Research Article

Received: 3 September 2019 Revised: 27 November 2019 Accepted article published: 5 December 2019 Published online in Wiley Online Library: 28 December 2019

(wileyonlinelibrary.com) DOI 10.1002/jsfa.10178

Interaction and multi-objective effects of

multiple non-thermal treatments of sour
cherry juice: pesticide removal, microbial
inactivation, and quality preservation
Gulsun Akdemir Evrendilek,a,b* Eda Keskina and Ozgur Golgec

Abstract
BACKGROUND: The consumption of pesticide-contaminated sour cherries as fruit or juice has become a major health concern,
and so the search for alternative processing technologies, such as pulsed electric fields (PEF), ozone (O), and ultrasonication
(US) has intensified. The objectives of this experimental study of sour cherry juice were fourfold: (1) to quantify the removal
efficiency of new processing technologies (PEF, O, US), and their combinations, for the pesticides chlorpyrifos ethyl, 𝝉-fluvalinate,
cyprodinil, pyraclostrobin, and malathion; (2) to detect their impact on physical, bioactive, and sensory properties; (3) to
determine their microbial inactivation levels for Escherichia coli O157:H7, Bacillus cereus, Pseudomonas syringae subs. Syringae,
and Penicillum expansum; and (4) to jointly optimize multiple responses of physical, quality, and sensory properties, pesticides,
and microbial inactivation.
RESULTS: Except for all the O treatments, the physical, bioactive and sensory properties of sour cherry juice were not adversely
affected by the treatments. The joint optimization suggested PEF1 (24.7 kV cm−1 for 327 𝛍s), PEF2 (24.7 kV cm−1 for 655 𝛍s),
PEF2 + O + US, US, and PEF2 + O as the five best treatments. PEF2 + O + US best achieved both pesticide removal and microbial
inactivation.

CONCLUSION: PEF2 + O + US provided promising reductions in pesticide and microbial loads.

© 2019 Society of Chemical Industry

Keywords: sour cherry juice; pesticide removal; pulsed electric fields; bioactive compounds; physical properties; microbial inactivation

INTRODUCTION
With its antioxidant, anti-inflammatory, antibacterial, and antidi-
abetic properties, and high nutritional value, sour cherry (Prunus
cerasus L.) is one of the most attractive fruits1 with a global pro-
duction of 1.2 million tons in 2017.2,3 Sour cherries suffer from
contamination with pesticides sprayed at different stages of their
production to increase yield. Pesticides remain in end products
such as fruit or juice.4 Due to their carcinogenic, toxic, and muta-
genic effects,5,6 pesticide residues have become a major health
concern with important economic consequences.7
Although it is not effective, washing with or without reagents
such as sodium chloride (NaCl), sodium carbonate (Na2 CO3 ), or
acetic acid (CH3 COOH) is the most common first step to remove
dirt particles, microbial load, and pesticides.8–11 The search for
alternative and practical food-processing technologies to degrade
or remove pesticides in food products has been intensified
recently. The focus for such innovative technologies for pesticide
removal has been on ozone, non-thermal plasma (NTP), pulsed
electric fields (PEF), gas phase surface discharge plasma (GPSDP),
ultrasonication (US), and alkaline electrolyzed water (AEW). Ozone
is mostly used for surface decontamination and to extend the
shelf life of fruit and vegetables: 4 μg L−1 dissolved ozone con-
centration in water was effective in removing the carbosulfan
pesticide removal was reported for lettuce, grape, apple, mustard,
lemon, orange, grapefruit, corn, wheat, and lychee.13–16 Pulsed
electric fields with 8–20 kV cm−1 electric field strength (EFS) and
6–26 pulses (P) achieved the removal of methamidophos and
chlorpyrifos spiked in apple juice.17 Acoustic cavitation gener-
ated by ultrasonic radiation destroys the chemical and organic
contaminants such as pesticides in aqueous solution.18,19 How-
ever, a large knowledge gap exists in the related literature about
the comparison of the interaction and multi-objective effects of
ozone, US, PEF, and their combinations on multiple pesticides and
pathogens, and whether these measures compromise physical
and sensory properties. The objective of this experimental study
∗ Correspondence to: GA Evrendilek, Department of Food Engineering, Faculty
of Engineering, Bolu Abant Izzet Baysal University, Bolu, Turkey.
E-mail: gevrendilek@yahoo.com
a Department of Food Engineering, Faculty of Engineering, Bolu Abant Izzet
Baysal University, Bolu, Turkey
b Department of Food Engineering, Faculty of Engineering, Ardahan University,
Ardahan, Turkey
c Faculty of Tourism, Department of Gastronomy and Culinary Arts, Alanya
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residue in processed tomato juice.12 The efficacy of ozone in Alaaddin Keykubat University, Antalya, Turkey

