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Abstract

Objectives: The effects of different concentrations of Dracocephalum moldavica extract (DME) supplement on growth, survival, antioxidants, some biochemical parameters and innate immunity of White leg shrimp (Penaeus vannamei) juveniles investigated. Methods: For 56 days, shrimp (4.5-5 g) received diets that were enhanced with 0 (control), 50, 100, 200 mg DME/kg feed to attain apparent satiety. Results: The results revealed that feeding shrimp with DME significantly improved Feed efficiency and Feed conversion ratio with an optimum level of 200 mg/kg diet. Dietary DME supplementation had no significant effects on their carcass composition. Total albumin and protein higher (P > 0.05) in DME-fed particularly at 200 mg/kg treatment On the other hand, shrimp fed 200 mg DME/kg feed experienced significant decreases in aspartate and alanine aminotransferase levels. As dietary extract levels increased, there was a significant (P < 0.05) increase in SOD and CAT activities, as well as LYZ and PO levels, so that treatments with 100 and 200 mg DME/kg feed had the highest values, and Significant (P < 0.05) reductions in MDA and NO levels were observed at high dietary extract levels of 100 and 200 mg DME/kg. Conclusion: P. vannamei's growth, antioxidant capacity and innate immunity were boosted by diets that contained 200 mg DME/kg feed.

Keywords

White leg shrimp immunity biochemical parameters antioxidant innate immunity

Introduction

Aquaculture is a crucial way to meet the protein requirements of humans.¹ The risk of fish diseases and environmental pollution has been elevated as a result of the development of intensive and super-intensive aquaculture.² Aquaculture frequently uses P. vannamei, which are found in the eastern Pacific Ocean.³ Drugs, antibiotics and hormones are commonly used to treat diseases in shrimp. Resistant bacterial strains may be created by the continued use of these chemicals. As a consumer, there is a risk to human health posed by the accumulation of these chemicals in shrimp meat. In addition, the flora and fauna may be negatively impacted by the release of their derivatives into natural aquatic environments. Researching an alternative source of natural herbal origin is necessary for the entire food web of that environment.⁴ Numerous studies have shown that medicinal plants have beneficial effects on aquatic animals.^5-11

The high medicinal properties of Dracocephalum sp. make it a popular drug in many parts of the world. There are more than 60 species in this genus that are native to temperate regions of Asia and Europe.¹² The extract of aerial parts of this species is contain hydrox-ycinnamic acids (rosmarinic and caffeic acids) and flavonoids such as luteolin, apigenin and their quercetin, glycosides, acacetin, diosmetin, kaempferol, agastachioside and salvigenin.^13,14 31 compounds including flavonoids, flavonols and flavonoids glycosides and 13 phenylpropanoids compounds including phenylpropionic acid, lignans and coumarins were isolated from DME.¹⁵ Antibacterial properties, antioxidant effects, and cardioprotective effects were observed in the Moldavian dragonhead extract.¹⁶ Also therapeutic effects of DME such as sedative¹⁷ cardioprotective, antiplatelet,¹⁶ neuroprotective,¹⁸ and antiaging¹⁹ have revealed. Researchers have reported that diets containing Dracocephalum kotschyi essential oil can enhance growth and immunity in aquatic vertebrates,²⁰ but this is the first study to measure DME on aquatic invertebrates.

Materials and Methods

Experimental Animals

A private shrimp farm in Choebdeh Abadan provided healthy P. vannamei juveniles (4.5-8 g). 360 shrimp with 4 treatments in three replicates (5 g initial weight) and at a rate of 30 individuals per aquarium stocked into 12 aquaria. The, salinity pH, temperature and dissolved oxygen of the water was kept at 16 ± 3‰, 7.7 ± 0.7, 26 ± 5 ◦C, and 7 ± 0.6 mg/L respectively.

Preparation of DME

D. moldavica were collected from Tabriz (Iran). Extraction by mercerization method was done according to Zohouri et al²¹ instructions. DME was preserved at 4 °C until use.

Preparation of Diet

A diet with no DME were used as a control. DME were added to the experimental diets at concentrations of 50, 100 and 200 mg/kg.²² For each experimental treatment, DME was sprayed on food at the concentrations and was ready for consumption after drying. For 56 days, shrimp fed experimental diets four times per day at 7:00, 13:00, 17:00, and 21:00.

