4 respectively.

4.1 Serum biochemistry

Diets F3 and F4 produced marginal but significant (p < 0.05) hypoproteinemia at 7 days of feeding compared with the control diet (Diet F0) and the other diets (Diet F1 and F2). At days 28 and 56 of the dietary experiment, the results obtained for the serum total protein analysis showed that there was no significant variation (p > 0.05) between the serum total protein concentration of fish fed the control diets (diet F0) and fish fed the diets amended with various amounts of fumonisin B1 (i.e diets F1; F2; F3 and F4). Feeding on diets F3 and F4 elicited mild but significant (p < 0.05) hyperalbuminemia in exposed fishes at 7 days of feeding compared to fishes fed the control diet and fishes feed diet F1 and F2 at the same time intervals. At days 28 and 56, fishes fed diet F4 had significantly (p < 0.05) elevated serum albumin concentration compared with fishes fed the control diet (diet F0) and diets F1, F2 and F3 (Table 3; Table 4).

Dietary exposure to varied amounts of fumonisin B1 caused significant (p < 0.05) elevation of serum globulin concentration in fishes fed diet F2 and marked reduction in serum globulin concentration in fishes fed diet F3 and F4. One way analysis of variance (ANOVA) revealed significant (p < 0.05) increases in the serum globulin concentration of fishes fed diet F1 and F2 compared with fishes fed the control diet (Diet F0) and significant (p < 0.05) decreases in the serum globulin concentration of fishes fed diets F3 and F4 compared to the fish fed the control diet (Diet F0). Furthermore, a similar trend was observed 28 days post commencement of the feeding experiment, although at this time point, there was mild hyperglobulinemia in fishes fed diet F2 compared with fish fed the control diet. ANOVA revealed this value was not significantly different (p > 0.05) from the values obtained for the fish fed the control diet.

Dietary fumonisin B1 elicited marginal but significantly increased (p < 0.05) serum creatinine kinase activity. ANOVA revealed the serum creatinine kinase activity of fishes fed diet F1 were not significantly (p > 0.05) different from those of fishes fed diet F2 at 7 days post commencement of the feeding. Also, at the same time interval, the serum creatinine kinase activity of fish fed diet F3 were not significantly different (p > 0.05) from those of fish fed diet F4. At day 28 and 56 of the feeding exposure, whereas there were no variations (p > 0.05) in the serum creatinine kinase activity of fish fed diet F1 and F2 compared to the fish fed the control diet (diet F0); there were significant variations (p < 0.05) in the serum creatinine kinase activity in fish fed diets F3 and F4 compared to fish fed the control diet (diet F0). ANOVA further revealed that at both day 28 and day 56 post commencement of the feeding, the serum creatinine kinase activity of fish fed diet F3 were significantly different (p < 0.05) from those of fish fed diet F4 (Table 4; Table 5).

Dietary exposure to varied concentrations of fumonisin B1 caused significant increases (p < 0.05) in serum activity of AST and ALT compared to those of fish fed the control diet at day 7, 28 and 56 (Table 3; Table 4; Table 5). Table 3, Table 4, and Table 5 further showed that fish fed diet F2 had consistently higher serum AST and ALT activity compared with fish fed the other diets. The serum alkaline phosphatase (ALP) activity increase from 6.17 ± 1.00 IU to 23.00 ± 1.66 IU (at day 7). At day 28 of the dietary experiment, the serum ALP activity increased from 8.39 ± 1.70 IU (in the fish fed the control diet) to 29.11 ± 1.03 IU (in fish fed diet F4). ANOVA revealed the serum ALP activity varied significantly (p < 0.05) between fish fed the control diet and fish fed diets amended with varied concentrations of fumonisin B1. Further, ANOVA also revealed significant variations (p < 0.05) in the serum activity amongst the fish fed the various concentrations of fumonisin B1.