J Sci Food Agric 2020; 100: 1653–1661 www.soci.org © 2019 Society of Chemical Industry
 www.soci.org
Table 1. Pesticides and their properties
Pesticide Group Classification
Chlorpyrifos ethyl Insecticide Organothiophosphate
𝜏-Fluvalinate Insecticide Synthetic pyrethroid
Cyprodinil Fungicide Anilinopyrimidine
Pyraclostrobin Fungicide Strobilurin
Malathion Insecticide Organothiophosphate
was therefore to quantify comparatively the efficacy of ozone, US,
PEF, and their combinations for the removal of five pesticides and
four pathogens without significant adverse impacts on physical
and sensory properties of sour cherry juice.
MATERIALS AND METHODS
Sour cherry juice
Sour cherry juice was acquired from Dimes Gıda San. Tic. Anon. Şti
(Tokat, Turkey). The samples were kept at 4 ∘ C until used for further
analyses.
Microbial cultures
Escherichia coli O157:H7 (EDL 931040504) culture was obtained
from National Type Culture Collection of Refik Saydam Hıfzısıhha
Center (Ankara, Turkey) in the lyophilized form. Bacillus cereus and
Pseudomonas syringae subs. syringae were isolated from infected
plants, and Penicillium expansum was isolated from an infected
orange plant. These cultures were obtained from the Department
of Plant Pathology of Mustafa Kemal University (Hatay, Turkey).
Escherichia coli O157:H7, B. cereus, P. syringae subs. syringae, and P.
expansum were activated by transfer into Escherichia enrichment
broth (Becton Dickinson, Maryland, USA), nutrient broth (Becton
Dickinson), and Pseudomonas enrichment broth (Becton Dickin-
son), respectively. Activated cultures of E. coli O157:H7 and B. cereus
were incubated at 35 ± 2 ∘ C for 2 days, whereas P. syringae subs.
syringae and P. expansum were incubated at 22 ± 2 ∘ C for 3–5 days,
respectively. The cultures that were grown were centrifuged at
5200 g for 15 min, while the pellets were resuspended with 10 mL
pre-sterilized phosphate-buffered saline (PBS, pH 7.2). Viable bac-
terial concentrations were determined using a tenfold serial dilu-
tion of 0.1 mL aliquot on a tryptic soya agar (TSA, Fluka, Germany)
plates. Each of the final bacterial concentrations inoculated into
the juice samples was at the level of 106 to 107 cfu mL−1 .
Pesticides
Chlorpyrifos ethyl, 𝜏-fluvalinate, cyprodinil, pyraclostrobin, and
malathion pesticide standards with 92-to-98 μg mL−1 purities
(Table 1) were obtained from Sigma-Aldrich (Munich, Germany).
Stock solutions at 1000 mg L−1 concentration (w v−1 ) were pre-
pared with acetonitrile (Sigma-Aldrich, St Louis, MO, USA). The
juice samples were contaminated with them, with the final con-
centrations of 50 mg L−1 before the treatments.
Pulsed electric fields
A bench-scale PEF system (OSU-4A, The Ohio State University,
Columbus, OH) was used to treat the control samples. Six treat-
ment chambers of the co-field flow type, with 0.23 cm diame-
ter and 0.292 cm gap distance, were adopted as the PEF sys-
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tem. Square-wave bipolar pulses with 3 μs pulse duration and
wileyonlinelibrary.com/jsfa © 2019 Society of Chemical Industry
GA Evrendilek, E Keskin, O Golge
Formula CAS number
C9 H11 Cl3 NO3 PS 2921-88-2
C26 H22 ClF3 N2 O3 102 851–06-9
C14 H15 N3 121 552–61-2
C19 H18 ClN3 O4 175 013–18-0
C10 H19 O6 PS2 121–75-5
20 μs pulse delay time were applied. The PEF parameters that
were used were 500 pps frequency, 24.7 kV cm−1 EFS, 60 mL min−1
flow rate, and the two treatment times of 327 μs (PEF1), and
655 μs (PEF2). The initial temperature of the juice before PEF treat-
ments was 10 ± 2 ∘ C, and it increased to 22 ± 2 ∘ C during PEF
treatments.
Processing temperature before and after each treatment was
monitored using K-type thermocouples (Fisher Scientific, Pitts-
burgh, PA, USA). Frequency, pulse width, and pulse delay time
were adjusted using a pulse generator (Model 9310 Pulse Gen-
erator, Quantum Composer Inc., Bozeman, MT, USA) and were
monitored using an oscilloscope (Model TDS 210 Two Channel
Digital Real Time Oscilloscope, Teknotronix Inc., Beaverton, OR,
USA). Constant pulseless flow was provided using a gear pump
(EW-07002-23 model, Cole-Palmer, Inst. Company, Vernon Hills,
IL, USA).
Ozone
A bench-scale ozone generator (OXYTIME 7F 5 mini model, Ankara,
Turkey) with a corona-discharge technology to produce ozone
gas was used. Ozone at 20.2 g m−3 dose for 3 min was applied
to the samples at room temperature. Ozone dose was measured
using a dissolved ozone analyzer (ATI model Q45H/64, Analyt-
ical Technology Inc., Collegeville, PA, USA) with an accuracy of
±0.02 ppm.
Ultrasonication
The ultrasonication (US) treatments were conducted using a soni-
cator (Bandelin Sonorex, Berlin, Germany) with 160/640 W power,
2.5 A, and 35 kHz frequency. Ultrasonication at 35 kHz frequency
was applied for 3 min at room temperature.
Combined applications
A dual or triple combination of PEF (PEF1 and PEF2), O, and
US was applied as PEF1 + O, PEF2 + O, PEF1 + US, PEF2 + US,
PEF1 + O + US, and PEF2 + O + US at room temperature.
Physical properties
The pH was measured using an Orion 420 A model pH meter
(Inolab WTW, Weilheim, Germany). Total soluble solid (TSS) mea-
surements were made using a 507–1 model refractometer (Nip-
pon Optical Works Co. Ltd, Tokyo, Japan). Hand-held conductivity
meter (Sension 5 model, Hach, Loveland, CO, USA) was used to
determine conductivity (mS cm−1 ). Turbidity after centrifugation
at 2300 g for 5 min was measured using a turbiditimeter (Micro TPI,
Model 20 008, HF Scientific, Fort Myers, FL,USA) whose results were
recorded as Nephelometric Turbidity Unit (NTU). The color values
of L*, a* and b*, and associated estimates of chroma (C*) hue (h∘),
and total color difference (ΔE), were obtained using a Hunter Lab
Color Flex spectrophotometer (Hunter Associates Laboratory Inc.,
Reston VA, USA).
J Sci Food Agric 2020; 100: 1653–1661
Non-thermal treatments of sour cherry juice
Total antioxidant capacity
The DPPH (2,2-diphenyl-1-picryl-hydrazyl-hydrate) free radical
method was used, with some modifications, to determine the
