Vol.1, No.2, 41-47 (2011)
http://dx.doi.org/10.4236/oje.2011.12005
Open Journal of Ecology
Copyright © 2011 SciRes. OPEN A CCESS
Impact profenophos (pesticide) on infectivity of
Biomphalaria alexandrina snails with schistosoma
mansoni miracidia and on their physiological
parameters
Ragaa Mohamed
Zoology Department, Faculty of Science, Fayoum University, Fayoum, Egypt. mragaall@yahoo.com
Received 22 May 2011; revised 22 June 2011; accepted 1 July 2011.
ABSTRACT
Profenophos is an organophosphoru s pesticide
which are used effectively against cotton in-
sects and mites.The present work was carried
out to evaluate the molluscicidal activity of
pesticides (Profenophos) against Biomphalaria
alexandrina snails. Also, the effect of sublethal
concentrations of pesticide on the infection of
B. alexandrina with Schistosoma mansoni and
some enzymes of energy metabolism were stu-
died. The results showed that the infection of B.
alexandrina with schistosoma mansoni was gr-
eatly reduced after exposure to LC0, LC10, LC25
of pesticide and also, reduction in number of
cercariae per snail during the patent period and
in the period of cercarial shedding. The present
study indicated that the increase in levels of
aminotransaminases, acid phosp hate-se and al-
kaline phosphatases enzymes in haemolymph
and soft tissue of snails and the activity level of
lactate dehydrogenase, hexoki-inase and py-
ruvatekinase was also significantly reduced in
response to treatmen t.
Keywords: Biomphalaria Alexandrina;
Profenophos; S chist osoma Mansoni; Physiology
1. INTRODUCTION
Excessive use of pesticides in agriculture has spar-
kled researchers’ interest in investigating the harmful
effects of these compounds. Consequently, there has
also been an increase in the number of studies aiming at
evaluating the action of the residues of such chemicals
on non-target organisms. Pesticides are ubiquitous con-
taminants of the environment and have been found in air,
soil, water, and human and animal tissues in samples
from all over the world. These cover a wide range of
compounds used in pest control, such as fungicides,
herbicides, molluscicides, insecticides, rodenticides and
others [1]. Pesticide may play an important role in the
disappearance of snail vectors on reaching water bodies
as residues from pesticide activities and consequently
hindering schistosomiasis transmission in these sites [2].
Profenophos is an organophosphorus pesticide which
are used effectively against cotton insects and mites.
Improper use of pesticides combined with their persis-
tence, volatilization and mobility lead to frequent detec-
tions of the pesticide residues in the atmosphere, soil, sur-
face water and in vegetable fruits and cereal grains [3, 4].
The use of pesticides may engender biological effects
beyond those for which they were originally manufac-
tured [5,6]. As example of these is the agricultural in-
secticides which may interfere in the life, reproduction
and infection of snail vectors of schistosomiasis when
they reach water bodies [7]. Many authors studied the
effect of agricultural pesticides that may reach water
courses as residues on different biological parameters of
snail vectors of schistosomiasis [8].
Organophosphate pestic i de re present one of the worl-
d’s most commonly used agrochemical. Consequently,
many of its residues are frequently found in the envi-
ronment. Of the organophosphates, Profenophos has
been extensively used because of its low toxicity on
non-targ organisms. The present work aimed to study
the mode of action of Profenophos as molluscicides
against Biomphalaria alexandrina as indicated by sub-
lethal concentrations action on infection of Biomphalar-
ia alexandrina to Schistosoma mansoni and some en-
zymes such as aminotransaminases, acid phosphatase
and alkaline phosphatases enzymes in haemolymph and
tissues of B. alexandrina. Moreover, lactate dehydro-
genase (LDH), pyruvatekinase (PK) and, Hexokinase
(HK) activity in soft tissue of treated snails.
R. Mohamed / Open Journal of Ecology 1 (2011) 41-47
42
2. MATERIAL AND METHODS
2.1. Snails
Laboratory bred Biomphalaria alexandrina snails (6 -
10 mm in shell diameter) were obtained from Schisto-
some Biological Supply Program (SBSP), Theodor Bil-
harz Research Institute (TBRI), Egypt.
2.2. Ova
Schistosoma mansoni ova were obtained from the
Schistosome Biological Supply Program (SBSP), Theo-
dor Bilharz Research Institute (TBRI), Egypt.