Growth Performance Indices

Feed utilization and indices of shrimp's growth was done according to Mosavi Dehmordi et al²³ instructions.

Chemical Analysis of Carcass

AOAC²⁴ standard methods were used to analyze the dried sample for total lipids, crude protein, and ash.

Plasma Antioxidant, Innate Immunity and Biochemical Analyse

Four animals from each aquarium were chosen to be anestetized by immersion in 20 μL/L of eugenol after the feeding trial.²⁵ The activity of superoxide dismutase (SOD), catalase (CAT), phenoloxidase (PO) and glutathione peroxidase (GPx) were determined using the techniques described by Dhindsa et al,²⁶ Beers & Sizer,²⁷ Kitikiew et al,²⁸ and Lucio et al,²⁹ respectively. The content of malondialdehyde (MDA) was measured using a thiobarbituric acid reaction to estimate lipid peroxidation.³⁰ Turbidimetric methods have been utilized to assess the activity of lysozyme (LYZ).³¹ A total nitric oxide assay kit and the Griess reaction were used to evaluate the serum nitric oxide (NO) level.³² Doumas et al³³ was followed by the measurement of total protein (TP) and albumin (ALB) levels. Calorimetrically, the activity of aspartate (AST) and alanine aminotransferases (ALT) was measured.³³

Statistical Analysis

Shapiro-Williams, Bartlett's tests, tukey's Studentized Range Test and one-way ANOVA analysis of variance were used to analyze statistical significance of difference between groups at P < 0.05.

Results

Growth Indices and Mortality Parameter

Weight gain percent, Specific growth rate and mortality rate showed no significant differences between the treatments throughout 56 days of feeding trial (Table 1, p > 0.05). Animals treated with 200 mg of DME/kg of feed performed better than those on the control diet, but there was no significant difference between them. The highest feed efficiency (24.58 ± 0.91) was observed in the treatments of 200 mg DME/kg feed. FE and FCR values were significantly (P < 0.05) differed among various treatments (Table 1).

Table 1.

Growth and Survival of P. vannamei With Diet Containing Different Levels of DME After 56 Days of Supplementation.

	DME levels (mg/kg diet)				P value
	0.0	50	100	200	P value
Final weight (g)	11.15 ± 0.02	11.13 ± 0.01	11.20 ± 0.0	11.27 ± 0.06	0.06
Final length(cm)	6.7 ± 0.05	6.7 ± 0.03	6.8 ± 0.03	6.9 ± 0.03	0.22
Weight gain %	5.65 ± 0.02	5.3 ± 0.01	5.70 ± 0.0	5.77 ± 0.06	0.06
Specific growth rate (%/day)	3.09 ± 0.0	3.08 ± 0.0	3.11 ± 0.0	3.13 ± 0.01	0.08
Feed conversion ratio	2.67 ± 0.03^a	2.47 ± 0.05^ab	2.57 ± 0.02^ab	2.36 ± 0.09^b	0.02
Feed efficiency	20.03 ± 0.28^a	21.69 ± 0.47^ab	20.79 ± 0.19^ab	22.75 ± 0.91^b	0.03
Condition factor	3.71 ± 0.08	3.59 ± 0.06	3.61 ± 0.05	3.53 ± 0.06	0.39
Shrimp survival (%)	87.3 ± 0.0	87.3 ± 0.33	88 ± 0.0	88.3 ± 0.33	0.06

Carcass Composition

Feeding shrimp with diets supplemented with DME had no significant (P > 0.05) effect on the moisture, crude protein, ash levels and total lipids of their carcass for 56 days (Table 2).

Table 2.

Proximate Chemical Composition of Carcass P. vannamei After 56 Day Fed on DME-Enriched Diets.

