Postharvest Biology and Technology 86 (2013) 91–99
Contents lists available at ScienceDirect
Postharvest Biology and Technology
journal homepage: www.elsevier.com/locate/postharvbio
Effect of gamma irradiation treatment at phytosanitary dose levels on
the quality of ‘Lane Late’ navel oranges
Heather McDonald a , Mary Lu Arpaia b , Fred Caporaso a , David Obenland c , Lilian Were a ,
Cyril Rakovski d , Anuradha Prakash a,∗
a
Food Science Program, School of Earth and Environmental Sciences, Chapman University, One University Drive, Orange, CA 92866, USA
Kearney Agricultural Center, University of California, Parlier, CA 93648, USA
c
San Joaquin Valley Agricultural Sciences Center, USDA-ARS, Parlier, CA 93648, USA
d
Math Faculty, School of Computational Sciences, Chapman University, One University Drive, Orange, CA 92866, USA
b
a r t i c l e
i n f o
Article history:
Received 6 September 2012
Accepted 10 June 2013
Keywords:
Gamma irradiation
Phytosanitary
Navel oranges
Sensory
Quality
a b s t r a c t
The objectives of this study were to determine the dose tolerance of ‘Lane Late’ navel oranges (Citrus
sinensis L. Osbeck) to irradiation for phytosanitary purposes, identify the sensory attributes that may
be affected by the treatment, and determine which changes, if any, influence consumer liking. ‘Lane
Late’ navel oranges on Carrizo citrange (C. sinensis Poncirus trifoliate) rootstock were irradiated at target
dose levels of 200, 400 and 600 Gy (actual absorbed doses were in the range of 100–300, 300–500, and
500–700 Gy, respectively) then stored for 1 d at 5 ◦ C, 3 weeks at 5 ◦ C (to simulate sea shipment to Asia) or
4 weeks (3 weeks at 5 ◦ C and 1 week at 20 ◦ C to simulate distribution to retail following sea shipment).
Trained sensory panelists found increased pitting and visual damage in oranges treated at doses of 400
and 600 Gy. Consumer liking scores for appearance were significantly lower for oranges treated at 400 Gy,
however, their overall liking scores for those same oranges were not significantly different than control.
Color, total phenolic content, vitamin C and ORAC (oxygen radical absorbance capacity) values were not
affected by irradiation. Dose effects were seen in terms of visual damage, increased weight loss and
increased concentration of certain volatiles and as well as decreased SSC (soluble solids concentration) at
doses 400 and 600 Gy. The primary effect of irradiation on fruit quality was external damage and pitting
at doses of 400 and 600 Gy. Further research should consider pack configuration and/or combination
treatments to possibly mitigate negative irradiation effects on appearance of the fruit.
© 2013 Elsevier B.V. All rights reserved.
1. Introduction
Navel oranges are an important crop in California. In 2010–2011,
California produced over 90 million cartons of navel oranges (18 kg
carton equivalents, 1,620,000 MT), primarily in the San Joaquin
region (USDA NASS, 2011–2012). Nearly 670,000 MT of Navel
oranges, or 41% of the total crop, were exported from California in
2010, with South Korea, Canada, Hong Kong, Australia, and Japan
comprising the top 5 export markets (Elliot, 2011). Oranges are
susceptible to green mold (Penicillium digitatum), blue mold (Penicillium italicum), Phomopsis stem-end rot (Phomopsis citri), stem
end rot (Lasiodiplodia theobromae), brown rot (Phytophthora citrophthora), and sour rot (Geotrichum candidum) (Arpaia and Kader,
2013). These diseases are controlled by chemical disinfectants
and fungicides, such as imidazoles, applied postharvest (Ladaniya,
2008). In addition to microbial infections, citrus fruits are also
∗ Corresponding author. Tel.: +1 714 744 7826; fax: +1 714 532 6048.
E-mail address: prakash@chapman.edu (A. Prakash).
0925-5214/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.postharvbio.2013.06.018
susceptible to insect pests. These include the citrus peelminer,
citrus leafminer, light brown apple moth, thrips, scales, ants,
katydid, grasshoppers, earwigs, bean thrip, fuller rose beetle, glass
winged sharpshooter, fruit flies, and asian citrus psyllid (CCQC,
2009). The occurrence of these pests can restrict movement of the
fruit within the state, nation, and to importing countries, with light
brown apple moth, fruit flies, thrips, fuller rose beetle and the Asian
citrus psyllid being of special interest as quarantine pests. Efforts
to minimize and control infestation include establishing fly-free
zones, chemical control (fumigation), cold and heat treatments,
and irradiation (Ladaniya, 2008).
Ionizing irradiation is effective in the disruption of deoxyribonucleic acid (DNA) molecules in the cell of an organism leading
to the inability of the cell to replicate and resulting in sterilization or death (Diehl, 1995). The United States Animal and Plant
Health Inspection Service (APHIS) has approved a generic dose of
150 Gy for Tephritidae and 400 Gy for all insects except pupae and
adults of Lepidoptera (Follett, 2009; USDA APHIS PPQ, 2012). The
150 Gy generic dose is being used for export of citrus, manzano peppers, and mangoes from Mexico to the US (Hallman, 2012) while
92
H. McDonald et al. / Postharvest Biology and Technology 86 (2013) 91–99
the 400 Gy generic dose is being used to export a variety of fruit
(mangoes, dragon fruit, guavas) from countries such as Thailand,
India, Pakistan, Vietnam, and Mexico to the US. A maximum of 1 kGy
(1000 Gy) is allowed for use on fresh fruits and vegetables (FDA,
2008), thus fresh fruit can be treated between 400 and 1000 Gy for
phytosanitary purposes. There is an ongoing international effort
to develop additional generic phytosanitary irradiation treatments
and reduce the generic dose of 400 Gy for all insects except pupae
and adults of Lepidoptera. Key pest groups that have been identified
for research are Lepidoptera (eggs and larvae only), mealybugs and
scale insects (IAEA, 2009; Hallman, 2012). Because irradiation is a
volumetric treatment that penetrates through the entire product, it
can simplify risk assessment processes often associated with chemical fumigants (Ferrier, 2010). Furthermore, continuous irradiation
systems can treat large pallet loads in minutes whereas cold and
fumigation treatments can take days and treatment of the product can occur in its final package (Hallman, 2011). Irradiation has
not been adopted for any fruit being exported from the US, most
likely due to a combination of various factors including the availability of alternate and lower cost phytosanitary treatments, lack
of knowledge regarding irradiation, and concerns about consumer
perception. But strong consumer demand for these irradiated fruit
and changes in available technologies, such as the phase-out of
methyl bromide, might spur greater interest in irradiation. In the
last few years, New Zealand has imported irradiated mangoes and
lychees from Australia (Hallman, 2011), signaling a shift in attitudes
about irradiation even among historically opposed consumers.
