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Review
Effects of ozone treatment on pesticide residues in food: a review
Shan Wang, Jiayi Wang, Tianyu Wang, Chen Li & Zhaoxia Wu*
College of Food Science, Shenyang Agricultural University, 120 Dongling Rd. 110866 Shenyang, China
(Received 6 June 2018; Accepted in revised form 11 August 2018)
Summary In agriculture, pesticide residues have always posed a major safety hazard to human health. With the
development of agricultural production and improvements in science and technology, additional methods
for degradation of pesticide residues have emerged. Amongst them, ozone treatment recently became a
popular method owing to its outstanding technical advantages. This review is an in-depth analysis of the
mechanisms by which ozone treatment degrades pesticide residues. The main mechanism involves direct
oxidation by oxygen atoms, and indirect oxidation driven by hydroxyl radicals. The effects of ozone treat-
ment on pesticide residues in food with respect to the ozone concentration, duration of ozone treatment,
type of food, variety of pesticides, level of pesticide residues and environmental factors have been dis-
cussed. Furthermore, the impact of ozone treatment on the quality of food is highlighted. Low levels of
ozone result in minor changes to the visual and sensory characteristics of food. In addition, this article
discusses several restrictions surrounding the current application of ozone treatment for the degradation
of pesticide residues. More specifically, the most crucial issue is the potential toxicity of ozonation
byproducts generated by the process, which is also the current focus of research on ozone treatment for
the degradation of pesticide residues. After weighing the advantages and disadvantages of ozone treat-
ment, it is recommended as a method of degrading pesticide residues.
Keywords Degradation, ozonation byproducts, ozone, pesticide residues.
Food safety is a major issue related to the economy of
a nation and livelihood of people. In recent years, the
frequency of pesticide poisoning incidents has
increased. During agricultural production, spraying of
chemical pesticides to control and prevent the negative
effects of pests and insects is a necessary measure to
increase crop yields, which equates to preventing
approximately 30% of economic losses. Nonetheless,
these pesticides are often toxic and leave residues that
are difficult to degrade, especially when they are used
excessively or in an unregulated manner (Lozowicka
et al., 2014). Currently, various levels of pesticide resi-
dues are found in agricultural produce worldwide
(Dalvie & London, 2009; Jardim & Caldas, 2012;
Łozowicka et al., 2012; Wang et al., 2013; Szpyrka
et al., 2015), which creates a bottleneck in the interna-
tional trade of food commodities. Consequently, this
becomes a focus area for producers and consumers
alike.
It is estimated that more than 95% of pesticides
potentially affect non-target organisms, are widely dis-
persed in the environment, and cause various types of
pollution. Moreover, the effects of certain pesticides
may even span several decades and this negatively
affects the soil quality and soil conservation efforts
(Jacobsen & Hjelmsø, 2014; Racke et al., 2015). Addi-
tionally, many pesticide residues show bioaccumula-
tion and biomagnification at levels that are deleterious
to the human body (Crinnion, 2009), because they are
amplified through the food chain and can be detected
in meat, poultry, fish, vegetable oils, nuts and various
fruits and vegetables (Chung & Chen, 2011). Trace
amounts of pesticide residues in the human body can
result in chronic hazards. Long-term consumption of
food containing pesticide residues can lead to the
development of numerous diseases such as asthma,
diabetes, leukaemia, Parkinson’s disease and cancer
(Kim et al., 2017). These effects can even extend to the
next generation by causing birth defects, low fertility
rates, high infant mortality rates and certain hereditary
diseases (Wickerham et al., 2012). In fact, because of
their behavioural and physiological state, a child is
more susceptible to the effects of pesticides than an
adult (Mascarelli, 2013). Therefore, it is urgently nec-
essary to develop ‘green’ and effective strategies to
reduce the amount of pesticide residues in food.
