In vitro study of short-term antiparasitic effect of alcoholic
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Iranian Journal of Fisheries Sciences 20(4) 1138-1148 2021
DOI: 10.22092/ijfs.2021.124565
Research Article
In vitro study of short-term antiparasitic effect of alcoholic
extract of Terminalia catappa L. leaves on Ichthyophthirius
multifiliis theronts
Yazdani Anaraki E.1; Mirzargar S.S.1*; Rahmati Holasoo H.1,3; Sharif
zadeh A.2; Ebrahimzadeh Mousavi H.A.1
Received: November 2020 Accepted: January 2021
Abstract
Ichthyophthirius multifiliis is one of the parasitic diseases of fish infecting both farmed
and wild freshwater fishes at all ages. This parasite penetrates into the fish skin epidermis
and creates white spots on the skin accordingly, the disease caused by this parasite is also
called white spot disease. Formalin, chloramine-T, malachite green, and other chemical
compounds may be used against this disease; however, each of these compounds leads
to harm to humans and the environment in some way; hence, it seems necessary to find
natural alternative compounds to treat this disease. This study aimed at determining the
effectiveness of alcoholic extract of Terminalia catappa L. at different concentrations (0-
850 mg/L) and exposure times (1-3 h) in vitro. The findings were statistically compared
with those of the control and positive control groups (formalin at a dose of 15 ppm). The
results of the present study revealed that the effectiveness of T. catappa L. alcoholic
extract on the theront stage of the I. multifiliis parasite is a function of time and
concentration and with increasing concentration and time, its effect will enhance. The
results of this study indicated that after two hours, a dose of 850 mg/L killed 100% of the
theronts and it is the most appropriate dose, even though the possibility of applying this
dose to treat live fish should be investigated.
Keywords: White spot disease, Terminali catappa L., Ichthyophthirius, Acute toxicity,
Fatality rate, Antiparasitic effects, Theronts.
1-Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran,
Tehran, Iran.
2-Department of Microbiology and immunology, Faculty of Veterinary Medicine, University of
Tehran, Tehran, Iran.
3-Centre of Excellence for Warm Water Fish Health and Disease, Shahid Chamran University of
Ahvaz, Ahvaz, Iran.
*
Corresponding author's Email:zargarm@ut.ac.ir1139 Yazdani Anaraki et al., A study of short-term antiparasitic effect of alcoholic extract of...
Introduction mutagenic effects on humans and the
Both in tropical aquatic environments environment (Srivastava et al., 2004).
and temperate regions, one of the Other compounds like potassium
significant freshwater fish diseases, all permanganate (Straus and Griffin,
over the world, is Ichthyophthiriasis or 2002); sodium percarbonate (Buchmann
white spot disease caused by the ciliated et al., 2003); chloramine-T (Rintamaki-
Holotrich protozoa called kinnunen et al., 2005); hydrogen
Ichthyophthirius multifiliis (Matthews, peroxide (Rintamaki-kinnunenen et al.,
2005). This parasite results in significant 2005); copper sulfate (Rowland et al.,
economic losses in a wide range of 2009); formalin (Rowland et al., 2009),
farmed and wild fish species (Dickerson peracetic acid (Sudova et al., 2010), and
and Daw, 2006) and high mortality rate bronopol (Shinn et al., 2012) also have
in farmed and ornamental fish (Song et antiparasitic properties; however, these
al., 2015); so that it can kill farmed fish agents are often dangerous to human
at different ages (Aguilar et al., 2005). health and the environment (Tieman and
The rapid replication of this parasite, Goodwin, 2001). Hence, we have to find
displacement of infected hosts, as well as herbal medicine with both high-
the wide range of hosts are among the performance antiparasitic properties and
factors leading to the widespread no side effects on human health and
prevalence of this disease worldwide environment. In general, compared to
(Matthews, 2005; Forwood et al., 2015). chemical compounds, synthetics, and
The life cycle of this parasite is antibiotics, herbal compounds have rare
straightforward. Ich cyclically harmful side effects, while lacking
transforms between an obligate fish- toxicity and harmful accumulation in
associated trophont and a free-living living tissues, in some cases they are
reproductive stage, the tomont. The cheaper, degradable and reversible, and
theront is the infective stage of the compounds of plant origin are more
parasite (Woo, 2006). Since the environmental friendly compared to the
trophonts of this parasite are replaced in other substances (Citarasu et al., 2003).