The effect of irradiation on quality of citrus fruit depends upon
various factors such as dose, fruit maturity, and cultivar (Miller
et al., 2000; Bustos and Mendieta, 1988; Monselise and Kahan,
1966; Ahmed et al., 1966; Belli-Donini et al., 1974). Miller et al.
(2000) evaluated the effect of phytosanitary doses up to 450 Gy on
various cultivars of oranges (Citrus sinensis (L.) Osbeck), including
‘Washington’ navel. They observed that irradiation even at 150 Gy
caused peel pitting in the ‘Washington’ and ‘Hamlin’ varieties but
firmness, weight loss, juice color, juice flavor, and pulp flavor were
not affected. The same study also found ‘Ambersweet’ and Valencia
oranges and Minneola and Murcot mandarins to have good tolerance up to doses of 500–600 Gy. Storage time and conditions can
also impact sensitivity of fruit to irradiation damage. O’Mahony
et al. (1985) found that navel oranges irradiated at 600–800 Gy were
more blemished as compared to untreated oranges as determined
by a trained panel 5–6 weeks after treatment and that dampness
of the fruit exacerbated external damage of the fruit.
The objectives of this study were to evaluate the radiotolerance
of ‘Lane Late’ navel oranges packed in 18 kg export cartons to irradiation up to dose levels of 600 Gy using analytical tests. Results
of analytical tests were compared to scores given by a trained sensory panel to determine the dose at which the changes become
noticeable. While previous studies performed difference testing
to determine if consumers could identify irradiated versus nonirradiated fruit, in this study we evaluated consumer liking of ‘Lane
Late’ navel oranges treated at the minimum phytosanitary treatment level of 400 Gy. Thus, this study was designed to determine
the dose to which ‘Lane Late’ navel oranges can tolerate irradiation
treatment used for phytosanitary purposes, identify the sensory
attributes that may be affected by the treatment, and determine
which changes, if any, impacted consumer liking.
While there has been previous experimentation to examine
the impact of irradiation on navel oranges (Miller et al., 2000;
O’Mahony and Goldstein, 1987; O’Mahony et al., 1985), this prior
work only incompletely answered the question of the degree to
which treatment impacted fruit quality, especially from the perspective of the consumer. In the studies that have performed
consumer evaluations (O’Mahony and Goldstein, 1987; O’Mahony
et al., 1985), difference testing was used to determine if consumers
could differentiate irradiated versus non-irradiated fruit, without
a complete attempt to determine the basis for these differences.
In addition, the impact of irradiation on some of the quality factors that are key to navel orange flavor, such as aroma volatiles,
has never been previously assessed. The objective of this study was
to thoroughly evaluate consumer liking of navel oranges irradiated
at the minimum phytosanitary treatment level of 400 Gy and to
relate these changes, if any, to alterations in sensory and quality
attributes to determine the basis behind any observed changes in
sensory quality.
2. Materials and methods
2.1. Sample procurement
On April 7, 2011, ‘Lane Late’ navel oranges on Carrizo citrange (C.
sinensis Poncirus trifoliate) rootstock were harvested in Sanger, CA.
‘Lane Late’ was selected for use in the study as it is a common late
season variety that is exported by the California citrus industry. The
fruit were packed at a commercial packinghouse in Orange Cove, CA
on April 9, 2011 following standard commercial practices. The fruit
were washed with 50–150 mg/L chlorine at the point of dumping,
then with a mixture of 1–2% sodium bicarbonate and 100–200 mg/L
chlorine in a high pressure washer which was followed by a fresh
water rinse. The fruit were then treated with 200–300 mg/L heated
Imazalil applied just after the 862 kPa (125 psi) pressure washer.
The fruit were waxed with a carnauba-based wax that also had
2.00 g/L imazalil and 3.50 g/L thiabendazole mixed in. Oranges were
bulk packed in 18 kg cartons with approximately 72 oranges in each
carton. After packing, fruit were refrigerated at 5 ◦ C.
2.2. Gamma irradiation
Fifty cartons of export fruit grade oranges (size 72) were
obtained on April 11, 2011. The fruit were transported approximately 390 km from Orange Cove, CA to Sterigenics (Tustin, CA). The
fruit were transported and held overnight at ambient temperature.
The fruit were irradiated on April 12, 2011 at ambient temperature
(∼20 ◦ C). Ten cartons were not irradiated and served as controls.
The remaining 30 cartons were irradiated in groups of 10 cartons
placed at a fixed distance from the source to receive precise doses
from a Co60 source (≈37 PBq) at a dose rate of 0.27 Gy s−1 . The cases
were arranged in rows of five stacked two high. To ensure uniformity of dose, dose mapping was conducted with a dummy sample in
exactly the same configuration using nine alanine pellet dosimeters
per case (Far West Technology, Inc.; Goleta, CA, USA). During treatment, dosimeters were placed at minimum and maximum dose
locations, which had been previously determined by dose mapping.
Midway through the treatment, the boxes were rotated 180◦ to
ensure uniform treatment. The fruit were irradiated at target dose
levels of 200, 400 and 600 Gy and actual absorbed doses were in the
range of 100–300, 300–500, and 500–700 Gy, respectively. Following treatment, the orange cases were transported to the University
of California Kearney Agricultural Center in Parlier, CA (∼390 km)
under ambient conditions. The fruit were stored at RH 90–95% for
1 d at 5 ◦ C, 3 weeks at 5 ◦ C (to simulate sea shipment to Asia) or
4 weeks (3 weeks at 5 ◦ C and 1 week at 20 ◦ C to simulate distribution to retail following sea shipment). At 3 weeks (5 ◦ C) and 4
weeks (3 weeks at 5 ◦ C and 1 week at 20 ◦ C), 1.5 cases of control and 400 Gy oranges and 0.5 case of 200 and 600 Gy oranges
were transported to Chapman University (Orange, CA) (∼390 km)
for sensory testing under ambient conditions. Control and 400 Gy
oranges were used in analytical and consumer testing. Fruit were
refrigerated (5–7 ◦ C) overnight then was taken out of storage and
allowed to come to room temperature, which took approximately
2 h at 20 ◦ C.
