Assessment of Safety, Effects, and Muscle-Specific Accumulation of Dietary Butylated Hydroxytoluene (BHT) in <i>Paralichthys olivaceus</i>

Lee, Seunghan; Kim, Min-Gi; Hur, Sang-Woo; Katya, Kumar; Kim, Kang-Woong; Lee, Bong-Joo

doi:https://doi.org/10.1155/2023/1381923

Aquaculture Nutrition

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Abstract Introduction Materials and Methods Results Discussion Conclusions Data Availability Conflicts of Interest Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2023 | Article ID 1381923 | https://doi.org/10.1155/2023/1381923

Assessment of Safety, Effects, and Muscle-Specific Accumulation of Dietary Butylated Hydroxytoluene (BHT) in Paralichthys olivaceus

Seunghan Lee,¹Min-Gi Kim,¹Sang-Woo Hur,¹Kumar Katya,²Kang-Woong Kim,¹and Bong-Joo Lee³

Academic Editor: Houguo Xu

Received22 Sept 2022

Revised20 Nov 2022

Accepted20 Dec 2022

Published02 Feb 2023

Abstract

Butylated hydroxytoluene (BHT) is a commonly used antioxidant added to animal/fish feed to limit lipid autoxidation and peroxidation. Although there have been reviews and reports of BHT toxicity in animals, limited information is available with respect to the toxic effects and accumulation of BHT due to oral exposure in aquaculture species. Therefore, 120 days of feeding trial was conducted to evaluate the effects of dietary BHT on the marine fish olive flounder Paralichthys olivaceus. Graded levels of BHT were added to the basal diet in increments of 0, 10, 20, 40, 80, and 160 mg BHT/kg, corresponding to 0 (BHT₀), 11 (BHT₁₁), 19 (BHT₁₉), 35 (BHT₃₅), 85 (BHT₈₅), and 121 (BHT₁₂₁) mg BHT/kg diets, respectively. Fish with an average weight of g () were fed one of the six experimental diets in triplicate groups. Growth performance, feed utilization, and survival rate were not significantly affected by the dietary BHT levels among all experimental groups, whereas BHT concentration in the muscle tissue was found to increase in a dose-dependent manner up to 60 days of the experimental period. Thereafter, BHT accumulation in muscle tissue showed a declining trend among all treatment groups. Furthermore, the whole-body proximate composition, nonspecific immune responses, and hematological parameters (except triglycerides) were not significantly influenced by the dietary levels of BHT. Blood triglyceride content was significantly higher in fish fed the BHT-free diet compared to all other treatment groups. Thus, this study demonstrates that dietary BHT (up to 121 mg/kg) is a safe and effective antioxidant without exhibiting any adverse effects on the growth performance, body composition, and immune responses in the marine fish olive flounder, P. olivaceus.

1. Introduction

Seafood is widely known as a healthy source of animal protein owing to its unique polyunsaturated fatty acid (PUFA) profile, particularly eicosapentaenoic acid (EPA, C20:5n-3) and docosahexaenoic acid (DHA, C22:6n-3) [1]. In commercial fish farming, PUFAs are supplied via feed composed of multiple ingredients, including fish oil, fishmeal, and microalgae. However, the presence of PUFAs in fish lipids makes them highly susceptible to autoxidation and peroxidative damage [2]. Such autoxidation initiates a series of other changes and produces toxic reactive oxygen species (ROS) such as superoxide, peroxides, hydroxyl radicals, and singlet oxygen in the food system. Furthermore, these products react with other native dietary nutrients and reduce the bioavailability of proteins, lipids, and vitamins. Feeding farmed species feeds containing oxidized fats may cause a reduction in growth and feed intake and sudden disease outbreaks, resulting in a higher mortality rate [3]. In seafood, such changes reportedly have detrimental effects on the nutritional profile, wholesomeness, safety, color, flavor, and texture [4], whereas consumer interest in the quality and safety of farmed fish as well as the absence of concomitant pollutants, antibiotics, and carcinogens has increased recently [5–7].

A commonly used method to improve product stability and extend the shelf-life of seafood is dietary manipulation using commercial antioxidants [8–13]. Antioxidants are highly effective in lowering or delaying the chances of oxidation of food and feed by retarding the formation of toxic oxidative products [14]. Butylated hydroxytoluene (BHT) is a commercially popular synthetic antioxidant used to preserve and stabilize the freshness, nutritive value, flavor, and color of foods and feed products [3, 15–19]. The pathway of BHT function involves blocking free radicals and converting them into stable products [17]. In order to prevent autoxidation and nutrient loss, BHT inclusion has long been practiced in animal feeds containing high levels of unsaturated fatty acids [20]. Dietary inclusion of commercial antioxidant ethoxyquin (EQ) at the rate of 150–1500 mg/kg has been reported to effectively relieve oxidative stress induced by fish oil oxidation in largemouth bass (Micropterus salmoides) [21]. Commercially, EQ, BHT, and butyl-hydroxyanisole (BHA) are authorized for use in animal and aquaculture feed up to a maximum concentration of 150 mg/kg. The use of BHT as a direct or indirect food/feed additive is authorized in approximately 40 countries around the world [22, 23]. However, an overdose of BHT has been reported to adversely affect various tissues and organs in rats and several other species [24–26]. Recently, Liang et al. [27] reported that exposure to BHT can influence hyperactivity and dopamine-related gene expression, which induce abnormal anxiety-associated behavior in larval zebrafish.

