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Article history: The citrus essential oil (EO) has several industrial applications due to its antioxidant and
Received 10 February 2020 antifungal properties. However, as the peels are susceptible to microbiological contamina-
Received in revised form 8 June 2020 tion, their by-products may undergo oxidation and reduction of bioactive compounds. For
Accepted 17 June 2020 this reason, this work aimed to evaluate the quality of the processed orange peel (albedo +
Available online 24 June 2020 flavedo), obtained after ozone application (for 2 h at 4 g L−1 and 40 g L−1 ) and drying (at 40,
50 and 60 ◦ C). The parameters evaluated in the study include drying kinetics, color, fungal
Keywords: count, pectin, EO yield, and antioxidant activity of the peels. The main results demonstrate
Orange peel by-products an improvement in the drying process, where the use of ozone boosted moisture diffusion.
Postharvest treatment Increased yield of extracted EO and the antioxidant capacity of peels were also described.
Oil yield Overall, this study contributed to a better understanding of how ozone acts on the physical,
Bioactive compounds chemical, and biological parameters of the citrus by-products.
© 2020 Institution of Chemical Engineers. Published by Elsevier B.V. All rights reserved.
1. Introduction (Yeoh et al., 2008), and sugars. Thus, a more profitable and
environmentally sound use would be the conversion of these
Citrus fruits account for a large portion of the world’s fruit wastes into biorefineries for the production of compost, ani-
tree crop, with over 129 million tons in 2018, of which oranges mal feed, biofuels, food additives, among other industrial and
make up about 58.4% of total production, followed by tanger- pharmaceutic uses (Zema et al., 2018).
ines with about 26.6%. Lemons and limes make up the third After extraction, the peel can be a nutrient-rich food in
most essential citrus species, with 15% of the produced total dry form, increasing the potential return for the orange juice
(FAO, 2020). Orange fruit wastes, consisting mainly of peel, industry and reducing organic wastes (Yeoh et al., 2008).
may account for 45% of total volume (Yeoh et al., 2008), and Orange peel EO is used to add orange flavor to various prod-
are available as by-products. However, these wastes, when ucts, for example, carbonated drinks, ice cream, cakes, air
not adequately treated, can cause environmental problems, fresheners, and essences (Braun and Cohen, 2015).
notably water pollution, due to the presence of compounds However, inadvertent contamination by chemical agents
with high biological activity, in particular essential oils and and fungi during the citrus production stages can also lead
polyphenols (Berna et al., 2000; Ferhat et al., 2008, 2006), pectin to a decline in safety and quality (Lee, 2013; Steinmetz and
∗
Corresponding author at: Department of Agricultural Engineering, Prototype Development Building, Western Paraná State Univer-
sity/PGEAGRI, Universitária Street, 2069 Cascavel-PR, 85819-110, Brazil.
E-mail addresses: taisebechlin@hotmail.com (T.R. Bechlin), suiangranella@hotmail.com (S.J. Granella).
https://doi.org/10.1016/j.fbp.2020.06.012
0960-3085/© 2020 Institution of Chemical Engineers. Published by Elsevier B.V. All rights reserved.
Food and Bioproducts Processing 1 2 3 ( 2 0 2 0 ) 80–89 81
Potter, 1996). In addition, the presence of fungi on the fruit peels (kgwater kg−1 dry matter ). Me values were obtained for each
surface reduces its quality and usefulness (Amaral et al., time interval studied since the equilibrium moisture content
2017; Shuping and Eloff, 2017). Also, under certain conditions, in longer drying times is not constant, it changes gradually
some of the fungal contaminants may secrete toxic metabo- according to the pressure of water vapor in the drying air
lites, namely mycotoxins, that are not destroyed by heat (intrinsic to temperature and water activity). Therefore, mois-
treatments, like convective drying. They have a cumulative ture desorption isotherms of the orange peel obtained by
capacity and are hardly eliminated by the human organ- Kammoun Bejar et al. (2011) were considered to obtain Me.
ism (Hashem and Alamri, 2010; Kumar et al., 2017; Tola and
Kebede, 2016). 2.2. Kinetic model-based on Fick’s second law
The traditional antimicrobial chemicals used in agriculture
for pest control are associated with several problems. There is For representing the drying curves, reduction of water content
currently a vigorous debate about the safety aspects of chem- on the orange peel, a kinetic model based on Fick’s second law
ical preservatives as they are considered dangerous to human was used (Eq. 2, according to Crank (1975)).
health (Stevic et al., 2014). Thus, the use of alternative tech-
−(2i−1)2 2 D
8
nologies, in particular the ozone application in food products, ∞ eff t
Mt – Me 1 4L2
has a significant advantage, besides leaving no residue on the MR = = 2 2
exp (2)
M0 – Me (2i − 1)
food surface; it is a powerful oxidizing agent against fungi, i=1
bacteria, and insect pests.