H. McDonald et al. / Postharvest Biology and Technology 86 (2013) 91–99
93
Table 1
Sensory attributes determined by trained panel. Their respective definitions define the extremes of the unstructured scale.
Attributes
Definitions
Reference materials
Appearance (outside)
Color
Intensity of orange color
Pitting
Degree of pitting
Dehydration
Dry appearance of peel
Visual damage
Amount of visual damage on peel, other than pitting
Weak: light orange
Strong: bright orange
None: no pitting
Intense: severe pitting
None: smooth appearance
Intense: dry/withered
None: no damage
Intense: severe damage
Texture/tactile
Fruit Firmness
Amount of resistance when squeezing whole fruits with all fingers
Juiciness
Amount of juice released while chewing
Dryness/granulation
Degree of dryness in regard to pulp
Aroma
Orange aroma (outside and inside)
Fresh orange peel aroma
Off-aroma (outside and inside)
Any off aroma
Appearance (internal)
Flesh color
Intensity of orange color
Dryness/granulation
Dry appearance of pulp and interior of fruit
Flavor
Tart
Degree of sourness
Sweet
Degree of sweetness
Orange flavor
Fresh orange fruit flavor
Off flavor
Any off flavor
2.3. Sensory evaluation
2.3.1. Trained sensory panel
Panelist selection was based on interest and performance on
preliminary screening tests. Eight panelists were selected to evaluate the effect of 200, 400, and 600 Gy on the quality of oranges using
descriptive analysis. A sensory professional facilitated the training sessions for the eight individuals chosen for this trained panel.
The eight members of the trained panel were either graduate students or staff members of Chapman University and were taught to
evaluate navel oranges in an analytical manner. Three 60-min training sessions were utilized to establish vocabulary describing key
orange characteristics: color, pitting, dehydration, visual damage,
skin firmness, aroma, off aroma, flesh color, dryness/granulation,
juiciness, pulp texture, tart, sweet, orange flavor, and off-flavor
(Table 1). These characteristics were rated from none to intense on
a 15-point unstructured, anchored scale (15-cm horizontal lines)
(Chambers and Wolf, 1996). Reference points were identified by
anchors placed on the scale and defined as “Control”. “Controls”
were defined as freshly harvested untreated oranges. After the
appropriate vocabulary and anchor placement was established, two
practice evaluation sessions were administered to evaluate panel
readiness. Anchors and any other reference points used in training
were available on the questionnaire during all evaluations.
Oranges were selected randomly from the cases of oranges
available for each testing period. Fruit were not excluded based
on appearance. Sixteen oranges were sliced using a Sunkist citrus cutter (Fruit Growers Supply, Fontana, CA, USA). Each panelist
evaluated the slices for flesh color, granulation, aroma, off-aroma,
juiciness, pulp texture, tart, sweet, overall flavor, and off-flavor.
None: soft fruit
Intense: hard fruit
None: no juice (cracker)
Intense: very juicy (watermelon)
None: moist, cannot feel pulp sections
Intense: dry pulp
None: absence of orange aroma
Intense: strong orange aroma
None: absence of off aroma
Intense: strong off aroma
Weak: light orange
Strong: bright orange
None: moist
Intense: dry/granulated
None: not sour
Intense: very sour
None: not sweet
Intense: very sweet
None: no orange flavor
Intense: strong orange flavor
None: no off flavor
Intense: strong off flavor
Oranges were presented monadically in a randomized and balanced
order on white paper plates marked with 3-digit random codes.
Eight to ten whole oranges were placed in a bowl for the trained
panelists to evaluate color, pitting, dehydration, visual damage, skin
firmness, aroma and off aroma. Samples were evaluated after 2 d
of storage held at 5 ◦ C (fresh), 3 weeks after being held at 5 ◦ C (to
simulate distribution to Asia) and 4 weeks (3 weeks at 5 ◦ C and 1
week at 20 ◦ C). Panelists were provided with unsalted soda crackers
and filtered water at each evaluation for palate cleansing between
samples.
2.3.2. Consumer testing
Oranges treated at a target dose level of 400 Gy were evaluated
by 75 consumers at the beginning of storage and 88 consumers near
the end of shelf life (4 weeks of storage). The panelists were 41%
male and 59% female, with age distribution of 18–27 years (75%),
28–37 years (10%), 38–47 years (6%), 48–57 years (5%), 58 and older
(4%). Oranges were selected randomly from the cases of oranges.
To mimic culling of damaged fruit as would occur in a supermarket, heavily pitted fruit (approximately 15%) was not used for
consumer evaluation. Consumers rated overall appearance, overall flavor, overall texture, overall juiciness and overall liking on a
9-point hedonic scale (Like Extremely = 9, Dislike Extremely = 1).
Consumers evaluated overall appearance of a group of 6–8 whole
oranges and overall flavor, overall texture, overall juiciness, overall
liking of sliced oranges. Three to four slices taken from a composite group of 3–4 sliced oranges were served on white paper
plates labeled with 3-digit numbers. Samples were served to consumers monadically in a randomized and balanced order to prevent
any position bias. Consumers were asked to cleanse their palates
94
H. McDonald et al. / Postharvest Biology and Technology 86 (2013) 91–99
with an unsalted soda cracker and filtered water between samples
(Chambers and Wolf, 1996).
subtracting TA from SSC (BrimA = SSC − k(TA)). A k factor of 4 was
used based on the data of Obenland et al. (2009).
2.4. Fruit quality analytical tests
2.5.2. Total phenolic content, vitamin C and ORAC analysis
sample preparation
Frozen juice samples from the fruit stored for 4 weeks (3 weeks
at 5 ◦ C and 1 week at 20 ◦ C), prepared as previously mentioned,
were lyophilized using an FTS Dura-Dry II Condenser Module freeze
dryer (SP industries, Warminster, PA). Following lyophilization,
samples were stored at −20 ◦ C until analysis (maximum storage
time before analysis was 10 weeks).