The marine fish olive flounder (Paralichthys olivaceus) is a commercially popular aquaculture species, particularly in the Republic of Korea, Japan, China, and other East Asian countries. Olive flounder aquaculture ranked first in terms of production volume and economic value (43,813 metric tons and US $369 million in 2021) in the Republic of Korea [28, 29]. Owing to its excellent taste, high market demand, and rapid growth rate, the olive flounder is also considered an ideal candidate for US land-based aquaculture [30]. The nutrient requirements of this species have been well defined, and commercial feeds are locally available and exported to other countries. Being a carnivorous species, commercial feed formulations for this species typically include high lipid levels (8%–12%) and antioxidants, such as BHT [29, 31]. With the growing concern for safety and consumer-friendly seafood, this study was undertaken to assess muscle-specific BHT accumulation, toxicity, and its effects on the growth performance, body nutritional integrity, hematological characteristics, and nonspecific immunity in P. olivaceus.

2. Materials and Methods

2.1. Experimental Diets

The composition and proximate analysis of the experimental diets are presented in Table 1. Six isonitrogenous and isocaloric diets were supplemented with BHT (Sigma-Aldrich, MO, USA) in increments of 0, 10, 20, 40, 80, and 160 mg BHT/kg, which corresponded to the dietary levels of 0 (BHT₀), 11 (BHT₁₁), 19 (BHT₁₉), 35 (BHT₃₅), 85 (BHT₈₅), and 121 (BHT₁₂₁) BHT/kg. The experimental diets were prepared by mixing the dry ingredients thoroughly in an electric mixer, followed by the addition of oil and distilled water. The mixture was passed through a screw pelleting machine (SMC-32, SL Co., Incheon, Korea) to produce pellets, which were then dried for 48 h. After drying, the pellets were broken up, sieved to the required pellet size, packed, and stored at −20°C until feeding.

2.2. Fish and Feeding Trial

Juvenile P. olivaceus were obtained from a private hatchery (Geoje-si, Gyeongsangnam-do, Republic of Korea). Juveniles (initial g) were weighed and randomly stored in 300 L tanks with 35 fish per tank, with three replicate tanks per treatment. Fish were fed twice a day (09:00 and 18:00) for 120 days until apparent satiation. The feeding trial was conducted using flow-through seawater ( ppt) at a flow rate of 4 L/min. Water temperature (°C) and dissolved oxygen levels ( mg/L) were maintained throughout the feeding trials. A natural photoperiod was maintained during the feeding trials, at 14 h light : 10 h dark using fluorescent lights controlled by electric timers. The fish sampling and experimental protocols were approved by the Animal Care and Use Committee of the National Institute of Fisheries Science, Republic of Korea (2021–NIFS–IACUC–7).

2.3. Sample Collection and Analysis

At the end of the feeding trial, all the fish were counted and weighed to calculate weight gain (WG), feed conversion ratio (FCR), and survival rate. To evaluate the pattern of BHT accumulation in the muscle between the dietary BHT levels throughout the feeding trial, six fish (starved for 24 h before sampling) from each treatment (two fish from each of three replicate tanks per treatment) were collected at the starting point and at the end of the 60 days and 120 days of feeding trials. The collected fish were euthanized with tricaine methanesulfonate (MS-222, 200 mg/L, buffered to pH 7.4) and dissected to sample the dorsal muscle. Muscle samples were snap-frozen in liquid nitrogen and stored at −80°C until BHT analysis. At the end of the feeding trials, blood was collected from the caudal vein of six randomly selected fish per aquarium using a 5 mL heparinized syringe. The collected blood samples were centrifuged at for 15 min at 4°C, and plasma was collected for investigating blood chemistry and immune responses. Additionally, four fish per tank were euthanized and stored at −20°C for whole-body proximate composition analyses after the feeding trials.

BHT determination was performed on muscle samples according to the AOAC official method [32], which measures BHT after sample dissolution in hexane and extraction of antioxidants into acetonitrile. The concentrated acetonitrile solution was diluted with an equal volume of isopropanol. The diluted solution was injected into a high-performance liquid chromatography (HPLC) machine, with detection at 280 nm using a UV detector (Agilent 1260 System, Agilent Technologies, Waldbronn, Germany).

