The Effects of Dietary Thyme Oil (Thymus vulgaris) Essential Oils for Common Carp (Cyprinus carpio): Growth Performance, Digestive Enzyme Activity, Antioxidant Defense, Tissue and Mucus Immune Parameters, and Resistance against Aeromonas hydrophila

Ghafarifarsani, Hamed; Hoseinifar, Seyed Hossein; Sheikhlar, Atefeh; Raissy, Mehdi; Chaharmahali, Fatemeh Heidarinezhad; Maneepitaksanti, Worawit; Faheem, Mehwish; Van Doan, Hien

doi:https://doi.org/10.1155/2022/7942506

Aquaculture Nutrition

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

Research Article | Open Access

Volume 2022 | Article ID 7942506 | https://doi.org/10.1155/2022/7942506

The Effects of Dietary Thyme Oil (Thymus vulgaris) Essential Oils for Common Carp (Cyprinus carpio): Growth Performance, Digestive Enzyme Activity, Antioxidant Defense, Tissue and Mucus Immune Parameters, and Resistance against Aeromonas hydrophila

Hamed Ghafarifarsani,¹Seyed Hossein Hoseinifar,²Atefeh Sheikhlar,³Mehdi Raissy,⁴Fatemeh Heidarinezhad Chaharmahali,⁵Worawit Maneepitaksanti,^6,7Mehwish Faheem,⁸and Hien Van Doan^6,7

Academic Editor: Shouqi Xie

Received20 Apr 2022

Revised02 Aug 2022

Accepted09 Aug 2022

Published14 Sept 2022

Abstract

This study evaluated the effects of dietary supplementation of thyme (Thymus vulgaris) essential oil (TVO) on growth performance, digestive enzymes, biochemical parameters, hematological indices, liver enzymes, and pathogen resistance in common carp (Cyprinus carpio). Triplicate groups of fish (15.36 ± 0.10 g) were fed daily with diets supplemented with TVO at 0, 0.5, 1, and 2 percent for 60 days then challenged with Aeromonas hydrophila. The results determined that supplementation of thyme resulted in significantly higher final body weights (FBW) and lower feed conversion ratios (FCR). Furthermore, no mortality was observed in the thyme-supplemented treatments. Regression analysis showed that fish growth parameters were polynomially related to dietary TVO levels. The optimum dietary TVO level, based upon the varied growth parameters, was 1.344 to 1.436%. Digestive enzymes activity, including amylase and protease, significantly increased in fish fed the supplemented diets. The thyme-supplemented diets also significantly increased the biochemical parameters, including total protein, albumin, and acid phosphatase (ACP), compared to the control group. We also observed significant increases in hematological indices, including red blood cells (RBC), white blood cells (WBC), hematocrit (Hct), and hemoglobin (Hb) in common carp fed diets containing thyme oil (). Liver enzymes activity including alanine aminotransferase (ALT), alkaline phosphatase (ALP), and aspartate aminotransferase (AST) was also reduced (). Immune parameters, including total protein and total immunoglobulin (total Ig) levels, alternative complement pathway hemolytic (ACH₅₀), lysozyme, protease, and ALP in the skin mucus, and lysozyme, total Ig, and ACH₅₀ in the intestine were higher () in TVO-supplemented fish. Catalase (CAT), superoxide dismutase (SOD), glutathione reductase (GR), and glutathione peroxidase (GPx) in the liver were also elevated () in TVO administered groups. Lastly, thyme-supplementation resulted in higher survival rates after the A. hydrophila challenge compared to the control (). In conclusion, dietary inclusion of thyme oil (1 and 2%) effectively improved fish growth, immune systems, and resistance to A. hydrophila.

1. Introduction

The annual production of common carp has been estimated at 4.2 million tons, accounting for 7.7% of the entire aquaculture industry [1]. Intensive carp production is associated with various threats and infectious diseases, which endanger the development of sustainable carp farming [2]. Regrettably, using antibiotics and chemical disinfectants is generally the first approach by fish farmers to control infectious agents. Recent statistics have indicated that global antibiotic consumption in aquaculture is estimated at 10,259 tons in 2017 and predicted to rise to 13,600 tons by 2030 [3].

Numerous side effects from antibiotics and chemicals have raised public health concerns due to residues in the flesh, which create environmental hazards [4, 5]. One alternative and preventive approach to these consequences is the utilization of natural compounds to enhance the immune system through non-specific immune responses [6, 7]. Such natural compounds are categorized into several classes: complex carbohydrates; animal extracts; nutritional factors; lectins; cytokines; and plant extracts [8–11].

Plants and their derivates have been comprehensively proven to improve growth performance and elevate immune responses, thereby generating antimicrobial and anti-stress characteristics [12–16]. Over the past few decades, herbal agents have been extensively investigated and have been reported to have worthwhile potential concerning the therapeutic control over fish pathogens [9, 17–24].

Thyme (Thymus vulgaris), an aromatic herb belonging to the family Lamiaceae, contains thymol, carvacrol, cymene, eugenol, and 4-allylphenol and has been proven to enhance growth promotion, antimicrobial, immunostimulation, and antioxidant characteristics [25–31]. As reported, dietary supplementation of this plant influenced the growth and immune parameters in gibel carp (Carassius auratus gibelio), common carp (Cyprinus carpio), and rainbow trout (Oncorhynchus mykiss) [32–34].

According to recent literature, the effects of thyme oil on common carp’s immunity and bacterial resistance against A. hydrophila are not comprehensively studied. Therefore, this study was designed to investigate the effects of thyme oil on growth, digestive enzymes, biochemical parameters, hematological indices, liver enzymes, mucus and intestinal immunity, and resistance against A. hydrophila in common carp.

2. Materials and Methods

2.1. Diet Preparation and Feeding Trial

The chemical composition of the commercial thyme (Thymus vulgaris) essential oil (Maleki Commercial Co., Fars, Iran) is presented in Table 1, based on their report. The experimental diets were prepared based on a commercial diet containing 37% crude protein, 6% crude lipid, 6% crude fiber, 8% ash, and 1.25% phosphorus, with 7% moisture (Faradaneh, Shahrekord, Iran). The essential oils (0.5, 1, and 2%) were sprayed on the appropriate weights of the basal diet pellets using a fine mist spray [35, 36]. No essential oil was added to the control diet. The pellets (3.0 ± 0.3 mm) were then coated with 1% bovine gelatin solution (Ramsden et al., 2009). Lastly, they were dried at room temperature in darkness, kept in waterproof black zipper storage bags, and stored at 4°C. Diets were fed to fish twice a day for 60 days, with a 3% body weight ratio per day.