2.4.1. External damage
Three cartons for each irradiation dose were evaluated 1 d, 3
weeks and 4 weeks after irradiation. There were 4 layers of fruit
pattern packed in each carton. Fruit were returned to the same
layer after each evaluation. Fruit were visually rated for external
damage on a 1 to 6 scale where 1 = no damage, 3 = slight damage
and 6 = very severe damage. External damage was due to surface
pitting and/or discoloration.
2.4.2. Weight loss
Twenty fruit per treatment were weighed after 1 d of storage.
Fruit weight measurements were taken following 3 or 4 weeks
of storage on the same 20 fruit and the percent weight loss was
calculated.
2.4.3. Peel color, internal color, and firmness
External peel color, internal flesh color, peel compression force
were measured on 8 individual fruit per treatment. Peel compression force was measured (2 measurements per fruit) on the fruit
equatorial axis using GUSS Fruit Texture Analyzer (Model GS-15;
Strand, South Africa) using a flat plate probe. Peel color was also
measured on the equatorial axis. The fruit then were cut in half and
the flesh color was measured. Two measurements per fruit were
taken for color determination using a Minolta CR300 colorimeter
(Ramsey, NJ, USA).
2.4.4. Granulation and internal drying
Eight fruit were cut per each of the three replications and evaluated for presence or absence of granulation after 1 d and then after
3 and 4 weeks of storage. Fruit were determined to be granulated if
one or more fruit segments had a dry, crystalline appearance. At the
final evaluation (4 weeks), the fruit were also rated for the number
of segments showing drying.
2.5. Juice sample preparation
Eight fruit per replicate were juiced and then pooled for subsequent analyses. There were three replicates for each treatment.
The fruit were weighed to determine % juice content. After weighing, the fruit were juiced by hand using a commercial table-top
juicer (Model 932, Hamilton-Beach, Washington, NC, USA). The
juice was weighed and the percent juice calculated by dividing the
juice weight by the weight of the unpeeled portion. The juice was
then filtered through a screen sieve and placed into a 15-mL centrifuge tube for quality factors determination. The juice samples
were either kept at 5 ◦ C until analysis or frozen if it was necessary
to store the juice for more than a few days. This juice was used
for all subsequent analyses except that for aroma volatiles, which
required storage in special headspace vials. Juice for aroma volatile
analysis was placed into 12 mm × 32 mm glass vials and sealed with
a Teflon-coated septum, the samples being frozen at −20 ◦ C until
the time of analysis.
2.5.1. Soluble solids concentration, titratable acidity, and BrimA
Soluble solids concentration (SSC) was measured in filtered juice
by using a temperature-compensated refractometer (AO Scientific,
Model 10423, Buffalo, NY, USA) and titratable acidity (TA) by titration with 0.1 N NaOH to an end point of pH 8.2 using a Mettler T50A
automatic titrator (Columbus, OH, USA). Acidity was expressed as
percent citric acid. BrimA (Jordan et al., 2001) was derived from
2.5.2.1. Colorimetric total phenolics determination. Total phenolics
were assayed using the Folin–Ciocalteau colorimetric assay using
a method based on Waterhouse (2002), as described by Harrison
and Were (2007). Lyophilized solutions were prepared by dissolving 0.5 g lyophilized sample in 15 mL MeOH, stirring, and filtering
through 20–25 um filter paper. Once analytical solutions were prepared, 1 mL of gallic standard (0–0.4 mg/ml) or sample was added
to 15 mL HPLC grade H2 O in a 25 mL volumetric flask, followed by
1.25 mL of Folin–Ciocalteau’s reagent (MP Biochemicals, Solon, OH,
USA). The solutions were incubated at room temperature for 5 min,
and then 3.75 mL of 20% sodium carbonate solution was added to
each flask. The flasks were brought to volume with HPLC grade H2 O,
inverted, agitated, and incubated at room temperature for 90 min.
Following incubation, absorbance of three samples per treatment
was measured at 760 nm.
Individual phenolics of oranges were assayed via RP-HPLC–DAD
using an Agilent HP1100 liquid chromatography instrument
according to a modified method used by Borges et al. (2010).
Samples were prepared by dissolving 0.1 g of sample in 10 mL
of methanol:H2 O (1:1) solution and filtered through an Acrodisc
0.45 ␮m syringe filter. A sample injection volume of 10 ␮L was run
at a flow rate of 1 mL/min for 24 min at 40 ◦ C. Separation occurred
on a C18 Kinetex 2.6 ␮m 100 × 4.6 mm column (Phenomenex, Inc,
Torrance, CA). A binary gradient from 5% to 25% solvent B in 20 min
and returning back to 5% solvent B in 4 min was used; solvent A
being 0.1% formic acid in H2 O and solvent B being HPLC grade
acetonitrile. Wavelength used was 280 nm.
2.5.2.2. Vitamin C determination using 2,6-dichloroindophenol titrimetric method. Ascorbic acid content of oranges was measured
according to AOAC method 967.21 (AOAC, 2007). Samples were
prepared by dissolving 2 g lyophilized orange juice in 15 mL water,
then filtered through Fisher brand Grade Q8 filter paper (20–25 ␮m
particle retention). Two millilitres of the filtered solution was combined with 5 mL of metaphosphoric acid–acetic acid solution then
titrated with indophenol dye solution. The results were expressed
as the mass of l-ascorbic acid per kg of lyophilized orange juice
powder. Three measurements per treatment were averaged.
2.5.2.3. Oxygen radical absorbance capacity (ORAC) assay. The ORAC
values were assayed using a method adapted from Prior et al.
(2003). Sample solutions were prepared by dissolving 0.1 g of
sample in 10 mL of 1:1 MeOH:H2 O solution and filtering through
Fisherbrand Grade Q8 filter paper (20–25 ␮m particle retention),
1 mL of this solution being combined with 9 mL phosphate buffer
solution (pH 7.4). The top left well of a 96-well Falcon microplate
was filled with 200 ␮L of fluorescein working solution for gain
adjustment, and the remaining perimeter plates were filled with
200 ␮L of phosphate buffer solution. 20 ␮L of Trolox standards,
samples, and blanks (phosphate buffer). Three repeated measurements of the standards and samples were taken. The plate was
covered, inserted into the FLUOstar Omega microplate reader (BMG
Labtech, Cary, NC, USA) set with an emission of 520 nm and excitation of 485 nm. 20 ␮L of AAPH (21.6 g/L) was auto-injected into
H. McDonald et al. / Postharvest Biology and Technology 86 (2013) 91–99
95
Table 2
Predicted pitting and visual damage values for ‘Lane Late’ navel oranges treated at four different dose levels after 1d, 3 weeks, and 4 weeks following irradiation treatment
and measured by a trained sensory panel using unstructured, anchored 15 cm-scales where 0 = none and 15 = intense.
