Potentiality of Moringa oleifera aqueous extract as a growth modulator and antistress in acute hypoxic Nile tilapia
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
Iranian Journal of Fisheries Sciences 19(1) 67-84 2020
DOI: 10.22092/ijfs.2019.119208
Potentiality of Moringa oleifera aqueous extract as a growth
modulator and antistress in acute hypoxic Nile tilapia
Oreochromis niloticus
Shourbela R.M.1; El-Hawarry W.N.1*; Abd El-Latif A.M.2; Abo-
Kora S.Y.3
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
Received: April 2017 Accepted: December 2017
Abstract
This study aims to get a comprehensive evaluation of the growth promoting effects and
the hypoxic stress relief potentiality of Moringa oleifera aqueous extracts. Oreochromis
niloticus fingerlings were arbitrarily allocated into five duplicated fish groups (30 fish
tank-1). The fish groups were labeled according to the M. oleifera aqueous extract
dietary inclusion level (G1:G5). MOAE had fundamentally promoted tilapia growth.
Serum total protein levels were considerably higher in the M. oleifera fed fish, whereas
the levels of liver enzymes diminished significantly in G5 fish. Additionally, the dietary
M. oleifera resulted in a noticeable hypoglycemic effect together with a pronounced
decline in the antioxidant activities. The use of M. oleifera supplemented diet decreased
the hypoxia-related stress as conveyed by the gradual descent in the serum cortisol
levels of the hypoxic-stressed tilapia. This study proposes the potentiality of M. oleifera
aqueous extract as a growth promoter, antistress and antioxidants. It also validates its
safe application in commercial tilapia culture. Future study is required to comprehend
the influence of this plant extract in relieving chronic stress and its possible toxic effect
as well. Feasibility study for its commercial usage is required too.
Keywords: Plant extracts, Moringa oleifera, Oreochromis niloticus, Growth,
Antioxidant activity, Hypoxic stress.
1-Department of Animal Husbandry and Animal Wealth Development, Faculty of
Veterinary Medicine, Alexandria University, Edfina, 22758, Rosetta line, Egypt.
2-Department of Fish Diseases and Management, Faculty of Veterinary Medicine,
Benha University, Egypt.
3-Department of Pharmacology, Faculty of Veterinary Medicine, Benha University,
Egypt.
*Corresponding author's Email: waleed.elhawarry@alexu.edu.eg68 Shourbela et al., Potentiality of Moringa oleifera aqueous extract as a growth modulator and…
Introduction had evolved regarding the consumer
Tilapia is a popular aquatic species perceptions as influenced by safety and
being cultured worldwide. In 2012, the quality of the animal crop. In this
world tilapia production had boomed to manner, imperative needs to search
reach 4.5 MT (FAO, 2014) and is different choices to antimicrobials were
anticipated to increase exponentially of primary concerns. Such choices
over the coming years. Indeed, Tilapia would guarantee better growth
intensification is an essential requisite performance and pathogens control and
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
to cover the existent necessity for fish afterward, would polish the sustainable
protein. The generated stress and fish production under intensive culture
limited disease control associated with systems. Plants are the warehouses of
intensive aquaculture have made sound safe and inexpensive chemicals. Natural
management and biosecurity critical plants may represent better substitutes
challenges to aquaculture (Kautsky et for antimicrobials in aquaculture as
al., 2000; Schreck, 2000; Moss et al., they impound various actions like
2012). As an important water quality growth enhancement, antimicrobial and
criterion; Dissolved oxygen (DO) may antioxidant activities together with their
represent a significant constraint for antistress potentialities (Reverter et al.,
successful aquaculture. For instance 2014). Indeed, this is related to the
oxygen depletion may occur under several active constituents they have,
different culture conditions especially such as pure volatile oils, alkaloids,
in intensive culture systems prompting phenolics, terpenoids, saponins,
fish hypoxia. Hypoxia has many flavonoids and numerous other
adversative consequences on cultured compounds (Anwar et al., 2007;
fish. It can antagonistically affect varied Chakraborty and Hancz, 2011;
kind of physiological and biochemical Huyghebaert et al., 2011).
activities including growth (Wang et The drumstick tree, Moringa
al., 2009) and hematological indices oleifera, is angiosperm plant
along with stress response stimulation demonstrating varied and valuable
(Simi et al., 2016). impacts, in accord to the plant part and
Antimicrobials and other chemicals inception. Different portions of this
are regularly administered as additives plant have been used all through history
in fish diets or water baths as growth for its nourishing and healing
promoters, prophylactics or importance (Mbikay, 2012; Leone et
therapeutants (Bulfon et al., 2015). al., 2015). The seeds, for instance,
Their continuous application resulted in possess potential antimicrobial action
various adversarial effects for the against certain pathogens. They also
environment and health safety (Menz et can be utilized for water cleansing since
al., 2015). Accordingly, numerous they contain particular proteins with
countries have rigid regulations that coagulation properties (Nikkon et al.,
limit their application in aquaculture. In 2003; Suarez et al., 2003).
this concern, a new worldwide trend Nevertheless, the information availableIranian Journal of Fisheries Sciences 19(1) 2020 69
about its influences on the immune selected and gathered from one area
response, antioxidant activity and (Abu-hammad, Sharkia, Egypt). The air
growth of various fish species including dried leaves were crushed using mortar
Nile tilapia Oreochromis niloticus. To and pestle. The Bioactive substances of
the best of our information, there is no M. oleifera leaves were extracted using
data in the literature on the influence of infusion technique. The leaves were
dietary M. oleifera, in evoking a better immersed in distilled water for 24 h
fish response to stressful culture using 1:2 ratios (weight /volume)
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
conditions, such as hypoxia. Therefore; (Fernandez, 1990). After that, a suction
this study aims to get a comprehensive apparatus and doubled Whatman no. 1
evaluation of growth promoting effect filter paper used to spate the debris and
of M. oleifera aqueous extracts filtrate. Then a concentrated filtrate was
(MOAE) on O. niloticus fingerlings. In obtained through a vacuum rotary
addition, the MOAE influences on the evaporator (Buchi R-110 Rotavapor,
enzymes antioxidant activities and Switzerland) at (40°C) the dry extract
some serum biochemical indices of kept frozen at 0°C.
acutely hypoxic Nile tilapia fingerlings.