total antioxidant capacity (% TAC).20
Total phenolic compounds
The Folin–Ciocalteu method at 720 nm was performed with some
modifications with a standard curve prepared using 50, 100, 200,
300, and 400 mg gallic acid mL−1 stock solutions to determine the
concentration of total phenolic compounds (TPC).21
Total monomeric anthocyanin capacity
The pH differentiation method was utilized using a spectropho-
tometer to measure the total monomeric anthocyanin content
(TMAC) as mg 100 mL−1 .22
Total ascorbic acid concentration
Total ascorbic acid concentration (TAAC) was determined using a
spectrophotometer at 254 nm. It results were expressed using Eqn
(1):
Abs(sample 254 nm) xcurve factor
ascorbic acid mL−1 (mg 100) = x100
DF
(1)
where DF represents the dilution factor.
Pesticide analyses
Sample preparation
QuEchERS pesticide analyses were applied with some
modifications:23 15 mL of the samples was placed into 50 mL
Teflon tubes and 15 mL of acetonitrile-acetic acid mixture (99:1 v
v−1 ), 6 g magnesium sulfate, and 1.5 g sodium acetate were added.
After being mixed for 1 min (Nuve NM-110, Ankara, Turkey), the
mixture was centrifuged for 2 min at 5200 g (Eppendorf 5804,
Hamburg, Germany); 8 mL of the sample from the upper layer was
transferred into tubes containing 1.2 g MgSO4 and 0.4 g primary
secondary amine (PSA) and was centrifuged for 2 min at 5000 rpm,
and 1.5 mL was taken from the upper layer into 1.5 mL vials for
liquid chromatography – mass spectrometry / mass spectrometry
(LC–MS/MS) analyses.
Pesticide analyses by LC–MS/MS
The Shimadzu Prominence/20 series (Shimadzu, Tokyo, Japan)
LC–MS/MS system was used with a LC-20 AD binary pump, a
SIL-20 AHT autosampler, a DGU-20A3 online degasser, and a
CTO-10AS VPI column oven coupled to an Applied Biosystems
(Foster City, CA, USA) 3200 triple quadrupole tandem mass spec-
trometer equipped with a Turbo V electrospray ionization (ESI)
interface source. Nitrogen gas, at 99% purity, produced from a Peak
Scientific nitrogen gas producer (Billerica, MA, USA) was used in the
ESI source and the collision cell.24
Chromatographic separation was performed at 30 ∘ C using an
Intersil ODS-4 column (50 mm × 2.1 mm i.d., 3 μm) (GL Sciences
Inc., Tokyo, Japan) connected to a fusion-RP guard column (4 mm
× 2.0 mm i.d., 3 μm) (Phenomenex, Torronce, CA, USA). Mobile
phase was formed using solvents A (ammonium format in 5 mM
water) and B (ammonium format in 5 mM methanol) with 0–8 min
95 v v−1 B and 8–12 min 5 v v−1 B. Mass spectrometry analyses
were conducted using an ESI source either in a positive or negative
mode. The ESI parameters adopted were thus 4.5 kW ion spraying
J Sci Food Agric 2020; 100: 1653–1661 © 2019 Society of Chemical Industry
www.soci.org
voltage, 500 ∘ C source temperature, 30 psi curtain gas, 1 40 psi
ionizing gas source, 2 × 60 psi ionizing gas sources, and 5 psi
collision gas (nitrogen). Aliquots of 15 μL of sample extract or
standards were injected into the column.24
A scheduled multiple reaction monitoring mode (MRM)
was used in the ESI-MS/MS system. Two of the most intense
precursor-to-product ion transitions were registered for each ana-
lyte. Quantification and confirmation were carried out processing
the transitions. Data acquisition was performed using Analyst
Software 1.6.1 (Concord, Ontario, Canada).24
Microbial enumeration
Appropriate dilutions from both the control and treatment groups
were plated on McConkey sorbitol agar (MCSA) for E. coli O157:H7,
potato dextrose agar (PDA) acidified with tartaric acid (10% w v−1 )
for P. expansum, plate count agar (PCA) for P. syringae subs. syringae,
and tryptone soya agar (TSA) for B. cereus. The MCSA, PCA and TSA
plates were incubated at 35 ± 2 ∘ C for 48 h, whereas PDA plates
were incubated at 22 ± 2 ∘ C for 3–5 days, respectively. Results were
expressed as log cfu mL−1 .
Sensory analyses
Samples with randomly given three-digit numbers were randomly
served at room temperature to 25 trained panelists from the
Department of Food Engineering of Bolu Abant Izzet Baysal Uni-
versity (Bolu, Turkey). Panelists were asked to take a bite from an
unsalted cracker, drink a glass of water to clean their palate, and
then test the next sample. A nine-point hedonic scale was adopted
for the sensory analysis of color, aroma, sweetness, sourness, and
aftertaste.
Statistical data analysis
Statistical data analyses were performed using Minitab 17
(Minitab, Inc., State College, PA). Tukey’s multiple comparison
tests following one-way ANOVA were performed to determine
mean significant differences in terms of the ten physical prop-
erties (pH, TSS, conductivity, L*, a*, b*, h∘ , C*, ΔE, and turbidity);
the four bioactive properties (TAC, TPC, TMAC, and TAAC); the
five pesticides (chlorpyrifos ethyl, 𝜏-fluvalinate, cyprodinil, pyr-
aclostrobin, and malathion); the inactivation levels of the four
micro-organisms (B. cereus, P. syringae subs. syringae, P. expansum,
and E. coli O157:H7); and the five sensory properties (color, aroma,
sweetness, sourness, and aftertaste).
The joint optimizations of the multiple (24) responses as a func-
tion of the ten treatments were based on the best fit linear regres-
sion models according to the composite desirability function (D),
a geometric average of individual desirabilities. The five best con-
ditions were presented for each. The objective functions of the
joint optimization consisted of the minimization of the responses
for the pesticide and microbial loads, and the target values for
the physical and bioactive properties determined as the respective
mean values of the control groups.
RESULTS AND DISCUSSION
Changes in sour cherry properties
The mean initial pH, TSS, and conductivity were not affected by the
treatments (P > 0.05). The mean initial L*, a*, b*, C*, and turbidity
were adversely affected by O, PEF1 (2)+O, and PEF1 (2)+O + US
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(P ≤ 0.05). Except for PEF1 + US, the other treatments adversely
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 www.soci.org GA Evrendilek, E Keskin, O Golge