2.2. Fish and the Rearing System

Three hundred healthy common carp fingerlings were obtained from a local farm in Karaj, Iran, and kept for two weeks to adapt to our experimental conditions. During the acclimatization period, fish were fed the control diet’s maintenance ratio (0.5% of the biomass per day). Twenty-five fish with an average body weight of 15.36 ± 0.10 g were randomly allocated to each aquarium (150 liters). Treatments in three replications continued twice a day for 60 days, with a 3% body weight ratio per day [16]. The mean values for water temperature, dissolved oxygen, pH, and hardness were 23.4 ± 1.5°C, 6.4-6.7 mg L^-1, 7.1-7.3, and 188.56 ± 12.35, respectively. The photoperiod was adjusted to 12L:12D using artificial light. Aeration was performed using an air stone, and 50% of each aquarium’s water was replaced daily with fresh de-chlorinated water from reservoir tanks to maintain water quality.

2.3. Sampling Procedure

At the end of the 60-day feeding trial, all fish were sampled to evaluate the parameters. Three fish from each tank were then randomly selected and anesthetized using 100 mg L^-1 eugenol [38] to study the blood parameters. Blood samples were taken from the caudal vein using a 2 ml syringe then centrifuged (Heraeus Labofuge 400) at 1600 g for ten minutes to obtain serum. The serum samples were stored at -20°C for future evaluation.

Cutaneous mucus was collected through the indirect method, according to [39]. Four fish from each tank were anesthetized and individually transferred to plastic bags. They were then mildly rubbed in the bag for approximately one minute then moved back to the tanks. The mucus samples were immediately centrifuged at 1600 g for ten minutes at 4°C in 15 ml sterilized tubes and then stored at -80°C for further evaluation.

For intestine and liver sampling, three fish per tank were euthanized using 100 mg L^-1 eugenol and head concussion [40, 41]. Samples were then taken out and washed with distilled water. Cold saline solution (0.9%) [10 volumes (w/v)] was used to homogenize the samples on ice using a disperser (IKA T25 digital, Ultra Turrax). Homogenates were centrifuged at 6000 g for 20 minutes at 4°C. The resulting supernatants were stored at -80°C for future analysis.

2.4. Growth Parameters

A digital scale (Sartorius Digital Gram Scale TE1502S) with 0.1 g precision was used to measure fish weight. Growth parameters, weight gain, specific growth rate, feed conversion ratio, and survival rate were then calculated through the following equations; and mortalities (if any) were recorded throughout the trial to compare the treatment survival rates.

2.5. Digestive Enzymes

Digestive tract samples were homogenized in 25 mM Tris-HCl buffer at pH 7.2 and centrifuged at 25,000 g for 20 minutes. The resulting supernatants were then collected, and lipase, protease, and amylase activities were determined [16].

2.6. Liver-Specific Enzymes

Liver-specific enzymes activity, consisting of alkaline phosphatase (ALP), alanine aminotransferase (ALT), and aspartate aminotransferase (AST), was assessed with a commercial kit (Pars Azmun, Co., Tehran, Iran), based on the method designed by [42].

2.7. Hematological Parameters

The measurements of hematological indices were carried out according to the method described [43]. Red and white blood cell counts were performed using a hemocytometer slide. Hematocrit (Hct) was measured based on the microhematocrit technique and expressed as the percentage of packed cell volume. Hemoglobin (Hb) was quantified according to the cyanomethemoglobin method via a commercial kit. The following equations were used to calculate mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), and mean corpuscular hemoglobin concentration (MCHC):

2.8. Serum Biochemical Parameters

Total protein and albumin levels were measured by a commercial spectrophotometry kit (Pars Azmun Co, Tehran, Iran) based on the colorimetric method [44]. We determined acid phosphatase (ACP) activity according to the protocol of [45], expressed as nanomoles (nM) of p-nitrophenol released/min/mg protein at 25°C with an acetate buffer (0.2 M, pH 5).

2.9. Immunological Parameters

Immunological parameters were analyzed in intestine and mucus samples through conventional techniques. According to a slightly modified method of [46]), lysozyme activity was determined. In brief, 0.2 mg/ml of the bacterium (Micrococcus luteus) suspension was prepared with the sodium phosphate buffer (0.05 M, pH 6.2). Sixty μL of the sample was mixed with the bacterium suspension (2 ml) and incubated for three minutes. The absorbance was then read, in which a single unit of lysozyme was considered a decrease (0.001 per min) in absorbance. Alternative complement pathway hemolytic activity (ACH₅₀) was measured in the intestine and mucus samples through the method developed by Ortuno et al. (2000), which is based on sheep red blood cells (SRBC) hemolysis. For the measurement of total immunoglobulin (total Ig), the samples were sedimented with 12.5% polyethene glycol solution (Sigma). Total Ig was then determined after calculating protein concentrations before and after sedimentation [48].

Protease activity in the mucus was measured via the azocasein hydrolysis approach [39], and mucus alkaline phosphatase (ALP) activity and total protein (TP) levels were determined through the use of a commercial kit (Pars Azmun Co., Tehran, Iran).

2.10. Liver Antioxidant Parameters

The function of glutathione reductase (GR), superoxide dismutase (SOD), and catalase (CAT) activity, as well as the function of glutathione peroxidase (GPx) (where glutathione is converted to glutathione disulfide), was measured through the use of commercial equipment (Zellbio®, Berlin, Germany). Malondialdehyde (MDA) concentrations were also measured using thiobarbituric acid, based on the calorimetric method defined by Buege and Aust [49].

2.11. Bacterial Infection

Aeromonas hydrophila (AH04) was obtained from the Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran, Iran. The bacteria were cultured on a tryptone soya agar (TSA) medium with a 0.85% saline solution. After the 60-day feeding trial, fifteen fish from each replicate were injected intraperitoneally with the bacterial suspension (0.1 ml, 10⁸ CFU per fish). The mortality rates were recorded for 14 days [16]. The relative percentage survival (RPS) and survival rate (%) of infected fish were calculated based on the following formulas [17]:

2.12. Statistical Analysis

Growth responses to dietary TVO were assessed through polynomial regression. The research herein was conducted in a completely randomized approach. Normality tests were conducted (Kolmogorov-Smirnov), and the analysis of variance (one-way ANOVA) was applied. The Kaplan-Meier method was applied for mortality rate data. Duncan’s post hoc test with a 95% level of confidence was performed, and SPSS 20 software was employed for statistical analysis. Data were represented as the mean of three measurements ± standard error (SE).

3. Results

3.1. Growth Performance

The inclusion of thyme oil influenced final body weight (FBW), feed conversion ratio (FCR), and survival rates (SR) (Table 2). The final weights of fish supplemented with the diet containing 1% TVO were significantly higher than that of the control group (). FCR was also significantly lower in the fish fed the thyme-supplemented diets (). The survival rates (SR) in all groups provided the TVO diets were 100% versus the control group at 93%. Fish responded exponentially to graded levels of dietary TVO levels (Figure 1). Accordingly, the lowest FCR and highest SGR and WG were observed at 1.436, 1.366, and 1.344% dietary TVO levels, respectively.

3.2. Digestive Enzymes

Table 3 presents the levels of digestive enzymes, including amylase, lipase, and protease in the experimental fish. Resultingly, amylase and protease were significantly higher in the fish fed the supplemented diets (), whereas lipase levels presented no significant differences among each treatment ().

