1502 International Journal of Food Science and Technology 2016, 51, 1502–1508

Original article
Effects of UV-C irradiation on the physiological and antioxidant
responses of button mushrooms (Agaricus bisporus) during
storage

Yuanyuan Lu,1 Jie Zhang,1 Xiaotuo Wang,1 Qiong Lin,1 Wei Liu,1 Xinfang Xie,1 Zhidong Wang1* &
Wenqiang Guan1,2*
1 Institute of Food Science and Technology, Ministry of Agriculture, Chinese Academy of Agricultural Sciences/Key Laboratory of
Agro-products Processing, Beijing 100193, China
2 Tianjin Key Laboratory of Food Biotechnology and Food Sciences, Tianjin University of Commerce, Tianjin 300134, China
(Received 10 February 2016; Accepted in revised form 24 February 2016)

Summary Novel postharvest technology not only preserves the freshness of fruits and vegetables, but also triggers
the biosynthesis of antioxidant compounds as a secondary response. This study examined the browning
and antioxidant properties of button mushrooms (Agaricus bisporus) treated with UV-C irradiation in
combination with cold storage. Three sample preparation methods for antioxidant activity analysis, simu-
lative gastrointestinal digestion (GAR), direct evaluation (QUENCHER) and traditional solvent extrac-
tion (TSE), were used to evaluate the samples, and followed analysing by both FRAP and ABTS assays.
Broadly, the results indicated that, following an initial increase, UV-C irradiation suppressed browning
during a cold storage period of 18 days. And the total phenolic content of the treated mushrooms were
higher than that of the control, while the ascorbic acid content decreased sharply during storage, and
UV-C treatment had negative effects on ascorbic acid content. Results from the QUENCHER and GAR
methods showed that UV-C treatment significantly increases the total antioxidant capacity (TAC) of
mushrooms throughout the entire storage period, and have a larger magnitude than that of TSE method.
In conclusion, the combination of UV-C irradiation and cold storage showed great potential for improv-
ing mushroom quality as a new postharvest technology.
Keywords Antioxidant, brown, button mushrooms, GAR, UV-C.

cancer, diabetes, obesity and neurodegenerative dis-

Introduction
Numerous epidemiological studies have shown an
inverse correlation between fruit and vegetable con-
sumption and chronic diseases. These studies have
shown that people who avoid or consume very few
fruits and vegetables are at increased risk of chronic
diseases. White button mushroom (Agaricus bisporus)
has been consumed globally for a long time and is one
of the most economically important edible cultivated
mushrooms (Guan et al., 2012). It has been considered
to be not only a nutraceutical but also as a functional
food, as it contains enriching components such as
ergothioneine, vitamins, minerals, polysaccharides and
polyphenols (Dubost et al., 2007; Liu et al., 2013; Tian
et al., 2012). Button mushroom has been found to have
significant antioxidant and anti-inflammatory bioactivi-
ties in maintenance of health and the prevention of
*Correspondent: E-mails: wangzhidong@caas.cn; gwq18@163.com
Yuanyuan Lu and Jie Zhang contributed equally to the study.
eases (Chen et al., 2006; Jeong et al., 2010; Kozarski
et al., 2011; Moro et al., 2012). However, maintaining
the quality of button mushroom after harvest is diffi-
cult, as it is easily prone to browning and microbial
spoilage (Brennan et al., 2000).
Ultraviolet C (UV-C) is an important nonthermal
sterilisation technology. It has been used and approved
as a disinfectant for the surface treatment of food
products (US-FDA, 2002). In our previous study, UV-
C treatment was shown to have great potential as an
alternative to chemical sterilisation for postharvest
preservation of button mushroom. UV-C treatment
induced a 0.67–1.13 log reduction of E. coli O157:H7
inculcated on mushroom cap surfaces. (Guan et al.,
2012). In addition to the disinfection, low doses of
UV-C irradiation can trigger some favourable
reactions in biological tissue that can lead to various
beneficial effects such as the extension of shelf life
and/or increases in the content of health promoting
components (Carlos Ribeiro et al., 2012).