affected the mean initial h∘ (P ≤ 0.05). All the treatments changed

59.64 ± 4.03b
60.85 ± 4.30b

60.28 ± 3.34b
62.48 ± 2.19b
70.38 ± 2.80a
70.85 ± 2.34a
71.98 ± 3.07a

71.85 ± 3.07a

73.64 ± 3.62a
72.46 ± 3.43a
44.62 ± 4.33c
Turbididty
the mean initial ΔE (P ≤ 0.05) (Table 2).

(NTU)
The PEF, O, and US treatments revealed results that were similar
to those of previous studies, although the treatment parameters
were different. For example, the PEF treatment of sour cherry juice
with increased EFS up to 30 kV cm−1 did not cause adverse effects
for pH, TSS, conductivity, or color values of L*, a* and b*,25 and

58.00 ± 3.28b
54.95 ± 3.14b
76.71 ± 2.22a

76.38 ± 4.10a
75.49 ± 4.34a
3.36 ± 0.33d
2.75 ± 0.26d
0.89 ± 0.12e
0.88 ± 0.17e

4.61 ± 0.38c
0.00 ± 0.00f
treatment time up to 210 μs did not cause significant changes to

ΔE
the pH, TSS, conductivity, and color a* (P > 0.05) but significant
changes occured in both L* and b*.26 Except for h∘ and ΔE, PEF
treatment with 24.7 kV cm−1 , with lower EFS than those used in the
previous studies but treatment times of 327 μs (PEF1) and 655 μs

−0.68 ± 0.04b

−0.59 ± 0.06b
−0.93 ± 0.09a
−0.91 ± 0.07a

−0.89 ± 0.05a

−1.03 ± 0.04a
0.35 ± 0.06d

0.39 ± 0.08d
0.35 ± 0.09d

0.47 ± 0.04c
0.47 ± 0.04c
(PEF2), which are longer than those of the previous studies, did not
significantly affect the physical properties of the sour cherry juice

h∘
in this study.
The US treatment of different juices such as grapefruit,27
tomato-based beverage,28 orange juice,29 red grape,30 and goose-
berry juice31 but sour cherry juice, was reported previously. No

69.07 ± 3.18b
68.17 ± 4.16b
80.73 ± 3.03a

81.64 ± 4.34a
77.70 ± 4.44a
38.14 ± 2.05c
38.01 ± 2.15c
38.09 ± 2.16c

33.65 ± 4.08c

34.78 ± 2.16c
36.08 ± 3.18c
significant changes in pH and TSS, and higher L* for tomato-based

C*
beverage,28 higher pH for orange juice,29 and enhanced a* value
for red grape30 and gooseberry juice31 were reported as a result
of US treatment. Results from the present study were compara-
ble with the previous studies in that significant changes were

63.15 ± 1.21b
60.57 ± 2.18b
76.48 ± 3.05a

76.41 ± 4.24a
73.58 ± 4.45a
13.90 ± 1.09c
14.67 ± 1.18c
14.65 ± 1.15c

12.90 ± 1.17c

12.46 ± 1.88c
14.64 ± 2.36c
reported only in h∘ and ΔE for the sour cherry juice.

Color b*
Ozone treatment of freshly squeezed orange juice with
0.6–10.0%w w−1 O for up to 10 min caused no significant changes
in pH, ∘ TSS, but L*,a*, b* were significantly changed.32 Ozone
treatment of blackberry juices at 4% w w−1 ozone concentration
Table 2. Changes in physical properties of sour cherry juice with PEF, ozone, US, and their combinations (n = 3)

for 10 min caused an increase in L, and a decrease in a, b and ΔE.33

35.07 ± 3.13ab

24.94 ± 2.08bc

27.97 ± 2.43bc
26.64 ± 2.03bc
25.87 ± 3.15b

28.74 ± 1.44b
35.51 ± 2.09a

35.16 ± 2.12a

31.08 ± 3.13a

32.48 ± 2.17a
32.98 ± 1.09a
Compared to PEF and US, O, as suggested in the previous studies,
Color a*

caused significant changes in the physical properties of the sour

cherry juice.
Differences in ΔE can be analytically classified as very distinct
(ΔE > 3), distinct (1.5 < ΔE < 3), and small (ΔE < 1.5).34 Both PEF-1

* Data in the same column with different superscript letter are significantly different (P ≤ 0.05).
and PEF-2 caused small differences, PEF1 + US caused distinct

38.25 ± 2.01b
36.17 ± 3.03b
51.86 ± 4.08a

51.93 ± 3.42a
53.55 ± 2.44a
7.75 ± 1.57a
8.55 ± 0.59c
8.40 ± 0.46c
8.24 ± 0.76c

8.75 ± 0.73c
9.34 ± 0.82c
Color L*

differences and the rest of the treatments caused a very distinct

difference in ΔE of the sour cherry juice samples (Table 2).
Except for pH, TSS, and conductivity, O alone and in combi-
nation with PEF and US, caused significant changes in physical
properties (Table 2). A combination of PEF and US with O could
not prevent significant changes to the physical properties of sour
Conductivity

1.25 ± 0.12a
1.05 ± 0.18a
1.17 ± 0.13a
1.16 ± 0.42a
1.16 ± 0.15a
1.23 ± 0.12a
1.21 ± 0.15a
1.09 ± 0.12a
1.15 ± 0.21a
1.26 ± 0.12a
1.26 ± 0.14a
(mS cm−1 )

cherry juice due to O itself. Although previous studies do not

include processing of fruit juices by the combination of PEF + O
or PEF + O + US, a combination of PEF with US for fruit juice pro-
cessing is available for grapefruit and orange juice. The effects of
combined PEF (20 kV cm−1 for 600 μs) and US (28 kHz for 30 min)
treatment for grapefruit juice,27 and PEF (40 kV cm−1 for 150 μs)
13.00 ± 0.27a
11.83 ± 0.97a
12.86 ± 0.15a
13.03 ± 0.26a
13.00 ± 0.14a
12.83 ± 0.23a
12.70 ± 0.30a
12.53 ± 0.29a
12.47 ± 0.21a
11.30 ± 0.69a
13.00 ± 0.40a

and US (30 kHz) for orange juice35 . In paralell to present study, no

(∘Brix)
TSS

significant change was observed in pH, TSS, conductivity, and ΔE.