deep skin and protect themselves from With the Persian name Garom Zangi,
the drugs commonly used to treat skin Terminalia catappa L. belongs to the
parasites and the theronts separate Combretaceae family (Cashew). This
themselves from the fish body, they are plant is widely grown in tropical areas,
the most sensitive step of parasite life such as East Asian countries. It is native
against treatment (Noga, 2011). to countries e.g. India, Malaysia,
Various combinations have been Cameroon, and Madagascar (Noumi and
reported to use against Ich. Malachite Yomi, 2001). Found in some southern
green is the most effective substance provinces of Iran, including Hormozgan
among these compounds to combat Ich. and Sistan and Baluchestan, Garom
Nevertheless, the use of malachite green Zangi is a tall tree of 25 meters height
is prohibited given its toxic and with horizontal branches (Zargari,Iranian Journal of Fisheries Sciences 20(4) 2021 1140
1988). In various countries, the leaves Materials and methods
and bark of this tree are extensively Preparation of Terminalia catappa L.
employed in traditional medicine. leaves
Antibacterial, antifungal, antiparasitic, Terminalia Catappa L. leaves were
anticancer, anti-inflammatory, anti- collected from Hormozgan province and
diabetic, antioxidant, and liver then, the samples were sent to the
protective properties are of the medical herbarium of the Faculty of Pharmacy,
properties which are reported for this University of Tehran to confirm the
plant (Anand, 2015). In addition to the desired plant, and the plant was
role of this plant in regulating pH, its definitively identified.
inhibitory feature against some bacteria
and parasites has been proven in Preparation of alcoholic extract of
aquaculture (Chitmanat et al., 2005; Terminalia catappa L.
Chansue, 2007; Lee et al., 2016; In order to get the extract, 175 g of
Nugroho et al., 2017). powder of fully dried leaves of the plant
Many studies have suggested that with 950 mL of fully soaked 96%
plant extracts can eliminate the free- methanol was placed in an incubator
living (floating) stages of Ich parasite shaker for 2 hours at 25 °C.
(Buchman et al., 2003; Ekanem et al., Subsequently, the sample was exposed
2004; Yao et al., 2010, 2011; Ling et al., to laboratory temperature for 18 hours.
2012; Yi et al., 2012). These studies After that, the mixture was filtered using
have revealed that some plants, such as Whatman filter paper, the supernatant
herbal medicine, have effective was isolated from the precipitate, and
antiparasitic properties. In fish and 750 mL of 96% methanol was added to
water, these compounds can be the remaining precipitate. This was
degradable and do not create any repeated for up to 4 days and all isolated
dangerous effect in human or supernatants were mixed together and
environmental health. As Ich disease is after refining, distilled by vacuum
very common in aquaculture, the use of distillation.
antiparasitic compounds extracted from
plants is a safe, modern and eco-friendly Isolation of Ich parasite
way to cure Ich disease. Since the effect Five fish infected with Ich parasite were
of Garom Zangi extract on Ich parasite bought from ornamental fish supply
has not been studied but its antiparasitic centers. Subsequently, wet mount was
effect on other parasites such as carefully prepared from the infected fish
Trichodina has been proven before, this and all the contents of the petri dish were
study is aimed to investigae the washed. Then, the fish were killed
antiparasitic effect of Garom Zangi on I. through merciless slaughter and placed
multifiliis parasite in vitro. in small beaker (Bécher) containing
water similar to the original aquarium
water. They were examined under1141 Yazdani Anaraki et al., A study of short-term antiparasitic effect of alcoholic extract of...
stereomicroscope. After about an hour, for 10 minutes). Toma and Neobaur
the tomonts detached from the fish’s slides were used to count the theronts.
body slowly moved by the freestyle and
landed on the beaker floor. Then, the Preparation of alcoholic extract
beaker contents were transferred to concentrations of Terminalia catappa L.