3.3. Biochemical and Hematological Indices

Tables 4 and 5 display the biochemical and hematological indices. Total protein, albumin, and ACP levels were significantly enhanced compared to those of the control group (). Differences in globulin, MCHC, MCH, and MCV values among treatments were not statistically significant. However, significant increases were found within the hematological indices, including RBC, WBC, Hct, and Hb in common carp fed the TVO diets ().

3.4. Liver-Specific Enzymes

Liver enzyme levels are presented in Table 6. ALT decreased in the fish that received 1 and 2% TVO, though not significantly. AST levels were significantly reduced in the fish supplemented with thyme oil in comparison to that of the control ().

3.5. Skin Mucus and Intestine Immune Parameters

Skin mucus and intestinal immune parameters are outlined in Figures 2 and 3, respectively. Total Ig and total protein level, ACH₅₀, protease, ALP, and lysozyme activity in common carp skin mucus were significantly higher in treatments supplemented with thyme oil than in those of the control group (). Lysozyme activity and total Ig level were significantly elevated in the fish supplemented with TVO (). Increases in ACH₅₀ activity were not statistically significant compared to the control.

3.6. Liver Antioxidant Parameters

The level of antioxidant enzymes, including CAT, SOD, MDA, GR, and GPx, are shown in Figure 4. While CAT, SOD, GR, and GPx increased in fish that received the TVO-supplemented diets, MDA content significantly decreased compared to control ().

3.7. Challenging Test

According to Table 7 and Figure 5, mortality in the control group started earlier (the five^th day) than the other treatments. In contrast, mortality in the specimens fed with T2 diet occurred later (the eight day) than others. At the end of the experimental infection, the CMR of fish fed with diets containing T2 (20%) decreased to about 3.30 folded compared to the control group (% 66.33) (). Furthermore, the highest SR (%) and RSP (%) were obtained in fish fed with diet supplemented with T2 (Table 7). However, SR among groups fed thyme oil were statistically similar.

4. Discussion

Thyme and its derivatives have frequently been used as supplements in fish diets primarily to enhance growth and immunity [26, 50–58]. In the present study, the dietary supplementation of TVO improved fish survival rates, FCR, and final body weight (FBW), in which the FCR values were lower, and the FBWs higher in fish fed the TVO-supplemented diets (1%).

In agreement with our results, several studies have reported the growth-enhancing effects of TVO supplementation. In rainbow trout, fish fed a diet containing 0.5 mg/kg thyme essential oil exhibited higher WG (30.9%) and SGR (18.36%) compared to the control [34]. Similar results were also observed in the study by Sönmez et al. [59], where higher WG was obtained in rainbow trout supplemented with thyme oil. The beneficial effects of thyme and its derivatives have also been reported for Nile tilapia (Oreochromis niloticus) [31], Oncorhynchus mykiss [59], Dicentrarchus labrax (Volpatti et al., 2013), and Cyprinus carpio AlSafah and Al-Faragi [32]. In our study, improved growth in the TVO-supplemented fish can be attributed to the enhancing effects of TVO on the digestive abilities of the fish. We observed a significant increase in amylase and protease enzyme activities in TVO-supplemented fish compared to the control. Based on recent literature review, very little data is available on the effects of thyme and its derivatives on fish digestive enzymes. In the study of AbdEl-Naby et al. [61], a combination of chitosan nanoparticles and thymol significantly enhanced lipase and protease activities, and subsequent feed utilization. The inclusion of 4% thyme in the common carp diet modified digestive enzymes’ activity in fish exposed to aflatoxin-B₁ [62]. Khalil et al. [54] observed significant elevations in amylase activity of Nile tilapia, having consumed supplemental thyme (Thymus vulgaris) powder. Plant extracts, essential oils, and the bio-compounds have been extensively reported as growth enhancers in fish [63–69]

In the present study, the biochemical components of blood, total protein, albumin, and ACP, which are indicators of the health status of fish, increased in fish fed the diets containing TVO. Serum total protein is an important indicator of fish nutrition and health status [70–72]. Albumin is synthesized in the liver and acts as an antioxidant against oxidative stress induced by free radicals [73], and acts as a carrier in transferring hormones, vitamins, and minerals in the blood [74–76]. Another serum protein, globulin, is considered an essential component of the innate immune system of fish [77–79].

Similar to the biochemical components of blood, hematology indices are also evaluated to determine the health status of fish [80, 81]. In this study, RBC, WBC, Hct, and Hb values increased in TVO-supplemented fish compared to the control group. Hematological alterations have also been reported in fish supplemented with thyme and thyme derivatives. In the study of Valladão et al. [82], the numbers of lymphocytes and leukocytes increased in the blood of Nile tilapia fed thyme essential oil supplements, which may be attributed to the immunostimulatory effects of the essential oil on the cellular components of the non-specific immune system. Similarly, Zadmajid and Mohammadi [33], confirmed the immunostimulatory effects of thyme essential oil in gibel carp (Carassius auratus gibelio), where the dietary essential oil enhanced RBC and WBC, Hct, and Hb. Bioactive phytochemicals such as polyphenols, with interesting properties, like anti-inflammation [83], may also play immunostimulatory roles in the body.

Based on recent literature, elevated levels of hepatic metabolic enzymes (HMEs) can indicate hepatic damage [84]. In the present study, TVO supplementation had seemingly no deteriorating effect on hepatocytes, demonstrated by the HME blood levels, in which the TVO-supplemented fish showed no differences from that of the control. In agreement with our results, decreased ALT and AST levels in gibel carp (Carassius auratus gibelio) were attributed to the protective effects of thyme essential oil on hepatocytes [33]. Zargar et al. [34] observed that the addition of thymol oil to the diets of rainbow significantly reduced serum ALP and AST levels. Similarly, the addition of 10 g/kg thyme extract to the diets of rainbow trout significantly decreased AST and ALT activity levels [52]. The supplementation of Channa argus with 300 and 450 mg thymol/kg significantly decreased the serum activity of ALT and AST [85]. In African catfish (Clarias garipenus), dietary T. vulgaris essential oil reduced ALT, AST, and ALP levels in thiamethoxam intoxicated fish [86]. And, in Nile tilapia, ALT and AST activities were significantly reduced by adding thyme powder (5 g kg^-1 diet) to their diets [87]. Some compounds, such as flavonoids and phenols, are responsible for the protective effects of essential oils on hepatocytes due to their stabilizing effects on the fish cell membrane [33]. Additionally, thyme essential oil may exert antioxidative effects by enhancing the bioavailability of the antioxidants in vitamins C and E [33].