2.3. Pesticides (Profenophos)
Organophosphorus pesticide, having the chemical
formula C11H15BrClO3PS [O-(4-Bromo-2-chlorophen-
yl)-O-ethyl-S-propy l phospho rothioate], Synonyms: Cu-
racron; Polycron; Selecron; Nonacron and properties
(M.Wt 373.6 and boiling point 110˚C). Profenophos
was obtained from the Ministry of Agriculture, Egypt.
2.4. Biological study
2.4.1. Molluscicidal Screening
The efficacy of pesticide (Profenophos) against adult
snails was determined according to the standard proce-
dure recommended by WHO (9). Stock solution (1000
ppm) were prepared using dechlorinated water and a
series of concentrations was prepared from each ex-
perimental pesticide on the basis of weight/volume that
would permit the computation of LC50 and LC90 values
were prepared [10]. Dead snails were counted and re-
corded. LC25 LC50 and LC90 values slop function and
95% confidence limits of compound were obtained from
the curve in which serial concentrations in ppm were
plotted against % mortality of snails [11]. While LC0
was determined as 1/10 LC50 [9].
2.4.2. Effect of Sublethal Concentration of Pes-
ticides on Infectivity of S. Mansoni Mirac-
idia to B. Alexandrina Snails.
Exposing 3 groups of snails (each of 50 snails) indi-
vidually to a dose of 10 miracidia/snail and maintained
in each sublethal of concentrations of Pesticide (LC0,
LC10 and LC25 of Profenophos) for 24 h under room
temperature (24 1˚C). After exposure to miracidia,
snails were maintained in their corresponding pesticide.
Another group of 50 snails was exposed to miracidia in
the absence of the tested pesticide an d maintained under
the same conditions (control group). The snails were
daily fed lettuce (Lactuca sativa plant) leaves and dead
ones were removed. Examination of snails for cercarial
shedding was carried out twice weekly, 25 days post
exposure, and the cercarial suspension was poured in a
graduated Petri dish, then a few drops of Bouin’s fluid
(Dye for coloring cercariae) were added and all cer-
cariae were counted, using a dissecting microscope.
Shedding snails were then isolated and kept in special
aquaria in complete darkness.
2.4.3. Effect of Sublethal Concentration of
Pesticides on Physiological Parameters
of B. Alexandrina Snails.
For studying some physiological parameters of B. al-
exandrina snails, four identical groups of snails (each of
six replicates) of which three groups of snails were ex-
posed for one month to sublethal of concentrations of
Pesticide (LC0, LC10 and LC25 of Profenophos). A four
group was left unexposed under the same laboratory
conditions as control. Snails surviving after exposure
was used to study selected enzymatic activities were
investigated both in treated and untreated snails. The
measured enzymes included aminotransaminases [As-
partate aminotransferase (AST) and alanine ami-
notransferase (ALT), (AST and ALT are the most fre-
quently measured for hepatic diseases, the enzymes may
be released from hepatocytes into the circulation by
necrosis [12]), acid phosphatase and alkaline phos-
phatases enzymes (these are a lysosomal enzymes con-
cerning with digestion of foreign substances and bacte-
ria inside the cells and is involved in the defense
mechanisms of both vertebrates and invertebrates [13])
in haemolymph and tissues of B. alexandrina. Moreover,
lactate dehydrogenase (LDH), pyruvatekinase (PK) and
Hexokinase (HK) activity [glycolytic enzymes] in soft
tissue of treated snails.
2.4.3.1. Biochemical Analysis
For preparation of tissue extracts of treated and con-
trol snails, one gram of the soft tissues of the snail was
homogenized in 5 ml distilled water, pH 7.5. A glass
homogenizer was then used to grind the tissue, and the
homogenate was centrifuged for 10 min at 300 rpm and
the fresh supernatant was decanted. Haemolymph of
infected and control snails was collected in accordance
with techniques described by Michelson [14]. The
haemolymph was obtained via small hole made in the
shell into which capillary tube was inserted then it was
drawn into tube by capillary suction. The haemolymph
was pooled from 10 snails collected in a vial tube (1.5
ml) and kept in ice-bath.