Superoxide dismutase (SOD), glutathione peroxidase (GPx), immunoglobulin M (IgM), and lysozyme (LZM) activity was determined using ELISA kits according to the manufacturer’s protocols (SOD, cat. No. MBS705758; GPx, cat. No. MBS705700; IgM, cat. No. MBS700823; LZM, cat. No. MBS705758, MyBioSource, USA). Plasma aspartate transaminase (AST), glucose, total protein, total cholesterol, and triglyceride levels were determined using an automated blood analyzer (Clinical Chemistry Analyzer; Thermo Fisher Scientific, Finland), following the manufacturer’s protocol.

The crude protein, crude lipid, ash, and moisture content of the experimental diets and whole body were analyzed according to standard methods [32]. Briefly, moisture content was determined by oven drying at 105°C, crude protein content was analyzed using the Kjeldahl method, crude lipid content was analyzed by Soxhlet extraction using a Soxhlet 1046 system (Tacator AB, Sweden), and ash content was determined by incineration (550°C) for 4 h.

2.4. Statistical Analysis

The homogeneity of variance was tested using Levene’s test. All data were subjected to one-way analysis of variance (ANOVA) using SAS version 9.3 (SAS Institute, Cary, NC, USA). When a significant effect was observed, post hoc Duncan’s test was performed to compare the treatment means.

3. Results

3.1. Growth Performance

Table 2 summarizes the growth performance (final body weight, weight gain %, FCR, and survival rate) of olive flounders fed different levels of BHT-supplemented diets for 120 days. Butylated hydroxytoluene had no significant effects on the growth and survival rate of P. olivaceus (). Experimental diets were well accepted and consumed by the experimental fish, as evidenced by the excellent FCR (1.01–1.04) and survival rate (97%–100%) recorded among different dietary treatments. Average weight gain ranged from 523% to 550% among different treatment groups, without any significant differences (), whereas BHT intake per fish significantly increased in a dose-dependent manner and was significantly higher in the group fed the BHT₁₂₁ diet, followed by the BHT₈₅, BHT₃₅, BHT₁₉, BHT₁₁, and BHT₀ diets ().

3.2. Muscle-Specific BHT Accumulation in P. olivaceus

Figures 1 and 2 show BHT accumulation in the muscle tissues of olive flounder fed various levels of BHT-supplemented diets. The muscle BHT concentrations increased with a corresponding increase in the BHT intake up to 60 days (). Thus, the highest BHT accumulation was recorded in the fish fed the BHT₁₂₁ diet followed by those fed the BHT₈₅, BHT₃₅, BHT₁₉, BHT₁₁, and BHT₀ diets.

In contrast, the effects of culture duration on muscle-specific BHT accumulation were clearly observed (Figure 2). At the end of the 60-day culture period, the BHT concentration among the fish fed BHT₁₂₁ diet was significantly higher than those of fish fed BHT₈₅ followed by BHT₃₅, BHT₁₉, BHT₁₁, and BHT₀ diets (), respectively. However, no significant differences were detected in the muscle tissue BHT content among the groups of fish fed the BHT₃₅, BHT₁₉, and BHT₁₁ diets (). Interestingly, after 60 days, the BHT concentrations among all treatment groups tend to gradually decline; however, at the end of 120 days, the muscle BHT content of the flounders fed the BHT₁₂₁ diet was significantly higher than those of fish fed other experimental diets ().

3.3. Nonspecific Immune Responses

Table 3 shows the nonspecific immune responses of the experimental fish fed diets supplemented with different levels of BHT for 120 days. The immune parameters SOD, GPx, IgM, and lysozyme activity responded differently to the dietary treatments. Although numerical differences were observed between the treatments, BHT had no significant effects on the overall nonspecific immune responses in P. olivaceus ().

3.4. Hematological Parameters

Table 4 shows the hematological parameters of the fish that were fed diets supplemented with various levels of BHT for 120 days. It appeared that BHT had no significant effects on the hematological parameters () except for decreased serum triglycerides in P. olivaceus. The triglyceride content of the fish fed the BHT₁₁, BHT₁₉, BHT₈₅, and BHT₁₂₁ diets was significantly lower than that of fish fed the BHT₀ diet (). However, the triglyceride content of the BHT₃₅ groups was not significantly different from that of the other experimental groups (). Although numerical differences were recorded in the AST, glucose, total protein, and cholesterol content among the different treatment groups, no clear trend could be observed ().

3.5. Whole-Body Proximate Composition

The effects of different levels of BHT-supplemented diets on the whole-body proximate composition of the olive founders are shown in Table 5. Butylated hydroxytoluene had no significant effects on the whole-body proximate composition, including moisture, crude protein, crude lipid, and crude ash among the treatment groups ().