doi:10.1111/ijfs.13100
© 2016 Institute of Food Science and Technology

Antioxidants have been recognised as important
nutritional and functional components of human
diets. It has been reported that UV-C irradiation can
induce increases in antioxidant activity in strawberry,
tomato, broccoli and other foods (Erkan et al. 2008;
Liu et al., 2012; Shen et al. 2013; Topcu et al. 2015).
Generally speaking, the alcohol aqueous solution,
namely traditional solvent extraction (TSE), is the
most common method used for the evaluation of
antioxidant in fruits and vegetables. However, because
different solvents extraction applied could make differ-
ent results of antioxidant capacity for the same sam-
ple, it is hard to evaluate the antioxidant activities
accurately (Zulueta et al., 2009; Delgado-Andrade
et al., 2010). To overcome this problem, Gokmen
et al. (2009) proved to add the antioxidant assay
reagents to the solid samples directly (QUENCHER),
and the antioxidant capacity is not related to the sol-
ubility of samples. This extraction-dependent method
skips all time-consuming solvent extraction. More-
over, because it is the digestion mechanism in human
body, the antioxidant in vitro does not stand by its
true bioactivity, a stimulation method by enzymatic
digestion through the gastrointestinal tract was
described by Pastoriza et al. (2011). The antioxidant
capacity is sufficiently close to the bioactivity in vivo,
called as globe antioxidant response (GAR). There-
fore, in this study, on the one hand, we focused on
the UV-C effect on the colour of surface of mush-
room, and measured the total phenolic content and
ascorbic acid content. On the other hand, we explored
three sample preparation methods as mentioned
above, namely simulative gastrointestinal digestion
(GAR), direct evaluation (QUENCHER) and tradi-
tional solvent extraction (TSE), to evaluate the effect
of UV-C treatments on the antioxidant activities of
button mushroom.
Materials and methods
Biological materials
Button mushroom (Agaricus bisporus) was harvested
from a local edible fungus cultivation centre in the
Tongzhou District of Beijing, China. Mushrooms were
immediately transported to the laboratory after har-
vest. Whole, closed and uniform samples (mushroom
cap diameter of 3.0–5.0 cm) with fresh white colour
were selected for use in the experiments. Samples were
irradiated by UV-C within 12 h after postharvest at
ambient temperature.
UV-C irradiation, packaging and storage
A low-pressure mercury (LPM) UV light reactor was
assembled using a UV tube (Ruisente Ltd., Tianjin,
© 2016 Institute of Food Science and Technology
UV-C and antioxidants of mushrooms Y. Lu et al. 1503
China); it delivered UV photons at 253.7 nm. The
UV-C dose rate was determined by a digital ILT1700
radiometer (10 Technology Drive, Peabody, MA,
USA). The different UV-C illumination doses were
obtained by altering the duration of the exposure at
a fixed distance. The mushrooms were placed 20 cm
below the lamps, with their caps facing the UV-C
lamp, and irradiated for durations of 50 s, 100 s and
200 s, for exposures of, respectively, 0.5, 1.0 and
2.0 kJ m
2. Nonirradiated mushrooms were used as
controls. After irradiation treatment, mushrooms were
sealed in 28 9 20 cm bags of low-density polyethy-
lene (LDPE), which were of 0.04 mm thickness (Hua
Feng Plastic Co., Ltd., Heyuan, China). The samples
were then stored in a refrigerator at 4  1 °C, with a
relative humidity (RH) of approximately 80%. Sam-
ples were collected on day 1 and subsequently at
6-day intervals until day 18. Mushroom caps were
manually separated from the stipe, ground to a pow-
der and were then frozen with liquid nitrogen. The
powder was stored in sealed plastic bags at
80 °C
until analysis.
Colour analysis
At the time of sampling, the surface colour of the
mushroom caps was measured with a WSC-S
Colorimeter (Shanghai precision instrument Co. Ltd.,
Shanghai, China). Each mushroom was measured at
three equidistant points on the cap, and each measure-
ment contained L*(light/dark), a*(red/green) and
b*(yellow/blue) values in triplicate. The browning
index (BI), which represents the purity of the brown
colour of samples, was calculated according to the fol-
