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Research Article
Hypolipidemic and Antioxidant Activity of
Enoki Mushrooms (Flammulina velutipes)
Ming-Yei Yeh,1Wen-Ching Ko,1and Li-Yun Lin2
1Department of Bioindustry Technology, Dayeh University, Dacun, Changhua 51591, Taiwan
2Department of Food Science and Technology, Hungkuang University, Shalu, Taichung 43302, Taiwan
Correspondence should be addressed to Wen-Ching Ko; wcko@mail.dyu.edu.tw and Li-Yun Lin; lylin@sunrise.hk.edu.tw
Received June ; Accepted August ; Published August
Academic Editor: Chia-Jui Weng
Copyright © Ming-Yei Yeh et al. is is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
According to the literatures, Flammulina velutipes contains biologically active components such as dietary ber, polysaccharide,
and mycosterol, whose eects in reducing blood sugar, blood pressure, and cholesterol have been proven. is study used the active
components extracted from Flammulina velutipes powder (FVP) and Flammulina velutipes extract (FVE) to investigate the impact
of these active components on lipid metabolism of hamsters. e results show that the total dietary ber content in FVP and FVE
is . mg/ g and . mg/ g , respectively. e total mycosterol content is . ±. mg/ g and . ±. mg/ g,
respectively. e male hamsters were subjected to lipid metabolism monitoring by adding , , and % FVP or FVE into their diets
for a period of weeks. e animal assay results show that the % FVP and FVE groups have the lowest concentration of TC (total
cholesterol), TG (triacylglycerol), LDL (low density lipoprotein cholesterol), and LDL/HDL (high density lipoprotein cholesterol)
in the serum and liver (P<.). Our results demonstrate that the addition of % FVP or FVE has a signicant eect on the lipid
metabolism in hamsters whose increased level of HDL in the serum was induced by high fat diet.
1. Introduction
Flammulina velutipes is also known as enoki mushroom,
golden mushroom, Basidiomycotina, Agaricales, Tricholo-
mataceae, and Flammulina. It is rich in vitamin B and
contains traces of zinc. As a dietary supplement, F. velutipes
is known to be benecial to people with hypertension, the
elderly, and growing children []. Its biological activity can
help reduce blood sugar, blood pressure, and cholesterol in
addition to its antithrombotic eects. It has no known toxic
eect on the human body and is very benecial to human
health []. Dietary ber is an active polysaccharide, which is
part of the edible portion of F. velutipes and cannot be decom-
posed by lytic enzyme or digested in human alimentary
tract. is water-soluble dietary ber can be combined with
cholesterolorcholicacidbyadsorption,reducingtheamount
of cholic acid returned to liver and increasing the metabolism
of cholesterol and its transformation into cholic acid. e
cholesterol concentration is reduced and the absorption
of lipids in the small intestine is disturbed; therefore, the
lipid content in blood and the probability of cardiovascular
diseasecanbereduced[]. e higher the concentration of
water-soluble dietary ber ingested, the better its ecacy in
reducing blood cholesterol. It has been shown that feeding
mice with % water-soluble ber is sucient to reduce lipids
and triglyceride (TG) in their blood and the level of TG
in their liver []. It has been reported that water-soluble
ber is signicantly more capable of regulating hypolipidemic
activity compared with non-water-soluble ber []. us,
water-soluble dietary ber is capable of combining bile
salts and rendering a hypolipidemic eect []. It has been
demonstrated that mycosterol can reduce the concentration
of total cholesterol and LDL in blood and plasma [].
e polyphenol compounds in mushrooms are known to
reduce the risk of cardiovascular disease and cancer. ese
polyphenol compounds, such as quercetin, catechin, gallic
acid ester, and caeic acid ester, can prevent the cytotoxicity
caused by H2O2andtheoxidativedamagecausedbyanti-
free radicals is also useful in reducing LDL oxidation, DNA
damage, and the incidence of cancer []. It has also been
Hindawi Publishing Corporation
BioMed Research International
Volume 2014, Article ID 352385, 6 pages
http://dx.doi.org/10.1155/2014/352385
BioMed Research International
T : Ingredients of the experimental animal meals (%)a.
Ingredients Group
N H FVP FVP FVP FVE FVE FVE
Casein . . . . . . . .