2.4.3.2. Assay Methods
Aspartate aminotransferase (AST) activity in the
haemolymph and soft tissues of exposed and unexposed
Copyright © 2011 SciRes. OPEN A CCESS
R. Mohamed / Open Journal of Ecology 1 (2011) 41-47 43
snails was determined according to the method of
Reitman and Frankel [15], the oxaloacetate formed re-
acts with 2, 3-dinitrophenyl-hydrazine in alkaline solu-
tion(PH = 7.5 at 22˚C). The product of the reaction can
then be determi ned p hotometrically at 500 nm to560 nm
Alanine aminotransferase (ALT) activities in the
haemolymph and soft tissues of exposed and unexposed
snails were determined according to the method of
Reitman and Frankel [15], the pyruvate formed reacts
with 2, 4 dinitrophenyl-hydrazine in alkaline solu-
tion(PH = 7.5 at 22˚C). The product of the reaction can
then be determined spectrophometrically at 500 nm to
560 nm
Acid phosphatase (ADP) and alkaline phosphatase
(ALKP) activities were determined spectrophotometer
by measuring absorbance at 340 - 410 nm according to
Bessey et al. [16], Acid phosphatases have pH optima
below 7, whereas alkaline phosphatases are most active
above pH 7 at 22˚C.
Hexokinase (HK) was determined spectrophotometer
by measuring absorbance at 340 nm (PH = 7.5 at 22˚C)
according to the method of Uyeda & Racker [17] in
which glucose-6-phosphate formed by the hexokinase
reaction is measured by adding glucose-6-phosphate
dehydrogenase and NADP and following NADPH for-
mation.
Pyruvatekinase (PK) activity was measured spectro-
phometrically as the rate of decrease in extinction at 340
nm (PH = 7.5 at 22˚C) due to the oxidation of NADH
by coupling the system with excess of lactate dehydro-
genase [18].
Lactate dehydrogenase activity was measured spec-
trophometrically by measuring absorbance at 340 nm
((PH = 7.5 at 22˚C) according to the method of Cabaud
& Wroblewski [19]. In this method pyruvate is reduced
by incubation with the enzyme in the presence of coen-
zyme nicotinamide adenine dinucleotide (NADH).
All physiological parameters determined in this study
were determined spectrophotometrically, using reagent
kits purchased from BioMerieux Company, France.
2.5. Statistical Analysis
Analysis of data was carried out by student’s “t”-test
for comparing the means of experimental and control
groups Spiegel [20].
3. RESULTS
The molluscicidal activity of Profenophos on Biom-
phalaria alexandrina snails after 24 hours of exposure
under laboratory conditions is presented in Table 1. The
data obtained indicate that the recorded LC50 values for
this pesticide was 4.6 ppm and LC 90 values was 10.7
ppm for B. alexandrina. The sublethal concentrations
(LC0, LC10 and LC25) were found to be 0.46, 1.8 and 2.5
ppm for B. alexandr ina.
The effect of the tested sublethal concentrations of
Profenophos on infection of B. alexandrina with S.
mansoni miracidia was presented in Table 2. The infec-
tion rate was significantly (p < 0.001) lower than that of
control snails (55%) being 40%, 16.66% and 10% for
snails exposed to LC0, LC10 and LC25 of Profenophos
respectively with a reduction rate –27.7%, –69.70%
and 81.82% respectively.
There is no significant difference between prepatent
period of the snails exposed to LC0, LC10 and LC25 of
pesticide and the control group. Prepatent period (Table
3) of exposed snails to LC0, LC10 and LC25 of Profeno-
phos was prolonged to be 36.2 + 4.8, 31.6 + 2.6 and
33.2 + 3.2 days compared to 35.6 + 4.1 days for the
control group. Meanwhile, the duration of cercarial
shedding was significantly (p < 0.01) shortened among
these snails, being 8.2 + 1.2, 6.3 + 0.82 and 4.8 + 0.85
days for LC0, LC10 and LC25, respectively, compared
with 16.2 + 4.3 days for control snails. Highly signifi-
cant (p < 0.001) reductions of total cercarial production
per snails was also detected in experimental snails in
comparison with the control group.
The results showed that (Ta ble 4.) the concentration
of transaminase enzymes (AST and ALT) in haemo-
Table 1. Molluscicidal activity of profenophos (pesticide)
against adult Biomphalaria alexandrina snails after exposure
for 24 hours.