4. Discussion

The growing safety concerns associated with seafood production and consumption require a clear understanding of both nutrients and contaminants throughout the production chain. In recent years, the production of consumer-friendly seafood using feeds that are low in contaminants and antioxidants has received considerable attention. The synthetic antioxidant BHT, through the carry-over process from fish feed, can have toxic and negative health impacts on both fish and consumers [33]. However, observations from the current 120-day-long study showed no beneficial or adverse effects of BHT inclusion on olive flounder fed up to a concentration of 121 mg/kg.

As evidenced by the excellent survival rate (97%–100%), growth performance, and FCR, the experimental diets were well accepted and consumed by the fish in all treatment groups (Table 4). Studies on the effects of dietary BHT in commercial aquaculture species are scarce but have grown in the last few years. In a two-decade-old study, Bautista-Teruel and Subosa [3] examined the effects of BHT inclusion on the diet of marine shrimp, Penaeus monodon, reared at various temperatures for 60 days. These authors observed that dietary BHT resulted in a substantial improvement in the growth of juvenile shrimp only after 45 days, although the number of treatments was limited in this study. In contrast, in a more recent study, Yu et al. [34] reported no significant improvement in the growth of largemouth bass (Micropterus salmoides) fed various levels of BHT-supplemented diets for 10 weeks. Similarly, in the present study, no evidence was found suggesting any positive/negative impact of BHT inclusion up to 121 mg/kg (BHT₁₂₁) on the growth performance of P. olivaceus reared for 120 days.

Interestingly, published reports also suggest weight loss in rats fed BHT-supplemented diets at 125–150 mg/kg body weight [24]. Similarly, growth reduction in rats fed BHT-supplemented diets at 1,500 mg/kg body weight has also been reported [24]. Notably, carnivorous fish, such as olive flounder and largemouth bass, have comparatively higher lipid requirements than rats and most mammals [35, 36] and may also have a higher tolerance to dietary antioxidants such as BHT. The results of the present study are in agreement with a previous study [34], suggesting no beneficial or adverse impacts of dietary BHT on the growth performance of P. olivaceus.

The residue levels of synthetic antioxidants in food products, including seafood, have become a matter of serious concern. Despite the urgency driven by the growing awareness and interest in healthy human food, only limited published data are available on the residue levels of synthetic antioxidants in commercial fish fillets [21]. A previous study [37] found BHT to be the most abundant antioxidant in Atlantic salmon fillets (420 mg/kg) followed by ethoxyquin dimer (EQDM) and BHA. Similarly, BHT was found to be the most prominent antioxidant in Atlantic salmon, Atlantic halibut, and rainbow trout fillets [21]. In the present study, an increase in whole-body BHT concentrations in fish was observed with the corresponding increase in dietary inclusion (Figure 1); however, whole-body BHT accumulation gradually declined among all the treatment groups after 60 days of culture (Figure 2). Notably, the measured BHT concentrations in olive flounder were lower than those reported for Atlantic salmon [37]. This may reflect differential BHT accumulation in the fish body due to differences in the fish size, species, and dietary inclusion level.

Interestingly, BHT accumulation was also observed in the BHT-free (BHT₀) diet treatment. Although 1,000–4,000 mg/kg of BHT is typically included in fishmeal production to prevent spontaneous combustion during overseas transport and storage [21, 38], the fishmeal used in this experiment was BHT-free (Table 1). Therefore, the accumulation of BHT in the tissues of the BHT₀ treatment group likely reflects accumulation during the 10-day acclimation period, when all the fish were fed the BHT₃₅ diet. Overall, BHT accumulated in the muscle tissues of P. olivaceus in a dose-dependent manner during the first 60 days of the culture period and afterwards gradually declined.

In contrast to BHT accumulation in muscle issues, there was no difference in whole-body moisture, crude protein, crude lipid, and ash contents among the different treatment groups (Table 5). Among the few reports on dietary BHT in aquaculture species, only one study has reported the effects of BHT on the proximate composition and muscle tissues of fish [23]. Importantly, further long-term studies are needed to better understand the effects of BHT dose and culture period on the pattern of BHT accumulation in fish tissues and the whole-body nutrient profile.

Nonspecific immunity is the major defense system in fish and shellfish and plays a vital role in acquiring immune responses and homeostasis through a system of receptor proteins. In aquaculture, optimized antioxidants and immunity are important for combating stress, maintaining health, and ensuring optimal survival and growth [39, 40]. Among them, SOD is one of the most important antioxidant enzymes, known for its efficiency in controlling reactive oxygen species in cells and catalyzing the dismutation of hydrogen peroxide and normal oxygen from superoxide radicals [41, 42]. Lysozyme is another cationic protein synthesized in the liver and extrahepatic sites in aquaculture species and is well known for its bacteriolysis, opsonization, and antimicrobial activity [43], whereas IgM is the only class of serum immunoglobulin reported in fish and is known to play a key role in a variety of immune processes, including the neutralization of pathogenic bacteria, viruses, and toxins [44, 45]. Substantial changes in these parameters could be a potential indicator of stress in fish caused by biotic or abiotic factors. In the present study, nonspecific immune parameters (Table 3) were recorded in the optimal range and were not significantly affected by the dietary BHT inclusion up to 121 mg/kg (BHT₁₂₁). Similarly, Yu et al. [34] reported no significant variation in the levels of SOD and other antioxidants in largemouth bass fed a BHT-supplemented diet of up to 1,500 mg/kg.