separate petri dishes. The tomonts were Given the initial tests and reviewing the
ultimately isolated under a references, five different concentrations
stereomicroscope at 40x magnification of alcoholic plant extract (50, 100, 250,
and using a sampler. 500, and 850 mg/L), formalin
concentration (15 ppm, positive control),
Preparation of theronts of Ich parasite as well as a control group without extract
Petri dishes containing tomonts were (containing aquarium water) were
incubated at 23.5°C for 22 hours. Tiny prepared. The seven treatments
theronts with the feature of fast investigated in the present study are as
swimming in water were detectable after follows:
22 hours. Density of theronts reached a
fixed level by centrifuge (at 4000 rpm
Group 1) Control, only chlorine-free aquarium water and alcoholic plant extract
Group 2) Positive control containing 15 ppm formalin
Group 3) Concentration of 50 mg/L alcoholic plant extract
Group 4) Concentration of 100 mg/L alcoholic plant extract
Group 5) Concentration of 250 mg/L alcoholic plant extract
Group 6) Concentration of 500 mg/L alcoholic plant extract
Group 7) Concentration of 850 mg/L alcoholic plant extract
Conditions of exposing theronts to Calculating the survival and mortality
Terminalia catappa L. alcoholic extract rates of theronts
concentrations At the end of the exposure time of the
Fifty microliters of theront suspension theronts, their losses were specified by
(600 theronts) was first poured into three this method. In summary, 10 μl of the
replicates (3 wells) in 96-well plates contents of each well was placed on the
based on the above seven treatments. Toma slide. In order to obtain the
The concentration treatment was number of live theronts per cubic
subsequently applied in accordance with millimeter, the number of live theronts in
the numbers specified in the previous nine large squares of Toma slide was
section with a volume of 50 μl and the counted and 10% was added to their
mortality rate was calculated and number. Specification of theronts
recorded at 1, 2 and 3 hours. mortality rate was accordance to a
morphologic change in parasitic theronts
from an almost cylindrical to rounded-Iranian Journal of Fisheries Sciences 20(4) 2021 1142
oval form caused by cell lysis. Given the relationship of the mortality rate of
initial density of 600 theronts per 100 parasitic theronts with the concentration
mL, the results were calculated based on of the compound and the exposure time.
the number of live theronts per 100 mL. The shortest interval to kill more than
80% of parasites is related to the
Data analysis concentration of 850 mg/L. After two
One‐way analysis of variance (ANOVA) hours, concentration of 500 mg/L was
procedure followed by Duncan's able to kill more than 90% of parasites.
testusing the SPSS software (Version 22, As observed in Fig. 1, the dose of 850
SPSS Inc., Chicago, IL, USA) was mg/L after one to three hours does not
applied to determine the significant significantly differ, although killing
difference (p1143 Yazdani Anaraki et al., A study of short-term antiparasitic effect of alcoholic extract of...
After one hour of exposure of I. The results of the current study revealed
multifiliis theronts, Terminalia catappa the antiparasitic effect of the alcoholic
L. at a dose of 850 mg/L showed the best extract of Terminalia catappa L. on I.
performance, so that it had a significant multifiliis parasite. Increasing the
difference with this performance at a concentration and exposure time led to a
dose of 500 mg/L. After one hour, significant increase in the antiparasitic
formalin performance was between 500 properties of the extract. The highest
and 850 mg/L and did not significantly anti-theront effect (100% decline in the
differ between these two doses. shortest possible time) was related to the
After two hours of exposure of I. concentration of 850 mg/L in 2 hours.
multifiliis theronts, Terminalia catappa Hence, it can be claimed that its
L. at a dose of 850 mg/L killed 100% of antiparasitic effect against the I.
the theronts; however, formalin and the multifiliis parasite was appropriate.
dose of 500 mg/L alcoholic extract of Previously, Chitmanat et al. (2005)
Terminalia catappa L could not kill employed various concentrations of
100% of the theronts, no significant grounded dried leaf solution of
difference was observed between the Terminalia catappa L. against tilapia
performance of 15 ppm formalin and pathogens, observing that 800 mg/L of
doses of 500 and 850 mg/L of alcoholic crude extract of this plant after 48 hours
extract of Terminalia catappa L. 15-ppm killed Trichodina in this fish. This may
formalin and concentrations of 500 and suggest the high resistance of
850 mg/L of the alcoholic extract of Trichodina parasite and show that I.
Terminalia catappa L. could kill 100% multifiliis parasite is much more
of the parasites after 3 hours and no sensitive to this alcoholic extract
significant difference was observed. compared to Trichodina.