No adverse effect occurred in TAC, TPC, TAAC, and TMAC with PEF1
(2), US, and PEF1 (2) + US (P > 0.05). A decrease occurred in TAC,
TMAC, TPC, and TAAC with PEF1 (2) + O, PEF1 (2) + O + US, and O
3.31 ± 0.22a
3.56 ± 0.32a
3.57 ± 0.18a
3.47 ± 0.11a
3.52 ± 0.16a
3.48 ± 0.18a
3.51 ± 0.20a
3.53 ± 0.16a
3.53 ± 0.11a
3.46 ± 0.21a
3.47 ± 0.16a

(P ≤ 0.05) (Table 3). The PEF treatment of sour cherry juice up to

30 kV cm−1 and 54 J s−1 energy did not adversely affect TAA and
pH

TMAC (P > 0.05).25 Similarly, PEF treatment with 24 kV cm−1 elec-

tric field strengths with 26.9 J s−1 energy did not adversely affect
TAAC but TMAC of sour cherry juice.26
PEF1 + O + US
PEF2 + O + US

A combination of US and mild heat was reported to have

improved the TAAC, TPC, and TAC of the grapefruit juice.27
PEF1 + US
PEF2 + US
PEF1 + O
PEF2 + O
Control

Enhancement of bioactive compounds has also been reported

PEF1
PEF2

in US-processed red grape30 and gooseberry juice,31 as well

US
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as in simultaneously blanched and sonicated carrot juice.36 As

wileyonlinelibrary.com/jsfa © 2019 Society of Chemical Industry J Sci Food Agric 2020; 100: 1653–1661
Non-thermal treatments of sour cherry juice
Table 3. Changes in bioactive properties of sour cherry juice with PEF, ozone, US, and their combinations (n = 3)*
TAC (%) TMAC (mg 100 mL−1 )
Control 40.31 ± 0.99b 18.99 ± 2.37a
PEF1 43.92 ± 1.07a 15.09 ± 1.45a
PEF2 43.91 ± 0.52a 15.82 ± 1.74a
O 27.95 ± 3.91c 2.22 ± 0.48c
US 43.54 ± 0.22a 18.02 ± 0.97a
PEF1 + O 25.47 ± 8.4c 4.14 ± 0.78b
PEF2 + O 32.02 ± 4.76c 4.39 ± 0.96b
PEF1 + US 44.59 ± 0.47a 16.20 ± 3.93a
PEF2 + US 45.11 ± 0.40a 16.44 ± 4.48a
PEF1 + O + US 24.17 ± 6.65c 5.84 ± 0.8b
PEF2 + O + US 28.70 ± 4.30c 6.13 ± 0.78b
* Data in the same column with different superscript letter are significantly different (P ≤ 0.05).
in previous studies, PEF and US alone or in combination with
different treatments did not cause adverse changes in TAC, TMAC,
TPC, and TAAC of the sour cherry juice samples. All the O treat-
ments had an adverse effect on TAC, TMAC, TPC, and TAAC. Ozone
causes degradation of color compounds in orange juice37 as
oxidative agents caused the breakdown of conjugated double
bonds, which resulted in the oxidative cleavage of chromophores
with bioactive properties.38
Removal of pesticides
The mean quantity of chlorpyrifos ethyl declined with all the
treatments (P ≤ 0.05). Both PEF2 + O + US and PEF2 + O provided
the highest level of pesticide removal followed by PEF1 + O + US,
PEF1 + O, O, PEF2 + US, PEF1 + US, PEF2, PEF1, and US (P ≤ 0.05).
Except for US, the other treatments significantly reduced the mean
initial 𝜏-fluvalinate concentration. PEF2 + O exerted the highest
impacts followed by PEF2 + O + US, PEF1 + O, PEF1 + O + US,
O, PEF1 + US, PEF2, PEF2 + US, and PEF1 (P ≤ 0.05) (Table 4).
All the treatments dropped the mean initial cyprodinil con-
centration significantly in the following order: PEF2 + O + US
> PEF2 + O > PEF1 + O + US > PEF1 + O > O > PEF2 + US >
PEF1 + US > PEF2 > US > PEF1 (P ≤ 0.05) (Table 4). The mean
initial pyraclostrobin concentration fell with all the treatments in
the following order: PEF2 + O + US > PEF2 + O > PEF1 + O + US
> PEF1 + O > O > PEF2 + US > PEF1 + US > PEF2 > PEF1 > US
(P ≤ 0.05) (Table 4). All the treatments reduced the mean initial
malathion concentration in the following order: PEF2 + O + US
> PEF2 + O > PEF1 + O + US > PEF1 + O > O > PEF2 + US >
PEF1 + US > PEF2 > PEF1 > US (P ≤ 0.05) (Table 4). The com-
bined treatments achieved a higher removal efficiency than did
the individual treatments.
The PEF treatment of apple juice with 8–20 kV cm−1 EFS and
6–26 pulses was reported to achieve the removal of methami-
dophos and chlorpyrifos, with chlorpyrifos being more labile.17
The removal efficiency for 16 pesticide residues (ten fungicides,
and six insecticides) in raw strawberries ranged from 42.8 to
92.9% w w−1 with boiling and up to 91.2% w w−1 with ultrasonic
cleaning.15 Ozone (5 and 10 mg L−1 ) applied to carrot roots for
120 min removed more than 80% w w−1 of difenoconazole and lin-
uron,linuron, and efficiacy of ozone increased with increased con-
centration and exposure time.39 The treatment efficacy found in
the present study was in the following order: the triple combina-
tions > the dual combinations > the individual treatments.
J Sci Food Agric 2020; 100: 1653–1661 © 2019 Society of Chemical Industry
www.soci.org
TPC (mg GAE mL−1 ) TAAC (mg 100 mL−1 )
2.39 ± 0.17a 56.11 ± 3.27a
2.45 ± 0.12a 52.75 ± 3.29a
2.44 ± 0.14a 53.36 ± 4.53a
1.44 ± 0.25b 43.66 ± 3.44b
2.33 ± 0.11a 54.36 ± 3.48a
1.33 ± 0.15b 45.70 ± 2.23b
1.26 ± 0.14b 46.77 ± 1.48b
2.31 ± 0.27a 55.19 ± 3.83a
2.40 ± 0.18a 58.09 ± 4.53a
1.18 ± 0.23b 47.13 ± 2.87b
1.32 ± 0.11b 47.66 ± 1.08b
Microbial inactivation
The mean initial B. cereus count declined with all the treat-
ments in the following order: PEF2 + O + US > PEF1 + O + US
> PEF2 + O > PEF1 + O > PEF2 > PEF2 + US > PEF1 + US >
O > PEF1 > US (P ≤ 0.05) (Table 5). All the treatments reduced
the mean initial P. syringae subs. syringae, P. expansum and E. coli
O157:H7 counts. The order of the treatments was PEF2 + O + US >
PEF1 + O + US > PEF2 + O > PEF2 + US > PEF1 + O > PEF1 + US >
O > PEF2 > US > PEF1 for P. syringae subs. syringae; PEF2 + O + US
> PEF1 + O + US > PEF2 + O > PEF1 + O > PEF2 + US > PEF1 + US
> PEF2 > O > PEF1 > US for P. expansum; and PEF2 + O + US
> PEF1 + O + US > PEF2 + O > PEF1 + O > O > PEF2 + US >
PEF1 + US > PEF2 > PEF1 > US for E. coli O157:H7 (P ≤ 0.05)
(Table 5). The combined treatments achieved a higher inactivation
level than did the individual treatments.
Inhibitory effects of PEF on microorganisms in various juices
under different treatment parameters have been reported. Pulsed
electric fields with 35 kV cm−1 for 1 μs reduced Kloeckera apicu-
lata, Saccharomyces cerevisiae, Lactobacillus plantarum, Lactobacil-
lus hilgardii, and Gluconobacter oxydans in grape juice by 2.24
to 3.94 log.40 Pulsed electric fields for E. coli O157:H7 in apple
juice provided 0.4- to 3.6-log reductions with the range of 20
to 30 kV cm−1 for 5 to 125 μs.41 Pulsed electric fields for fungal
pathogens in sour cherry juice were also reported to reduce ger-
mination tube elongation and spore germination rate.42 Pulsed
electric fields were reported to lead to 1.3- and 2.6-log reductions
of L. plantarum and E. coli, and to 4.26- and 3.61-log reductions for
yeast and molds, respectively, for orange-carrot juice.43 An inter-
action effect of PEF and thermal treatment on microbial inacti-
vation was also found with the application of PEF at 25 kV cm−1
and 65 ∘ C for 63 μs with more than 5-log reductions in E. coli
O157:H7, Listeria monocytogenes, Staphylococcus aureus, and S.
enterica serovar Typhimurium strains in media with pH 4 and 7.44
There were inhibitory effects of O against different microorgan-
isms: 12 min of 10 or 18 ppm O exposure provided 4.3 log reduc-
tions in E. coli, 1 log reduction in S. cerevisiae, and 3.9-to-4.9 log
reductions in L. innocua in peach juice.45 Ultrasonication applied to
blueberry46 and Chokanan mango47 juice reduced coliforms, aer-
obic bacteria, yeast, and molds to safe acceptable limits. Results
in the present study correlated with the literature that found that
PEF, O, and US treatments are effective against bacteria and fungi
even though the magnitude of applied treatment parameters was
1657
different.
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 www.soci.org GA Evrendilek, E Keskin, O Golge