Dose (Gy)
Pitting
Visual damage
1d
0
200
400
600
*
0.96
0.27
0.87
0.77
3 weeks
*
ax
ax
ay
ax
0.65
1.05
2.04
3.39
4 weeks
bx
by
bz
ay
0.42
2.06
0.18
7.39
1d
bx
bz
bx
az
0.46
0.37
0.60
0.36
3 weeks
ax
ax
ax
ax
1.25
2.21
3.44
3.26
4 weeks
by
by
az
ay
1.25
2.71
0.86
4.44
by
bz
by
az
Values in the same row (x–z) or column (a and b) that are followed by the same letter are not significantly different (p ≤ 0.05).
each well immediately before auto-injection of 200 ␮L of fluorescein solution (0.036 mg/L). Fluorescence was measured every 140 s
and the measurement was repeated 35 times during the 120 min of
analysis, additional shaking being applied before each cycle. ORAC
Trolox Equivalents (TE) were calculated using Omega data analysis
software, and expressed as TE/kg freeze dried fruit.
2.5.3. Analysis of aroma volatiles
Samples for volatile analysis were removed from the freezer
and placed into a cooled (4 ◦ C) rack where they were held just
prior to analysis. Identification and quantification of volatiles was
conducted by solid-phase microextraction (SPME) using a 75-␮m
carboxen/polydimethylsiloxane fiber (Supelco, St. Louis, MO, USA)
and a Gerstel MPS-2 robotic system as previously documented
(Obenland et al., 2011). The measurement cycle was initiated by
transferring the vial into a heated (40 ◦ C) agitator where the vial
remained for 15 min, followed by insertion of the SPME fiber and
a 30 min trap time. Agitation speed was 4.2 s−1 . Following the end
of the trapping time, the SPME fiber was removed from the vial
and moved to the 280 ◦ C inlet of an Agilent 7890 GC (Palo Alto, CA,
USA) where the trapped volatiles were desorbed from the fiber over
a 2 min period and then analyzed in an Agilent 5975 mass spectrometer. Separation was accomplished using an Agilent HP-5ms
ultra-inert column (30 m × 0.250 mm I.D., 0.25 ␮m film thickness).
Details of the analytical run are provided in Obenland et al. (2008).
Volatile identification utilized comparison to Wiley/NBS library
spectrum, retention times of authentic standards and comparison
of retention indices based on n-alkane standards to published values. Volatiles were semi-quantified by comparison of analyte peak
areas to a standard curve of 1-pentanol and the resulting concentrations expressed as 1-pentanol equivalents. Three replicate samples
were measured per treatment with each replicate being run in
duplicate.
2.6. Statistical analysis
2.6.1. Sensory data
A linear mixed model was used to detect and assess the effects of
statistically significant variables (irradiation dose and age) on various measures for quality attributes (Laird and Ware, 1982). Model
building and goodness-of-fit analysis were carried out using the
R statistical software package (R Development Core Team 2011,
Vienna, Austria). For the sensory data analyses, regression models
were built for each of the following dependent variables, color, pitting, dehydration, visual damage, skin firmness, aroma, off aroma,
flesh color, granulation, juiciness, pulp texture, tart, sweet, overall
flavor, and off-flavor. For the consumer data analyses, regression
models were built for each of the following dependent variables
measuring the degree of liking of oranges in regards to overall appearance, overall flavor, overall texture, overall juiciness,
and overall liking. The appropriate complex correlation structure
induced by the repeated measurements corresponding to individual panelists were modeled via random effects. Model diagnostics
such as Q–Q plot, fitted versus residual plot and goodness of fit,
indicate no departures from the linear regression model assumptions.
2.6.2. Fruit quality analytical data
The best predictive model for each analytical test was selected
through model forward selection and backward elimination of
covariates using linear regression with the corresponding analytical test (color, visual appearance, peel firmness, SSC, TA, BrimA and
weight loss) as the outcome variable. For the volatile data a oneway analysis of variance was performed with SPSS (SPSS, Chicago,
IL, USA) and mean separations within storage time conducted using
Tukey’s test.
3. Results
3.1. Sensory evaluation
3.1.1. Trained panel
Irradiation, at any dose, did not affect the following sensory attributes throughout the shelf life of 4 weeks: color, aroma, off aroma, dryness, granulation, aroma
inside, off aroma inside, juiciness, pulp texture, orange flavor, off flavor, sweetness,
tartness, aftertaste, skin firmness (data not shown). However, a significant interaction was found between irradiation dose and age for pitting and visual damage
attributes. The irradiated oranges displayed significantly (p ≤ 0.05) increased pitting and visual damage, especially after 3 and 4 weeks storage (Table 2). Oranges
treated with 600 Gy dose were 6.97 units (based on a structured 15 cm scale) more
pitted compared to control after 4 weeks of storage. The overall visual damage of
the fruit treated with a 400 Gy dose were rated 2.19 units (based on a structured
15 cm scale) higher compared to control after 3 weeks while oranges treated with
a 600 Gy dose were rated 2.01 units higher compared to control also after 3 weeks.
On week 4, oranges treated with a 600 Gy dose were rated 3.19 units (based on a
structured 15 cm scale) higher compared to the control. Trained panelists determined that appearance attributes were primarily affected at dose levels of 600 Gy.
Also, age (or storage time) was a statistically significant factor affecting dehydration
(increased) and flesh color (lighter) for all oranges, control and irradiated (data not
shown).
3.1.2. Consumer panels
The regression models for appearance, overall liking, flavor, texture and juiciness
indicate that all oranges (control and irradiated) scored at or above 7 on the 9-point
hedonic scale, which translates to “Like Moderately” (Fig. 1). Overall liking hedonic
scores of irradiated oranges were not significantly different than untreated controls. Furthermore, acceptability scores for flavor, texture and juiciness for irradiated
oranges were not significantly different than the scores of control fruit. However,
consumers’ acceptability for overall appearance of irradiated oranges was significantly (p ≤ 0.05) different than control (Fig. 1). In terms of appearance, a significant
interaction was found between age and irradiation. The interaction more specifically
alludes to a significant (p ≤ 0.05) decrease in liking scores for overall appearance
when irradiated oranges are stored up to 35 d.