Hematological parameters, such as triglycerides, total protein, AST, cholesterol, and glucose, are known to be promising indicators of animal health [42, 46, 47]. In the present study, the AST, total protein, glucose, and cholesterol contents of P. olivaceus were not significantly affected by the dietary BHT treatments. In comparison, triglyceride content tended to decrease as the BHT concentration increased and was lowest among the BHT₁₂₁ treatment group. Decreasing plasma triglyceride levels with a corresponding increase in BHT levels could be a potential indicator of enhanced lipid metabolism [34]. Indeed, similar observations in the hematological parameters of largemouth bass have been reported [34]. It is worth mentioning that a previous study with rats reported a decrease in plasma triglyceride levels caused by dietary BHT inclusion [48]. Likewise, another study with BHA also reported a decrease in triglyceride levels with a corresponding increase in dietary BHA inclusion [49]. A possible reason for such observations with triglyceride levels has been attributed due to the antioxidant activity of BHT, which may alleviate the abnormal intracellular events involved in lipid metabolism [30, 32, 33]. Furthermore, considerable changes in the hematological parameters of aquatic species have been reported following exposure to different stress conditions caused by pollutants, diseases, and hypoxia [50]. Hence, any stressful condition caused by poor nutrition could have a visible impact on the hematological characteristics of fish [51]. However, in the present study, hematological parameters, including AST, total protein, glucose, and cholesterol content, were not considerably affected by BHT supplementation up to 121 mg/kg.

5. Conclusions

The inclusion of BHT in the diet of P. olivaceus up to 121 mg/kg was found to be safe and effective with no beneficial/adverse effects on the fish growth, nonspecific immunity, and whole-body nutrient profiles. However, observations for the hematological characteristics showed an adverse effect on the triglyceride levels with a corresponding increase in the dietary BHT levels. Nevertheless, the observation of BHT accumulation in the fish muscle tissues during the first 60 days of exposure and its subsequent gradual decline warrants further examination using long-term farm trials for P. olivaceus and other important aquaculture species.

Data Availability

The data used to support the findings of this study are included in the article.

Conflicts of Interest

The authors declare that there is no conflict of interest regarding the publication of this paper.

Acknowledgments

This work was supported by a grant (R2023036) from the National Institute of Fisheries Science, Republic of Korea.