Sucrose . . . . . . . .
Corn starch . . . . . . . .
Corn oil . . . . . . . .
Lard . . . . . . . .
Mineral . . . . . . . .
Vitamin . . . . . . . .
Choline . . . . . . . .
Methionine . . . . . . . .
-Cellulose . . . . . . . .
Total
aOn the basis of AIN- formula (American Institute of Nutrition (AIN)).
Amounts of corn oil, buckwheat seeds, and sprouts added were based on percent weight. N: normal diet; H: high fat diet; FVP, FVP, and FVP: feed with
%, %, and % FVP; FVE, FVE, and FVE: feed with %, %, and % FVE.
shown that fruiting body extracts from F. v e lutip e s eectively
scavenged -,diphenyl-picrylhydrazyl (DPPH) free radicals
and displayed reducing power [].
e aim of this study is rst to analyze the functionally
active components extracted from F. ve l u t i p e s powder (FVP)
and F. velutipes extracts(FVE).BothFVPandFVEarethen
added to the diet of hamsters to investigate whether, and to
what extent, the active components in F. velutipes regulate the
metabolism of lipids and antioxidant activity in hamsters with
a high fat diet.
2. Materials and Methods
2.1. Chemicals. Cholesterol, LDL-C, HDL-C, and triglyceride
were obtained from ICN Biomedicals, Inc. (Irvine, CA).
Bioassay kits, including the triglyceride kit, cholesterol kit,
LDL-C kit, and HDL-C kit, are manufactured by Teco Diag-
nostics (Anaheim, CA). Acetonitrile (LC grade, purity %)
is provided by Tomowa Chemical Co. (Taichung, Taiwan).
Authentic oxalic, citric, malic, -,diphenyl-picrylhydrazyl
(DPPH), free radicals, linoleic acid, butylated hydroxyanisole
(BHA), rutin, quercetin, and decanoic acid are obtained from
Sigma Chemical Co. (St. Louis, MO). Ethylenediaminete-
traacetic acid (EDTA) is purchased from Mallinckrodt Co.
(Hazelwood, MO). Phosphotungstic acid is obtained from J.
T. Baker Chemical Co. (Phillipsburg, NJ).
2.2. Material. Flammulina velutipes used in this study was
purchased from Taishen Mushroom located in Taichung,
Taiwan. e experimental procedures are as follows.
() FVP: g of fresh F. ve l u t i p e s was dried with a hot
air dryer at ∘C for h and then powdered by a
grinding machine for future use.
() FVE: g of fresh F. velutipes wascookedinmL
ofboilingwaterformininbatchesandthen
removed. e blanching water was concentrated
(. Brix) and freeze-dried for future use.
() Ingredients of the experimental animal meals are
given in Tab l e .
2.3. Chemical Characterization
2.3.1.DeterminationofDietaryFiber. Dietary ber was ana-
lyzed according to the AOAC method [].gofthesampleis
used for the test of insoluble and soluble bers, respectively.
2.3.2. Determination of Polysaccharide. We used a modied
version of the method described by Liu et al. []. mg/mL
sample solution was prepared with . M NaCl for gel ltra-
tion chromatography; the bed volume of the chromatography
column was measured with mg/mL blue dextran when
it was conrmed that there was no sugar reaction in the
leaching liquor. e nm absorbance of the solution was
detected by a UV/VIS detector (UA-, ISCO, USA) before
being collected with a fraction collector (Retriever TM ,
ISCO,USA).Each.mLwascollectedinatesttube.
e total sugar of the collected samples was measured by
phenol-sulfuric acid coloration, and the protein standard was
used to preliminarily measure the molecular weight of the
polysaccharide molecules. e chromatographic conditions
are described as follows: column: Pharmacia column (.
× cm), gel: Sephacryl S--HR (Sigma Chemical Co.,
USA), mobile phase: . M NaCl, sample concentration:
mg/mL, and ow rate: . mL/mg, . mL/min.
2.3.3. Determination of Mycosterol. Mycosterol was analyzed
by the method described by Feng et al. []. g samples were
mixed at a : (v/v) ratio with normal hexane for h reux
extraction; this procedure was repeated twice. e residues
were then mixed at a : (v/v) ratio with a methanol solvent
for h reux extraction. e ltered solutions were merged
and then concentrated by decompression until they were dry.