In the present study, TVO supplementation enhanced the immune responses and antioxidant enzyme activities in fish skin and intestines, thereby demonstrating the role of TVO as an immunostimulant. The immunostimulatory effects of thyme have also been reported in previous studies. Zargar et al. [34] reported a significant elevation in complement and lysozyme gene expressions following the administration of 1-2 ml/kg of thyme essential oil in rainbow trout. Mirghaed et al. [55] observed significant increases in the humoral and skin mucus immune components and immune-related gene expressions in rainbow trout supplemented with 2-3 g/kg thyme (Zataria multiflora) extract. Similar results were reported by Hoseini and Yousefi [52] in which thyme (Thymus vulgaris) extract significantly increased serum total protein, total Ig, lysozyme, and ACH₅₀ activity. In the study of Emeish and El-Deen [50], GPx and CAT significantly increased in fish received thyme. Serum and hepatic SOD and CAT activities were also elevated in rainbow trout in response to diets containing 2-3 g/kg thyme [55]. The immune stimulant property of TVO could be attributed to the presence of the bioactive ingredients, which are proved to boost immune response in the body by reduction of inflammation as well as preventing oxidation process [88].

In the present study, TVO supplementation significantly increased fish survival rate after the A. hydrophila challenge. The most significant influence of thyme oil on post-challenge survival rates was evidenced in the 1% TVO-supplemented diet, which may be attributed to the enhancing effects of the essential oil on the fish immune system. Several compounds with antibacterial properties in thyme’s chemical composition, such as 1, 8-cineole, borneol, alpha-pinene, beta-pinene, and terpinen-4-ol, may also be responsible for added resistance to bacterial infections [89, 90]. Therefore, the main reason for the antibacterial activity of TVO can be related to the presence of phenolic compounds (7.3 mg/g GAE) as the main bioactive ingredient in this oil. This compound possesses high antibacterial potentials due to the ability to (1) inhibit bacterial virulence factors such as enzymes and toxins, (2) interact with cytoplasmic membrane, (3) suppress biofilm formation, and (4) exert a synergistic effect with antibiotics [91, 92]. The review study of Alagawany et al. [18] concluded that the protective effects of thymol (as a main active compound in the composition of thyme) against oxidative stress and infections might be due to its antimicrobial, antiviral, antioxidant, immunomodulatory, and anti-inflammatory properties. The antibacterial effects of thyme and other plant-based supplements in controlling fish infections have been widely investigated [93, 94]. The supplementation of rainbow trout diets with thyme essential oil (Thymus vulgaris) significantly decreased fish mortality after a challenge with Yersinia ruckeri [27]. Zargar et al. [34] reported higher survival rates in rainbow trout (Oncorhynchus mykiss) that received thyme essential oil in the diet.

In conclusion, our results successfully show that dietary thyme essential oil (1% and 2%) positively influenced the growth parameters, digestive enzymes, hematology, immunity, and resistance to A. hydrophila infection in common carp. Most notably, the highest fish survival rate was achieved by supplementation 1% TVO. Accordingly, both 1 and 2% TVO inclusions may be recommended as dietary supplementations in the diets of common carp (Cyprinus carpio).

Data Availability

The data that support the findings of this study are available upon reasonable request to the corresponding authors.

Ethical Approval

All experiments were performed following the protocol approved by the Committee of Ethics of the Faculty of Sciences, University of Tehran (357; 8 November 2000). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Conflicts of Interest

The authors have no conflict of interest to declare for the publication of the work herein.

Acknowledgments

This research work was partially supported by Chiang Mai University, Chiang Mai, Thailand.