References

C. H. S. Ruxton, S. C. Reed, M. J. A. Simpson, and K. J. Millington, “The health benefits of omega-3 polyunsaturated fatty acids: a review of the evidence,” Journal of Human Nutrition and Dietetics, vol. 17, no. 5, pp. 449–459, 2004.
View at: Publisher Site | Google Scholar
S. V. Hosseini, A. Abedian-Kenari, M. Rezaei, R. M. Nazari, X. Feás, and M. Rabbani, “Influence of the in vivo addition of alpha-tocopheryl acetate with three lipid sources on the lipid oxidation and fatty acid composition of Beluga sturgeon, Huso huso, during frozen storage,” Food Chemistry, vol. 118, no. 2, pp. 341–348, 2010.
View at: Publisher Site | Google Scholar
M. N. Bautista-Teruel and P. F. Subosa, “Butylated hydroxytoluene: its effect on the quality of shrimp diet stored at various temperatures and on growth and survival of Penaeus monodon juveniles,” Aquaculture, vol. 179, no. 1-4, pp. 403–414, 1999.
View at: Publisher Site | Google Scholar
F. Shahidi, P. K. J. P. D. Wanasundara, and C. Hong, “Antioxidant activity of phenolic compounds in meat model systems,” in Phenolic Compounds in Food and Their Effects on Health I, Analysis, Occurrence and Chemistry, C.-T. Ho, C. Y. Lee, and M. T. Huang, Eds., ACS Symposium Series 506, pp. 214–222, American Chemical Society, Washington, DC, 1992.
View at: Publisher Site | Google Scholar
M. Jahncke, “A review: processing parameters needed to control pathogens in cold smoked fish,” in International Smoked Seafood Conference Proceedings, pp. 15–21, Alaska, 2007.
View at: Publisher Site | Google Scholar
J. H. Hwang, S. W. Lee, S. J. Rha et al., “Dietary green tea extract improves growth performance, body composition, and stress recovery in the juvenile black rockfish, Sebastes schlegeli,” Aquaculture International, vol. 21, no. 3, pp. 525–538, 2013.
View at: Publisher Site | Google Scholar
C. C. Lee, L. Y. Jiang, Y. L. Kuo et al., “Characteristics of nonylphenol and bisphenol A accumulation by fish and implications for ecological and human health,” Science of the Total Environment, vol. 502, pp. 417–425, 2015.
View at: Publisher Site | Google Scholar
A. Álvarez, B. G. García, M. J. Jordán, C. Martínez-Conesa, and M. D. Hernández, “The effect of diets supplemented with thyme essential oils and rosemary extract on the deterioration of farmed gilthead seabream (Sparus aurata) during storage on ice,” Food Chemistry, vol. 132, no. 3, pp. 1395–1405, 2012.
View at: Publisher Site | Google Scholar
S. V. Hosseini, A. A. Kenari, J. M. Regenstein et al., “Effects of alternative dietary lipid sources on growth performance and fatty acid composition of beluga sturgeon, Huso huso, juveniles,” Journal of the World Aquaculture Society, vol. 41, no. 4, pp. 471–489, 2010.
View at: Publisher Site | Google Scholar
A. K. Lundebye, E. J. Lock, J. D. Rasinger et al., “Lower levels of persistent organic pollutants, metals and the marine omega 3-fatty acid DHA in farmed compared to wild Atlantic salmon (Salmo salar),” Environmental Research, vol. 155, pp. 49–59, 2017.
View at: Publisher Site | Google Scholar
J. Ortiz, M. A. Larraín, J. P. Vivanco, and S. P. Aubourg, “Rancidity development during the frozen storage of farmed coho salmon (Oncorhynchus kisutch): effect of antioxidant composition supplied in the diet,” Food Chemistry, vol. 115, no. 1, pp. 143–148, 2009.
View at: Publisher Site | Google Scholar
L. S. Sant'Ana and J. Mancini-Filho, “Influence of the addition of antioxidants in vivo on the fatty acid composition of fish fillets,” Food Chemistry, vol. 68, no. 2, pp. 175–178, 2000.
View at: Publisher Site | Google Scholar
S. Chaiyapechara, M. T. Casten, R. W. Hardy, and F. M. Dong, “Fish performance, fillet characteristics, and health assessment index of rainbow trout (Oncorhynchus mykiss) fed diets containing adequate and high concentrations of lipid and vitamin E,” Aquaculture, vol. 219, no. 1-4, pp. 715–738, 2003.
View at: Publisher Site | Google Scholar
S. K. Sau, B. N. Paul, K. N. Mohanta, and S. N. Mohanty, “Dietary vitamin E requirement, fish performance and carcass composition of rohu (Labeo rohita) fry,” Aquaculture, vol. 240, no. 1-4, pp. 359–368, 2004.
View at: Publisher Site | Google Scholar
M. T. Younathan, J. K. Oon, and R. B. M. Yusof, “Control of heat induced oxidative rancidity in refrigerated shark and mackerel,” Journal of Food Science, vol. 48, no. 1, pp. 176–178, 1983.
View at: Publisher Site | Google Scholar
D. M. Gatlin III, S. C. Bai, and M. C. Erickson, “Effects of dietary vitamin E and synthetic antioxidants on composition and storage quality of channel catfish, Ictalurus punctatus,” Aquaculture, vol. 106, no. 3-4, pp. 323–332, 1992.
View at: Publisher Site | Google Scholar