BioMed Research International
An internal standard ( mL of mg/mL -cholestane) was
added and saponied at room temperature for h and was
then mixed with mL of chloroform and extracted twice.
e lower layer was then taken and mixed with g of anhy-
drous sodium sulfate to remove water and was then ltered;
the ltered solution was concentrated by decompression at
∘Cuntilitwasdry.AtotalofLofBSTFA+TMCS
( + ) was added to the concentrate, and the reaction was
allowed to proceed for h at ∘C. e mycosterol content is
measured with GC-FID and GC-MS.
2.4. Antioxidative Ability Assay
2.4.1. DPPH Radical Scavenging Ability. e radical scaveng-
ing ability was analyzed with the method by Shimada et al.
[].mLsamplewasmixedwithmLofmethanolandthen
uniformly mixed with mL of . M DPPH methanol solu-
tion. Samples then rested for min before their absorbance
at nm was measured by a spectrophotometer. e formula
for calculating scavenging eect is as follows:
Scavenging eects%
=1− sample absorbance value
absorbance value of control group without sample
×100%.()
2.4.2. Ferrous Ion Chelating Ability. Ferrous ion chelation was
analyzed according to Dinis et al. []. . mL sample was
mixed with . mL methanol and .mL of MFeCl
2and
waited for seconds before mixing with . mL of mM
ferrozine. e sample rested at room temperature for min
andthenwascollectedfornmabsorbancetestbyHitachi
U- spectrophotometer.
e formula for calculating chelating ability is as follows:
Chelating ability (%)
=1− sample absorbance value
absorbance value of control group without sample
×100%.()
2.4.3. Reducing Power. e reducing power was analyzed
according to Oyaizu []. . mL samples were mixed with
. mL of . M pH . phosphate buer solution and
. mL of % potassium ferricyanide solution, reacted in a
water bath at ∘Cformin,andcooledinanicebath
for min. Samples were then uniformly mixed with . mL
of a % trichloroacetic acid solution and centrifuged and
then . mL of the supernatant was collected and uniformly
mixed with . mL of deionized water and . mL of .%
ferric chloride solution. e mixture reacted in the dark at
room temperature for min and then the absorbance at a
wavelength of nm was measured by spectrophotometer.
2.5. Animal Experiments. All the animal studies performed
were approved by the Supervising Animal Ethic Committee
of Hungkuang University in accordance with the Helsinki
Declaration of .
2.5.1. Animals and Diets. e animal diet is detailed in
Table . Selected --week old male Syrian hamsters were
used in this study and housed individually in stainless steel
cages. e temperature was 24±1∘C, the humidity was 40 ∼
60%,andthedailylightcyclewash.Aeroneweekof
ambience adaptation, they were randomly divided into
groups of hamsters each. One group of hamsters was given
a normal diet (N) and groups of hamsters were given a
high fat high cholesterol diet (H). Aer two weeks of high
fat inducement, either , , and % FVP or , , and %
FVE was added to the diet of one of the high fat groups and
no addition was made in one high fat group (see Table ).
e experiment lasted for weeks. Animal body weight
wasrecordeddaily,whereastheintakeofwaterandfood
was recorded every two days (Tab l e ). e animals fasted
overnight at the end of the experiment, and samples were
collected for analysis, including feces, liver, and blood. e
animals were etherized and dissected; the blood samples were
extracted from abdominal aorta to analyze total triglyceride
(TG), total cholesterol, low density lipoprotein (LDL), and
high density lipoprotein (HDL) content. All samples were
stored at −∘C so that they were ready for the measurement
of the blood lipid.