In the study on the effect of dried leaf
Discussion extract of Terminalia catappa L. on
In the present study, the effect of monogenic parasites of goldfish,
Terminalia catappa L. alcoholic extract Chansue (2007) indicated that the using
at different concentrations (50-850 5.1 g/L of this substance for two weeks
mg/L) and at different intervals (1, 2, and had the greatest effect on killing
3 hours) on the mortality rate of I. Gyrodactylus sp. and Dactylogyrus sp.
multifiliis theronts was examined in parasites in goldfish. Moreover, the
vitro. Mortality and survival rates of present study has revealed that the
parasitic theronts have been chosen as extract of dried leaves of Terminalia
the indices of the effectiveness of catappa L. may be effective in killing
parasites over different intervals. This Ich parasite.
study was performed at regular intervals Moreover, studies have shown that
since exposure time is another indicator this extract may be helpful for improving
to assess the potential of antiparasites. survival, blood profiles, as well as
resistance to A. hydrophila. Also theIranian Journal of Fisheries Sciences 20(4) 2021 1144
antibacterial effects of this extract have acid (TA) in a dose- and time-dependent
been previously assessed. Bacteria such pattern through the damage of parasite
as S. aureus, E. coli, Corynebacteria, plasma membrane could be 100%
Staphylococci, Enterococci, effective against I. multifiliis theronts at
Escherichia, Salmonella, S. typhi, and P. concentrations of 8 and 11 ppm during
aeruginosa were the antimicrobial all the exposure times (45-270 min).
effects of Terminalia catappa L. on These authors then showed the short-
which were assessed (Shahina et al., term effectiveness of TA at different
2007; Opera et al., 2012). concentrations (0.0-7.0 mg/L) and in
Goun et al. (2003) reported that various exposure times (1-3 h) on the
methylene chloride and methanolic parasite theronts of I. multifiliis
extracts of Terminalia catappa L. have (Alavinia et al., 2019).
antifungal activity against Pythium The results of the study of Yao et al.
ultimum, Rhizoctonia solani, Sclerotium (2011) indicated that the use of an
rolfsii, Aspergillus fumigatus and alkaloid called dihydrosanguinarine, in
Phytophthora parasitica, so that the the concentration range of 5.18 to 9.43
antifungal effects of this extract against mg/L, has a very effective lethal
Pythium ultimum and Phytophthora coefficient on theronts of Ich parasite in
parasitica is very noticeable. vitro. They have previously revealed that
The I. multifiliis parasite is one of the different concentrations of sanguinarine
parasites causing great damage to the extracted from a native plant in China,
aquaculture industry. Since employing Macleaya cordata, could significantly
the malachite green and formalin as kill the Ich parasitic theronts in vitro
chemical compounds in the treatment of (Yao et al., 2010). Shan et al. (2014)
edible fish to control the I. multifiliis reported the strong lethal effect of two
parasite has been forbidden due to alkaloid compounds, including
carcinogenicity, extensive studies have chloroxynol and chlorithrin, on Ich
been proposed to introduce safe and parasitic theronts in vitro. The positive
effective alternative methods to control effect of garlic extract on the inhibition
this disease. of parasites and theronts of Ich parasite
Liang et al. (2015) examined the has been reported by Buchman et al.
effect of two flavonoids (kuwanons G, (2003).
O) extracted from Morus alba. Their Ekanem et al. (2004) assessed the effect
findings revealed a 100% lethal effect of of crude extracts of Mucuna pruriens
these flavonoids on the theronts of Ich leaves and Papaya seeds rich in phenolic
parasite. compounds (particularly tannins) and
Alavinia et al. (2018) investigate the antioxidants on the inhibition of Ich
in vitro and in vivo effect of tannic acid parasite. The number of parasites
on I. multifiliis in zebrafish (Danio generally reduced to 90% after exposure
rerio) to treat ichthyophthiriasis. In vitro to each treatment at a concentration of
antiparasitic assays revealed that tannic 200 mg/L compared to the control group.1145 Yazdani Anaraki et al., A study of short-term antiparasitic effect of alcoholic extract of...
A 100% reduction count of this parasite providing equipment and technical
was observed at the 150 mg/L support.
concentration of Mucuna pruriens leaf
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