W. Torres-Arreola, H. Soto-Valdez, E. Peralta, J. L. Cárdenas-López, and J. M. Ezquerra-Brauer, “Effect of a low-density polyethylene film containing butylated hydroxytoluene on lipid oxidation and protein quality of sierra fish (Scomberomorus sierra) muscle during frozen storage,” Journal of Agricultural and Food Chemistry, vol. 55, no. 15, pp. 6140–6146, 2007.
View at: Publisher Site | Google Scholar
G. M. Williams, M. J. Iatropoulos, and J. Whysner, “Safety assessment of butylated hydroxyanisole and butylated hydroxytoluene as antioxidant food additives,” Food and Chemical Toxicology, vol. 37, no. 9-10, pp. 1027–1038, 1999.
View at: Publisher Site | Google Scholar
W. T. Fairgrieve and M. B. Rust, “Interactions of Atlantic salmon in the Pacific northwest: V. Human health and safety,” Fisheries Research, vol. 62, no. 3, pp. 329–338, 2003.
View at: Publisher Site | Google Scholar
S. S. Hung, T. W. Moon, J. W. Hilton, and S. J. Slinger, “Uptake, transport and distribution of dl-α-tocopheryl acetate compared to d-α-tocopherol in rainbow trout (Salmo gairdneri),” The Journal of Nutrition, vol. 112, no. 8, pp. 1590–1599, 1982.
View at: Publisher Site | Google Scholar
A. K. Lundebye, H. Hove, A. Måge, V. J. B. Bohne, and K. Hamre, “Levels of synthetic antioxidants (ethoxyquin, butylated hydroxytoluene and butylated hydroxyanisole) in fish feed and commercially farmed fish,” Food Additives & Contaminants: Part A, vol. 27, no. 12, pp. 1652–1657, 2010.
View at: Publisher Site | Google Scholar
International Life Sciences Institute, Butylated hydroxytoluene (BHT). A Monograph, ILSI, Washington, DC, 1984.
S. V. Hosseini, A. Abedian Kenari, M. Rezaei, R. M. Nazari, M. Mohseni, and X. F. Sanchez, “Influence of the dietary addition of butylated-hydroxytoluene and lipid level on the flesh lipid quality of beluga sturgeon (Huso huso) during frozen storage,” Journal of Aquatic Food Product Technology, vol. 23, no. 4, pp. 394–408, 2014.
View at: Publisher Site | Google Scholar
L. A. Faine, H. G. Rodrigues, C. M. Galhardi et al., “Butyl hydroxytoluene (BHT)-induced oxidative stress: effects on serum lipids and cardiac energy metabolism in rats,” Experimental and Toxicologic Pathology, vol. 57, no. 3, pp. 221–226, 2006.
View at: Publisher Site | Google Scholar
Y. Nakagawa, K. Tayama, T. Nakao, and K. Hiraga, “On the mechanism of butylated hydroxytoluene-induced hepatic toxicity in rats,” Biochemical Pharmacology, vol. 33, no. 16, pp. 2669–2674, 1984.
View at: Publisher Site | Google Scholar
Y. Nakagawa and K. Tayama, “Nephrotoxicity of butylated hydroxytoluene in phenobarbital-pretreated male rats,” Archives of Toxicology, vol. 61, no. 5, pp. 359–365, 1988.
View at: Publisher Site | Google Scholar
X. Liang, Y. Zhao, W. Liu, Z. Li, C. L. Souders II, and C. J. Martyniuk, “Butylated hydroxytoluene induces hyperactivity and alters dopamine-related gene expression in larval zebrafish (Danio rerio),” Environmental Pollution, vol. 257, article 113624, 2020.
View at: Publisher Site | Google Scholar
KOSIS, Fisheries Production in Korea, Korean Statistical Information Service, Daejeon, Korea, 2021.
H. S. Jeong, J. Kim, O. S. Olowe, and S. H. Cho, “Dietary optimum inclusion level of jack mackerel meal for olive flounder (Paralichthys olivaceus, Temminck & Schlegel, 1846),” Aquaculture, vol. 559, p. 738432, 2022.
View at: Publisher Site | Google Scholar
J. D. Stieglitz, R. H. Hoenig, J. K. Baggett, C. E. Tudela, S. K. Mathur, and D. D. Benetti, “Advancing production of marine fish in the United States: olive flounder, Paralichthys olivaceus, aquaculture,” Journal of the World Aquaculture Society, vol. 52, no. 3, pp. 566–581, 2021.
View at: Publisher Site | Google Scholar
M. G. Kim, B. E. Gunathilaka, J. Shin et al., “Evaluation of Bacillus sp. SW1-1 as a dietary additive in diets for olive flounder Paralichthys olivaceus,” Animal Feed Science and Technology, vol. 290, article 115367, 2022.
View at: Publisher Site | Google Scholar
AOAC, Official Methods of Analysis International, AOAC International, Gaithersburg, MD, USA, 2000.
E. Holaas, V. B. Bohne, K. Hamre, and A. Arukwe, “Hepatic retention and toxicological responses during feeding and depuration periods in Atlantic salmon (Salmo salar) fed graded levels of the synthetic antioxidant, butylated hydroxytoluene,” Journal of Agricultural and Food Chemistry, vol. 56, no. 23, pp. 11540–11549, 2008.
View at: Publisher Site | Google Scholar
L. L. Yu, H. H. Yu, X. F. Liang et al., “Dietary butylated hydroxytoluene improves lipid metabolism, antioxidant and anti-apoptotic response of largemouth bass (Micropterus salmoides),” Fish & Shellfish Immunology, vol. 72, pp. 220–229, 2018.