2.5.2. Determination of Lipoproteins in Serum and Liver. Sera
collectedfromtheabovewereassayedforlevelsoftotal
cholesterol, low density lipoprotein cholesterol (LDL-C), high
density lipoprotein cholesterol (HDL-C), and triglyceride
(TG) according to Richmond [,]. erefore, an enzy-
matic CHODPAP method with a Teco Diagnostics kit was
used for the determination of serum total cholesterol. A
cholesterol control reference supplied by the manufacturer
was treated with the same manner for calibration. LDL-
C was measured spectrophotometrically at nm. On the
other hand, the enzyme GDP-PAP triglyceride kit (Teco
Diagnostics) was used to determine the serum TG content
by following the instructions given by the manufacturer (Lin
et al.) [].
e extraction of hepatic phospholipids contents was
carried out according to Folch et al. []. e following
procedures were described elsewhere by Lin et al. []. e
method of Bartlett [] was followed for its determination.
e color reaction proceeded with perchloric acid (%)-
ammonium molybdate (.%)-ascorbic acid (%) method of
Bartlett []. e absorbance was measured at nm. e
concentration of hepatic phospholipids was calculated from
thecalibrationcurveestablishedusingastandardsample
supplied by the manufacturer.
2.6. Statistics. e experimental results were analyzed by a
single factor ANOVA using a computer statistics analysis
soware SPSS . (SPSS, Chicago, USA) for intergroup com-
parisons, and Duncan’s multiple range test analysis method
was used to determine the signicant dierences among the
various groups (<0.05).
BioMed Research International
T : Contents of dietary ber and polysaccharide of FVP and
FVE.
Components Contents (mg/ g)
FVP FVE
Total dietary ber . ±. . ±.
Insoluble dietary ber . ±. . ±.
Soluble dietary ber . ±. . ±.
Polysaccharides . ±. . ±.
Reported values are the mean ±standard deviation (S.D.) (𝑛=3).
3. Results and Discussion
3.1. Dietary Fiber, Polysaccharide, and Mycosterol Content.
Dietaryberisoenfoundinmushroom.Itisnotdigestible
by the human alimentary tract, but it increases the solid
mass of feces because it is unabsorbed. However, it stimulates
gastrointestinal peristalsis and bonds to bile salt, which is
then excreted. It can also accelerate the decomposition of
cholesterol which reduces its concentration in the blood. e
total dietary ber content in FVP and FVE was . mg/ g
and . mg/ g, respectively (Ta b l e ); the insoluble ber
content was . mg/ g and . mg/ g, respectively;
and the water-soluble ber content was . mg/ g and
.mg/g,respectively.emajorityofsolublebers
were dissolved by blanching; therefore, the content of soluble
ber in FVE was equivalent to that in FVP. e content of
rawberandtotalsolublesugarinF. v e l u t i p e s are higher than
in other mushrooms, as shown in the following descending
order: F. velutipes >Lentinus edodes >Oyster cap fungi >
Cap fungi []. It is known that, among these mushrooms,
the more viscous the water-soluble dietary ber is, the more
signicantly it can reduce blood cholesterol []. e FVP
and FVE polysaccharide content was . mg/ g and
. mg/ g, respectively (Table ). e fruiting body of
FVP had a high content of insoluble bers. More polysac-
charides were found in FVE (. mg/ g) than in FVP
(. mg/ g) since polysaccharides are water soluble.
In the natural environment, mycosterol mainly exists in a
free, esteried, and glycoside form. e chemical structure of
mycosterol resembles a fat-soluble substance; its mechanism
of action is similar to that of cholesterol in vertebrates []. It
has been reported that both the spores and the tube tissue in
the polypore fungus G.lucidum have a considerably higher
percentage of ergosterol esters than the pileus and stipe
tissues [] because of the presence of the higher amount
of crude ber []. It is possible that free ergosterol in
the cell membrane of the dead fungal hyphae undergoes
either degradation or esterication. e results suggest that
free ergosterol (not total ergosterol) should be used as a
beach marker for fungal biomass []. is experiment used
GC/MS for verication and identied types of steroids
in addition to the total mycosterol in FVP and FVE. e
mycosterol content was 46.57 ± 0.37mg/ g and 9.01 ±
0.17mg/ g, respectively (Table ). e total mycosterol
content in FVP was more than ve times higher than that
in FVE, which may be due to the short-term blanching
eects on dissolution of mycosterol. e common mycosterol
T : Mycosterol composition of FVP and FVE.
Components Contents (mg/ g)
FVP FVE
Stigmastan-,-diene ND . ±.
Ergosterol . ±. ND
Ergosta-,,-trienol . ±. ND
Ergosta-,-dienol . ±. . ±.