Diet preparation
Materials and methods Five diets were prepared (Table 1),
Fish and rearing include the control one which was non-
Apparently, healthy monosex tilapia M. oleifera supplemented diet and the
fingerlings obtained from a private fish other four ones were supplemented with
hatchery at Kafr El Sheikh graded levels (50, 100, 200 and 400 mg
Governorate, Egypt. The fish were Kg-1 diet) of M. oleifera watery extract.
transferred into polyethylene bags filled Then, tap water was added to each until
with oxygen to the Lab of Fish a firm paste was acquired. Each doughy
Breeding and production, Vet. Med, diet was then separately passed through
Alex. University, Egypt. Fingerlings a mincer with a 16 mm die, the resulted
were firstly acclimated in rectangular strands were gently broken into pellets,
white plastic tanks (500 L capacity) air dried at ambient temperature for two
supplied with 300 L of underground days and finally kept at 4°C in plastic
freshwater and equipped with bags till need.
individual biofilters along with constant
air supply. During the adaptation Experimental setup and fish
period, fish were fed twice daily (09:00; management
14:00) with a diet previously After adaptation periods, fish with an
formulated to obtain a 30% crude average body weight of 4.48±0.22 g
protein. and average body length of 6.27±0.19
cm were arbitrarily allocated into five
Preparation of aqueous extract of M. replicated fish groups (two replicates
oleifera leaves group-1). The fish groups were
Mature leaves of M. oleifera were differentiated according to the MOAE70 Shourbela et al., Potentiality of Moringa oleifera aqueous extract as a growth modulator and…
dietary inclusion level. They were day (09:00; 14:00), six days a week
labeled as G1; fed a control diet (0% until apparent satiation. Likewise, the
MOAE kg-1 feed), G2; fed 50 mg adaptation period, the water quality of
MOAE kg-1 feed, G3; fed 100 mg each tank was similarly preserved and
MOAE kg-1 feed, G4 was fed 200 mg managed throughout the experimental
MOAE kg-1 feed and G5; fed 400 mg period. Moreover, 1/3 of the water in all
MOAE kg-1 feed. The stocking density tanks was replaced each other day.
was maintained at 30 fish tank-1. One Accordingly, the tanks water quality
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
day after stocking, each fish group was was within the permissible limits
hand-fed with its corresponding diet. (temperature; 26±0.42 °C, pH;
The trial was continued for 60 days, 7.87±0.36, and DO; 6.94±0.56 mg L-1).
with a feeding frequency two times per
Table 1: Composition and proximate analysis of the basal
diet (g 100 g-1 dry matter).
Feed ingredients Proportion
Fish meal (60%) 16
Soybean meal (47%) 27.5
Yellow corn 27
Rice bran 13
Wheat bran 15
Dicalcium phoshate 1
Methionin 0.05
Cholin chloride 0.05
Vitamin and mineral premix* 0.2
Binder 0.2
Total 100
Composition Proximate analysis
(%)
Dry matter 88.09
Crude protein 29.33
Crude Fiber 5.58
Ash 8.15
*Vitamin mineral premic (Technomix) (quantity per 1 kg).
Vitamin premix: Vitamin-A: 12,000,000 IU; Vitamin-D3:
2,000,000 IU; Vitamin-E: 10,000 mg; Vitamin-K3: 2,000 mg;
Vitamin-B1: 1,000 mg; Vitamin-B2: 5,000 mg; Vitamin-B6:
15,000 mg; Vitamin-B12: 1.0 mg; Biotin: 50 mg; Pantothenate:
10,000 mg; Nicotinic acid: 30,000 mg; Folic acid: 1,000 mg.
Mineral premix (mg per 2 kg): FeSO4: 30,000; ZnSO4:
50,000; MnSO4: 60,000; CuSO4: 10,000; calcium iodine:
1,000; cobalt: 100; choline: 250,000.Iranian Journal of Fisheries Sciences 19(1) 2020 71
Fish growth and survival step with Lowry et al. (1951) and Drupt
The body weight and the total length of et al.(1974). Immunoglobulin M (IgM)
all experimental fish groups were noted was assessed via spectrophotometric
24 h after the end of the feeding trial. examination of fish serum. Also, the
The performance data and the survival hepatic transaminase activities (ALT
rate (%) were appraised; and AST) were tested in serum based
Weight gain (g)=W2-W1 on the method displayed by Reitman
Average daily gain (g day-1)= and Frankel (1957). Whereas serum
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
(W2-W1)/ T urea levels were analyzed according to
Specific growth rate (% day-1)= Fawcett and Scott (1960) and creatinine
[loge (W2)-loge (W1)/ T]×100 levels were estimated after Husdan and
Condition factor (K)=(W/L3)× Raporpot (1968). Serum glucose levels
100 were evaluated by the methodology of
Where; W2 is final weight (g), W1 is Cooper and Mc Daniel (1970).