*Correspondent: E-mail: wuzxsau@163.com
International Journal of Food Science and Technology 2018
doi:10.1111/ijfs.13938
©2018 Institute of Food Science and Technology
1
In response to this issue, various countries have for-
mulated and abide by various laws, regulations and
national standards, and provide technical guidance to
producers according to the production specification to
ensure the regulated use of pesticides. Strict supervi-
sion of the various departments in agricultural produc-
tion helps control the levels of pesticide residues from
the beginning of the process. In addition to regulating
pesticide use during the preprocessing of raw material
production, pesticide residues can be degraded post-
processing by technical methods (Bajwa & Sandhu,
2014), such as physical, electrolysed water, chemical,
photochemical, microbial, enzymatic and genetic engi-
neering methods. Amongst these, ozone treatment is
an emerging technology with great potential and
several advantages.
Advantages of ozone treatment in the
degradation of pesticide residues
Ozone treatment provides numerous advantages in
the degradation of pesticide residues, such as exhibit-
ing a broad spectrum of action against pesticides
and bacteria, high efficiency, ease of use, a relatively
low cost, guaranteed quality of raw materials and
user safety. Hence, ozone is widely used to treat
drinking water and to preserve food; it is now begin-
ning to be applied to the process of cleaning fruits
and vegetables and degrading pesticide residues to
ensure food safety (Bros
eus et al., 2009; Alexandre
et al., 2012; Miller et al., 2013; Trombete et al.,
2016).
Broad spectrum against pesticides and bacteria
Ozone treatment can be used for the degradation of a
broad spectrum of pesticide residues, including several
major categories, such as organophosphorus pesti-
cides, organochlorine pesticides, pyrethroids pesti-
cides, carbamates pesticides, etc. The application
range of the photochemical method that is also
employed for the degradation of pesticide residues
has many advantages as well. However, the photo-
chemical method can only be applied under ideal con-
ditions of lighting; therefore, it cannot be used
indoors or in overcast weather. For instance, pyre-
throid and organophosphate pesticides are unstable
and sensitive to light. When the pesticides reach an
excited state upon exposure to light, molecular bonds
are fractured, and the pesticides break down. The
microbial method has long been used to degrade pes-
ticide residues. For example, Sethunathan & Yoshida
(1973) isolated the first Flavobacterium species that
biodegrades diazinon and parathion in soil exposed
to these organophosphate pesticides. Wolf & Martin
(1976) discovered that fungal mycelia decompose
chlorpropham. However, the microbial method
involves the isolation and screening of specific bacte-
rial or fungal strains, which can effectively degrade
only certain pesticides; therefore, these strains cannot
meet the requirements of bioremediation. Although
ozone is widely used to degrade pesticide residues, it
also plays a role in the inactivation of microorgan-
isms, such as a wide variety of bacteria, fungi, pro-
tists and viruses (de Alencar et al., 2012; Xu & Wu,
2014). Ozone can inactivate many pathogens on the
surface of food, thereby preserving freshness and
extending the shelf life. For example, the sterilisation
rate of ozone was demonstrated to be as high as
93.00% with 1.2 mg L
1
ozonated water against Peni-
cillium expansum on apples after treatment for 5 min
(Qiao et al., 2012b). Moreover, ozone is a fumigant
for control of insects and microorganisms and for
reducing the abundance of mycotoxins (Jian et al.,
2013). Once the concentration of ozone reaches the
threshold necessary to kill various microorganisms,
sterilisation and disinfection by ozone treatment is
rapid and accomplished almost instantaneously
(Khadre et al., 2001).