Table 4. Degradation of pesticides in sour cherry juice with PEF, ozone, US, and their combinations (n = 3)*

Chlorpyrifos ethyl 𝜏-Fluvalinate Cyprodinil Pyraclostrobin Malathion

(mg kg−1 ) (mg kg−1 ) (mg kg−1 ) (mg kg−1 ) (mg kg−1 )

Control 52.90 ± 0.52a 24.10 ± 0.82a 79.03 ± 0.91a 80.03 ± 4.48a 24.77 ± 0.06a
PEF1 23.83 ± 0.61c 22.10 ± 0.10b 59.30 ± 0.53b 40.43 ± 4.14c 12.05 ± 0.13c
PEF2 22.30 ± 2.70c 17.35 ± 0.05b 56.13 ± 0.23c 34.87 ± 2.42c 10.00 ± 0.10d
O 9.82 ± 0.02e 14.57 ± 0.06c 27.07 ± 0.81d 4.99 ± 0.81d 7.67 ± 0.16h
US 36.70 ± 4.24b 23.70 ± 0.20a 56.47 ± 2.14bc 55.40 ± 0.30b 18.93 ± 1.05b
PEF1 + O 5.03 ± 0.01f 12.86 ± 0.25d 19.77 ± 0.58e 4.90 ± 0.32d 6.47 ± 0.03i
PEF2 + O 4.96 ± 0.04f 10.80 ± 0.17e 10.93 ± 1.00g 3.93 ± 0.23e 5.57 ± 0.1j
PEF1 + US 14.77 ± 3.14d 16.73 ± 0.06de 52.30 ± 6.58bc 32.47 ± 3.54cd 9.16 ± 0.01f
PEF2 + US 13.77 ± 3.97d 17.47 ± 3.74b 50.07 ± 2.45bc 27.23 ± 2.99cd 8.50 ± 0.10g
PEF1 + O + US 4.99 ± 0.14f 13.73 ± 3.06cd 14.00 ± 1.00f 3.99 ± 0.33e 6.27 ± 0.26i
PEF2 + O + US 4.46 ± 0.03f 12.83 ± 2.05cd 9.31 ± 0.54g 2.64 ± 0.02f 4.26 ± 0.01d
* Data in the same column with different superscript letter are significantly different (P ≤ 0.05).