lowing equation (Gao et al., 2014):
BI ¼ ½100ðx
0:31Þ=0:172;
where x = (a + 1.75L*)/(5.645 L* + a*
3.012b*)
*
Sample preparation
For the evaluation of antioxidant capacity, three sam-
ple preparation methods were applied, namely simula-
tive gastrointestinal digestion (GAR), direct evaluation
(QUENCHER) and traditional solvent extraction
(TSE), and the detailed procedure is summarised in
Fig. 1, which were performed, with modifications,
based on the methods reported by Pastoriza et al.
(2011). All these methods were finally indentified by
ABTS and FRAP assays.
Antioxidant assay
Absorbance was evaluated using a spectrophotometer
(ONLAB UV Pro; Shanghai On lab Instruments Co,
Shanghai, China). Aqueous solutions of tert-butylhy-
International Journal of Food Science and Technology 2016
1504 UV-C and antioxidants of mushrooms Y. Lu et al.
droxytoluene (BHT) were used for calibration, and the
results were expressed as n mol equivalents of BHT
per g of sample.
ABTS method
The ABTS assay was performed as in Pastoriza et al.
(2011), with some modifications. The ABTS+ • was
produced by mixing 40 mL of 7 mM ABTS stock solu-
tion and 712 lL of potassium persulphate; this was
stored in the dark at room temperature for a minimum
of 13 h. The stable ABTS+ • working solution was
diluted with 95% ethanol solution to an OD730 absor-
bance of 0.70  0.02. For the soluble fraction, 100 lL
(20 lL supernate after digestion and 80 lL 95% etha-
nol solution) was added to 3 mL diluted ABTS+ •
solution. After shaking for 10 s and being allowed to
stand still for 6 min, the OD730 absorbance was
measured. For the insoluble fraction from the GAR
and QUENCHER samples, 0.0100 g samples were
added to 7.5 mL of diluted ABTS+ • solution. The
mixture was vortexed for 20 min, and the absorbance
of the supernatant was measured at 730 nm after
centrifugation.
FRAP method
The FRAP assay was conducted as described by Pas-
toriza et al. (2011) with modifications. The FRAP
reagent solution was composed of 40 mL 10 mM
TPTZ solution in 40 mMHCl, 40 mL of 20 mM FeCl3
and 400 mL of 0.3 M acetate buffer (pH 3.6). For the
soluble fraction, 100 lL (20 lL of supernatant after
digestion, 80 lL water) was added to 3 mL of FRAP
International Journal of Food Science and Technology 2016
Figure 1 Overview of the general proce-
dures of the TSE, QUERCHER and GAR
methods (modified from Pastoriza et al.,
2011). TSE, QUENCHER and GAR refer
to three sample preparation methods for
antioxidant analysis, which represent tradi-
tional solvent extraction, direct method of
no extraction and gastrointestinal digestion,
respectively.
reagent solution, and shaken for 30 min at 37 °C
before measuring at 595 nm. For the insoluble fraction
or for the mushroom caps from the GAR and
QUENCHER samples, 0.0100 g samples were added
to 9 mL FRAP, and the mixture was vortexed for
30 min at 37 °C. The absorbance of the supernatant
was measured at 595 nm after centrifugation.
Measurement of the total phenolic compound and
ascorbic acid content
Quantification of the total phenolic compound content
was estimated using the method proposed by Gao
et al. (2014). Five grams of mushroom caps were
homogenised with 25 mL 80% ethanol in an ice bath,
and the mixture was centrifuged at 1725 g for 10 min
at 4 °C. The supernatant liquid was diluted four times
with distilled water. A known volume of 2 mL of
sodium carbonate solution (20% w/v) was mixed with
0.8 mL of diluent, and the mixture was reacted with
1 mL of Folin Ciocalteu solution. The mixtures were
kept at ambient temperature for 30 min before mea-
suring absorbance at 760 nm. A standard curve for
gallic acid was used for quantification (calibration
range was 5–30 lg).
Ascorbic acid content was determined according to
Mishra et al. (2013). Mushroom caps (5 g) were
homogenised with 20 mL of 5% metaphosphoric acid
in an ice bath for 1.5 min. The slurry was centrifuged
at 5284 g for 20 min at 4 °C. The supernatant (1 mL)
was mixed with 9 mL 2, 6-dichloroindophenol, and
after the blue colour disappeared, the absorbance was
measured at 515 nm. Ascorbic acid content was calcu-
lated on the basis of a calibration curve of authentic
© 2016 Institute of Food Science and Technology