The fresh orange peel has a high moisture content that where: Deff is the effective moisture diffusion coefficient (m2
needs to be reduced for proper processing; subjecting the s−1 ), i is a positive integer, L is half of the slice thickness (m),
product to convective drying after ozone application can and t is the drying time (s).
guarantee more excellent safety during their processing in Since this theory assumes that moisture diffusion occurs in
agro-industries and biorefineries. Over 85% of industrial dryers the same dimension (infinite slab); and simplified first-order
used for processing products are of convective type, utilizing kinetic model can describe the global moisture of product with
combustion gasses or hot air as drying medium (Mujumdar, 2 mm of thickness, represented by Eq. 3, considering long dry-
2015). Knowledge of the kinetic mechanisms of drying is ing times (MR < 0.6)
essential to investigate the behavior of a product during the −2 D
eff t
drying process (Isik et al., 2019). Mt – Me 8 4L2
Oxidation capacity of ozone leads to qualitative and quan- MR = = 2 exp (3)
M0 – Me
titative losses of the products that may occur substantially
depending on the dosage applied (Alwi and Ali, 2014; Rodoni 2.3. Anomalous model for super-diffusion
et al., 2010). Also, it may influence the moisture diffusivity of
pretreated biological materials during drying. Therefore, the According to (Simpson et al., 2013), the anomalous diffusion
objective of this work was to evaluate the application of ozone model (Eq. 4) that uses the fractional time for porous biolog-
gas on the orange peel and subsequent convective drying. ical materials can adequately represent super-diffusion (n>1)
Effects on fungal count, color, oil and pectin yields, antioxi- using temporary fractional orders.
dant activity, and secondary compounds of the dried orange −2 D n
peels were determined. eff t
Mt – Me 8 4L2
MR = = 2 exp (4)
M0 – Me
2. Principles of drying theory
This model is also associated with long drying times and
Samples of 50 g of peels were used to monitor mass loss during was also used in the studies by Galaz et al. (2017) and Simpson
the drying process accompanied by the use of a balance with et al. (2015), both with satisfactory results. It is noteworthy that
a resolution of 0.01 g by gravimetric method. Drying was inter- when the anomalous model (Eq. 4) admits n = 1, it returns to
rupted when the moisture content of the orange peel was 12% Eq. 3 of the water diffusion of Fick’s law.
(wb), estimated mathematically by reducing the mass accord-
ing to the initial moisture content of the product. During the 2.4. Mathematical model
drying process, the air temperature and relative humidity were
monitored with the aid of two thermo-hygrometers. Relative For the study of the drying curves of orange peel, the Page
humidity into dryer was obtained mathematically through the model (Eq. 5) was used. In general, it has shown a good fit for
air’s psychometric principles. Thus, with these data, it was drying data applied to long drying periods, as in drying hydro
possible to obtain and study the drying curves (time × mois- of orange peels (R2 >0.99, Casso-Hartmann et al. (2016)).
ture ratio).
MR = k1 exp(−k2 tn ) (5)
2.1. Moisture ratio
where k1 is a constant dependent on material geometry (k1 =
Moisture ratio (MR) was determined according to the Eq. 1: 0.81 for an infinite slab), k2 is a constant dependent on the Deff
and geometry, and n assumes value 1 for the Fickean drying
Mt – Me process or different to 1 for anomalous cases.
MR = (1)
M0 – Me The differences in diffusion processes during drying are
mainly related to the food microstructure; therefore, just one
where Mt is the moisture content at some time (kgwater kg−1 value of n should represent all the processes, independent of
−1
dry matter ), Me is equilibrium moisture content (kgwater kg the drying temperature (n constant), while k2 must be increas-
dry matter ), and M0 is the initial moisture content of the orange ing with temperature. Under these constraints, it is possible
82 Food and Bioproducts Processing 1 2 3 ( 2 0 2 0 ) 80–89
to fit all the drying data (considering the three temperatures) Three replicates of the drying process and drying kinetics anal-
and search for a unique value of n and k2 for each temperature yses were performed. Three replicates of the drying process
(Simpson et al., 2015). and drying kinetics analyses were performed.