LC50
ppm*
Confidence
limit of LC50
ppm
LC90
ppm* Slope
function LC0
ppm LC10
ppm* LC25
ppm*
4.6 5.98 - 3.5410.71.64 - 3.54 0.46 1.8 2.5
*using SPSS computer program under windows.
Table 2. Effect of sublethal concentrations of profenophos
(pesticide) on infection of Biomphalaria alexandrina with
Schistosoma mansoni.
Survived snails
at first shedding Infected snails
Treatment Number of
exposed
snails Number% Number %
Reduction
%
Control50 40 80 22 55
LC0 50 30 60 12 40–27.7*
LC10 50 18 36 3 16.66–69.70***
LC25 50 10 20 1 1081.82***
p < 0.05, ** p < 0.01, *** p < 0.001.
Copyright © 2011 SciRes. OPEN A CCESS
R. Mohamed / Open Journal of Ecology 1 (2011) 41-47
Copyright © 2011 SciRes.
44
OPEN ACCESS
Table 3. E ffect of sublethal concentrations of profe nophos ( p e s-
ticide) on cercarial production of Schistosoma mansoni from
infected snails.
Concentration
(ppm)
Prepatent
period
(days)
Duration of
shedding
(days)
Number of
cercariae/
snail
LC0 36.2 ± 4.8 8.2 ± 1.2* 621.5 ± 55.5 ***
LC10 31.6 ± 2.6 6.3 ± 0.82* 245.23 ± 44.2***
LC25 33.2 ± 3.2 4.8 ± 0.85*** 88.6 ± 12.4***
Control 35.6 ± 4.1 16.2 ± 4.3 2834.12 ± 213
lymph and soft tissue of experimental B. alexandrina
snails showed significant (p < 0.05) increase than that in
the control snails, The percentage of elevation 32.8%,
73.44% and 90.24% for AST and 37.11%, 41.41% and
61.71% for ALT in haemolymph and 29.33%, 83.47%
and 88% for AST, and 27.77%, 43.77%, 72.22% for
ALT in soft tissue of snails exposed to LC0, LC10 and
LC25 of pesticide, respectively than that in control
snails.
The present results (Table 5) indicated that there were
significant (p < 0.05) elevations in the level of acid
phosphatase 21.57%, 27.45% and 39.22% in haemo-
lymph and 27.27%, 31.82% and 40.91% in soft tissue of
snail treated LC0, LC10 and LC25 of pesticide, respec-
tively. The increase of alkaline phosphatase was 40%,
56% and 92% in haemolymph and 12.5%, 27.1% and
41.67% in soft tissue of LC0, LC10 and LC25 of pesticide,
respectively than that in control snails.
The levels of hexokinase (HK), pyruvatekinase (PK),
and lactate dehydrogenase (LDH) in the soft tissue in
normal and treated snails are displayed in Tab le 6. The
HK activity in snails exposed to sublethal concentra-
tions of the pesticide for one month was 21.4 1.4, 18.7
1.1 and 13.5 1.6 mol/min/g, respectively. Such
reduced values were statistically significant than those
of the corresponding controls (30.2 1.7). The activity
levels of PK, LDH were also significantly reduced in
response to treatment with plant extract, those of PK
being 0.10 0.018, 0.082 0.011 and 0.066 0.016
mol/min/g wet tissue, as compared to the control being
0.12 0.042 mol/min/g.
4. DISCUSSION
Most of the chemical compounds residues found in
the environment, such as pesticides, end up being dis-
charged into water resources. In these environments, the
substances become more and more diluted and are,
therefore, usually found at low concentrations. In the
current study, residual/environmental concentrations of
commercial Profenophos were evaluated in order to
investigate their possible effects on biological and
physiological parameters of snails. The Profenophos
(pesticide) showed considerable molluscicidal effect
against B. alexandeina. The LC50 and LC90 were found
to be 4.6 ppm & 10.7 ppm respectively. This result is
supporting with Wafaa and Ragaa [8] indicated that
Chlorpyrifos and Profenophos have a considerable kill-
ing effect against B. truncatus with LC50, 1.32 ppm and
2.5 ppm of the two compounds, respectively. Similar
results were obtained by El-Fiki and Mohamed [21],
using the herbicides Gramaxone, Preforan and Trefla.