High efficiency
The water cleaning method is the most common and
popular way to reduce pesticide residues. It is effec-
tive at removing water-soluble pesticides, but it does
not considerably degrade many water-insoluble pesti-
cides. For example, in an experiment conducted by
Zhang et al. (2013), lettuce was cleaned with tap
water, 2% salt water, or 2% sodium bicarbonate
(NaHCO
3
) in an aqueous solution, and the elution
rates of trichlorfon were only 9.21%, 19.02% or
25.00%, respectively. In addition, the flushing time
and removal rate of pesticides of the cleaning method
cannot be accurately controlled. The effects are not
ideal when food is flushed and soaked for only a
short period. Conversely, the removal rate of pesticide
residues are greatly reduced when the soaking time is
too long, because pesticides will remain bound to the
surface. Use of ozone to degrade pesticides does not
involve such problems. Ozone treatment can effi-
ciently and accurately degrade a large amount of pes-
ticide residue in a short period of time. For example,
de Freitas et al. (2017) confirmed that 0.86 mg L
1
gaseous ozone effectively degrades more than 91% of
pirimiphos-methyl residue in maize grains within
60 min. Bourgin et al. (2013) found that imidacloprid
on loaded seeds almost fully decomposes (95%) by
32 min under the influence of ozone gas
(100 mg L
1
). Heleno et al. (2014) tested 0.8 mg L
1
ozone gas to fumigate strawberries for 60 min, and
the concentration of difenoconazole that was dis-
solved in strawberries decreased to <0.5 mg kg
1
,
©2018 Institute of Food Science and TechnologyInternational Journal of Food Science and Technology 2018
Use of ozone to remove pesticides from food S. Wang et al.2
which was equivalent to a 95% reduction in the
amount of pesticide residue.
Ease of operation
Guo et al. (2009) immobilised organophosphorus
hydrolase (OPHC2) in ADS-5 macroporous micro-
spheres and prepared enzymes immobilised on a solid
medium by cross-linking enzyme aggregates: the
hydrolytic rate of methyl parathion degradation was
greater than 90%. This is one example of an enzymatic
method, which has the advantage of precise targeting;
however, enzymatic activity can be inhibited under cer-
tain environmental conditions, reducing the efficiency
of degradation of pesticide residues by this method.
Similarly, methods involving microbes require highly
regulated environmental conditions, given that micro-
bial strains can be easily inactivated. In contrast,
ozone treatment decomposes pesticide residues under
almost any environmental condition, making its opera-
tion and application simple, convenient and easily reg-
ulated, thus saving time and labour, and facilitating
factory processing. The process of ozone treatment will
prove simpler and more efficient once household ozone
equipment can be mass produced, because fruits and
vegetables will need to be washed with water only once
after the equipment has cleaned them.
Relatively low cost
Ozone is easy to produce, and hence the cost of ozone
treatment for the degradation of pesticide residues is
low. The maximum effective cost estimation of ozona-
tion is $100. In contrast, chemical methods, despite
their efficiency, are relatively expensive. For example,
the use of hydrogen peroxide, chlorine dioxide, or
other chemical reagents to degrade pesticide residues is
very effective. Zohair (2001) used 10% hydrogen per-
oxide to degrade pesticide residues in potatoes, and
found that the degradation rates of pirimiphos-methyl,
malathion and profenofos were 100%, 93% and
100%, respectively. Although the degradation of pesti-
cide residues by this method is relatively complete,
transportation and storage of hydrogen peroxide
require special tools and conditions, increasing the cost
of utilising this method. Hwang et al. (2002) applied
10 mg L
1
chlorine dioxide to degrade pesticide resi-
dues in apples, and the degradation rates of mancozeb
in whole fruit, slices, jam and juice were 87.9%, 100%,
100% and 68.7%, respectively, while the degradation
rates of ethylenethiourea were 97%, 100%, 100% and
93.4%, respectively. Nevertheless, this method may
require additional processing steps, such as elimination
of residual substances in the environment; these steps
may increase the cost of this method to a certain
extent.
Guaranteed quality of raw materials
Ozone treatment can serve to remove pesticide residues
to ensure the integrity of fruits and vegetables, and
this method results in minimal loss of raw materials
and in waste reduction, in comparison to the peeling
method (which is more effective at removing non-sys-
temic pesticides) that is often use in our daily life
because of its convenience (Bonnech
ere et al., 2012).