Serum lactase dehydrogenase (LDH) concentration increased from 198.07 ± 6.44 (in fishes fed the control diet) to 739.89 ± 10.28 (in fish fed diet F4) 7 days post commencement of the feeding experiment (Table 2). ANOVA revealed significant variations (p < 0.05) in the serum LDH concentration in the fish fed the control diet compared to the fish fed diets amended with the various concentrations of fumonisin B1; further, the serum LDH concentration varied significantly amongst the fishes fed the various concentrations of fumonisin B1. At day 28 post commencement of the feeding, the serum LDH concentration increased from 195.78 ± 2.04 (in fish fed the control diet) to 718.13 ± 11.47 (in fish fed diet F4); and at day 56 post commencement of the feeding experiment, the serum LDH concentration ranged from 192.79 ± 3.27 (in fish fed the control diet) to 710.16 ± 21.19 (in fish fed diet F4). ANOVA revealed significant variations (p < 0.05) in the serum LDH concentration in a comparison between fishes fed the control diet and fish fed the diets amended with the varied concentrations of fumonisin B1. Further, ANOVA also, revealed the serum LDH concentration varied significantly (p < 0.05) amongst fishes fed the various concentrations of dietary fumonisin B1.

4.2 Serum lipids profile

Diets amended with the varied concentrations of FB₁ produced significantly elevated serum total cholesterol concentration compared to the fish fed the control diet at day 7 post commencement of the fumonisin B1 amended diets (Figure 1). Further, the serum total cholesterol concentration in fishes fed the diet amended with FB₁ varied significantly (p < 0.05) from one another and increased along the gradient of FB₁ inclusion. Also dietary exposure to FB₁ produced significant (p < 0.05) elevation of the serum HDL concentration compared with fish fed the control diet. ANOVA further revealed that at day 7, except for fish fed diet F4, the serum HDL concentration were not significantly different (p > 0.05) amongst the groups of fish fed diets amended with FB₁. Serum very low density lipids (VLDL) in fishes fed the control diet at day 7 post commencement of the dietary exposure was 16.56 ± 7.09 while the serum VLDL for fishes fed the diets amended with FB₁ ranged from 24.03 ± 4.11 (in fish fed diet F1) to 32.64 ± 7.63 (in fish fed diet F4) (Figure 1); dietary exposure to FB₁ for 7 days also caused significant elevation (p < 0.05) in the serum triglycerides (TRG) concentration compared to fishes fed the control diet. Fishes fed the control diet (diet F0) had serum TRG concentration of 82.79 ± 10.07 whereas, the serum TRG concentration in fishes fed the diets amended with FB₁ ranged from 120.14 ± 9.13 (in fishes fed diet F1) to 163.17 ± 23.15 (in fishes fed diet F4).

Figure 2 depicts serum lipids profile of Heterobranchus longifilis catfishes at 28 days of dietary exposure to FB₁. It shows fish fed diet F0 (the control diet) had serum total cholesterol concentration of 97.20 ± 8.79 whereas the serum total cholesterol concentration of fish fed the diets amended with FB₁ ranged from 106.83 ± 10.54 (in fishes fed diet F1) to 117.34 ± 18.39 g/dL. ANOVA revealed the serum total cholesterol concentration of fishes fed diets amended with FB₁ to be significantly higher than those of fish fed the control diets; further, ANOVA also showed that the serum total cholesterol concentration varied significantly (p < 0.05) amongst the fishes fed the diets amended with FB₁. At this same period, the serum TRG concentration ranged from 78.84 ± 17.04 (in fish fed diet F0) to 167.09 ± 21.09 (in fish fed diet F4). ANOVA further showed that the serum TRG concentration varied significantly between fish fed the control diet compared to fish fed the diets amended with FB₁.

The serum lipids profiles of fish fed the control and the fumonisin B1 amended diets at day 56 of dietary exposure are as depicted in Figure 3. It shows serum cholesterol concentration of fish fed the control diet to be 93.56 ± 8.11 whereas those of fish fed the diets containing varied amounts of FB₁ ranged from 103.12 ± 20.17 (in fish fed diet F1) to 129.33 ± 15.09 (in fish fed diet F4). ANOVA reveals the serum total cholesterol concentration of fish fed diets amended with fumonisin B1 to be significantly higher than those of fish fed the control diet. Also, whereas, the total cholesterol concentration of fish fed diet F1 was not significantly different from those of fish fed diet F2, they however, significantly differ (p < 0.05) from those of fish fed diet F3 and diet F4. Furthermore, the serum total cholesterol concentration of fish fed diet F4 was significantly higher than those of fish fed diet F3.