Table 5. Microbial inactivation of sour cherry juice with PEF, ozone, US, and their combinations (n = 3)*

B. cereus P. syringae subs. syringae P. expansum E. coli O157:H7

(log cfu mL−1 ) (log cfu mL−1 ) (log cfu mL−1 ) (log cfu mL−1 )

Control 5.52 ± 0.46a 6.72 ± 0.38a 5.45 ± 0.51a 6.73 ± 0.05a

PEF1 4.92 ± 0.32ab 5.76 ± 0.26b 4.41 ± 0.38b 5.53 ± 0.09c
PEF2 4.26 ± 0.23b 5.58 ± 0.03b 4.26 ± 0.14b 5.37 ± 0.08c
O 4.72 ± 0.45a 4.69 ± 0.79bc 4.27 ± 0.11b 4.52 ± 0.01d
US 5.05 ± 0.43a 5.64 ± 0.85b 4.90 ± 0.19ab 6.42 ± 0.06b
PEF1 + O 4.05 ± 0.09bc 4.39 ± 0.03bc 3.30 ± 0.13c 3.62 ± 0.22e
PEF2 + O 3.89 ± 0.18bc 4.08 ± 0.04d 3.15 ± 0.01d 3.42 ± 0.46e
PEF1 + US 4.35 ± 0.31b 4.43 ± 0.03c 4.18 ± 0.11b 5.14 ± 0.44c
PEF2 + US 4.28 ± 0.15b 4.09 ± 0.27d 3.56 ± 0.33bc 4.65 ± 0.32d
PEF1 + O + US 3.79 ± 0.16bc 3.22 ± 0.21e 2.87 ± 0.03e 3.36 ± 0.01e
PEF2 + O + US 3.58 ± 0.13c 3.11 ± 0.34e 1.07 ± 0.07f 3.20 ± 0.22e
* Data in the same column with different superscript letter are significantly different (P ≤ 0.05).

Sensory properties Interaction effects

The sensory properties, except for color, were not significantly
affected by the treatments (P > 0.05). The mean color value fell
with O, PEF2 + O, PEF2 + O + US, PEF1 + O + US, and PEF2 + O
(P ≤ 0.05) (Table 6). All the ozone treatments adversely changed
color due to its oxidative effect. No significant changes in sen-
sory properties were reported in sour cherry juice with the PEF
treatment.26 Sonication did not cause significant differences in
panel-tested color, aroma and flavor of calcium added orange
juice.48 As in the present study, PEF and US treatment of juices
mostly resulted in insignificant changes to the sensory properties
of the juices.
Joint optimization and multi-objective functions
The joint optimization of the 24 responses pointed to PEF1,
PEF2, PEF2 + O + US, US, and PEF2 + O as the five best treat-
ments (Table 7). For each treatment, the predicted responses are
illustrated in Table 7. The smallest and largest variations in the
responses among the five best treatments belonged to pH and
turbidity, respectively. Considering the maximum reduction in
the microbial loads and the pesticides, without compromising the
physical, bioactive, and sensory properties, PEF2 + O + US was the
1658
The mechanisms of action for each treatment are different, so their
effects on physical properties, bioactive compounds, microbial
inactivation, and pesticide removal are different. The electropo-
ration effects of PEF would enhance color and bioactive com-
pounds due to their release from damaged cell membranes to
the cytoplasm. Enhancement of the bioactive compounds by US,
on the other hand, can be attributed to the cavitation phenom-
ena that ultimately caused the release of anthocyanins from the
plant cell membrane.30,31 Ozone, on the other hand, causes oxi-
dation on the chromophore of the conjugated double bonds of
the anthocyanins or carotenoids responsible for the juice color
and bioactive properties.49 The O and hydroxyl radicals (OH−)
generated by O in the aqueous solution may cause an opening
in aromatic rings in compounds leading to the partial oxidation
of products such as organic acids, aldehydes, and ketones. The
ring-opening phase due to formation of ozonide is a crucial step
in degradation.50–52 Ozone plays an important role in the forma-
tion of other degradation-facilitating high-reactive species, such
as UOH, HO2 U, UO2 −, and UO3 .51,52
In terms of microbial inactivation, PEF affected the cell mem-
brane in such a way that the electroporation increased its perme-

most successful treatment followed by PEF1 + O + US. ability due to the formation of the membrane pores surrounding

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Non-thermal treatments of sour cherry juice www.soci.org

Table 6. Changes in sensory properties of sour cherry juice with PEF, ozone, US, and their combinations (n = 3)*

Color Flavor Sweetness Sourness Aftertaste

Control 6.33 ± 1.15a 7.00 ± 2.00a 5.67 ± 1.15a 7.00 ± 1.15a 7.67 ± 1.15a
PEF1 6.33 ± 1.15a 5.67 ± 1.15a 7.00 ± 2.00a 5.67 ± 1.15a 7.00 ± 2.00a
PEF2 6.33 ± 1.15a 5.00 ± 2.00a 7.00 ± 2.00a 4.33 ± 2.16a 5.33 ± 1.52a
O 3.00 ± 2.00c 5.67 ± 1.15a 3.66 ± 1.15a 3.33 ± 2.31a 5.00 ± 3.46a
US 6.33 ± 2.31a 5.67 ± 1.15a 7.00 ± 2.00a 5.67 ± 1.15a 7.67 ± 2.31a
PEF1 + O 4.67 ± 0.60b 6.33 ± 1.15a 6.33 ± 1.15a 3.67 ± 1.15a 3.67 ± 1.15a
PEF2 + O 4.33 ± 1.1bb 7.00 ± 2.00a 5.00 ± 0.00a 4.33 ± 1.31a 6.33 ± 1.15a
PEF1 + US 5.67 ± 1.15ab 5.67 ± 1.15a 3.66 ± 1.15a 6.33 ± 1.15a 5.00 ± 2.00a
PEF2 + US 6.00 ± 1.00ab 5.33 ± 0.58a 5.66 ± 1.15a 5.67 ± 1.15a 5.00 ± 2.00a
PEF1 + O + US 4.40 ± 1.00b 6.33 ± 1.15a 5.00 ± 2.00a 5.67 ± 1.15a 4.33 ± 2.00a
PEF2 + O + US 4.33 ± 0.35b 6.33 ± 1.15a 4.33 ± 1.15ab 6.33 ± 1.15a 5.00 ± 2.00a
* Data in the same column with different superscript letter are significantly different (P ≤ 0.05).