For instance, the peeling method reduced the amount
of captan in apples by 98% (Rawn et al., 2008) and
removed 87.3% of carbendazim and 84.2% of thio-
phanate-methyl in tomatoes (Liu et al., 2014). On the
other hand, the nutritional value contained in the epi-
dermis of fruits and vegetables is extremely high, as
expected; therefore, the ozone method ensures that
greater amounts of nutrients can be absorbed by the
human body. Compared to the Chinese population,
the European population’s eating habits include raw
and cold fruits and vegetables; hence, ozone treatment
of food is undoubtedly a desirable method owing to
its ability to degrade pesticide residues at room tem-
perature. Cooking methods, such as steaming, boiling,
stewing and frying, involve high temperatures that can
degrade some thermolabile pesticides well. For exam-
ple, the degradation rate of chlorpyrifos in stir-fried
cabbage is approximately 86.6% (Zhang et al., 2007).
Nonetheless, this method partially degrades nutrients
and changes the colour and taste of food. Sometimes,
though, some changes may make food more palatable.
Safety of the ozone treatment
Ozone is also known as reactive oxygen and has poor
stability at room temperature and atmospheric pres-
sure, with a half-life of 20–50 min. Furthermore,
ozone decomposes into oxygen without producing any
additional traces of byproducts. Therefore, ozone does
not cause secondary pollution, and there is no residual
gas to remove after use. For instance, the reaction of
ozone with malathion generates phosphoric acid, sulfu-
ric acid, carbon dioxide and water. Given the relative
environmental friendliness of ozone, its use is generally
welcomed. Some physical and biological methods may
also be safe, whereas other techniques, such as use of
hypochlorite, despite being effective, are not very safe.
Gao et al. (2011) observed that treating freshly cut let-
tuce with 300 mg L
1
calcium hypochlorite for 15 min
results in significant reduction of pesticide residues,
compared to untreated lettuce. On the other hand,
hypochlorite is unstable and undergoes a dispropor-
tionation reaction to produce chloride, which can lead
to chemical contamination. Another example is the
electrolysed water method. One study revealed that
soaking spinach with electrolysed reducing water and
electrolysed oxidising water for 30 min degraded 86%
©2018 Institute of Food Science and Technology International Journal of Food Science and Technology 2018
Use of ozone to remove pesticides from food S. Wang et al.3
and 74% of acephate, respectively (Hao et al., 2011).
Electrolysed water is easy to prepare. However, it does
not contain the minerals and trace elements that the
human body must obtain from water. Furthermore,
there are currently no identified ecological security
problems related to ozone treatment for degradation
of pesticide residues. The genetic engineering method,
on the other hand, may have a negative impact on
ecological security. For example, a recent study was
conducted to genetically engineer a microorganism
that degrades both methyl parathion and fen-
propathrin (Hong et al., 2010). Although genetic engi-
neering has always been a ‘hot’ technology, it can
solve many complex problems, although it has not
been evaluated whether genetically engineered strains
could cause any adverse effects when applied to the
natural environment.
Mechanism underlying the degradation of
pesticide residues by ozone
Ozone, or trioxygen, is an inorganic molecule with
the chemical formula O
3
. It is a pale blue gas with a
distinctive, pungent smell. Ozone is an allotrope of
oxygen that is much less stable than the diatomic
allotrope O
2
. It breaks down to O
2
or dioxygen.
Compared to oxygen, ozone has greater oxidative
potential. It can decompose organic chlorides, dioxins
and other pollutants into carbon dioxide and other
innocuous substances. It can also oxidise toxic and
hazardous substances, such as phenol and cyanide,
into harmless substances. Water-soluble manganese
(Mn
2+
), iron (Fe
2+
), and other inorganic substances
can be oxidised by ozone into high-valence deposits
that are insoluble in water and can be removed physi-
cally. Ozone treatment can break the double bond of
members of the coloured group, playing a role in
decolourisation. The chemical bonds of functional
groups, such as =S, =NH, SH, NH, OH, and
CHO, in the molecular structure of a malodour can
be broken by ozone to reduce unpleasant smells.
Large molecular weight organics that are rarely
biodegradable can be oxidised by ozone into medium
and small molecular organics that are more easily
decomposed (Qiao et al., 2012a).