DME levels (mg/kg diet)	Crude protein	Moisture	Total lipids	Total ash
0.0	234.6 ± 3.91	710.7 ± 3.40	50.1 ± 1.21	48.3 ± 1.34
50	234.2 ± 4.19	709.6 ± 4.13	49.5 ± 1.64	48.1 ± 1.12
100	237.2 ± 4.93	707.4 ± 4.22	49.3 ± 1.16	48.2 ± 1.77
200	236.9 ± 4.87	709.5 ± 4.39	48.8 ± 1.57	47.5 ± 1.10
P value	0.83	0.90	0.63	0.78

Immune Responses and Antioxidant

The activities of LYZ and PO activities as well as SOD and CAT levels significantly (P < 0.05) increased with the increase of extract, compared to the control group. Their highest values revealed in 100 and 200 mg/kg feed (Table 3). With increasing the concentration of the extract at 100 and 200 mg/kg, the amount of NO and MDA levels significantly decreased (P < 0.05).

Table 3.

Immunological Reaction and Antioxidants of P. vannamei After 56 Day Fed on DME-Enriched Diets.

D. moldavica extract levels (mg/kg diet)	PO (O.D. at 490 n)	SOD (IU/L	MDA (nmol/mL)	GPx (IU/L)	CAT (IU/L)	NO (μmol/L)	LYZ (μg/mL)
0.0	0.62 ± 0.00a	25.6 ± 0.33a	96.6 ± 0.33a	0.09 ± 0.00a	14.3 ± 0.34a	2.4 ± 0.03a	0.80 ± 0.01c
50	0.64 ± 0.00 a	29.3 ± 0.33b	84.3 ± 0.33b	0.11 ± 0.00b	23.3 ± 0.33b	2 ± 0.12ab	0.90 ± 0.03bc
100	0.98 ± 0.00b	33.3 ± 0.33c	82.3 ± 0.33c	0.10 ± 0.01ab	21.6 ± 0.33c	1.6 ± 0.12bc	1.11 ± 0.06b
200	1.1 ± 0.05b	35.6 ± 0.33d	96.6 ± 0.33a	0.10 ± 0.00ab	28.3 ± 0.32d	1.2 ± 0.10c	1.40 ± 0.06a
P value	0.000	0.000	0.000	0.011	0.000	0.001	0.001

Biochemical Parameters

Serum TP and ALB were higher in the 200 mg DME/kg feed when compared to the control group, but there were no significant differences (P > 0.05) (Table 4). Conversely, animals with control diet revealed highest values of AST and ALT and Significantly reductions in ALT and AST were 200 mg DME /kg feed treatments (P > 0.05) (Table 4).

Table 4.

Biochemical Parameters of White Leg Shrimp After 56 Day Fed on DME.

	DME levels (mg/kg diet)
	0.0	50	100	200
TP (mg/L)	5.5 ± 0.30	5.6 ± 0.34	5.8 ± 0.21	5.9 ± 0.16
ALB (mg/L)	2.9 ± 0.39	3.0 ± 0.34	3.3 ± 0.23	3.5 ± 0.22
AST (IU/L)	4.0 ± 0.19^a	4.0 ± 0.22^ab	3.50 ± 0.17^bc	2.98 ± 0.14^c
ALT (IU/L)	5.4 ± 0.24^a	5.1 ± 0.19^ab	4.11 ± 0.32^bc	3.13 ± 0.22^c

Discussion

Medicinal plants’ effects on animals are influenced by the species consumed, feeding schedule, extraction, processing, plant maturity, and secondary metabolites. Several aquatic species have shown a significant improvement in physiological functions, growth performance, and innate immunity following the use of dietary herbal medicinal extracts.^34-40 In the current study, P. vannamei fed on diets enriched with DME at rates of 200 mg/kg feed showed higher performance. It's possible that these findings are caused by its high levels of bioactive chemicals, including flavonoids and terpenoids, such as hydroxycinnamic acids, caffeic acid, ferulic acid, rosmarinic acid, luteolin, luteolin-7-O-glucoside and apigenin, kaempferol, chrysoeriol, and quercetin-3-O-[α- L-rhamnopyranosyl (1 → 6)]-β- D –glucopyranoside, apigenin, luteolin, kaempferol, isorhamnetin, tilianin, agastachoside, acacetinglycoside and syringaresinol.¹⁶ All these materials can be effective in improve feed palatability or promote the production of digestive enzymes, resulting in the increased growth.