initial weight (g), T is the trial period
(days), L is total length (cm). Antioxidant enzymes assay
Hepatosomatic index (%)=[liver From each replicates three randomly
weight/W]×100 selected fish were seined and
Survival rate (%)=[Number of survived transferred directly into an anesthetic
fish / initial number of fish]×100 containing water. Each fish was then
dissected and the liver was extracted,
Biochemical parameters cleaned by 0.9% NaCl solution. After
To evaluate some of the biochemical that, each liver was homogenized in a
parameters, blood samples (three cooled phosphate buffer saline (pH 7.2
anesthetized fish tank-1) were collected at a ratio 1: 10) using electro-
from either the heart or the caudal homogenizer (Heidolph, Germany).
vessels 24 h after the last diet. The homogenate was then centrifuged
Hypodermic syringes were used to get (13,000 ×g at 4°C for 10 min) and the
the blood samples which were then supernatant was pipetted and stored at -
transmitted to Wassermann tubes. The 80°C until analysis. The antioxidant
serum samples were obtained through enzymes assay comprised; superoxide
allowing blood clotting at room dismutase (SOD), Glutathione
temperature for 45 min then centrifuged peroxidase (GPX), (Glucose 6-
at 3000 rpm (Hettich Centrifuge, phosphate dehydrogenase (G6PDH)
Tuttlingen, Germany) for 15 minutes and Nitric oxide (NO) which were
(Burnett et al., 2011). The sera were analysed according to Paglia and
pipetted into Eppendorf tubes, labeled Valentine (1967), Nishikimi et al.
and hold on in deep freeze at -20 °C for (1972), Bautista et al. (1988) and Van
further biochemical analysis. Bezooijen et al. (1998); respectively.
Biochemical indices such as total
protein and albumin were measured in Acute hypoxic stress
Toward the completion of this trial,72 Shourbela et al., Potentiality of Moringa oleifera aqueous extract as a growth modulator and…
tilapia from various treated tanks were inclusion level. Fish fed MOAE
exposed to acute hypoxic stress. The supplemented ration expressed
tilapia fish were retained out of their significantly (p0.05)
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
later from the same fish were sourced affected by the MOAE diet
out of water for blood sampling to supplementation.
detect the post-hypoxia cortisol profile Dietary MOAE significantly
(Knobil, 1980). (pIranian Journal of Fisheries Sciences 19(1) 2020 73
serum glucose concentrations.
Table 2: Growth performance of Oreochromis niloticus fed dietary Moringa oleifera aqueous
extract supplementation for 60 days.
Treatments
Dietary M. oleifera extract mg kg-1diet
Parameters 0 (Control) 50 100 200 400
IBW(g) 4.45±0.24 4.53±0.23 4.53± 0.24 4.48±0.23 4.40±0.12
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
FBW (g) 24.88±1.97c 28.58±0.76b 29.58±0.72b 26.88±1.94c 31.76±1.09a
WG (g) 20.43±2.18d 24.05±0.76b 25.05±0.72b 22.40±1.88c 27.36±1.02a
ADG(g day-1) 0.34±0.03d 0.40±0.01bc 0.41±0.01b 0.37±0.03c 0.45±0.01a
SGR (% day-1) 1.24± 0.09c 1.33± 0.03b 1.35±0.04b 1.29±0.05bc 1.43±0.02a
FCR (%) 1.79±0.16a 1.51±0.04b 1.37±0.04c 1.55±0.18b 1.28±0.06c
FL(cm) 11.60±0.43b 11.98±0.31b 12.23±0.61ab 12.01±0.51b 12.66±0.59a
CF 1.76±0.20 1.87±0.13 1.84±0.15 1.82±0.28 1.79±0.15
SR (%) 96.65±4.73 96.65±4.73 96.65±4.73 91.65±2.33 91.65±2.33
HSI (%) 1.74±0.27ab 1.67±0.17b 1.97±0.19a 2.02±0.22a 2.22±0.25a
Data are expressed as means±standard deviations. Values with the same superscripts of the same row are
not significantly different (p>0.05). Where, IBW= initial body weight, FBW=final body weight,
WG=weight gain, ADG=average daily gain, SGR=specific growth rate, FCR=food conversion ratio,
FL=fish length, CF=condition factor, HSI=Hepatosomatic Index.
Table 3: Some biochemical parameters, liver and kidney functions of Oreochromis niloticus 60 days
after dietary Moringa oleifera aqueous extract supplementation.
Treatments
parameters Dietary M. oleifera extract mg kg-1diet
0 (Control) 50 100 200 400
Total protein (g) 4.0±0.80b 5.16±1.26ab 5.15±1.05ab 5.23±1.43ab 6.20±1.89a
Serum IgM (μg ml-1) 117.34±14.24b 127.19±34.94ab 125.56±16.16ab 150.15±44.86a 112.77±11.62b
Albumin (g dl-1) 1.88±0.14 1.96± 0.52 1.89± 0.39 2.10±0.34 2.03±0.52
AST (U L-1) 58.08±12.64a 56.08±14.45a 56.50±11.00a 55.72±9.98a 44.00±6.28b
ALT ( U L-1) 39.33±19.93a 40.16± 14.62a 38.26±16.13a 40.98±18.64a 31.33±10.35b
Urea (mg dl-1) 13.14±1.78a 10.89± 2.60ab 9.10±1.57b 11.16±3.37ab 11.17±2.64ab
Creatinine (mg dl-1) 0.73±0.09 0.73±0.10 0.71±0.08 0.65±0.20 0.80±0.11
a b b a
Blood glucose (mg dl-1) 115.33±7.17 89.16±16.57 79.00±13.79 133.00±31.90 85.50±19.36b
Data are expressed as means ± standard deviations. Values with the same superscripts in the same row
are not significantly different (p>0.05).