3.2. Fruit quality analytical tests
3.2.1. Analytical color
Irradiation or age did not affect color of the navel oranges (data not shown).
3.2.2. Granulation and internal drying
After 3 weeks of storage, 25% and 29% of the fruit treated at doses of 400 and
600 Gy, respectively, showed some degree of segment drying, while none of the
control or fruit treated at 200 Gy did (data not shown). Granulation was present in
an average of 17% of the 600 Gy fruit and in none of the other treatments (data not
shown). In contrast, trained panel data did not show significant changes due to dose
or age.
96
H. McDonald et al. / Postharvest Biology and Technology 86 (2013) 91–99
Fig. 1. Hedonic scores (predicted) for overall appearance, overall flavor, overall texture, overall juiciness and overall liking of control and 400 Gy treated ‘Lane Late’ navel
oranges measured 1 d following irradiation and after 4 weeks of storage (3 weeks at 1 ◦ C and 1 week at room temperature). A hedonic score of 1 = dislike extremely, 5 = neither
like nor dislike, and 9 = like extremely. Different letter denotes a statistically significant (p ≤ 0.05) difference.
3.2.3. Visual
With respect to visual measurements for external damage, we found a significant interaction (p < 0.001) between irradiation dose and age, which indicates
that the relationship between dose and age are dependent on each other. A significant increase in amount of visual damage was observed on all irradiated oranges
compared to control after 3 weeks and throughout 4 weeks of storage (Table 3).
Irradiation at 400 and 600 Gy resulted in an increase in visual damage for each day
of storage compared to control oranges. Visual scores for control oranges remain
fairly constant over time.
10 were found to change significantly (p ≤ 0.05) in concentration as a result of irradiation for either the 1 d or 4 week storage times or both (Table 7). The volatiles
increased in concentration as dose increased, with the effect of irradiation being
most pronounced at doses of 400 Gy and above, following 4 weeks of storage. The
affected volatiles were most commonly esters, although two aldehydes a ketone and
an alcohol also increased in concentration as a result of irradiation.
3.2.4. Firmness
Irradiation and age both impacted firmness (Table 4). Oranges treated with
a dose of 600 Gy were significantly (p < 0.001) softer or less firm compared to
untreated controls, while doses of 200 and 400 Gy had no effect on firmness.
This study shows that trained panelists were able to detect
increased pitting and visual damage in fruit treated by irradiation at 400 and 600 Gy. The effect was exacerbated by storage
for 3 and 4 weeks. Similarly, trained panelists in a study done
by O’Mahony and Goldstein (1987) found increased brown blemishing and pitting of whole navel oranges irradiated at 300 and
600 Gy. Evaluation of the fruit by an expert evaluator during our
fruit quality evaluation also indicated that a high degree of external damage was caused by the 400 and 600 Gy doses. Irradiation
induced pitting may be caused by the accumulation of phenolic
compounds in flavedo cells leading to cell death and peel necrosis that is manifest as pitting (Riov, 1975). The sensitivity of citrus
to visual damage appears to be heavily dependent on variety. For
example, Miller et al. (2000) observed a large variation in tolerance of orange and mandarin cultivars to irradiation as evaluated
by two experienced persons. Nagai and Moy (1985) found that
Valencia oranges were tolerant to 750 Gy treatment and storage
for 7 weeks at 7 ◦ C. In this study, the effect on appearance detected
by the trained panel was corroborated by the consumer panels,
which showed lower liking scores in overall appearance for the
irradiated oranges compared to the control fruit. Interestingly however, overall liking was not affected by irradiation with similar
overall liking scores for the control and treated fruit. Although consumers told us that they liked the appearance of untreated fruit
significantly more than irradiated fruit, their overall liking of irradiated fruit was not different than control. This could be a result of
removal of the most heavily pitted fruit from consumer evaluation.
O’Mahony et al. (1985) also observed that untrained consumers
were not able to tell the difference between untreated and irradiated navel oranges (0.6–0.8 kGy) even though expert judges were
able to detect differences in brown blemishing and flavor of irradiated fruit after 5–6 weeks in storage. In our study, there was a
3.2.5. Weight loss
Weight loss was significantly impacted by dose levels of 400 and 600 Gy as well
as age (Table 4). Oranges treated with a dose of 400 and 600 Gy significantly lost more
weight compared to untreated controls. Age had the same effect on all oranges, as
oranges aged the amount of weight loss increased.
3.2.6. TA, SSC, and Brim A
The highest dose (600 Gy) was found to have a small but significant (p < 0.05)
lowering effect on TA (Table 5). Another significant (p < 0.05) predictor of TA was age,
where TA decreased as the fruits (control and irradiated) aged. Oranges treated with
doses of 400 and 600 Gy were found to be significantly (p < 0.05) lower compared
to control oranges in terms of SSC (Table 5) but the difference was less than 0.5.
Age did not affect SSC. The highest dose (600 Gy) was found to have a significant
(p = 0.02) effect on BrimA (Table 5). BrimA values were lower for oranges treated
with a dose of 600 Gy. A dose of 200 or 400 Gy did not have any effect in regards
to BrimA. Another statistically significant predictor of BrimA was age, where BrimA
values increased when the fruit (control and irradiated) was stored.
3.2.7. Vitamin C and phenolic content of reconstituted frozen lyophilized juice
There was no effect of irradiation on ascorbic acid, total phenolic content or
associated antioxidant activity as assessed by ORAC (Table 6). The predominant
flavonoids in the orange samples were naruritin and hesperidin as assessed by
RP-HPLC–DAD. Levels of ferulic acid, naringin, and hesperidin in oranges were
not significantly different across irradiation doses, while naruritin levels increased
above 400 Gy (0.512, 0.466, 0.715, and 0.657 ␮g/mg at 0, 200, 400 and 600 Gy respectively).
3.2.8. Volatiles
Statistical analysis of the volatile data indicated that there was a significant
interaction (p ≤ 0.05) present between irradiation dose and storage time for a substantial number of aroma volatiles examined, necessitating that the dose effect be
presented for the 1 d and 4 week storage regimes individually. A total of 67 aroma
volatiles were identified in control and treated oranges (data not shown) of which
4. Discussion
H. McDonald et al. / Postharvest Biology and Technology 86 (2013) 91–99
97
Table 3
Predicted external damage values for ‘Lane Late’ navel oranges treated at four different dose levels and evaluated after 1 d, 3 weeks and 4 weeks following irradiation treatment
and measured by expert evaluators using 1–6 scale where 1 = no damage, 4 = moderate damage, 6 = very severe damage. % of fruit rated moderate or above is indicated next
to predicted mean score.