Ergosta-,-dienone . ±. ND
Ergosta-,-dienol . ±. ND
Ergosta-,-dienol . ±. ND
Fungisterol . ±. ND
Other . ±. . ±.
Total mycosterol . ±. . ±.
ND: not detected.
T : Antioxidant activities of FVP and FVE.
Items mg/mL
FVP FVE
DPPH scavenging % . ±. . ±.
Chelating ability of ferrous % . ±. . ±.
FRAP reducing power % . ±. . ±.
Total phenols (ppm) . ±. . ±.
Reported values are the mean ±standarddeviation(S.D.)(𝑛=3).
componentinmushroomisergosterol;itscontentinFVPwas
. mg/ g, but it was not detected in FVE. Stigmastan-
,-diene was not detected in FVP, but it was . mg/ g
in FVE; the ergosta-,-dienol content was . mg/ g in
FVP and was . mg/ g in FVE.
3.2. Antioxidant Activity. From the data shown in Table ,
FVE has a strong antioxidative eect (.% DPPH scaveng-
ing rate). Yang et al. [] conducted tests with . mg/mL
methanol extract of assorted edible mushrooms; Pleuro-
tus geesteranus can scavenge .% of DPPH free radicals,
whereas Flammulina velutipes, Lentinus edodes, and Oyster
cap fungus can scavenge ∼% of DPPH free radicals. In
another test, when the sample concentration is at . mg/mL,
Flammulina velutipes, Pleurotus geesteranus, Oyster cap fun-
gus, and Lentinus edodes can chelate .∼.% of ferrous
ions. Medicinal mushroom may be used as a source of
oxidation-resistant substance and may scavenge free radicals.
Phenolic compounds represent the largest group of phyto-
chemical components and phenolic compounds which can
inhibit LDL oxidation. e results indicate that FVE can be
good antioxidants.
3.3. Animal Test. e maximum weight of a male adult
hamster can be – g. Although the hamsters of dierent
groups were fed with dierent levels of F. velut ipes daily
during the -week period, there was no signicant inuence
on the hamster feeding eciency.
e Syrian hamster is an animal that is widely used in
lipid research, as its lipoprotein metabolism and conversion
are similar to those of humans []. e current study
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T : Eect of dried FVP and FVE on food intake, body weight, and feed eciency of hamstera.
Grow the
parameters N H FVP FVP FVP FVE FVE FVE
Food intake . ±. . ±. . ±. . ±. . ±. . ±. . ±. . ±.
Body weight (g) . ±. . ±. . ±. . ±. . ±. . ±. . ±. . ±.
Feed eciency . ±. . ±. . ±. . ±. . ±. . ±. . ±. . ±.
aN: normal formula; H: high lipid diet; FVP, FVP, and FVP: feed with %, %, and % FVP; FVE, FVE, and FVE: feed with %, %, and % FVE. Feed
eciency = [wt gain (g)/total diet intake (g)] ×%.
T : Eects of dried FVP and FVE on the nutritional and biochemical parameters related to serum and hepatic levels in male hamstersa.
Grow the
parameters N H FVP FVP FVP FVE FVE FVE
Blood
TG . ±.e. ±.b. ±.bc . ±.cd . ±.de . ±.bc . ±.a. ±.cd
TC . ±.e. ±.a. ±.b. ±.cd . ±.d. ±.b. ±.bc . ±. b
LDL-C . ±.d. ±.a. ±.c. ±.cd . ±.cd . ±.b. ±.b. ±.c
HDL-C . ±.e. ±.c. ±.a. ±.abc . ±.bc . ±.bc . ±.ab c . ±.abc
LDL/HDL-C . ±.c. ±.a. ±.c. ±.c. ±.c. ±.ab . ±.c. ±.b
TC/HDL-C . ±.c. ±.a. ±.c. ±.c. ±.c. ±.ab . ±. c. ±.bc
Liver (mg/g)
TG . ±.a. ±.a. ±.b. ±.b. ±.bc . ±.b. ±.b. ±.b
TC . ±.e. ±.a. ±.a. ±.bc . ±. bc . ±.e. ±. cd . ±.cd
Phospholipid . ±. . ±. . ±. . ±. . ±. . ±. . ±. . ±.
aN: normal formula; H: high lipid diet; TC: total cholesterol; TG: triacylglycerol; LDL-C: low density lipoprotein cholesterol; HDL-C: high density lipoprotein
cholesterol; LDL/HDL-C = low density lipoprotein/high density lipoprotein cholesterol; TC/HDL-C = total cholesterol/high density lipoprotein cholesterol.
a–e in the same row with dierent superscripts are signicantly dierent (𝑃 < 0.05).
compared , , and % of FVP and FVE groups with the H
group to investigate the biochemical values in the blood of
hamsters. e hamsters were under monitoring for weeks.