Additionally, the dietary MOAE pronounced decrease in the SOD, GPX,
received fish groups showed a G6PDH and NO activities (Table 4).74 Shourbela et al., Potentiality of Moringa oleifera aqueous extract as a growth modulator and…
The dietary MOAE supplementation On the contrary to pre-hypoxic
had also triggered a substantial (pIranian Journal of Fisheries Sciences 19(1) 2020 75
Discussion increment in growth and diet utilization
MOAE was recently verified to possess could be related to its immuno-
a valuable range of active substances. nutritional components and the high
They possess growth promoting, feed digestibility, absorption and
antioxidant, tissue protective (liver, assimilation ability, through the
kidneys, heart and testes), anti-stressor, augmented digestive enzymes and
and immunomodulatory activities in healthy intestinal microflora boosted by
fish (Alishahi et al., 2010; Stadtlander the M. oleifera prebiotic activity.
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
et al., 2013). This study clarified that In the meantime, the usage of either
feeding tilapia with MOAE containing raw M. oleifera or its extracts as a
diet enhanced the growth performance dietary supplement or protein
of O. niloticus fingerlings distinctly. replacement has shown variable results.
The FCR was improved as the dietary Feeding Moringa leaf meal to Nile
inclusion level of MOAE increased. tilapia at a dietary inclusion level up to
Fish received 400 mg MOAE kg-1 had a 8-10% of the diets hindered tilapia
markedly high WG, SGR, and ADG. growth (Richter et al., 2003; Yuangsoi
The ethanolic extract of M. oleifera and Charoenwattanasak, 2011; Abo-
flower (250 and 500 mg kg-1 diet) as State et al., 2014). Similarly, Afuang et
well had improved tilapia growth al. (2003) incorporated methanol-
(Tekle and Sahu, 2015). Also, a extracted leaf meal containing fewer
growth-promoting potential of M. saponins and phenolics in the diets (at a
oleifera seed protein extracts was 30% inclusion level) of tilapia
reported by Stadtlander et al. (2013) fingerlings. The fish performance was
when added to tilapia diet at 400 mg kg- not hindered, but the body protein
1
in an eight weeks experimental period. content reduced. Whereas, the aqueous
Not only this but also the dried powder extracted leaf meal (15% of the diet)
of M. oleifera leaves (10 mg kg diet-1) had reduced the feed intake, feed
was able to promote the growth of utilization and fish performance
juveniles of Penaeus indicus as (Madalla, 2008). Also, Dongmeza et al.
reported by Rayes (2013). (2006) reported a considerable decrease
M. oleifera leaves is said to contain in the Nile tilapia feed intake and
vast amount of immuno- nutritional consequently its growth after receiving
components such as proteins, lipids, different dietary moringa leaf extracts
vitamins, enzymes, minerals, sugar, (tannin-reduced, saponin-reduced and
saponin and salicylates and other active saponin-enriched).
constituents (Leone et al., 2015). Measurement of the plasma
Moreover, Heidarieh et al. (2013) biochemical parameters is a
indicated that M. oleifera had enhanced fundamental step to judge the health
the gastrointestinal morphology of O. integrity of any aquatic species
mykiss (increased villi length) which (Ferreira et al., 2007). Plasma proteins
improved the food digestibility and carry out many functions, such as
absorption capacity. Herein, the adjusting the water balance in fish76 Shourbela et al., Potentiality of Moringa oleifera aqueous extract as a growth modulator and…
(Rudneva and Kovyrshina, 2011) and diminishing in the activity
the protective effects implemented by aminotransferase enzymes. This result
the body for the elimination of any supports the previous studies that
microorganisms (Gerwick et al., 2002). convey the potentiality of M. oleifera
This study displayed an increased level leaves extract to protect the membrane
of plasma protein in the dietary MOAE integrity of tilapia hepatocytes against
supplemented fish. Similar conclusions stressors (Tekle and Sahu, 2015). Also,
were revealed by Alishahi et al. (2010) the increased growth rate conveyed in
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
and Haghighi et al. (2014) who the current study give further support
informed that 0.5% and 1% M. oleifera for the liver integrity as a vital organ
dietary supplementation had implemented in the normal metabolic
significantly improved the serum total function of any aquatic organism.
protein and globulin in Cyprinus carpio Creatinine and urea are among the
and O. mykiss respectively. Conversely, dominant biochemical indices
the serum total protein levels obtained particularly determined to assess renal
in this work could not agree with either condition (Gross et al., 2005; Adeyemi
Dotta et al. (2014) for O. niloticus and Akanji, 2012). The fish received
(0.5% M. oleifera) nor Kavitha et al. 100 mg MOAE kg-1 exhibited a
(2012) for Cyprinus carpio (exposed to significant decrease in the urea level.
124.0 mg L-1 M. oleifera extract). They Such reduction may offer a further
reported that M. oleifera dietary support of the nephron-protection
supplementation was unable to activity of M. oleifera as reported by
considerably elevate the total serum Anwar et al. (2007) and Sharma and
protein in those fish as an outcome of Paliwal (2012). Also, the comparable
the metabolic degradation and creatinine levels distinguished in
utilization of protein. differently treated fish groups provide
Transaminase enzymes are of further support to the nephron-
dynamic importance in protein and protective potentiality of MOAE.
carbohydrate metabolism. Their levels Nevertheless, our results are dissimilar
(i.e. transaminases; AST and ALT) are to Mazumder et al. (1999) who clarified
used for judging the physiological and that a weekly dose (>46 mg kg-1 b.wt
healthy state of aquatic species extract) of M. oleifera methanol root
(Vutukuru et al., 2007). Therefore, they extracts had impaired function of mice
are indicative of organ dysfunction, kidney. Oyagbemi et al. (2013) as well
especially for hepatic dysfunction with reported elevated serum creatinine
a subsequent leakage of enzymes into levels in rats administered M. oleifera
the blood (Gabriel and George, 2005). (200 and 400 mg kg-1 b.w.).