The serum triglyceride (TRG) concentration following dietary exposure of H. longifilis catfish at 56 days of the experiment are as depicted in Figure 3. It shows the serum TRG concentration of fish fed the control diet to be 81.17 ± 23.04 while the serum TRG concentration of fish fed the diets amended with varied concentrations of ranged from 120.11 ± 25.07 (in fish fed diet F1) to 175.92 ± 18.44 (in fish fed diet F4). ANOVA revealed the serum TRG concentration of fishes fed diets amended with varied concentrations of FB₁ were significantly higher compared to those of fish fed the control diet; also, the serum TRG concentration varied significantly amongst fishes fed the diets amended with the varied amounts of FB₁ and increased along the gradient of concentration of dietary FB₁ inclusions.

5 Discussions and Conclusion

The FB₁ contents of the various diets were at variance with the amounts of purified FB₁ introduced to the diets at the time of the production of the experimental diets; this is not unexpected, as it has been reported that the Fumonisins especially FB₁ is ubiquitous in maize and in products made from maize (Bankole and Mabekoje, 2004; Binder et al., 2007; Griesler and Encarnacao, 2009), therefore, the difference in the concentration of the FB₁ in the produced diets and the amounts of purified FB₁ introduced in the diets at the time of production is indicative of the of the amounts of “endogenous” FB₁ present in the maize used for the production of the diets (McDonald and Milligan, 1992; McCue, 2010; Monbaliu et al., 2010).

The serum total protein concentration is often used as an indicator of physiological condition in fish (Maita, 2007). The serum total protein concentration consists of the serum albumin and serum globulin concentrations (Wagner and Congleton, 2004). An increase or decrease of serum total protein concentration is of clinical significance and relevance in animals as well as in fish (McDonald and Milligan, 1992; McCue, 2010). Serum total protein is altered mainly by changes in serum volume due to osmotic imbalances between extra- and intracellular compartments induced by pathophysiological situations which also impair hepatic synthesis of blood proteins; increase catabolism or losses of albumin in the urine and or promote synthesis of globulins by the immunocompetent cells (McDonald and Milligan, 1992). In this study, dietary FB₁ induced hypoproteinamia in the exposed H. longifilis catfish juvenile within the first 14 days and not after day 28 of the dietary exposure. This may be attributable to a reduction in the feed uptake within the first 14 days and or subsequent adjustments to the FB₁ amended diets starting from day 28 (Lemarie et al., 1991; Artacho et al., 2007).

Hypoproteinemia has been associated with malnutrition or malabsorption due to insufficient feed intake, digestion or absorption (LeMerie et al., 1991; Artacho et al., 2007; McCue, 2010), hyperalbuminemia and hyperglobulinemia on the other hand has been related to stress, inflammation or innate immune response in teleostan fishes (Svobodova et al., 2001; Maita, 2007; McCue, 2010). In this study, hyperalbuminemia was observed 7 days following dietary exposure of H. longifilis catfish juveniles to diets containing more than 40.0 mg FB₁/kg and not in fishes fed diets containing less than 20 mg FB₁/kg; this was not observed at and after 28 days of the feeding experiment, suggesting dietary FB1 at an inclusion rate greater than or equal to 20.0 mg FB₁/ kg may have produced an inflammatory condition in the exposed H. longifilis catfishes; similar to the reports in Clarias gariepinus catfish juveniles exposed to dietary FB₁, in which there was consistent leucocytosis at dietary inclusion levels of FB1 ≥ 20.0 mg per kg diet (Adeyemo et al., 2016), and in Wistar rats feed diets containing fumonisin B1 (Voss et al., 1992).