As shown in Ta b l e , the triglyceride (TG) level in the serum
of the FVP group is . mg/dL and that in FVE group
is . mg/dL, comparing to . mg/dL in the H group.
e total cholesterol in the FVP group is .mg/dL
and that in FVE group is . mg/dL, comparing to
. mg/dL in the H group. e LDL-C in the H group
is . mg/dL which is much higher than . mg/dL in
the FVP group and . mg/dL in the FVE group. e
HDL-C in the H group is . mg/dL which is much lower
than . mg/dL in the FVP group and . mg/dL in
the FVE group. We found that both ratios of LDL-C/HDL-
C and TC/HDL-C are lower in the groups with higher dosage
(up to %) of FVP and FVE. ese high FVP/FVE content
groups show an obvious trend in lower TG in serum, and
the LDL/HDL ratios are lower in FVP groups than in FVE
groups. Also, higher FVP and FVE contents have an impact
on decreasing the TC/HDL ratio (Tabl e ).
With regards to triglyceride in the liver, TG is . mg/dL
in the H group which is much higher than . mg/dL in
the FVP group and . mg/dL in the FVE group. e
total liver cholesterol in the H group is . mg/dL which
is much higher than . mg/dL in the FVP group and
.mg/dLintheFVEgroup.Also,asshowninTa b l e ,the
liver phospholipid in the H group is . mg/dL, compared to
. mg/dL in the FVP group and . mg/dL in the FVE
group. As shown in Table ,thesolubleberinFVPandFVE
was . mg/ g and . mg/ g, respectively. Previous
study indicates that adding % of soluble ber to the daily diet
of mice can reduce blood lipid and liver TC and TG con-
centrations signicantly. A higher concentration of soluble
dietary ber is more eective in reducing blood cholesterol
[] FVP and FVE reduce the TG and TC concentration in
the liver, and FVP has stronger eect than FVE (Tabl e ).
Studies also indicate that higher phospholipid content is more
helpful in reducing the total cholesterol level in liver []. In
Table , the total mycosterol contents in FVP and FVE are
. and . mg/ g, respectively, which can reduce blood
sugar, blood pressure, and cholesterol and resist thrombosis.
According to Ostlund Jr., [] an average person ingests
only .∼. g of mycosterol in his or her daily diet;
therefore, in order to benet from mycosterol for cholesterol
reduction, additional supplementary mycosterol is required
in the daily diet. Large amounts of meat and fat are ingested in
our daily diet; if sucient mycosterol is contained in the diet,
it would compete with cholesterol in the intestinal tract so less
cholesterol can be absorbed by body and the blood cholesterol
could be reduced.
4. Conclusion
() Flammulina velutipes is rich in polysaccharides and
canbeusedinhealthfoodandcosmeticproductsfor
its biological activity.
BioMed Research International
() e antioxidant activity test shows that FVE is dis-
played to be as high as .%, which could prevent
free radical and oxygen attacks. It also showed a metal
chelating ability.
() F. velutipes contains rich dietary ber, which acceler-
ates the decomposition of cholesterol and hence can
reduceTG,TC,andLDLlevelinthebloodandTG,
TC, and phospholipid in the liver.
() Mycosterol has the ability to reduce total cholesterol
and LDL in the blood. Taiwan has a high yield of
Flammulina velutipes all year round which has been
developed into nutritional supplementary foods, and
it is becoming an attractive research subject in the st
century.
Conflict of Interests
e authors declare that there is no conict of interests
regarding the publication of this paper.
Acknowledgments
is study was nancially supported in part by a grant from
Hungkuang University (Taiwan). e authors thank Hanyu
International Corporation Ranch for providing the enoki
mushrooms.
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