Table 7. Five best joint optimizations of the 24 responses (R) as a function of 10 treatments for sour cherry juice

Best solution

1 2 3 4 5

Treatment

No Response PEF1 PEF2 PEF2 + O + US US PEF2 + O

R1 Aftertaste 7 5.3 5 7.7 6.3

R2 Sourness 5.7 4.3 6.3 5.7 2.3
R3 Sweetness 7 7 4.3 7 5
R4 Flavor 5.7 5 6.3 5.7 7
R5 Color 6.3 6.3 4.3 6.3 6.3
R6 E. coli O157H7 5.4 5.5 3.4 7.6 3.6
R7 P. syringae subs. syringae 3.3 4.4 3.9 4.9 3.3
R8 P. expansum 5.8 6 5.1 3.6 5.5
R9 B. cereus 4.3 5 4.6 5.1 4.5
R10 𝜏-Fluvalinate 22.1 17.4 20.8 23.7 14.8
R11 Malathion 10.1 12 10.3 18.9 10.6
R12 Pyraclostrobin 40.4 58.9 5 36.7 5
R13 Cyprodinil 59.3 66.1 9.3 53.5 10.9
R14 Chlorpyrifos ethyl 13.8 22.3 5 36.7 5
R15 Turbidity 90.9 35 48.5 12.8 64.9
R16 Ascorbıc acid 52.7 53.4 53.7 1.4 75.5
R17 TCD 3.9 1.8 57.8 1.4 75.5
R18 h∘ 2.7 2.3 −0.3 2.6 −5.2
R19 C* 34.5 38.1 68.8 37.4 77.7
R20 TMAC 15 22.8 1.1 18.9 1.4
R21 TPSC 2.5 2.4 1.3 2.5 1.3
R22 TAC 43.9 43.9 28.7 43.5 32
R23 TSS 11.83 12.86 13 12 12.7
R24 pH 3.55 3.57 3.46 3.52 3.51
Composite desirability 0.542 0.511 0.481 0.380 0.370

the cells.53 Ozone is characterized by its high oxidation poten-
tial, which provides bactericidal and viricidal properties.54 Reac-
tions with the enzymatic systems and the unsaturated lipids of
the cell membranes damage membranes result in the leakage of
cytoplasm components, allow O to penetrate inside the cell, and
cause DNA breakage.54 The use of US in liquid or solvent gen-
erates the energy to disintegrate the wall of biological cells due
applied individually, some microbial inactivation results; however,
application of these treatments consecutively creates a multiple
effect, providing more inactivation.
The mechanism for pesticide removal / degradation is also dif-
ferent for each treatment. Degradation of contaminants under
US and O is mostly related to the formation of hydroxy radicals.
Ultrasound has been related to cavitation involving the sequen-
1659

to strong shear forces and pressure.55 When each treatment was tial formation, growth and collapse of millions of microbubbles

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 www.soci.org
in the liquid. Cavitation bubbles collapse very rapidly and that
leads to high localized temperatures (about 5000 ∘ C) and pressure
(50 MPa), resulting in pyrolysis reactions involving water, gener-
ating highly reactive hydroxyl radicals. Hydroxyl radicals gener-
ated by sonication could be responsible for the degradation of
pesticides.56 Hydroxyl radicals generated by O may also cause the
pesticide molecules to be transformed to primary oxidation prod-
ucts, which often undergo either spontaneous transformation
(e.g., protonation, dimerization, isomerization, and tautmeriza-
tion) or further oxidation by another ozone molecule or hydroxyl
radical.57
Studies regarding pesticide removal / degradation by PEF, on the
other hand, are very limited.17 Although the effect of PEF process-
ing parameters on pesticide removal is shown in the literature, the
mechanisms remain unsolved. Pulsed electric fields could increase
the vibration and rotation of molecules, and thus could facili-
tate the degradation of the pesticides,17 even though pesticide
removal mechanisms are much more complex due to the complex-
ity of their chemical structure and they differ greatly depending
on the treatment parameters. Combinations of PEF, O, and US are
efficient in reducing initial pesticide concentrations.
CONCLUSIONS
Combination of different treatments are an alternative approach
to increase treatment efficacy in microbial inactivation and
to increase food safety. This study was the first to determine,
comparatively, the interaction and multi-objective effects of
10 high-tech treatments (individually and in dual and triple
combinations) on physical and quality properties, microbial
inactivation, pesticide removal, and sensory properties of sour
cherry juice, and the first to optimize 24 responses for each
treatment concurrently. The physical properties were not
adversely affected by most of the treatments. O, PEF1 + O,
PEF2 + O, PEF1 + O + US, and PEF2 + O + US adversely influ-
enced the mean initial L*, a*, b*, C*, turbidity, TAC, TMAC, TPCS,
and TAAC. Except for PEF1 for 𝜏-fluvalinate, all the treatments
significantly reduced the spiked pesticides. The treatment effec-
tiveness in the pesticide removal was of the following order:
pyraclostrobin (96.7%) > chlorpyrifos ethyl (91.57%) > cyprodinil
(88.22%) > malathion (82.80%) > 𝜏-fluvalinate (46.76%). The
same treatments providing the pesticide removal also enriched
microbial inactivation. The treatment effectiveness in microbial
inactivation was of the following order: P. expansum (4.38 log
cfu mL−1 ) > P. syringae subs. syringae (3.61 log cfu mL−1 ) > E. coli
O157:H7 (3.53 log cfu mL−1 ) > B. cereus (1.94 log cfu mL−1 ). Overall,
except for the color with all the ozone treatments, the sensory
properties were not adversely affected by the treatments. The
joint optimization showed PEF1, PEF2, PEF2 + O + US, US, and
PEF2 + O as the five best treatments, respectively. The treatments
adopted in the study provided a promising alternative to con-
ventional food-processing technology in terms of food safety.
Further comparative interaction and multi-objective studies of
this nature remain to be conducted, with different pesticides,
micro-organisms, and foods.
ACKNOWLEDGEMENTS
This research was funded by the Republic of Turkey Ministry of
Development Government Planning Agency (Project no. 2009 DPT
K 120140) and the Scientific and Technological Research Council of
1660
Turkey (TUBITAK) (Project no. 1040585).
wileyonlinelibrary.com/jsfa © 2019 Society of Chemical Industry
GA Evrendilek, E Keskin, O Golge
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