Creatinine, a decomposition product of creatine and phosphocreatine; is an anhydride of creatine present in muscles and released into blood following muscular injury or necrosis. Free creatinine is not metabolized in the body and thus functions as a waste of creatine and excreted by the kidney. The serum concentration of creatinine has been determined to be constant and directly proportional to the creatine content of muscles undergoing degeneration and or necrosis. Because of its relative independence from such factors as protein intake, degree of hydration and protein metabolism, Maita (2007), proposed its usage as a useful index for renal function. In this study, there was a consistent elevation of serum creatinine concentration in fishes fed the FB₁ amended diets. An increase in serum creatinine concentration has been reported to occur in any or a combination of conditions in which blood urea is increased (Wagner and Congleton, 2004) or in conditions involving malfunctioning of the kidneys and also in extensive muscular degeneration and or necrosis (McCue, 2010).

Urea, described to be quantitatively the most important non protein nitrogenous constituent of blood (McDonald and Milligan, 1992) is the chief end product of protein metabolism excreted by the kidney. Its blood concentration is reported to be directly related to the protein content of the diet and to the excretory capacity of the kidney (Wagner and Congleton, 2004). In pathological conditions affecting the liver, urea formation is impacted resulting either in an increase or a decrease in blood urea nitrogen. In teleostan fishes, the main product of nitrogen metabolism is ammonia, and to a lesser degree, urea (Cnaani et al., 2004). Kidney conditions (principally nephritis and or nephrosis) and urinary tract obstructions have been reported to be main aetiologies of increases in blood urea nitrogen concentrations (Cnaani et al., 2004). Hence renal dysfunctions accompanied with severe renal insufficiencies and or excessive bodily breakdown of proteins have been reported to be associated with elevations of blood urea nitrogen concentration (Coz-Rakovac et al., 2005). The elevations of urea serum concentrations in H. longifilis catfish juveniles seen in this study may represents impairments in the kidney functions of the fishes fed diets amended with FB₁ similar to the findings in rats fed purified FB₁ (Voss et al., 1992).

The serum AST and ALT activities increased significantly in a dose and duration dependent manner compared with to the fish fed the control diets. Increases in the AST and the ALT serum activity in the fishes fed the diets amended with FB₁ is perhaps due to the hepatocellular injury and increased release of these enzymes (Tang and Chen, 2003). Lactate dehydrogenase (LDH), has been reported to catalyse the conversion of lactate to pyruvate under anaerobic conditions. An increase in the serum activity of LDH has been reported to indicate anaerobiosis due to hypoxia, limiting temperature or the activity of dietary or environmental toxins (Tang and Chen, 2003). Also, in this study, dietary FB1 caused significant increases in the serum concentration of ALP and LDH in fish fed diets amended with fumonisin B1 signifying injuries to the hepatobiliary tracts (Pepeljnjak et al., 2002; Tuan et al., 2003).

According to McCue (2010), serum lipids particularly serum total cholesterol and serum triglycerides concentrations are dependent on the nutritional and or physiological statuses of the fish. Malnutrition and or starvation cause a decrease in the serum concentration of total cholesterol and an increase in the serum triglyceride concentration (Perez-Jimerez et al., 2012). The serum lipids (cholesterols, high density lipids, very low density lipids, low density lipids and triglycerides) were significantly elevated in H. longifilis catfish juveniles fed the diets amended with FB₁ compared to fishes fed the control diets. These increases were dependent on the concentration of the FB₁ contents in the diets and also on the duration of the feeding exposure. Increased serum lipids concentration may be due to hepatocellular degeneration and dysfunction which ultimately impact on the activity of cytochrome P450 enzymes (Williams and Latropoulos, 2002). Further, the dietary FB₁ may also have caused a depression of the hepatic activity of lipogenic and cholesterolegenic enzymes (Soriano et al., 2005), a step precedent upon the development of toxicities reported in chronic FB₁ toxicity studies (Zhang and Du, 2012).

In conclusion, dietary fumonisin B1 initiated significant physio-pathological changes in Heterobranchus longifilis catfish juveniles. These changes marked by increased serum activities of liver and kidney marker enzymes, were also accompanied by significant increases in serum concentrations of total cholesterol, low density cholesterol and serum triglycerides. Further, dietary inclusions of fumonisin B1 ≤ 24.74 mg. kg ^-1 appears to be the safe and acceptable tolerance levels in juvenile H. longifilis catfishes.

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