Dose (Gy)
External damage score and % of fruit rated 4 (moderate) and above
1d
0
200
400
600
*
3 weeks
*
2.0
1.9
2.1
2.1
ax
ax
ax
ax
6.9%
4.5%
10.8%
9.4%
4 weeks
2.1
2.3
3.0
3.6
bx
by
ay
ay
6.6%
7.3%
33.0%
55.9%
2.0
2.4
3.4
3.8
bx
ay
ay
ay
3.5%
11.1%
50.3%
68.4%
Values in the same row (x–z) or column (a and b) that are followed by the same letter are not significantly different. Multiple R-squared: 0.87.
Table 4
Predicted firmness and weight loss values for ‘Lane Late’ navel oranges treated at four different dose levels and evaluated after 1 d, 3 weeks and 4 weeks following irradiation.
Firmness (N)a
Dose (Gy)
Weight loss (%)b
1d
0
200
400
600
a
b
*
3 weeks
ax*
ax
ax
bx
30.79
30.40
29.81
27.26
4 weeks
32.46
32.07
31.48
28.93
ay
ay
ay
by
3.36
3.32
3.26
3.00
3 weeks
ay
ay
ay
by
4 weeks
0.7
0.7
0.9
1.1
bx
bx
ax
ax
2.2
2.1
2.4
2.5
by
by
ay
ay
Multiple R-squared: 0.07.
Multiple R-squared: 0.86.
Values in the same row (x–z) or column (a and b) that are followed by the same letter are not significantly different.
Table 5
Predicted TA, SSC and BrimA values for ‘Lane Late’ navel oranges treated at four different dose levels and evaluated after 1 d, 3 weeks, and 4 weeks following irradiation
treatment.
Dose (Gy)
TA (%)a
1d
0
200
400
600
a
b
c
*
0.63
0.61
0.61
0.59
BrimAc
SSC (% soluble solids)b
3 weeks
ax*
abx
abx
bx
0.59
0.57
0.57
0.55
4 weeks
ay
aby
aby
by
0.53
0.51
0.51
0.49
1d
ay
aby
aby
by
3 weeks
11.03
10.91
10.80
10.52
ax
abx
bx
cx
11.13
11.01
10.90
10.62
4 weeks
ax
abx
bx
cx
10.95
10.83
10.72
10.44
1d
ax
abx
bx
cx
8.50
8.48
8.36
8.19
3 weeks
ax
ax
ax
bx
8.75
8.73
8.61
8.44
4 weeks
ay
ay
ay
by
8.83
8.81
8.69
8.52
ay
ay
ay
by
Multiple R squared: 0.59.
Multiple R squared: 0.47.
Multiple R squared: 0.37.
Values in the same row (x–z) or column (a and b) that are followed by the same letter are not significantly different.
Table 6
Effect of irradiation treatment and storage for 3 weeks at 5 ◦ C plus 7 d at 20 ◦ C (4 weeks) on navel orange juice pH, ascorbic acid, total phenolsa and ORACb values
(mean ± standard deviation).
Dose (Gy)
0
200
400
600
a
b
*
pH
3.99
3.94
3.97
4.01
Ascorbic acid (g/kg)
±
±
±
±
*
0.04ab
0.01b
0.01ab
0.01a
114.36
116.31
106.90
106.09
±
±
±
±
Total phenols (g/kg)
6.15a
8.38a
8.19a
11.50a
6.41
6.08
5.05
5.96
±
±
±
±
ORAC (␮g/kg)
1.52a
1.10a
3.39a
2.08a
0.60
0.60
0.70
0.70
±
±
±
±
0.10a
0.10a
0.10a
0.20a
Total phenols: Folin–Ciocalteau colorimetric data expressed as gallic acid equivalents.
ORAC: oxygen radical absorbance capacity in ␮g trolox equivalents/kg sample.
Data with the same letter in the same column are not significantly different (p ≤ 0.05).
Table 7
Concentrations of aroma volatiles present in oranges exposed to 0, 200, 400, 600 Gy and stored for either 1 d at 20 ◦ C or 3 weeks at 5 ◦ C plus 7 d at 20 ◦ C (4 weeks). Only those
volatiles that significantly changed as a result of irradiation dose are presented.
Compound
1 d (␮g/L)
Dose (Gy)
0
200
400
600
0
200
Ethanol
2-Butanone
Ethyl acetate
Ethyl propanoate
Methyl butanoate
Hexanal
Ethyl butanoate
Ethyl 2-methylbutanoate
Methyl hexanoate
E-2-hexenal
697b*
9b
103b
22a
89a
132b
1585a
12b
14a
65a
774b
11b
100b
17a
66a
360a
1402a
14b
14a
89a
917ab
17a
162a
24a
69a
344a
2164b
23a
14a
70a
1,126a
20a
173a
23a
69a
174ab
1977b
13b
14a
57a
904b
NDa
64b
16b
86b
48a
1916b
19b
11b
69b
1141b
ND
103b
24b
79b
60a
2308b
29b
11b
69b
a
*
4 week (␮g/L)
400
969b
ND
110b
31b
87b
62a
2,364b
22b
10b
69b
ND, not detectable. Three replications were performed per treatment with each replicate being composed of the pooled juice from 8 fruit.
Different letters following concentrations of a compound within a storage time indicate that the values are significantly different from each other (p ≤ 0.05).