L-ascorbic acid (calibration range
20–100 lg mL
1).
Statistical analysis
The experiments were carried out using a completely
randomised design. All measurements including colour
analysis, antioxidants capacity and antioxidant com-
pounds were performed in triplicate. The statistical sig-
nificance of the differences between experimental
groups was evaluated by one-way analysis of the vari-
ance (ANOVA) followed by Duncan’s tests to compare
means that showed variation. The means were
expressed with standard errors.
Results and discussion
Effect of UV-C treatment on mushroom colour
The browning index (BI) can comprehensively account
for the extent of brown colour on the surface of but-
ton mushrooms. As shown in Fig. 2, mushroom caps
turned brown gradually during storage at 4 °C, and
the browning trend flattened after 12 day. Immediately
after irradiation, the mushrooms treated with UV-C
had higher BI values than the control. By day 6 of
storage, the UV-C-treated group showed remarkably
lower BI values than the control, and the BI values
were found to be inversely proportional to the inten-
sity of the UV dose. At day 12, the BI of the control
reached 41.58  1.34, while the BI values for the 0.5,
1.0 and 2.0 kJ m
2 treatments were, respectively,
33.52  1.41, 32.83  0.80 and 34.76  1.18. At day
18 of storage, the control showed the highest overall
BI value (44.9  1.22), while the BI values were simi-
lar among the samples treated with various intensities
of UV-C treatment; the 1.0 kJ m
2 UV-C treatment
exposure showed the lowest BI value (35.4  0.96).
The results showed that UV-C can cause slight damage
to the mushroom cap surface tissue immediately after
irradiation, but that UV-C treatment obviously sup-
pressed the browning of button mushrooms during
cold storage. These results are in agreement with those
of Guan et al.(2012).
Effect of UV-C treatment on total phenolic content and
ascorbic acid content
Phenolic compounds have been reported as the major
antioxidant components in mushrooms (Elmastas
et al., 2007; Barros et al., 2008). These compounds
have been widely reported to have beneficial effects in
the prevention of chronic diseases, as they act as free
radical scavengers and terminate radical chain reac-
tions (Block et al., 1992; Liu et al., 2012). The total
phenolic content values of mushrooms treated with
© 2016 Institute of Food Science and Technology
UV-C and antioxidants of mushrooms Y. Lu et al. 1505
was
Figure 2 Browning index of mushroom caps irradiated by UV-C
during the an 18-day storage period.
different UV-C illumination dosages are shown in
Fig. 3. During the whole storage, the total phenolic
content of the treated mushrooms was higher than
that of the control, and this content increased with the
increase in the UV dose strength in the initial storage.
Ascorbic acid is another important antioxidant com-
pound. The ascorbic acid content decreased sharply
during storage, and UV-C treatment had negative
effects on ascorbic acid content (Fig. 3). The initial
ascorbic acid content of untreated group was
64.00  5.42 lg g
1, and it declined to
38.89  2.25 lg g
1 of mushrooms at day 6. These
trends do not agree with the findings of previous stud-
ies; ascorbic acid increased in the initial stage and then
descended latterly (Gonz
alez-Aguila et al., 2007; Jiang
et al., 2010; Guan et al., 2012). This discrepancy may
have been caused by UV-C exposure dosages and/or
illumination positions.
The amounts of phenolic acids have a larger magni-
tude than ascorbic acid contents, which was similar
with the result in which phenolic acids made a signifi-
cant contribution to the antioxidants of mushroom
compared to common antioxidant compounds, ascor-
bic acid, b-carotene and lycopene (Barros et al. 2007;
Elmastas et al., 2007; Barros et al., 2008; Guan et al.,
2012).
Effect of UV-C treatment on antioxidant activity
Three methods (TSE, GAR and QUENCHER) were
used to evaluate the total antioxidant capacity (TAC)
of mushroom caps treated by UV during cold storage.
TAC is the n mol equivalent of BHT in the FRAP
and ABTS assay (Table 1).
For the FRAP assay of mushrooms, the order of
TAC was, from smallest to largest, TSE, GAR and
International Journal of Food Science and Technology 2016
1506 UV-C and antioxidants of mushrooms Y. Lu et al.
QUENCHER. The TAC of TSE ranged from
3.44  0.49 to 5.39  1.14 during the entire storage
period. According to the TSE results, UV-C treatment
had no significant effects on the TAC of mushrooms.