References

FAO, The State of World Fisheries and Aquaculture 2020, Sustainability in action, Rome, 2020.
J. Pucher, S. Steinbronn, R. Mayrhofer, I. Schad, M. El-Matbouli, and U. Focken, “Improved sustainable aquaculture systems for small-scale farmers in Northern Vietnam,” Sustainable Land Use and Rural Development in Southeast Asia: Innovations and Policies for Mountainous Areas, Springer Environmental Science and Engineering. Springer, Berlin, Heidelberg, 2013.
View at: Publisher Site | Google Scholar
D. Schar, E. Y. Klein, R. Laxminarayan, M. Gilbert, and T. P. Van Boeckel, “Global trends in antimicrobial use in aquaculture,” Scientific Reports, vol. 10, no. 1, pp. 1–9, 2020.
View at: Publisher Site | Google Scholar
R. Brown, L. Moore, A. Mani, S. Patel, and I. Salinas, “Effects of ploidy and salmonid alphavirus infection on the skin and gill microbiome of Atlantic salmon (Salmo salar),” PLoS One, vol. 16, no. 2, article e0243684, 2021.
View at: Publisher Site | Google Scholar
C. Harper, “Chemical resistance of 19 pathogens in aquaculture,” Aquaculture Magazine, vol. 33, no. 2, pp. 40–43, 2007.
View at: Google Scholar
S. C. Ji, G. S. Jeong, G. S. Im, S. W. Lee, J. H. Yoo, and K. Takii, “Dietary medicinal herbs improve growth performance, fatty acid utilization, and stress recovery of Japanese flounder,” Fisheries Science, vol. 73, no. 1, pp. 70–76, 2007.
View at: Publisher Site | Google Scholar
V. Sivaram, M. M. Babu, G. Immanuel, S. Murugadass, T. Citarasu, and M. P. Marian, “Growth and immune response of juvenile greasy groupers (Epinephelus tauvina) fed with herbal antibacterial active principle supplemented diets against Vibrio harveyi infections,” Aquaculture, vol. 237, no. 1-4, pp. 9–20, 2004.
View at: Publisher Site | Google Scholar
M. Divyagnaneswari, D. Christy Babita, and D. Dinakaran Michael, “Enhancement of nonspecific immunity and disease resistance in Oreochromis mossambicus by Solanum trilobatum leaf fractions,” Fish and Shellfish Immunology, vol. 23, no. 2, pp. 249–259, 2007.
View at: Publisher Site | Google Scholar
H. Ghafarifarsani, G. H. Rashidian, A. Sheikhlar, M. Naderi Farsani, S. H. Hoseinifar, and H. Van Doan, “The use of dietary oak acorn extract to improve haematological parameters, mucosal and serum immunity, skin mucus bactericidal activity, and disease resistance in rainbow trout (Oncorhynchus mykiss),” Aquaculture Research, vol. 52, no. 6, pp. 2518–2527, 2021.
View at: Publisher Site | Google Scholar
J. Jian and Z. Wu, “Influences of traditional Chinese medicine on non-specific immunity of Jian Carp (Cyprinus carpio var Jian),” Fish and Shellfish Immunology, vol. 16, no. 2, pp. 185–191, 2004.
View at: Publisher Site | Google Scholar
G. Yin, G. Jeney, T. Racz, P. Xu, X. Jun, and Z. Jeney, “Effect of two Chinese herbs (Astragalus radix and Scutellaria radix) on non-specific immune response of tilapia, Oreochromis niloticus,” Oreochromis niloticus. Aquaculture, vol. 253, no. 1-4, pp. 39–47, 2006.
View at: Publisher Site | Google Scholar
M. A. Dawood, S. Koshio, and M. Á. Esteban, “Beneficial roles of feed additives as immunostimulants in aquaculture: a review,” Reviews in Aquaculture, vol. 10, no. 4, pp. 950–974, 2018.
View at: Publisher Site | Google Scholar
C. Faggio, A. Sureda, S. Morabito et al., “Flavonoids and platelet aggregation: a brief review,” European Journal of Pharmacology, vol. 807, pp. 91–101, 2017.
View at: Publisher Site | Google Scholar
H. Ghafarifarsani, S. H. Hoseinifar, M. Aftabgard, and H. Van Doan, “The improving role of savory (Satureja hortensis) essential oil for Caspian roach (Rutilus caspicus) fry: growth, haematological, immunological, and antioxidant parameters and resistance to salinity stress,” Aquaculture, vol. 548, article 737653, 2022.
View at: Publisher Site | Google Scholar
M. Reverter, N. Tapissier-Bontemps, P. Sasal, and D. Saulnier, “Use of medicinal plants in aquaculture,” Diagnosis and Control of Diseases of Fish and Shellfish, JohnWiley & Sons Ltd, New Jersey, pp. 223–261, 2017.
View at: Publisher Site | Google Scholar
M. Yousefi, H. Ghafarifarsani, S. H. Hoseinifar, G. Rashidian, and H. Van Doan, “Effects of dietary marjoram, Origanum majorana extract on growth performance, hematological, antioxidant, humoral and mucosal immune responses, and resistance of common carp, _Cyprinus carpio_ against Aeromonas hydrophila,” Fish and Shellfish Immunology, vol. 108, pp. 127–133, 2021.
View at: Publisher Site | Google Scholar
H. M. Abdel-Latif, M. Abdel-Tawwab, A. F. Khafaga, and M. A. O. Dawood, “Dietary origanum essential oil improved antioxidative status, immune-related genes, and resistance of common carp (Cyprinus carpio L.) to Aeromonas hydrophila infection,” Fish & Shellfish Immunology, vol. 104, pp. 1–7, 2020.
View at: Publisher Site | Google Scholar
M. Alagawany, M. R. Farag, S. A. Abdelnour, and S. S. Elnesr, “A review on the beneficial effect of thymol on health and production of fish,” Reviews in Aquaculture, vol. 13, no. 1, pp. 632–641, 2021.
View at: Publisher Site | Google Scholar
A. Hernández, B. García García, M. J. Caballero, and M. D. Hernández, “Preliminary insights into the incorporation of rosemary extract (Rosmarinus officinalis L.) in fish feed: influence on performance and physiology of gilthead seabream (Sparus aurata),” Fish Physiology and Biochemistry, vol. 41, no. 4, pp. 1065–1074, 2015.
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
G. Immanuel, M. Sivagnanavelmurugan, V. Balasubrama-nian, and A. Palavesam, “Effect of hot water extracts of brown seaweeds Sargassum spp. on growth and resistance to white spot syndrome virus in shrimp Penaeus monodon postlarvae,” Aquaculture Research, vol. 41, pp. 545–553, 2010.
View at: Publisher Site | Google Scholar
E. J. Nya and B. Austin, “Development of immunity in rainbow trout (Oncorhynchus mykiss, Walbaum) to Aeromonas hydrophila after the dietary application of garlic,” Fish and Shellfish Immunology, vol. 30, no. 3, pp. 845–850, 2011.
View at: Publisher Site | Google Scholar
V. Peraza-Gómez, A. Luna-González, Á. I. Campa-Córdova, J. A. Fierro-Coronado, H. A. González Ocampo, and J. C. Sainz-Hernández, “Dietary microorganism and plant effects on the survival and immune response of Litopenaeus vannamei challenged with the white spot syndrome virus,” Aquaculture Research, vol. 42, no. 4, pp. 559–570, 2011.
View at: Publisher Site | Google Scholar
S. Yılmaz, S. Ergün, and E. Ş. Çelik, “Effects of herbal supplements on growth performance of sea bass (Dicentrarchus labrax): change in body composition and some blood parameters,” Journal of Bioscience and Biotechnology, vol. 1, pp. 217–222, 2012.
View at: Google Scholar