The aminotransferase activities were Regarding the blood glucose levels
comparable among all the treated verified in the current study; the MOAE
groups except for the group fish supplemented diet had hypoglycemic
supplemented with 400 mg MOAE kg effect in all of the treated fish groups.
diet-1 which displayed a reasonable Similarly, fish received herbal additivesIranian Journal of Fisheries Sciences 19(1) 2020 77
showed hypoglycemia (Metwally, (polyphenols, glycosides, anthocyanin,
2009; Banaee et al., 2011; Ojha et al., tannins and thiocarbamates). These
2014). MOAE had successfully active compounds expel free radicals,
governed the glucose level in rabbits active antioxidant enzymes and inhibit
(Makonnen et al., 1997) and rats (Amin oxidases (Luqman et al., 2011) which
et al., 2016). The moringa leaf juices give a further clarification for the M.
contain α-glucosidase and amylase oleifera associated antioxidant activity.
inhibitors. These enzymes prevent the Furthermore, this study revealed that
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
assimilation of glucose into absorbable acutely hypoxic tilapia had exhibited an
metabolites, hence preventing the elevation in the cortisol level 30
increase in blood glucose (Abdulkarim minute's post-hypoxic stress. The
et al., 2005). elevated cortisol level was reduced
On the contrary; diabetes inducing distinctly two hours post-hypoxic stress
property was verified to green tea in those fish received 200 and 400 mg
extract indicated by the observed MOAE kg-1 feed. The retrieval towards
hyperglycemia in green tea extract normal cortisol level following MOAE
exposed Nile tilapia (Abdel-Tawwab et pretreatment proposed
al., 2010). hypocortisolemic effects of MOAE.
SOD and GPX are sensitive Additionally, the potent antioxidants of
oxidative stress biomarkers. They are Moringa supplemented diets was said to
considered the core line of the body be useful in compromising the
antioxidant defensive mechanism (Jiang adversative properties of stress related
et al., 2009). SOD is a dynamic enzyme hypoxia. Production of oxidative
responsible for both scavenging ROS radicals (especially ROS) is thought to
and protection of cells from being be boosted under hypoxic stress
damaged by free radicals (Chien et al., (Chandel and Budinger, 2007).
2003). In our study, the MOAE Accordingly, these inclusion levels
supplementation considerably were possibly capable of blocking the
diminished the SOD and GPX activity, hypercortisolemia elicited by the acute
indicating that M. oleifera might have stress caused by hypoxia or efficiently
the capability to reduce peroxide restored the homeostatic equilibrium of
radicals and converting it into oxygen the life helping physiological systems
and water due to an antioxidant (Van Rijn and Reina, 2010). Hammed
potential (Atli and Canli, 2007). M. et al. (2015) also reported that extracts
oleifera could also preserve the cell of Moringa leaves infiltrate to the cell
redox state by restricting the damaging membrane lipid bilayer, resulting in
effects of ROS (Halliwell and improved permeability, and ROS
Gutteridge, 2007). Furthermore, the elimination. Hence these fish groups
MOAE dietary supplementation could successfully tolerate and recover
resulted in reduced activity of other the hypoxic stress than the others. This
antioxidant enzymes. M. oleifera study verified the potentiality of M.
contains active biological compounds oleifera aqueous extract as a growth78 Shourbela et al., Potentiality of Moringa oleifera aqueous extract as a growth modulator and…
promoter, antistress and antioxidant for Evaluation of feeding raw moringa
O. niloticus fingerlings. M. oleifera (Moringa oleifera Lam.) leaves meal
aqueous extracts are proposed to in Nile tilapia fingerlings
replace synthetic antimicrobials and (Oreochromis niloticus) diets.
growth promoters. This study is Global Veterinaria, 13(1), 105-111.
valuable to validate the safe Adeyemi, O.S. and Akanji, M.A.,
administration of M. oleifera in 2012. Psidium guajava leaf extract:
commercial tilapia culture. In this Effects on rat serum homeostasis and
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
concern, future studies are required to tissue morphology. Comparative
comprehend the influence of this plant Clinical Pathology, 21(4), 401-407.
extract in relieving chronic stress and Afuang, W., Siddhuraju, P. and
its possible toxic effect as well. Becker, K., 2003. Comparative
Feasibility study for its commercial nutritional evaluation of raw
usage is required too. methanol extracted residues and
methanol extracts of moringa
Acknowledgements (Moringa oleifera Lam.) leaves on
This work was supported by the growth performance and feed
department of Animal Husbandry and utilization in Nile tilapia
Animal Wealth Development, Faculty (Oreochromis niloticus
of Veterinary Medicine, Alexandria L.). Aquaculture Research, 34(13),
University, Egypt. 1147-1159.
Alishahi M, Ranjbar, M.,
References Ghorbanpoor, M., Peyghan, R.
Abdel‐Tawwab, M., Ahmad, M.H., and Mesbah, M., 2010. Effects of
Seden, M.E. and Sakr, S.F., 2010. dietary Aloe vera on some specific
Use of green tea, Camellia sinensis and nonspecific immunity in the
L., in practical diet for growth and common carp (Cyprinus carpio).
protection of Nile tilapia, International Journal of Veterinary
Oreochromis niloticus (L.), against Research, 4(3), 189-195.
Aeromonas hydrophila Amin, A.Y., El Tobgy, K.M.K.,
infection. Journal of the World Salam, A. and Hemat, S., 2016.
Aquaculture Society, 41, 203-213. Phytochemical detection and
Abdulkarim, S.M., Long, K., Lai, Therapeutical properties of Moringa
O.M., Muhammad, S.K.S. and oleifera leaves. International
Ghazali, H.M., 2005. Some Journal of Chem Tech Research,
physico-chemical properties of 9(9), 156-168.