The GAR results were quite different. The TAC values
of the UV-C-treated mushrooms from the GAR exper-
iments were remarkably higher than those of the con-
trol samples throughout the entire storage period.
Immediately after irradiation, the 2.0 kJ m
2 intensity
treatment showed the highest TAC of 39.9  0.37; the
TAC of the control was only 21.8  1.89. The highest
TAC value observed in the whole study was for the
mushrooms treated with 0.5 kJ m
2at day 12
(42.2  4.64); the day-12 TAC value for the control
was only 29.4  2.12. The QUENCHER results also
showed that UV-C irradiation increased the antioxi-
dant activity of mushrooms; TAC was related linearly
with the UV-C dose on day 1. 0.5 kJ m
2 induced
peak value of TAC 122.10  0.23 at 6 day, and
1.0 kJ m
2 induced highest antioxidant capacity at
days 12 and 18.
The ABTS assays also indicated that the TSE
method yielded the lowest TAC values. According to
the TSE results, UV-C treatment had a negative effect
on the antioxidant activities of mushrooms, and UV-C
dose had positive effect on the TAC at 1 day. How-
ever, the TAC of the UV-C-treated mushrooms
increased gradually and tended to be higher than the
TAC of the control after day 6. At day 18, mushrooms
exposed to 2.0 kJ m
2 had the highest TAC value,
15.69  0.18; the TAC of the control at day 18 was
12.67  0.64. The GAR method yielded TAC values
that were 5–10 times higher than those observed with
the TSE method. The GAR results indicated that the
TAC values of the UV-C-treated mushrooms were sig-
nificantly higher than the control TAC values through-
out the entire storage period, but there was no clear
relationship between UV-C dose and the antioxidant
activities among the treated mushrooms. The
QUENCHER results also showed that the TAC values
of the UV-C-treated mushrooms were higher than
those of the controls. The TAC was positively related
to UV-C dose at days 1 and 6. The highest TAC value
International Journal of Food Science and Technology 2016
Figure 3 Total phenolic content and ascor-
bic acid content of button mushrooms irra-
diated by UV-C. Different lower-case letters
represent significant differences (P < 0.05).
Error bars represent standard error of means
(n = 3).
among the QUENCHER results was for the
2.0 kJ m
2-treated mushrooms at day 12
(114.62  4.84).
As a novel postharvest preservation technology,
UV-C illumination has been proven to be beneficial in
delaying postharvest fruit senescence and in reducing
decay in various fruits and vegetables (Carlos Ribeiro
et al., 2012; Shama & Alderson, 2005). Moreover,
UV-C is known to be able to induce hormetic
responses in plants that actually improve the quality
of various agro-products. In particular, UV-C treat-
ment has been confirmed to significantly increase the
antioxidant activities of tomato, strawberry and sat-
suma mandarin (Erkan et al. 2008; Shen et al. 2013;
Liu et al., 2012; Topcu et al. 2015). In this study, both
the QUENCHER and GAR methods indicated that
UV-C could increase the TAC of mushrooms. TSE,
however, showed that there was no positive effect on
TAC resulting from UV-C treatment. The compounds
extracted by sample preparation are vital for the sub-
sequent evaluation of total antioxidant capacity (TAC)
of samples. In traditional solvent extraction, the
polarity of solvents employed affects the bioactivity of
various soluble components and the insoluble fraction
is systematically discarded. Mushrooms are enriched
by polysaccharide distinct from common fruits and
vegetables, and this was not easily extracted by simple
solvents. Given this limitation, it is clear that we can-
not get comprehensive results about the effects of UV-
C on antioxidants on button mushrooms by TSE.
Guan et al. (2012) found that 0.225, 0.45 and
0.9 kJ m
2 treatment of UV-C had negative effect on
the antioxidant activities of button mushroom, while
Huang et al. (2015) and Jiang et al. (2010) found that
certain UV-C doses could actually increase the TAC
of mushrooms.
GAR simulates the digestion process through the
gastrointestinal tract that enables the comprehensive
evaluation of antioxidant compounds, including those
in the soluble and insoluble fractions. This method
was initially applied for the analysis of prebaked
bread, and its validity has been demonstrated in many
different foodstuffs such as fresh tomatoes, apples and
© 2016 Institute of Food Science and Technology
 UV-C and antioxidants of mushrooms Y. Lu et al. 1507