For modeling, the differences between the model predic-
tions and the experimental measurements were quantified 3.3. Methods
using the root-mean-square error (RMSE) and the residual sum
of squares (RSS), shown below through equations Eq. 6 and Eq. 3.3.1. Fungal count (FC)
7, respectively. The correlation coefficient (R2 ) was also used Fresh and dried orange milled peel samples (10 g) were added
for the analysis of the model. to 90 mL of 0.1% peptone salt solution, following by stirring
for 60 s, obtaining the first dilution (10−1 ). The second dilution
n 2 (10-2 ) was obtained by adding 1 mL of the first dilution to 9
i=1
xexperimental − xpredicted
SE = (6) mL of peptone water. Surface plating was carried out in DRBC
df
agar, with 0.1 mL inoculum in duplicate; plates were incubated
at 25 ± 2 ◦ C for 72 h in a B.O.D incubator (MAPA, 2003). Results
1 2
n
were expressed in cfu g−1 of orange peel.
RSS = xexperimental − xpredicted (7)
n
i=1
3.3.2. Color
where: n is the total number of measurements, and x is the The parameters CIELab (L*, a*, b*) of milled orange peel were
variable to be compared. measured using a colorimeter (Model CR410, Minolta Osaka,
Japan). L* indicates lightness with 0 = black and 100 = white,
a* indicates chromaticity on a green (−) to red (+) axis, and b*
3. Material and methods
indicates chromaticity on a blue (−) to yellow (+) axis. To read-
ings of the color indices, the samples were arranged in circular
3.1. Sampling and locale of study
containers, and readings were performed in triplicate. To eval-
uate the magnitude of color change, the three-dimensional
Sweet orange (Citrus sinensis) peels were obtained from local
parameter E was calculated using the following equation:
commerce in the city of Cascavel-PR, Brazil. The orange juice
was extracted using an industrial food juicer (EXB-N, Skym-
2 2 2
sen, Brusque, Brazil), and the peels transported on the same (L∗ ) + (a∗ ) + (b∗ )
E = (9)
day to the laboratory. The peels (flavedo + albedo) were sani- 2
tized, and the excess endocarp was removed with the aid of
a spoon. In sequence, peels were cut obtaining the follow- 3.3.3. EO yield
ing mean dimensions: 10.0 × 2.5 × 0.35 cm (length × width Samples of orange peel weighing 100 g were suspended in 500
× thickness) (Fig. 1). After homogenization, the material was mL of distilled water and subjected to conventional hydrodis-
packaged into polyethylene bags and stored at −5 ◦ C. The tillation for 3 h using a Clevenger apparatus, as described by
moisture content (73.89 ± 0.60 %, wb, n = 3) of the fresh peel Bustamante et al. (2016). Extraction was performed, and the
was determined using 20 g sample in an oven at 105 ◦ C for 24 obtained EO was collected, dried over anhydrous sodium sul-
h. fate (Na2 SO4 ), and stored at 5 ◦ C in amber glass flasks. The EO
yield was expressed g of EO per 100 g of dried peel.
Fig. 1 – Schematic representation of the orange peel slices obtaining and average dimensions.
Fig. 2 – Convective drying kinetics for the six treatments (ozone pretreated samples at (A) 4 g L−1 and (B) 40 g L−1 , and
dried at 40, 50 and 60 ◦ C). Dots are experimental data, the vertical bars are the standard deviation, and dotted lines are the
predicted data (MR < 0.6) using Fick’s second law model.
Fig. 3 – Convective drying kinetics for the six treatments (ozone pretreated samples at (A) 4 g L−1 and (B) 40 g l−1 , and
dried at 40, 50 and 60 ◦ C). Dots are experimental data, the vertical bars are the standard deviation, and dotted lines are the
predicted data (MR < 0.6) using the anomalous diffusion model with n dependent on temperature.
Table 2 shows the values of Deff calculated by anomalous same conditions negatively influenced (p < 0.05) the antiox-
diffusion and Fickean diffusion models. Based on the Deff idant activity by DPPH method (IC50 = 5.70 ± 0.04 mg mL−1 ,
results, in all conditions, the diffusivity for the Fickean solu- Table 3). Whereas, the highest antioxidant activity, presented
tion (n = 1) was lower than for the anomalous solution (n = / here by the lowest IC50 index, occurred when the sam-
1). The Deff values ranged from 0.23 ± 0.05 × 10−8 m2 s-1 to ples were subjected at 4 g O3 l−1 and 60 ◦ C (IC50 = 4.09
1.33 ± 0.02 × 10−8 m2 s-1 at 40 and 60 ◦ C and under ozone ± 0.12 mg mL−1 , Table 3). Thus, an increase in ozone con-
pretreatment at 4 g L-1 , and from 0.94 ± 0.06 × 10−8 m2 s-1 centration from 4 to 40 g O3 l−1 per 2 h exposure time
to 1.52 ± 0.01 × 10−8 m2 s-1 at 40 and 60 ◦ C under ozone pre- may have an inverse effect on the product’s antioxidant sys-
treatment at 40 g L-1 , by Fickean diffusion model. For the tem.