A suitable biomarker for aquaculture shrimp physiology can be obtained by examining the carcass composition, which can influence the nutrients contained in the carcass. Mosavi Dehmordi et al²³ found similar conclusions after feeding P. vannamei diets that included sweet basil (Ocimum basilicum) extract. The dietary supplementation of Origanum essential oil did not have a significant impact on total lipids, moisture, crude protein and total ash of the whole body in common carp (Cyprinus carpio) as demonstrated by Abdel-Latif et al.⁴¹ In aquatic animals, changes in lipid and protein content in their tissues have been linked to changes in muscle deposition rates, alterations in synthesis, and/or growth rates.⁴²

Oxidative stress can be caused by the production of reactive oxygen species (ROS) during metabolic processes. The enzymes GPx, SOD, and CAT function to decrease oxidative stress in aquatic animals. These enzymes are responsible for preventing ROS imbalance in biological system and maintaining normal redox homeostasis.⁷ According to these findings, DME has potent antioxidant and immune properties due to its high terpenoid, flavonoids, alkaloids, lignans, phenols, coumarins and phenylpropionic acid content. Lipid peroxidation is inhibited, free radicals are scavenged, and antioxidant and immune activity is enhanced by these compounds.⁴² Medicinal materials and extracts have been shown to have stimulatory effects on immune responses in similar studies. According to Halim et al,⁴³ Morinda citrifolia leaf extract incubating prawn (Macrobrachium rosenbergii) hematocytes resulted in an increase in phagocytolytic activities, particularly in lysosome and lymphocyte activity. According to Abdel-Tawwab et al,⁴⁴ sweet basil oil feeding resulted in a significant increase in Indian shrimp's LYZ and PO activities. Luteolin is recognized as the main component of the plant's antioxidant activity.¹²

Biochemical examinations are an essential tool to assess aquatic animals’ ability to adapt to rearing conditions and their nutritional and health status. TP, as a significant signal of the humoral defense system represents stress hormones, all defensive enzymes and metabolites circulating in the body's vital fluid.⁴⁵ According to our findings, high DME levels lead to an increase in TP and ALB, which could be connected to the increase in non-specific immune responses.⁴⁶ Indian shrimp fed diets enriched with sweet basil oil had significantly increased TP and ALB values, according to Abdel-Tawwab et al.⁴⁴ In thfe present study, the inclusion of DME in shrimp meals caused a significant decrease in AST and ALT activity compared to the control group, which imply that dietary D. moldavica extract may have hepato-renal protective effects. The decreased hemolysis and increased antioxidant capacity may be caused by lower AST and ALT activity.⁴⁷ Abdel-Tawwab et al⁴⁴ discovered that sweet basil oil was able to reduce the AST, ALT, creatinine, and urea values of Indian shrimp. The limitations of this research were that it was not possible to keep shrimps due to the lack of facilities. Perhaps if the culture period was longer, significant differences would have been better shown in higher doses of the extract.

Conclusions

According to the present study, feeding P. vannamei on diets supplemented with 200 mg DME/kg feed resulted in higher growth indices also improving immunity and antioxidant defense may be achieved through the use of DME in dietary supplements. In practical diets, P. vannamei can be boosted for growth, health, antioxidant, and immunological function by taking 200 mg/kg of DME.

Footnotes

Acknowledgments

The authors would like to thank Behbahan Khatam Alanbia University of Technology

Data Availability Statement

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

Declaration of Conflicting Interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Ethical Approval

Ethical Approval is not applicable for this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Statement of Human and Animal Rights

This article does not contain any studies with human or animal subjects.

Statement of Informed Consent

There are no human subjects in this article and informed consent is not applicable.

ORCID iD

Laleh Mosavi Dehmordi

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Antioxidant and Immunological Properties of Dracocephalum moldavica Extract in Penaeus vannamei

Abstract

Keywords

Introduction

Materials and Methods

Experimental Animals

Preparation of DME

Preparation of Diet

Growth Performance Indices

Chemical Analysis of Carcass

Plasma Antioxidant, Innate Immunity and Biochemical Analyse

Statistical Analysis

Results

Growth Indices and Mortality Parameter

Carcass Composition

Immune Responses and Antioxidant

Biochemical Parameters

Discussion

Conclusions

Footnotes

Acknowledgments

Data Availability Statement

Declaration of Conflicting Interests

Ethical Approval

Funding

Statement of Human and Animal Rights

Statement of Informed Consent

ORCID iD

References