600
2184a
12
366a
91a
199a
78a
6026a
116a
23a
101a
98
H. McDonald et al. / Postharvest Biology and Technology 86 (2013) 91–99
significant interaction of age and irradiation treatment suggesting
that irradiation stresses the fruit and makes it more sensitive to
handling. The fruit in this study were commercially packed for the
Pacific Rim (high export pack in which fruit are packed so as to place
as much fruit as possible in the box). The fruit packs for visual damage evaluation were kept intact for the entire storage period. For
other evaluations, fruit was removed from the original packs; this
latter sample did not show as much visual damage as the fruit that
was tightly packed. This observation suggests that packing compression in conjunction with the irradiation may enhance bruising
of navel oranges. O’Mahony and Goldstein (1987) also observed
greater pitting in navel oranges of damp oranges, although this
was not the case in our study. In addition, the fruit used in this
study were late season navels, which had suffered stress due to a
wet winter. This may also have contributed to the greater impact
of irradiation. The effect of handling, packing density as well as
time of harvest should be evaluated in future studies. In addition,
our study evaluated a single variety of navels harvested from a
one geographic area location at one time period. This work should
be expanded to include multiple varieties harvested at different
times (even years), and from varied locations. Minimal negative
effects were observed at target doses of 200 Gy which points to
the need for reducing generic dose levels and also exploring combination treatments. For example, Palou et al. (2007) observed
that combining cold treatment with x-ray treatment allowed the
dose to be lowered to 30 Gy from 150 Gy to eliminate Mediterranean fruit fly in “Clemenules” mandarins. Irradiation induced
softness has been reported previously. Valencia oranges treated
at 300 and 450 Gy exhibited approximately a 10% loss of firmness when compared to control oranges, similar to the results of
our study (Miller et al., 2000). Additionally, ‘Murcott’ and ‘Temple’ mandarins treated at 450 Gy and a minneola variety treated
with 300 Gy were also shown to be softer when compared to the
control. Irradiation induced loss of firmness is associated with an
accelerated breakdown of pectin and other structural polysaccharides such as cellulose and hemicelluloses (Prakash et al., 2002;
McDonald et al., 2012). However, our trained panelists were not
able to detect changes in texture. Similarly, a panel of expert judges
was unable to detect changes in firmness of navel oranges treated at
600–850 Gy (O’Mahony et al., 1985) although they rated the resistance to bite of the control oranges to be slightly higher compared
to the control.
Trained sensory panelists in this study were unable to determine differences in internal dryness or granulation among the
control and irradiation treatments, even though analytical testing
had indicated that there was a positive association of irradiation
with segment drying at 400 and 600 Gy and with granulation at
600 Gy. This difference in results could have been due to the fact
that the trained panelists were evaluating fruit sections rather than
whole slices or that the drying and granulation, although present
in a number of the fruit, was fairly minor on a whole fruit basis.
The low prevalence of the drying and granulation was also indicated by results from the consumer panels, which found there to
be no differences among treatments for either texture or juiciness.
The aroma volatiles identified and quantified in this study are
aroma-active and many have been identified in previous studies as
having a potential impact on citrus flavor quality (Ahmed et al.,
1978; Hinterholzer and Schieberle, 1998). The esters especially,
with their sweet fruity essences, often have low odor thresholds
and have been associated with the development of off-flavor in citrus when concentrations increase as a result of waxing (Obenland
et al., 2011; Tietel et al., 2010) or due to other postharvest treatments (Obenland et al., 2012). Although we found that the 400 and
600 Gy doses of irradiation enhanced the concentrations of aroma
volatiles present in the fruit, this did not appear to result in a loss
in flavor quality given that both our trained and consumer sensory
panels found there to be no significant differences in the flavor or
overall liking between the control and irradiated fruit. The lack of
sensory impact of the increases in volatile concentrations was also
noted in sensory panel evaluations of aroma of both whole and
cut fruit, which found no differences due to treatment. Although
there was no sensory impact of the increases in aroma volatiles
that we observed, these changes indicate that irradiation is inducing metabolic alterations in the fruit that have the potential to alter
flavor at higher dose levels.
Similar to our data, O’Mahony and Goldstein (1987) saw a
decrease in SSC and TA at irradiation dose levels between 0.3 and
0.6 kGy but Miller et al. (2000) did not report changes in TA or
pH of navel oranges treated at irradiation doses of 0.15–0.45 kGy.
Miller et al. (2000) also did not observe dose dependent changes in
weight loss between dose levels of 0.15–0.45 kGy for navel oranges.
Hallman and Martinez (2001) saw no change in TA or % soluble
solids in “Rio Red” grapefruit, “Marrs” oranges, and “Darcy” tangerines treated up to 500 Gy. The overall changes in combined SSC and
TA that we observed, as shown by changes in BrimA after 4 weeks
of storage, were relatively small (0.31 units). This, combined with
the results of our sensory testing, suggest that the effects of irradiation on SSC and TA may have limited importance in terms of an
impact on flavor.
Blood oranges treated with 500 Gy gamma irradiation at 500 Gy
had higher ascorbic acid levels compared to the untreated control
although storage for 42 d caused a significant decrease in ascorbic acid content (Khalil et al., 2009). In our study, there was no
effect of irradiation on ascorbic acid. Similarly, gamma irradiation at 300 Gy did not have a significant effect on the vitamin C
content of Citrus clementina (Mahrouz et al., 2002). Based on an
increase in phenylalanine ammonia-lyase (PAL) activity, Mahrouz
et al. (2002) reported that synthesis of total phenolic content of Citrus clementina was enhanced during storage. In contrast, our study
found there to be no effect of irradiation on total phenol content at
any of the doses that we examined. It is possible that navel oranges
respond differently than clementines.
5. Conclusions
The primary effect of irradiation on quality was external damage (pitting and visual damage) of navel oranges treated at 400 Gy
and higher. The damage observed was fairly extensive. By the end
of the storage period it was judged that more that 50% of the
fruit at 400 and 600 Gy sustained moderate damage or greater.
Fruit with moderate to very severe damage were considered to
be unsalable, indicating that a large percentage of the fruit would
become unmarketable following treatment and storage. On the
other hand, while consumers rated the irradiated oranges lower
for overall appearance compared to the non-treated control, overall liking of the irradiated oranges was not rated differently. Other
quality factors such as aroma volatiles, internal drying/granulation,
TA, and SSC were also impacted but did not influence perceived
flavor as indicated by the trained sensory panel or consumers.
Color and juiciness were not impacted by irradiation and neither were the phenolic content or antioxidant capacity. Further
research should consider pack configuration on sensitivity of fruit
and also evaluate the use of combination treatments such as
cold with irradiation, which would allow a lower dose to be
used.
Acknowledgements
The project was funded by a TASC Grant from USDA-FAS. The
authors wish to thank Mary McCulloch and Yiqui Xia for their
H. McDonald et al. / Postharvest Biology and Technology 86 (2013) 91–99
assistance in executing the sensory tests and all of the trained
panelists and consumers who participated in this study.
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