O. G. Dorojan, V. Cristea, M. Creţu, M. T. Coadă, L. Dediu, and I. R. Grecu, “Effect of thyme (Thymus vulgaris) and vitamin E on growth performance and body composition of Acipenser stellatus juveniles,” Aquaculture, Aquarium, Conservation and Legislation, International Journal of the Bioflux Society, vol. 8, no. 2, pp. 195–202, 2015.
View at: Google Scholar
O. G. Dorojan, S. Placinta, and S. Petrea, “The influence of some phytobiotics (thyme, seabuckthorn) on the growth performance of stellate sturgeon (A. stellatus, Pallas, 1771) in an industrial recirculating aquaculture system,” Scientific Papers Animal Science and Biotechnologies, vol. 47, no. 1, pp. 205–210, 2014.
View at: Google Scholar
A. K. Gulec, K. Azime, D. Durali, U. Mesut, S. Engin, and A. Ali, “Effect of mixed use of thyme and fennel oils on biochemical properties and electrolytes in rainbow trout as a response to Yersinia ruckeri infection,” Acta Veterinaria Brno, vol. 82, no. 3, pp. 297–302, 2013.
View at: Publisher Site | Google Scholar
M. C. Rota, A. Herrera, R. M. Martinez, J. A. Sotomayor, and M. J. Jordan, “Antimicrobial activity and chemical composition of Thymus vulgaris , Thymus zygis and Thymus hyemalis essential oils,” Food Control, vol. 19, no. 7, pp. 681–687, 2008.
View at: Publisher Site | Google Scholar
H. Sajed, A. Sahebkar, and M. Iranshahi, “Zataria multiflora Boiss. (Shirazi thyme) --an ancient condiment with modern pharmaceutical uses,” Journal of Ethnopharmacology, vol. 145, no. 3, pp. 686–698, 2013.
View at: Publisher Site | Google Scholar
E. Yilmaz, E. Sebahattin, and S. Yilmaz, “Influence of carvacrol on the growth performance, hematological, non-specific immune and serum biochemistry parameters in rainbow trout (Oncorhynchus mykiss),” Food and Nutrition Sciences, vol. 6, no. 5, pp. 523–531, 2015.
View at: Publisher Site | Google Scholar
M. A. Zaki, E. M. Labib, A. M. Nour, H. D. Tonsy, and S. H. Mahmoud, “Effect of some medicinal plants diet on mono sex Nile tilapia (Oreochromis niloticus), growth performance, feed utilization, and physiological parameters,” Asia-Pacific Chemical, Biological & Environmental Engineering Society, vol. 4, pp. 220–227, 2012.
View at: Google Scholar
A. H. AlSafah and J. K. Al-Faragi, “Influence of thyme (Thymus vulgaris) as feed additives on growth performance and antifungal activity on Saprolegnia spp. in Cyprinus carpio L,” Journal of Entomology and Zoology Studies, vol. 5, no. 6, pp. 1598–1602, 2017.
View at: Google Scholar
V. Zadmajid and C. Mohammadi, “Dietary thyme essential oil (Thymus vulgaris) changes serum stress markers, enzyme activity, and hematological parameters in gibel carp (Carassius auratus gibelio) exposed to silver nanoparticles,” Iranian Journal of Fisheries Sciences, vol. 16, no. 3, pp. 1063–1084, 2017.
View at: Google Scholar
A. Zargar, Z. Rahimi-Afzal, E. Soltani et al., “Growth performance, immune response and disease resistance of rainbow trout (Oncorhynchus mykiss) fed Thymus vulgaris essential oils,” Aquaculture Research, vol. 50, no. 11, pp. 3097–3106, 2019.
View at: Publisher Site | Google Scholar
H. Ghafarifarsani, R. Kachuei, and A. Imani, “Dietary supplementation of garden thyme essential oil ameliorated the deteriorative effects of aflatoxin B₁ on growth performance and intestinal inflammatory status of rainbow trout (Oncorhynchus mykiss),” Aquaculture, vol. 531, article 735928, 2021.
View at: Publisher Site | Google Scholar
M. Yousefi, H. Ghafarifarsani, S. M. Hoseini et al., “Effects of dietary thyme essential oil and prebiotic administration on rainbow trout (Oncorhynchus mykiss) welfare and performance,” Fish & Shellfish Immunology, vol. 120, pp. 737–744, 2022.
View at: Publisher Site | Google Scholar
C. S. Ramsden, T. J. Smith, B. J. Shaw, and R. D. Handy, “Dietary exposure to titanium dioxide nanoparticles in rainbow trout,” (Oncorhynchus mykiss): no effect on growth, but subtle biochemical disturbances in the brain. Ecotoxicology, vol. 18, no. 7, pp. 939–951, 2009.
View at: Google Scholar
F. CVM, “Concerns related to the use of clove oil as an anesthetic for fish,” Guidance for Industry, vol. 150, 2007.
View at: Google Scholar
N. W. Ross, K. J. Firth, A. Wang, J. F. Burka, and S. C. Johnson, “Changes in hydrolytic enzyme activities of naïve Atlantic salmon Salmo salar skin mucus due to infection with the salmon louse Lepeophtheirus salmonis and cortisol implantation,” Diseases of Aquatic Organisms, vol. 41, no. 1, pp. 43–51, 2000.
View at: Publisher Site | Google Scholar
H. Ghafarifarsani, A. Imani, T. A. Niewold, C. Pietsch-Schmied, and K. S. Moghanlou, “Synergistic toxicity of dietary aflatoxin B₁ (AFB₁) and zearalenone (ZEN) in rainbow trout (Oncorhynchus mykiss) is attenuated by anabolic effects,” Aquaculture, vol. 541, article 736793, 2021.
View at: Publisher Site | Google Scholar
M. M. Naderi, A. Sarvari, A. Milanifar, S. B. Boroujeni, and M. M. Akhondi, “Regulations and ethical considerations in animal experiments: international laws and islamic perspectives,” Avicenna journal of medical biotechnology, vol. 4, no. 3, pp. 114–120, 2012.
View at: Google Scholar
R. Peyghan and G. A. Takamy, “Histopathological, serum enzyme, cholesterol and urea changes in experimental acute toxicity of ammonia in common carp Cyprinus carpio and use of natural zeolite for prevention,” Aquaculture International, vol. 10, no. 4, pp. 317–325, 2002.
View at: Publisher Site | Google Scholar
M. R. I. Sarder, K. D. Thompson, D. J. Penman, and B. J. McAndrew, “Immune responses of Nile tilapia (Oreochromis niloticus L.) clones: I. Non- specific responses,” Developmental & Comparative Immunology, vol. 25, no. 1, pp. 37–46, 2001.
View at: Publisher Site | Google Scholar
C. R. Davis, G. D. Marty, M. A. Adkison, E. F. Freiberg, and R. P. Hedrick, “Association of plasma IgM with body size, histopathologic changes, and plasma chemistries in adult Pacific herring Clupea pallasi,” Diseases of Aquatic Organisms, vol. 38, no. 2, pp. 125–133, 1999.
View at: Publisher Site | Google Scholar
A. Garen and C. Levinthal, “A fine-structure genetic and chemical study of the enzyme alkaline phosphatase of E. Coli I. Purification and characterization of alkaline phosphatase,” Biochimica et Biophysica Acta, vol. 38, pp. 470–483, 1960.
View at: Publisher Site | Google Scholar
N. E. Demers and C. J. Bayne, “The immediate effects of stress on hormones and plasma lysozyme in rainbow trout,” Developmental & Comparative Immunology, vol. 21, no. 4, pp. 363–373, 1997.
View at: Publisher Site | Google Scholar
J. Ortuno, M. A. Esteban, and J. Meseguer, “High dietary intake of α-tocopherol acetate enhances the non-specific immune response of gilthead seabream (Sparus aurata L.),” Fish & Shellfish Immunology, vol. 10, no. 4, pp. 293–307, 2000.