In this study, the infection of B. alexandrina with S.
mansoni miracidia was greatly reduced by the tested
sublethal concentrations of Profenophos. The reduction
of infection rate was found to increase with the increase
of sublethal concentrations of Profenophos. Thia agree
with Wafaa and Ragaa, [8] found that increasing reduc-
tion of infection of snails maintained in LC25 of Chlor-
pyrifos and Profenophos pesticide. Similar inhibitory
effects were seen in the results were obtained in litera-
ture by several authors working on various che- mical
and plant molluscicides [22] using copper sulphate and
Tributylin fluoride; [23] using Bayluscide; [24] using
the plant Calendula micranth a officinalis; [25] using the
Table 4. Aspartate amino transferase (AST)), Alanine amino transferase (ALT) in Biomphalaria alexandrina exposed to sublethal
concentrations of profenophos (pesticide).
Aspartate amino transferase concentrations
(/mg protein) % increase Alanine amino transferase concentrations
(/mg protein) % increase
Parameter
Treatment Haemolymph
mg/ml % of
change Soft tissue
mg/g % of
change Haemolymph
mg/ml % of
charge Soft tissue
mg/g % of
charge
Unexposed
(control) 18.45 2.3 37.5 3.2 25.6 ± 4.1 50.4 3.5
lC0 24.5 1.1 32.8% 48.5 4.3* 29.33% 35.1 2.4* 37.11% 64.4 8.2* 27.77%
LC10 32 5.1* 73.44% 68.8 4.5**83.47% 36.2 3.2* 41.41% 72.43 10 .1* 43.77%
LC25 35.1 3.2** 90.24% 70.5 4.6**88% 41.4 2.7* * 61.71% 86.8 6.3** 72.22%
Values are expressed as means SD of 4 independent experiments;Enzymatic activities expressed as m ole NADH reacted/min/g wet. Tissue; *p < 0.05,**& p
< 0.01
R. Mohamed / Open Journal of Ecology 1 (2011) 41-47 45
Table 5. Acid phosphatase (ADP), Alkaline phosphatase (ALKP) in Biomphalaria alexandrina exposed to sublethal concentrations
of profenophos (pesticide).
ADP concentration
( mg protein) ALKP concentrations ( mg protein)
Parameters
Treatments Haemolymph
mg/ml % of
change Soft tissue
mg/g % of
charge Haemolymph
mg/m % of
change Soft tissue mg/g% of
charge
Unexposed
(control) 0.051 0.05 0.44 0.042 0.25 0.34 0.048 0.046
LC0 0.062 0.07* 21.57% 0.56 0.12* 27.27% 0.35 0.17** 40% 0.054 0.05* 12.5%
LC10 0.065 0.06* 27.45% 0.58 0.33* 31.82% 0.39 0.13** 56% 0.061 0.086*27.1%
LC25 0.071 0.048** 39.22% 0.62 0.55**40.91% 0.48 0.64*** 92% 0.068 0033**41.67%
Values are exp ress ed as means SD of 4 independent experiments; Enzymatic activities expressed as mole NADH reacted/min/g wet. Tissue; *p < 0.05,**&
p < 0.01
Tabl e 6 . Levels of lactate dehydrogenase (LDH), hexokinase (HK) and glucose phosphate isomerase (GPI) in the tissue of Biom-
phalaria alexandrina exposed to sublethal concentrations of profenophos (pesticide).
Enzyme activity ( U/mg tissue)
6 LDH % of change HK % of changePyruvate kinase (PK) % of change
Unexposed (control) 44.2 1.2 30.2 1.7 0.12 0.042
LC0 36.2 2.1* –18.1% 21.4 1.4 *–29.14% 0.10 0.018* –16.67%
LC10 24.4 1.8* –44.80% 18.7 1.1* –38.1% 0.082 0.011* 31.67%
LC25 17.5 2.1**–60.41% 13.5 1.6**–55.30% 0.066 0.016** –45%
Values are exp ressed as means SD of 4 independent experiment; Enzymatic activities expressed as mole NADH reacted/min/g wet. Tissue; *p< 0.05,**&
p< 0.01.