View at: Publisher Site | Google Scholar
K. D. Kim, Y. J. Kang, H. M. Lee et al., “Effects of dietary protein and lipid levels on growth and body composition of subadult olive flounder, Paralichthys olivaceus, at a suboptimal water temperature,” Journal of the World Aquaculture Society, vol. 41, pp. 263–269, 2010.
View at: Publisher Site | Google Scholar
B. Yun, M. Xue, J. Wang et al., “Effects of lipid sources and lipid peroxidation on feed intake, growth, and tissue fatty acid compositions of largemouth bass (Micropterus salmoides),” Aquaculture International, vol. 21, no. 1, pp. 97–110, 2013.
View at: Publisher Site | Google Scholar
H. Hove, K. Julshamn, B. Nielsen, and B. T. Lunestad, “Restmengder, forbudte og forurensende stoffer i fisk (Fremmedstoffprogrammet for fisk (96/23)). A° rsrapport 2007,” 2008, http://www.mattilsynet.no/.
View at: Google Scholar
International Maritime Organisation (IMO), Review of the BC code, including evaluation of properties of solid bulk cargoes, Report of the Working Group at DSC 7. I:\DSC\8\4.doc, IMO, London (UK), 2003.
C. H. Liu and J. C. Chen, “Effect of ammonia on the immune response of white shrimp Litopenaeus vannamei and its susceptibility to Vibrio alginolyticus,” Fish & Shellfish Immunology, vol. 16, no. 3, pp. 321–334, 2004.
View at: Publisher Site | Google Scholar
M. Castex, P. Lemaire, N. Wabete, and L. Chim, “Effect of probiotic Pediococcus acidilactici on antioxidant defences and oxidative stress of Litopenaeus stylirostris under Vibrio nigripulchritudo challenge,” Fish & Shellfish Immunology, vol. 28, no. 4, pp. 622–631, 2010.
View at: Publisher Site | Google Scholar
M. Hortsch, “The L1 family of neural cell adhesion molecules: old proteins performing new tricks,” Neuron, vol. 17, no. 4, pp. 587–593, 1996.
View at: Publisher Site | Google Scholar
X. P. Shao, W. B. Liu, W. N. Xu, W. Xia, and Y. Y. Jiang, “Effects of dietary copper sources and levels on performance, copper status, plasma antioxidant activities and relative copper bioavailability in Carassius auratus gibelio,” Aquaculture, vol. 308, no. 1-2, pp. 60–65, 2010.
View at: Publisher Site | Google Scholar
K. W. Samarakoon, S. H. Cha, J. H. Lee, and Y. J. Jeon, “The growth, innate immunity and protection against H₂O₂-induced oxidative damage of a chitosan-coated diet in the olive flounder Paralichthys olivaceus,” Fisheries and Aquatic Sciences, vol. 16, no. 3, pp. 149–158, 2013.
View at: Publisher Site | Google Scholar
A. Cuesta, J. Meseguer, and M. A. Esteban, “Total serum immunoglobulin M levels are affected by immunomodulators in seabream (Sparus aurata L.),” Veterinary Immunology and Immunopathology, vol. 101, no. 3-4, pp. 203–210, 2004.
View at: Publisher Site | Google Scholar
B. Magnadottir, “Immunological control of fish diseases,” Marine Biotechnology, vol. 12, no. 4, pp. 361–379, 2010.
View at: Publisher Site | Google Scholar
S. H. Lee, Y. K. Lee, K. Katya, J. K. Park, and S. C. Bai, “Natural dietary additive yellow loess as potential antibiotic replacer in Japanese eel, Anguilla japonica: effects on growth, immune responses, serological characteristics and disease resistance against Edwardsiella tarda,” Aquaculture Nutrition, vol. 24, no. 3, pp. 1034–1040, 2018.
View at: Publisher Site | Google Scholar
K. Katya, G. Park, A. S. Bharadwaj, C. L. Browdy, M. Vazquez-Anon, and S. C. Bai, “Organic acids blend as dietary antibiotic replacer in marine fish olive flounder, Paralichthys olivaceus,” Aquaculture Research, vol. 49, no. 8, pp. 2861–2868, 2018.
View at: Publisher Site | Google Scholar
A. F. Elgazar, “Effects of butylated hydroxytoluene and butylated hydroxyanisole against hepatotoxicity induced by carbon tetrachloride in rats,” World Applied Sciences Journal, vol. 22, pp. 63–69, 2013.
View at: Google Scholar
L. L. Yu, M. Xue, J. Wang, F. Han, and Y. H. Zheng, “Tolerance evaluation of butyl- hydroxyanisole in diets of largemouth bass (Micropterus salmoides),” Chinese Journal of Animal Nutrition, vol. 28, pp. 747–758, 2016.
View at: Google Scholar
G. G. Duthie and L. Tort, “Effects of dorsal aortic cannulation on the respiration and haematology of mediterranean living Scyliorhinus canicula L,” Comparative Biochemistry and Physiology-A Physiology, vol. 81, no. 4, pp. 879–883, 1985.
View at: Publisher Site | Google Scholar
K. Katya, S. Lee, H. Yun et al., “Efficacy of inorganic and chelated trace minerals (Cu, Zn and Mn) premix sources in Pacific white shrimp, Litopenaeus vannamei (Boone) fed plant protein based diets,” Aquaculture, vol. 459, pp. 117–123, 2016.
View at: Publisher Site | Google Scholar

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