Moringa oleifera seed oil extracted Anwar, F., Latif, S., Ashraf, M. and
using solvent and aqueous enzymatic Gilani, A.H., 2007. Moringa
methods. Food Chemistry, 93(2), oleifera: A food plant with multiple
253-263. medicinal uses. Phytotherapy
Abo-State, H., Hammouda, Y., El- Research, 21(1), 17-25.
Nadi, A. and AboZaid, H., 2014.Iranian Journal of Fisheries Sciences 19(1) 2020 79
Atli, G. and Canli, M., 2007. culture. Reviews in Aquaculture,
Enzymatic responses to metal 3(3), 103-119.
exposures in a freshwater fish Chandel, N.S. and Budinger, G.S.,
Oreochromis niloticus. Comparative 2007. The cellular basis for diverse
Biochemistry and Physiology Part responses to oxygen. Free Radical
C: Toxicology and Biology and Medicine, 42(2), 165-
Pharmacology, 145(2), 282-287. 174.
Banaee, M., Sureda, A., Mirvaghefi, Chien, Y.H., Pan, C.H. and Hunter,
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
A.R. and Rafei, G.R., 2011. Effects B., 2003. The resistance to physical
of long-term silymarin oral stresses by Penaeus monodon
supplementation on the blood juveniles fed diets supplemented
biochemical profile of rainbow trout with astaxanthin. Aquaculture,
(Oncorhynchus mykiss). Fish 216(1), 177-191.
Physiology and Biochemistry, 37(4), Cooper, G.R. and McDaniel, V.,
885-896. 1970. The determination of glucose
Bautista, J., Garrido-Pertierra, A. by the ortho-
and Soler, G., 1988. Glucose-6- toluidine method (filtrate and direct
phosphate dehydrogenase from procedure). Standard Methods of
Dicentrarchus labrax liver: Kinetic Clinical Chemistry. 6, 159-170.
mechanism and kinetics of NADPH Dongmeza, E., Siddhuraju, P.,
inhibition. Biochimica et Biophysica Francis, G. and Becker, K., 2006.
Acta (BBA)-General Effects of dehydrated methanol
Subjects, 967(3), 354-363. extracts of moringa (Moringa
Bulfon, C., Volpatti, D. and Galeotti, oleifera Lam.) leaves and three of its
M., 2015. Current research on the fractions on growth performance and
use of plant‐derived products in feed nutrient assimilation in Nile
farmed fish. Aquaculture tilapia (Oreochromis niloticus
Research, 46(3), 513-551. (L.)). Aquaculture, 261(1), 407-422.
Burnett, B.P., Pillai, L., Bitto, A., Dotta, G., de Andrade, J.I.A.,
Squadrito, F. and Levy, R.M., Gonçalves, E.L.T., Brum, A.,
2011. Evaluation of CYP450 Mattos, J.J., Maraschin, M. and
inhibitory effects and steady-state Martins, M.L., 2014. Leukocyte
pharmacokinetics of genistein in phagocytosis and lysozyme activity
combination with cholecalciferol and in Nile tilapia fed supplemented diet
citrated zinc bisglycinate in with natural extracts of propolis and
postmenopausal women. Aloe barbadensis. Fish and Shellfish
International Journal of Women’s Immunology, 39(2), 280-284.
Health, 3(1), 139-150. Drupt, F., Paris, M., Frydman, A.
Chakraborty, S.B. and Hancz, C., and Leclerc, M., 1974. Serum
2011. Application of phytochemicals albumin assay by bromocresol green
as immunostimulant, antipathogenic method: Application to different
and antistress agents in finfish automatic apparatus. Annales80 Shourbela et al., Potentiality of Moringa oleifera aqueous extract as a growth modulator and…
Pharmaceutiques Francaises, (Vol. Caramori, M.L. and Zelmanovitz,
32(5), 249). T., 2005. Diabetic nephropathy:
FAO., 2014. Food and agricultural Diagnosis, prevention, and
organisation of the United Nations. treatment. Diabetes Care, 28(1),
The state of world Fisheries and 164-176.
Aquaculture 2014. Rome. Italy. Haghighi, M., Rohani, M.S.,
Fawcett, J.K. and Scott, J.E., 1960. Pourmoghim, H., Toliat, T.,
Enzymatic, colorimetric method for Samadi, M., Tavoli, M., Islami, M.
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
determination urea in serum, plasma and Yusefi, R., 2014. Haemato-
and urine. Journal of Clinical immunological indices in rainbow
Pathology. 13, 156–162. trout (Oncorhynchus mykiss) fry fed
Fernandez, T.J., 1990. Medicinal with Aloe vera extract supplemented
plants for Haemophilus feed. Journal of Coastal Life
gallinarum infection in chickens. Medicine, 2, 350-356.
ASEAN Journal on Science and Halliwell, B. and Gutteridge, J.M.C.,
Technology for Development, 7(22), 2007. Antioxidant defences:
99-107. Endogenous and diet derived. Free
Ferreira, J.G., Hawkins, A.J.S. and Radicals in Biology and Medicine, 4,
Bricker, S.B., 2007. Management of 79-186.
productivity, environmental effects Hammed, A.M ,Amosu A.O, Awe,
and profitability of shellfish A.F., and Gbadamosi, F.F., 2015.