case of the anomalous diffusion model with n variable, the The values of color a* and b* for the control corresponded
Deff values ranged from 2.34 ± 0.75 × 10−8 m2 s-1 to 11.02 to 1.11 ± 0.14 and 57.12 ± 0.90, respectively. In the treated peel
± 1.23 × 10−8 m2 s-1 . However, this variation was not linear samples, the color a* varied from 5.67 ± 0.24–9.04 ± 0.38, and
with the increase in the drying temperature from 40 to 60 ◦ C, color b* varied from 37.90 ± 0.89–43.17 ± 1.50 (Table 3). The
since the values of n, also non-linear, affected the diffusiv- color parameter b*, positive, indicates more yellowish tones.
ity solution. Thus, although the Page model could represent Another observation can be noted by the color a*, in which
the drying experimental data, it lacks phenomenological sup- the values of ozonized and dry samples increased consider-
port (Simpson et al., 2013). In this case, ozone pretreatment for ably compared to control (p < 0.05). In this context, as the
drying can affect the parameters of the equation and directly color parameter a*, negative, indicates greenish tones, the
interfere with the properties of the materials. control sample presented coloration in the region between
green and yellow, with more influence of yellow. The color
4.2. Effects of the processing on orange peels parameter L was negatively affected (p < 0.05) by the use of
higher ozone concentrations and higher drying temperatures.
The EO yield was most positively influenced (p < 0.05) when This means that the increase in ozone concentration made
orange peels were submitted to a higher ozone concentra- the peel samples darker, with L* values ranging from 62.98 ±
tion of 40 g l−1 and drying air temperature at 40 ◦ C with 0.43–74.86 ± 0.12. Control samples obtained an L* value of 78.87
a value of 4.48 ± 0.07 g 100 g−1 (Table 3). However, these ± 0.18.
Food and Bioproducts Processing 1 2 3 ( 2 0 2 0 ) 80–89 85
0.45
0.29
0.37
RSS
activation energy for ozonized and dried orange peels.
Ozone Drying Fickean Anomalous
pretreatment Temperature diffusion diffusion
(g L−1 ) (◦ C)
Deff ×10−8 Deff ×10−8
0.51
0.56
0.58
RSS
RMSE×10−2
(m2 s −1 ) (m2 s− 1 )
1.58
0.67
1.73
4 50 1.15 ± 0.11 11.34 ± 1.23
60 1.33 ± 0.02 6.53 ± 2.11
40 0.94 ± 0.06 2.63 ± 0.61
RMSE*×10−2
0.994
0.997
0.996
3.33
4.18
3.76
R2
Table 1 – Coefficient values obtained for each drying curve modeling of the ozonized orange peels and their respective statistical parameters.
0.0029 ± 0.0004
0.0016 ± 0.0009
0.0039 ± 0.0011
5. Discussion
Ozone pretreatment at 4 g L
0.0020 ± 0.0003
0.0067 ± 0.0014
0.0049 ± 0.0006
k2
Temperature
40 ◦ C
50 ◦ C
60 ◦ C
Table 3 – Essential oil yield, antioxidant activity by the DPPH method, color parameters of ozonized and dried orange
peels, and control samples.
Ozone pretreatment Drying Temperature EO yield (g 100 g−1 Color
IC50 (mg mL−1 )
(g L−1 ) (◦ C) dried peel)
L* a* b*
Control 4.25 ± 0.08b 4.31 ± 0.20d 78.87 ± 0.18a 1.11 ± 0.14a 57.12 ± 0.90a
4 40 4.18 ± 0.07b 5.21 ± 0.21b 69.78 ± 0.28c 9.04 ± 0.38e 42.32 ± 3.05b
4 50 4.08 ± 0.06c 4.57 ± 0.01c 74.86 ± 0.12b 5.67 ± 0.24b 43.17 ± 1.50b
4 60 3.19 ± 0.01d 4.09 ± 0.12e 73.20 ± 0.18b 6.64 ± 0.52c 37.90 ± 0.89d
40 40 4.48 ± 0.07a 5.70 ± 0.04a 62.98 ± 0.43d 8.91 ± 0.19e 39.07 ± 0.75c,d
40 50 4.22 ± 0.02b 5.34 ± 0.02b 73.81 ± 0.42b 6.93 ± 0.39c 40.93 ± 0.58b,c
40 60 3.37 ± 0.05d 4.41 ± 0.28c,d 72.75 ± 0.57b 8.22 ± 0.33d 40.19 ± 1.05c
IC50 : concentration of the peel extract necessary to inhibit the formation of DPPH radicals in 50%.