View at: Google Scholar
A. Siwicki and D. Anderson, Nonspecific defense mechanisms assay in fish: II. Potential Killing Activity of Neutrophils and Macrophages, Lysozyme Activity in Serum and Organs and Total Immunoglobulin (Ig) Level in Serum, FAO project GCP/ INT/JPA, IFI, Olsztyn, Poland, 2000.
J. A. Buege and S. D. Aust, “Microsomal lipid peroxidation,” Methods in enzymology, Academic press, vol. 52, pp. 302–310, 1978.
View at: Google Scholar
W. F. Emeish and A. G. S. El-Deen, “Immunomodulatory effects of thyme and fenugreek in sharp tooth catfish, Clarias gariepinus,” Assiut Veterinary and Medical Journal, vol. 62, no. 150, pp. 45–51, 2016.
View at: Publisher Site | Google Scholar
N. Gültepe, S. Bilen, S. Yılmaz, D. Güroy, and S. Aydın, “Effects of herbs and spice on health status of tilapia (Oreochromis mossambicus) challenged with Streptococcus iniae,” Acta Veterinaria Brno, vol. 83, no. 2, pp. 125–131, 2014.
View at: Publisher Site | Google Scholar
S. M. Hoseini and M. Yousefi, “Beneficial effects of thyme (Thymus vulgaris) extract on oxytetracycline- induced stress response, immunosuppression, oxidative stress and enzymatic changes in rainbow trout (Oncorhynchus mykiss),” Aquaculture Nutrition, vol. 25, no. 2, pp. 298–309, 2019.
View at: Publisher Site | Google Scholar
V. Jahanjoo, M. Yahyavi, R. Akrami, and A. H. Bahri, “Influence of adding garlic (Allium sativum), ginger (Zingiber officinale), thyme (Thymus vulgaris), and their combination on the growth performance, hematoimmunological parameters, and disease resistance to Photobacteriumdamselae in sobaity sea bream (Sparidentex hasta) fry,” Turkish Journal of Fisheries and Aquatic Sciences, vol. 18, no. 4, pp. 633–645, 2018.
View at: Google Scholar
S. R. Khalil, Y. AbdElhakim, A. H. Abd El-fattah, M. R. Farag, N. E. Abd El-Hameed, and E. M. AbdElhakeem, “Dual immunological and oxidative responses in Oreochromis niloticus fish exposed to lambda cyhalothrin and concurrently fed with Thyme powder (Thymus vulgaris L.): Stress and immune encoding gene expression,” Fish & Shellfish Immunology, vol. 100, pp. 208–218, 2020.
View at: Publisher Site | Google Scholar
A. T. Mirghaed, S. M. Hoseini, S. H. Hoseinifar, and H. Van Doan, “Effects of dietary thyme (Zataria multiflora) extract on antioxidant and immunological responses and immune-related gene expression of rainbow trout (Oncorhynchus mykiss) juveniles,” Fish & Shellfish Immunology, vol. 106, pp. 502–509, 2020.
View at: Publisher Site | Google Scholar
S. Yilmaz, S. Ergün, and E. Ş. Çelik, “Effect of dietary herbal supplements on some physiological conditions of sea bass Dicentrarchus labrax,” Journal of Aquatic Animal Health, vol. 25, no. 2, pp. 98–103, 2013.
View at: Publisher Site | Google Scholar
S. Yilmaz, S. Ergün, and N. Soytaş, “Herbal supplements are useful for preventing streptococcal disease during first-feeding of tilapia fry, Oreochromis mossambicus,” Israeli Journal of Aquaculture Bamidgeh, vol. 833, no. 1, pp. 195–204, 2013.
View at: Google Scholar
S. Yilmaz, S. Ergün, and E. Ş. Çelik, “Effect of dietary spice supplementations on welfare status of sea bass, Dicentrarchus labrax L,” Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, vol. 86, no. 1, pp. 229–237, 2016.
View at: Publisher Site | Google Scholar
A. Y. Sönmez, S. Bilen, G. Alak, O. Hisar, T. Yanık, and G. Biswas, “Growth performance and antioxidant enzyme activities in rainbow trout (Oncorhynchus mykiss) juveniles fed diets supplemented with sage, mint, and thyme oils,” Fish Physiology and Biochemistry, vol. 41, no. 1, pp. 165–175, 2015.
View at: Publisher Site | Google Scholar
D. Volpatti, B. Chiara, T. Francesca, and G. Marco, “Growth parameters, innate immune response and resistance to L istonella (V ibrio) anguillarum of Dicentrarchus labrax fed carvacrol supplemented diets,” Aquaculture Research, vol. 45, no. 1, pp. 31–44, 2013.
View at: Google Scholar
A. S. AbdEl-Naby, A. A. Al-Sagheer, S. S. Negm, and M. A. Naiel, “Dietary combination of chitosan nanoparticle and thymol affects feed utilization, digestive enzymes, antioxidant status, and intestinal morphology of _Oreochromis niloticus_,” Aquaculture, vol. 515, article 734577, 2020.
View at: Publisher Site | Google Scholar
H. Tasa, A. Imani, K. S. Moghanlou, N. Nazdar, and M. Moradi-Ozarlou, “Aflatoxicosis in fingerling common carp (Cyprinus carpio) and protective effect of rosemary and thyme powder: growth performance and digestive status,” Aquaculture, vol. 527, article 735437, 2020.
View at: Publisher Site | Google Scholar
M. H. Ahmad, R. M. El-Gamal, M. M. Hazaa, S. M. Hassan, and D. A. El Araby, “The use of Origanium vulgare extract in diets as a growth and immuity promoter for Nile Tilapia, Orecohromis niloticus (L). fingerlinges challenged challenged with pathogenic Pseudomonas aeruginosa and Pseudomonas flourscence,” The Egyptian Journal of Experimental Biology (Zoology), vol. 5, pp. 457–463, 2009.
View at: Google Scholar
A. Dada and M. Ikuerowo, “Effects of ethanolic extracts of Garcinia kola seeds on growth and haematology of catfish (Clarias gariepinus) broodstock,” African Journal of Agricultural Research, vol. 4, pp. 344–347, 2009.
View at: Google Scholar
G. Francis, H. P. Makkar, and K. Becker, “Dietary supplementation with a Quillaja saponin mixture improves growth performance and metabolic efficiency in common carp (Cyprinus carpio L.),” Aquaculture, vol. 203, no. 3-4, pp. 311–320, 2002.
View at: Publisher Site | Google Scholar
M. Gaber, E. Labib, E. Omar, M. Zaki, and A. Nour, “Effect of partially replacing corn meal by wet date on growth performance in Nile Tilapia (Oreochromis niloticus) fingerlings, diets supplemented with Digestarom®,” Journal of Geoscience and Environment Protection, vol. 2, no. 2, pp. 60–67, 2014.
View at: Publisher Site | Google Scholar
S. C. Ji, O. Takaoka, G. S. Jeong et al., “Dietary medicinal herbs improve growth and some non-specific immunity of red sea bream Pagrus major,” Fisheries Science, vol. 73, no. 1, pp. 63–69, 2007.
View at: Publisher Site | Google Scholar
M. M. Khalafalla, “Utilization of some Med Oreochromis Niloticus ical plants as feed additives for Nile Tilapia, Oreochromis Niloticus, feeds,” Mediterranean Aquaculture Journal, vol. 2, no. 1, pp. 9–18, 2009.
View at: Publisher Site | Google Scholar
A. Shalaby, Y. A. Khattab, and A. Rahman, “Effects of garlic (Allium sativum) and chloramphenicol on growth performance, physiological parameters and survival of Nile Tilapia (Oreochromis niloticus),” Journal of Venomous Animals and Toxins Including Tropical Diseases, vol. 12, pp. 172–201, 2006.
View at: Publisher Site | Google Scholar