aquaculture—the Farm Aquaculture Effects of Moringa oleifera leaf
Resource Management (FARM) extracts on bacteria (Aeromonas
model. Aquaculture, 264(1), 160- hydrophila) infected adults African
174. mud cat fish. International Journal
Gabriel, U.U. and George A.O.I., of Current Research, 7(10), 22117-
2005. Plasma enzymes in Clarias 22122.
gariepinus exposed to chronic levels Heidarieh, M., Mirvaghefi, A.R.,
of roundup (glyphosate). Journal of Sepahi, A., Sheikhzadeh, N.,
Ecology and Environment, 23(2), Shahbazfar, A.A. and Akbari, M.,
271–276. 2013. Effects of dietary Aloe vera on
Gerwick, L., Steinhauer, R., Lapatra, growth performance, skin and
S., Sandell, T., Ortuno, J., gastro-intestine morphology in
Hajiseyedjavadi, N. and Bayne, rainbow trout (Oncorhynchus
C.J., 2002. The acute phase response mykiss). Turkish Journal of Fisheries
of rainbow trout (Oncorhynchus and Aquatic Sciences, 13, 367-373.
mykiss) plasma proteins to viral, Husdan, H. and Rapoport, A., 1968.
bacterial and fungal inflammatory Estimation of creatinine by the Jaffe
agents. Fish and Shellfish reaction. Clinical Chemistry, 14(3),
Immunology, 12(3), 229-242. 222-238.
Gross, J.L., De Azevedo, M.J., Huyghebaert, G., Ducatelle, R. and
Silveiro, S.P., Canani, L.H., Van Immerseel, F., 2011. AnIranian Journal of Fisheries Sciences 19(1) 2020 81
update on alternatives to phenol reagent. Journal of
antimicrobial growth promoters for Biologival Chemistry, 193(1), 265-
broilers. The Veterinary 275.
Journal, 187(2), 182-188. Luqman, S., Srivastava, S., Kumar,
Jiang, W.D., Feng, L., Liu, Y., Jiang, R., Maurya, A.K. and Chanda, D.,
J. and Zhou, X.Q., 2009. 2011. Experimental assessment of
Myo‐inositol prevents oxidative Moringa oleifera leaf and fruit for its
damage, inhibits oxygen radical antistress, antioxidant, and
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
generation and increases antioxidant scavenging potential using in vitro
enzyme activities of juvenile Jian and in vivo assays. Evidence-Based
carp (Cyprinus carpio var. Complementary and Alternative
Jian). Aquaculture Research, 40(15), Medicine, 2012, 1-12.
1770-1776. Madalla, N., 2008. Novel feed
Kautsky, N., Rönnbäck, P., ingredients for Nile tilapia
Tedengren, M. and Troell, M., (Oreochromis niloticus L.). In: PhD
2000. Ecosystem perspectives on Thesis, Inst. Aquaculture, Univ.
management of disease in shrimp Stirling, Scotland, UK.
pond farming. Aquaculture, 191(1), Makonnen, E., Hunde, A. and
145-161. Damecha, G., 1997. Hypoglycaemic
Kavitha, C., Ramesh, M., Kumaran, effect of Moringa stenopetala
S.S. and Lakshmi, S.A., 2012. aqueous extract in
Toxicity of Moringa oleifera seed rabbits. Phytotherapy Research,
extract on some hematological and 11(2), 147-148.
biochemical profiles in a freshwater Mazumder, U.K., Gupta, M.,
fish, Cyprinus carpio. Experimental Chakrabarti, S. and Pal, D., 1999.
and Toxicologic Pathology, 64(7), Evaluation of hematological and
681-687. hepatorenal functions of methanolic
Knobil, K., 1980. Hormonal extract of Moringa oleifera Lam.
researches. Recent Progress in root treated mice. Indian Journal of
Hormone Research, 36, 52-58. Experimental Biology, 7, 21-25.
Leone, A., Spada, A., Battezzati, A., Mbikay, M., 2012. Therapeutic
Schiraldi, A., Aristil, J. and potential of Moringa oleifera leaves
Bertoli, S., 2015. Cultivation, in chronic hyperglycemia and
genetic, ethnopharmacology, dyslipidemia: A review. Frontiers in
phytochemistry and pharmacology Pharmacology, 3, 24.
of Moringa oleifera leaves: An Menz, J., Schneider, M. and
overview. International Journal of Kümmerer, K., 2015. Usage
Molecular Sciences, 16(6), 12791- pattern-based exposure screening as
12835. a simple tool for the regional
Lowry, O.H., Rosebrough, N.J., Farr, priority-setting in environmental risk
A.L. and Randall, R.J., 1951. assessment of veterinary antibiotics:
Protein measurement with the Folin82 Shourbela et al., Potentiality of Moringa oleifera aqueous extract as a growth modulator and…
A case study of north-western H.O., 2013. Toxicological
Germany. Chemosphere, 12, 42-48. evaluations of methanolic extract of
Metwally, M.A.A., 2009. Effects of Moringa oleifera leaves in liver and
garlic (Allium sativum) on some kidney of male Wistar rats. Journal
antioxidant activities in tilapia of Basic and Clinical Physiology and
nilotica (Oreochromis Pharmacology, 24(4), 307-312.
niloticus). World Journal of Fish Paglia, D.E. and Valentine, W.N.,
and Marine Sciences, 1(1), 56-64. 1967. Studies on the quantitative and
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
Moss, S.M., Moss, D.R., Arce, S.M., qualitative characterization of
Lightner, D.V. and Lotz, J.M., erthyrocyte glutathione peroxidase.