plants Thymus capitatus and Piper nigrum; [26], [11]
using the plant Synadenium grantii. Tantawy [27] re-
ported that the herbicides, Butachlor and Fluazi-
fop-p-butyl reduced the survival and infection rates of
B. alexandrina snail s. Bakry [28] using plant extract.
However, there was no difference between the pre-
patent period of the snails exposed to sublethal concen-
tration of Profenophos pesticide and the control. De-
spite that, a h ighly redu ction in th e duration of cercarial
shedding and total cercarial production per infected
snails were reported. This reduction in cercarial shed-
ding period and total cercarial production per snail is
probably due to rupture of snails’ tissues through
miracidial penetration in the presence of those pesti-
cides which increased the harmful effects of these
plants [8]. These observations are in accordance with
many authors using different plant species as mollus-
cicides. Thus, Ibrahim et al. [29] stated that low con-
centrations of the organophosphorus pesticides Chlro-
pyrifos (Dursban) caused blockage of cercarial shed-
ding of infected of B alexandrina snails. Sharaf El-Din
et al. [30] obtained similar reduction in cercarial shed-
ding and cercarial production from B. alexandrina
treated with sublethal concentrations of aqueous sus-
pension of Zygophyllum simplex. This supports other
authors on various molluscicid es, e.g.
El-Ansary et al. [31] recorded longer prepatent pe-
riod in B. alexandrina infected with S. mansoni in
presenc e of Ambrosia maritima, and Gawish [32] found
that the period of cercarial shedding in snails treated
with the experimental molluscicides during their expo-
sure to miracidia are significantly short than that in
control snails. The results also indicated that treatment
of snails continuously with the methanol extract of
E.soongerica plant resulted in highly significant reduc-
tion of total cercarial production per snails in compari-
son with control.
The activity of aspartate aminotransferase (AST) and
alanine aminotransferase (ALT) enzymes in haemo-
lymph and tissue of B. alexandrina snails were signifi-
cantly increased than that in the control snails. This
result is in accordance with Bakry et al. [33] who re-
ported that the levels of AST and ALT in haemolymph
of Bulinus truncatus are increased significantly when
exposed to oreopanax reticulum and Furcraea selloea
plants. El-mam and Ebeid [34] reported that the activity
of AST and ALT of the heamolymph of B. alexand rina
were significantly decreased by S. mansoni infection.
Acid phosphatase enzyme plays an important role in
the defense mechanism of host snails Sabry et al. [35].
Copyright © 2011 SciRes. OPEN A CCESS
R. Mohamed / Open Journal of Ecology 1 (2011) 41-47
46
The present results indicated that there are signifi-
cant elevations in the level of acid phosphatase and
alkaline phosphatase which can be explained by the
destruction of internal snail cells.
This finding agrees with Bakry et al. [33] using ore-
opanax reticulum and Furcraea selloea plants. Also,
Michelson and Dubois [36] found an increase in alka-
line phosphatase levels in both the heamolymph and
digestive gland from infected B. glabrata with S. man-
soni. El-Emam and Ebeid [34] reported that the acid
phosphatase activity in the heamolymph of B. alexan-
drina was increased by S. mansoni infection. The pre-
sent study showed a significant decrease in LDH activ-
ity in the whole tissue extract of Bulinus truncatus in
response to treatment with the methanol extract of
E.soongerica plant. Several authors have reported a
significant decline in LDH activity of tissues of
vari]ous molluscs in response to some molluscicides
[Aboul-Zahab & El-Ansary, [351 and Bakry et al. [38].
4. CONCLUSIONS
It is concluded that Profenophos pesticide are toxic
to the intermediate snail host of S. mansoni. and there-
fore may have adverse effects on natural populations.
Sublethal concentration of this pesticide play also a
role in suppressing transmission of schistosomiasis by
reducing the infection of snails with schistosomes. In
addition, pesticides caused reduction in number of cer-
cariae per snail during the patent period and in the pe-
riod of cercarial shedding. The present study indicated
that the increase in levels of aminotransaminases, acid
phosphatase and alkaline phosphatases enzymes in
haemolymph and soft tissue of snails and the activity
level of lactate dehydrogenase, hexokinase and pyru-
vatekinase was also significantly reduced in response to
treatment. According to the results obtained, we can
observe that the Low concentrations of Profenophos
tested (residues found in the environment) induced
toxic to biological and physiological of snails.
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