steamed spinach, among others (Gokmen et al., 2009;

1.97bc
1.41b

2.24b

3.25b
5.99a

2.43a
5.01c

0.55c
QUENCHER
Delgado-Andrade et al., 2010; Pastoriza et al., 2011).

*TSE, QUENCHER and GAR refer to three sample preparation methods for antioxidant analysis, which represent traditional solvent extraction, direct method of no extraction and









This study was the first to evaluate the antioxidant

102.11
116.56

102.07
107.54

114.37
97.80
93.98

95.34
content of mushrooms using the GAR method. The
GAR results showed that UV-C treatment had a posi-

1.28ab
1.16bc

Number of analysed samples n = 3. All values are presented as means  standard error (n = 3). Means with different letters within a row differ significantly (P < 0.05).
1.12b

3.32b
6.14a

2.52a
2.12c

3.11c
tive effect on the TAC in button mushrooms. The
QUENCHER method lacks digestion process com-









100.85

107.97
90.79

90.40
29.4
37.5
31.3
38.7
pared to GAR. In this study, the TAC values observed
GAR

for the GAR-processed samples were slightly lower

than those observed for the QUENCHER-processed

0.63ab
0.64bc
0.16a
0.21a
0.81a
1.14a

0.18a
1.74c
samples. This result differed from the findings of the









previous study (Pastoriza et al., 2011). This is possibly
18 day

12.67
14.10
11.19
15.69
4.11
4.69
4.03
5.32
TSE

related to the polysaccharide in mushrooms. Variation

in the sample preparation methods used prior to
6.02ab
5.60b

2.91b
5.80a

0.50a

1.28a
7.87c

0.90c

antioxidant evaluation obviously causes huge variation

QUENCHER

in measured TAC values. Therefore, the method of










110.44

108.84

108.07
78.53

96.88
105.5

93.39

93.86

sample preparation used for the evaluation of TAC

must be chosen carefully, with attention paid to the
polarity of the potential antioxidant compounds and
1.21b

0.01b

1.26b
4.64a

5.03a

0.83a

2.96a
3.15c

the food matrix. We suggest that GAR offers a thor-











ough extraction method for bioactive compounds that

25.8
42.2
30.4
40.5

100.00

102.73
74.01

92.11
GAR

can facilitate the accurate evaluation of TAC of food.

0.55b

0.54b

1.23b
0.16a
0.31a

0.22a

0.13a

0.36a

Conclusions









12 day

11.37
12.85
10.83
12.85
4.31
4.80
3.51
4.27

The UV-C irradiation represents a very powerful

TSE

postharvest technology that can suppress browning of

1.35b

the mushroom surface, increase the phenolic acid con-

5.93b
0.23a

4.84a
3.63c

2.85c

0.31c
2.55c
QUENCHER

tent and increase the antioxidant capacity of button

Table 1 ABTS and FRAP of mushroom caps from three sample preparation methods











mushrooms. Additionally, we conclude that GAR pro-

100.09
114.62
76.54
92.68
122.1
75.15

89.14
99.60

vides a thorough extraction method for bioactive com-

pounds and that this procedure is highly suitable for
3.20b

0.51b
1.13a
0.55a
0.70a

5.37a
2.99c

0.29c

the accurate evaluation of TAC of mushroom, particu-











larly given that it assesses both the soluble and insol-

103.54

110.95
86.92

89.83
24.7
36.6
37.5
35.7
GAR

gastrointestinal digestion, respectively. The details are shown in Fig. 1.

uble fractions.
0.28ab

0.59ab
0.33b

0.98a

2.18a
1.12a
1.03a
0.70a

Acknowledgments










The authors are thankful for the financial support of

6 day

4.45
4.15
4.60
5.39

12.67
12.26
13.62
13.75
TSE

the Scientific and Technological Innovation pro-

gramme of CAAS and the Natural Science Founda-
5.74b

1.80b
1.56a
2.40a

4.69a
4.54c

5.30c

4.44c
QUENCHER

tion of China (31271949). None of our co-authors has











conflict of interest to declare.

110.97
116.64

113.98
83.72
94.83

77.60
92.43
87.92

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1.89d

1.96b

2.08b
0.37a

3.29a
1.94c

1.35c

1.56c
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