Results expressed with the mean ± standard deviation (n = 3). Different letters in each row indicate a significant difference (p < 0.05) according
to the LSD’s test.
Fig. 4 – Phenolic content, fungal count, and pectin yield of ozonized and dried orange peels, and control samples. Vertical
bars are the standard deviation obtained from the three replicates. Different letters indicate significant differences among
treatments (p < 0.05).
of small portions of ozone (4 g L-1 ) as a pretreatment was suf- as oxidation may occur by a peroxyl radical interceded chain
•
ficient to increase water diffusivity during the drying process reaction (ROO ), the applied ozone may accelerate the chain
of the orange peels. reaction by the ease of dissociation, accumulating peroxyl rad-
In convective drying, the transport of moisture (liquid and icals. The superoxide dismutase (SOD), ascorbate peroxidase
vapor) occurs in several ways. The liquid transport is slower, (APX), and catalase (CAT) enzymes are considered the main
and a higher temperature gradient is needed to accelerate the response mechanisms for stress-induced by ozone (Gutiérrez
moisture diffusion. However, the increase in temperature of et al., 2018; Wu et al., 2019), due to the accumulation of ROO
convective drying can affect the chemical constituents of the radicals. Due to the advancement of ozone-induced product
materials (Chua et al., 2019). The volatile molecules that form senescence, the increased activity of these enzymes gener-
the oils present in some biological materials are more sensitive ates ROS, which, in turn, improves antioxidant mechanisms
to heat. Thus, the loss of aromatic compounds due to the use for their protection. A hypothetical schema exhibiting possible
of higher drying temperatures helped to decrease the EO yield induction of some antioxidant enzymes by ozone treatment
of orange peels verified in our work. is shown in Fig. 5. Our results are also in agreement with
On the other hand, the weakening of the orange peel struc- those of Sudheer et al. (2016), where the application of 9 l
tures by ozone may also have influenced the yield of extracted O3 L−1 for 1 h was sufficient for a slight increase in antioxi-
essential oil. Although oil is not found in more internal regions dant activity in mushrooms, and utilization of 100 mg O3 L−1
like water, the weakening of the superficial layers that make for 90 min improved Juniper berries antioxidant status after
up the peel was sufficient to increase this yield. During the gas application (Brodowska et al., 2015). Regarding convective
hydrodistillation process, the heating of the plant material is drying, higher drying temperatures (60 ◦ C) best retained the
not sufficient to break entirely the structures accommodating antioxidant activity of the orange peel than the temperature
the fragrant molecules that are carried in the resulting steam; at 40 ◦ C. As also reported in the convective drying of strawber-
the use of an oxidizing agent like ozone, in this case, helps ries by Méndez-Lagunas et al. (2017). Heat treatments, such as
break down the oil glands located on the exocarp of the fruit hot-air drying, can induce antioxidant enzymes POD and CAT
and release these compounds under exogenous effect. (Wahid et al., 2007). The physiological response to heat can
Antioxidants are sometimes defined as agents capable of come with the accumulation of carotenoid and terpenoid com-
reacting with radicals, quantified in this work by the hydrogen pounds involved in the photoprotection of cells (Nisar et al.,
transfer reaction mechanism between the DPPH radical and 2015).
the antioxidant (AH). However, a better definition would be of Phenolic compounds are one of the primary phytochemi-
compounds capable of retarding the oxidation of an oxidizable cals with the antioxidant activity present in citrus peels. The
material (Amorati et al., 2013), focusing on biological mate- increased level of these compounds in ozone-treated products
rials, in particular orange peel, the organic constituents to may be due to the activation of the enzyme phenylalanine
protect against oxidation would be most essential oils. Thus, ammonium lyase (PAL) (Toivonen and Brummell, 2008), which
Food and Bioproducts Processing 1 2 3 ( 2 0 2 0 ) 80–89 87
Fig. 5 – Hypothetical model representing the oxidative stress caused by ozone treatment on orange peel and induction of
some antioxidant enzymes.
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