2012. The role of selective breeding Journal of Laboratory and Clinical
and biosecurity in the prevention of Medicine, 7, 158–169.
disease in penaeid shrimp Rayes, A.H., 2013. Study on the effect
aquaculture. Journal of Invertebrate of dietary probiotic bacteria
Pathology, 110(2), 247-250. Arthrobacter species, β-1, 3 glucan
Nikkon, F., Saud, Z.A., Rehman, and Moringa oleifera leaf on
M.H. and Haque, M.E., 2003. In protection of Penaeus indicus
vitro antimicrobial activity of the Juveniles from pathogenic Vibrio
compound isolated from chloroform harveyi. Researcher, 5(1), 24-31.
extract of Moringa oleifera Reitman, S. and Frankel, S., 1957. A
Lam. Pakistan Journal of Biological colorimetric method for the
Science, 22, 1888-1890. determination of serum glutamic
Nishikimi, M., Rao, N.A. and Yagi, oxalacetic and glutamic pyruvic
K., 1972. The occurrence of transaminases. American Journal of
superoxide anion in the reaction of Clinical Pathology, 28(1), 56-63
reduced phenazine methosulfate and Reverter, M., Bontemps, N.,
molecular oxygen. Biochemical and Lecchini, D., Banaigs, B. and
Biophysical Research Sasal, P., 2014. Use of plant extracts
Communications, 46(2), 849-854. in fish aquaculture as an alternative
Ojha, M.L., Chadha, N.K., Saini, to chemotherapy: Current status and
V.P., Damroy, S., Gupta, C.P. and future perspectives. Aquaculture,
Savant, P.B., 2014. Effect of 433, 50-61.
ethanolic extract of Pedalium murex Richter, N., Siddhuraju, P. and
on growth and haemato- Becker, K., 2003. Evaluation of
immunological parameters of Labeo nutritional quality of moringa
rohita. Proceedings of the National (Moringa oleifera Lam.) leaves as an
Academy of Sciences, India Section alternative protein source for Nile
B: Biological Sciences, 84(4), 997- tilapia (Oreochromis niloticus
1003. L.). Aquaculture, 217(1), 599-611.
Oyagbemi, A.A., Omobowale, T.O., Rudneva, I.I. and Kovyrshina, T.B.,
Azeez, I.O., Abiola, J.O., 2011. Comparative study of
Adedokun, R.A. and Nottidge, electrophoretic characteristics ofIranian Journal of Fisheries Sciences 19(1) 2020 83
serum albumin of round goby 2013. Effects of Moringa oleifera
Neogobius melanostomus from Lam. dietary seed protein extracts on
Black Sea and Azov growth, nutrient utilization and
Sea. International Journal of Science blood parameters in common carp
and Nature, 1, 131-136. (Cyprinus carpio, L.) and Nile
SAS., 2008. Statistical analysis system. tilapia (Oreochromis niloticus,
User’s Guide. SAS INT., Cary, NC. L.). Planta Medica, 79(13), PL21.
USA. Suarez, M., Entenza, J.M., Doerries,
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
Schreck, C.B., 2000. Accumulation C., Meyer, E., Bourquin, L.,
and long-term effects of stress in Sutherland, J., Marison, I.,
fish. In: Moberg, G.P., Mench, J.A. Moreillon, P. and Mermod, N.,
(Eds.), The Biology of Animal 2003. Expression of a plant‐derived
Stress: Basic Principles and peptide harboring water‐cleaning
Implications for Animal Welfare. and antimicrobial
CABI Publishing, CAB activities. Biotechnology and
International, Oxon and New York. Bioengineering, 81(1), 13-20.
pp. 147–158. Tekle, E.W. and Sahu, N.P., 2015.
Sharma, V. and Paliwal, R., 2012. Growth and immunodulatory
Chemo protective role of Moringa response of Nile tilapia Oreochromis
oleifera and its isolated saponin niloticus fingerlings to ethanolic
against DMBA induced tissue extract of Moringa oleifera flower.
damage in male mice: A International Journal of Scientific
histopathological analysis. and Research Publications, 5(7),
International Journal of Drug 285-296.
Development and Research, 4(4), Van Bezooijen, R.L., Que, I.,
215-228. Ederveen, A.G., Kloosterboer,
Simi, S., Peter, V.S. and Peter, M.S., H.J., Papapoulos, S.E. and Lowik,
2016. Zymosan-induced immune C.W., 1998. Plasma nitrate+ nitrite
challenge modifies the stress levels are regulated by ovarian
response of hypoxic air-breathing steroids but do not correlate with
fish (Anabas testudineus Bloch): trabecular bone mineral density in
Evidence for reversed patterns of rats. Journal of Endocrinology,
cortisol and thyroid hormone 159(1), 27-34.
interaction, differential ion Van Rijn, J.A. and Reina, R.D., 2010.
transporter functions and non- Distribution of leukocytes as
specific immune response. General indicators of stress in the Australian
and Comparative Endocrinology. swellshark, Cephaloscyllium
251, 94-108. laticeps. Fish and Shellfish
http://doi.org/10.1016/j.ygcen.2016. Immunology, 29(3), 534-538.
11.009 Vutukuru, S.S., Pauleena, J.S., Rao,
Stadtlander, T., Sander, C., Kumar, J.V. and Anjaneyulu, Y., 2007.
V., Makkar, H. and Becker, K., Architectural changes in the gill84 Shourbela et al., Potentiality of Moringa oleifera aqueous extract as a growth modulator and…
morphology of the freshwater fish,
Esomus danricus as potential
biomarkers of copper toxicity using
automated video tracking
system. Environmental
Bioindicators, 2(1), 3-14.
Wang, T., Lefevre, S., Van Cong, N.
andBayley, M., 2009. The effects of
Downloaded from jifro.ir at 3:44 +0430 on Monday April 13th 2020
hypoxia on growth and
digestion. Fish Physiology, 27, 361-
396.
Yuangsoi, B. and
Charoenwattanasak, S., 2011.
Utilization of moringa (Moringa
oleifera Lam.) leaf on growth
performance and protein digestibility
in Tilapia (Oreochromis niloticus
L.). Proceedings of the 49th
Kasetsart University Annual
Conference, Kasetsart University,
Thailand, 1-4 February, 2011. Vol.
3. Subject: Fisheries Kasetsart
University. pp. 317-326You can also read