H. Liu, S. Wang, D. Zhang et al., “Effects of dietary supplementation with Pediococcus acidilactici ZPA017 on reproductive performance, fecal microbial flora, and serum indices in sows during late gestation and lactation,” Asian-Australasian Journal of Animal Sciences, vol. 33, no. 1, pp. 120–126, 2020.
View at: Publisher Site | Google Scholar
T. Patriche, N. Patriche, and E. Bocioc, “Determination of some normal serum parameters in juvenile Sevruga sturgeons Acipenser stellatus (Pallas, 1771),” Archiva Zootechnica, vol. 14, no. 1, pp. 49–54, 2011.
View at: Google Scholar
M. Yousefian, A. Sheikholeslami, and M. Kor Davood, “Serum biochemical parameter of male, immature and female Persian sturgeon (Acipencer persicus),” Australian Journal of Basic and Applied Sciences, vol. 5, no. 5, pp. 476–481, 2011.
View at: Google Scholar
A. J. Adler and R. B. Edwards, “Human interphotoreceptor matrix contains serum albumin and retinol-binding protein,” Experimental Eye Research, vol. 70, no. 2, pp. 227–234, 2000.
View at: Publisher Site | Google Scholar
M. E. Baker, “Albumin, steroid hormones and the origin of vertebrates,” Journal of Endocrinology, vol. 175, no. 1, pp. 121–127, 2002.
View at: Publisher Site | Google Scholar
Y. Y. Chen, S. Y. Lin, Y. Y. Yeh et al., “A modified protein precipitation procedure for efficient removal of albumin from serum,” Electrophoresis, vol. 26, no. 11, pp. 2117–2127, 2005.
View at: Publisher Site | Google Scholar
T. Zenei and T. Hiroshi, “Specific and non-specific ligand binding to serum albumin,” Biochemical Pharmacology, vol. 34, no. 11, pp. 1999–2005, 1985.
View at: Publisher Site | Google Scholar
A. Nandi, G. Banerjee, S. K. Dan, K. Ghosh, and A. K. Ray, “Evaluation of in vivo probiotic efficiency of Bacillus amyloliquefaciens in Labeo rohita challenged by pathogenic strain of Aeromonas hydrophila MTCC 1739,” Probiotics and Antimicrobial Proteins, vol. 10, no. 2, pp. 391–398, 2018.
View at: Publisher Site | Google Scholar
M. R. Narra, “Haematological and immune upshots in Clarias batrachus exposed to dimethoate and defying response of dietary ascorbic acid,” Chemosphere, vol. 168, pp. 988–995, 2017.
View at: Publisher Site | Google Scholar
L. Sahoo, T. G. Choudhury, C. Debnath et al., “Immunostimulatory effect of vitamin C on hemato-biochemical parameters of Labeo bata (Hamilton, 1822),” Fishery Technology, vol. 53, no. 1, pp. 59–63, 2016.
View at: Google Scholar
F. Fazio, “Fish hematology analysis as an important tool of aquaculture: a review,” Aquaculture, vol. 500, pp. 237–242, 2019.
View at: Publisher Site | Google Scholar
M. Maita, “Fish health assessment,” Dietary Supplements for the Health and Quality of Cultured Fish, CAB International, Washington, pp. 10–34, 2007.
View at: Publisher Site | Google Scholar
G. M. R. Valladão, S. U. Gallani, S. Kotzent, I. M. Assane, and F. Pilarski, “Effects of dietary thyme essential oil on hemato-immunological indices, intestinal morphology, and microbiota of Nile tilapia,” Aquaculture International, vol. 27, no. 2, pp. 399–411, 2019.
View at: Publisher Site | Google Scholar
M. Cámara, M. C. Sánchez-Mata, V. Fernández-Ruiz, R. M. Cámara, E. Cebadera, and L. Domínguez, “A review of the role of micronutrients and bioactive compounds on immune system supporting to fight against the COVID-19 disease,” Food, vol. 10, no. 5, p. 1088, 2021.
View at: Publisher Site | Google Scholar
M. Yousefi, S. M. Hoseini, Y. A. Vatnikov, A. A. Nikishov, and E. V. Kulikov, “Thymol as a new anesthetic in common carp (Cyprinus carpio): efficacy and physiological effects in comparison with eugenol,” Aquaculture, vol. 495, pp. 376–383, 2018.
View at: Publisher Site | Google Scholar
Y. D. Kong, M. Li, C. G. Xia et al., “The optimum thymol requirement in diets of Channa argus: effects on growth, antioxidant capability, immune response and disease resistance,” Aquaculture Nutrition, vol. 27, no. 3, pp. 712–722, 2021.
View at: Publisher Site | Google Scholar
O. I. El Euony, S. S. Elblehi, H. M. Abdel-Latif, M. M. Abdel-Daim, and Y. S. El-Sayed, “Modulatory role of dietary Thymus vulgaris essential oil and Bacillus subtilis against thiamethoxam-induced hepatorenal damage, oxidative stress, and immunotoxicity in African catfish (Clarias garipenus),” Environmental Science and Pollution Research, vol. 27, no. 18, pp. 23108–23128, 2020.
View at: Publisher Site | Google Scholar
H. S. Abdo, “Effect of dietary phytobiotics supplementation on growth, serum biochemical and chemical composition of Nile Tilapia (Oreochromis niloticus),” Annals of Agricultural Science, Moshtohor, vol. 58, no. 2, pp. 273–282, 2020.
View at: Publisher Site | Google Scholar
A. Grigore, “Phenolic compounds-biological activity,” Intech Open, Plant phenolic compounds as immunomodulatory agents, London, UK, pp. 75–98, 2017.
View at: Google Scholar
N. Tabanca, N. Kırımer, B. Demirci, F. Demirci, and K. H. C. Başer, “Composition and antimicrobial activity of the essential oils of Micromeria cristata subsp. phrygia and the enantiomeric distribution of borneol,” Journal of Agricultural and Food Chemistry, vol. 49, no. 9, pp. 4300–4303, 2001.
View at: Publisher Site | Google Scholar
G. Vardar-Ünlü, F. Candan, A. Sökmen et al., “Antimicrobial and antioxidant activity of the essential oil and methanol extracts of Thymus pectinatus Fisch. et Mey. Var. pectinatus (Lamiaceae),” Journal of Agricultural and food chemistry, vol. 51, no. 1, pp. 63–67, 2003.
View at: Publisher Site | Google Scholar
M. D’Archivio, C. Filesi, R. Di Benedetto, R. Gargiulo, C. Giovannini, and R. Masella, “Polyphenols, dietary sources and bioavailability,” Annali dell Istituto Superiore di Sanita, vol. 43, no. 4, pp. 348–361, 2007.
View at: Google Scholar
D. M. Pereira, P. Valentao, J. A. Pereira, and P. B. Andrade, “Phenolics: from chemistry to biology,” Molecules, vol. 14, no. 6, pp. 2202–2211, 2009.
View at: Publisher Site | Google Scholar
M. A. E. Mabrok and A. Wahdan, “The immune-modulatory effect of oregano (Origanum vulgare L.) essential oil on Tilapia zillii following intraperitoneal infection with vibrio anguillarum,” Aquaculture International, vol. 26, no. 4, pp. 1147–1160, 2018.
View at: Publisher Site | Google Scholar
T. Q. Nhu, B. T. B. Hang, B. T. B. Hue et al., “Plant extract-based diets differently modulate immune responses and resistance to bacterial infection in striped catfish (Pangasianodon hypophthalmus),” Fish & Shellfish Immunology, vol. 92, pp. 913–924, 2019.
View at: Publisher Site | Google Scholar
T. Citarasu, “Herbal biomedicines: a new opportunity for aquaculture industry,” Aquaculture International, vol. 18, no. 3, pp. 403–414, 2010.
View at: Publisher Site | Google Scholar

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