The mechanism of ozone oxidation of target organ-
ics involves direct oxidation by oxygen atoms and indi-
rect oxidation driven by hydroxyl radicals, which are
generated by the self-decomposition of ozone mole-
cules. The reaction rate of direct oxidation is lower
than that of indirect oxidation, and the latter can
rapidly undergo a chain reaction. The degradation of
pesticides in water may occur through hydrolysis, pho-
tolysis and reduction–oxidation (Chamberlain et al.,
2012). When ozone reacts with organic pesticides, it
disrupts unsaturated aliphatic moieties, such as alkenes
and alkynes, in the molecular structure of pesticides by
breaking carbon chains and opening benzene rings,
and it also oxidises dichlorovinyl, nitro, methoxy,
amino and other functional groups. Oxidative cleavage
radically changes the molecular structure of organic
pesticides and causes them to lose their potency.
Moreover, the small-molecule compounds produced
further by the reaction between ozone and unsaturated
carbon chains in pesticide molecules, such as acids,
alcohols, amines, carbonyls, carboxylates and their
oxides, are primarily water-soluble. Therefore, they
can be washed away with tap water, leading to the
degradation and removal of pesticide residues. Some
examples of ozonation of several major classes of
pesticides have been listed in Table 1.
Ozone degradation of pesticide residues is essentially
based on two forms, the first is to wash or immerse
food in a solution containing ozone, and the second is
to add ozone gas continuously or intermittently into
the atmosphere of stored food. There are differences in
using ozone to degrade pesticides in aqueous and gas-
eous phases, because they have different properties and
are affected by environmental conditions in different
ways. The former has better degradation effects
because aqueous ozone has the dual action of ozone
and hydroxyl radicals (O
3
in water generally reacts
with OH
and H
2
O to generate OH˙). In contrast, the
latter usually requires multiple gaseous ozone concen-
trations and ozone treatment times to achieve the
desired effects.
Effects of ozone treatment on pesticide residues
in food
In recent years, many scholars have widely discussed
the degradation of pesticide residues in food by ozone
treatment. There is a plethora of literature showing
that the efficiency of ozone treatment on degrading
pesticide residues is primarily affected by ozone con-
centration, treatment duration, type of food, class of
pesticide and the level of pollution caused by the pesti-
cide residue. In addition, the degradation rates of pes-
ticide residues may be associated with environmental
factors, such as temperature, humidity and pH.
Table 2 lists some recent reports on the respective
reductions of different toxicities of pesticides in food
under treatment conditions involving gaseous or aque-
ous ozone.
Effects of ozone concentration and treatment
time on the degradation of pesticide residues
In theory, a higher ozone concentration and longer
treatment would increase the efficacy of degradation of
pesticide residues. It is generally believed that pesticide
degradation conforms to a first-order kinetic model,
©2018 Institute of Food Science and TechnologyInternational Journal of Food Science and Technology 2018
Use of ozone to remove pesticides from food S. Wang et al.4
i.e. the reaction rate is proportional to the first square
of the concentration of reactant.
Ct¼C0expðktÞð1Þ
where, kis the first-order degradation rate constant;
C
0
and C
t
are the concentrations of pesticide at time
‘0’ and at time ‘t’, respectively. However, the degrada-
tion of pesticide residues shows a trend of rapid turn-
over at the former stage, which gradually slows at the
latter stage, so the first +first-order kinetic model can
be fitted better (Banerjee et al., 2008).
Ct¼C1expðk1tÞþC2expðk2tÞð2Þ
where, C
t
is the concentration of pesticide at time ‘t’;
C
1
and C
2
are the initial concentrations of pesticide at
time ‘0’ degraded through first-order processes 1 and 2;
k
1
and k
2
are the degradation rate constants for 1 and
2. There are some studies regarding the effects of ozone
concentration on the degradation of pesticide residues.
For example, when Chen et al. (2013) treated Chinese
white cabbage and green-stem bok choy at an ozone
gas production rate of 250 mg h
1
for 15 min, the
degradation rates of chlorfluazuron, and chlorothalonil
increased by only approximately 10%. In contrast,
when ozone gas production rate was elevated to
500 mg h
1
, the degradation rates of the three pesticide
residues increased twofold. Similarly, Wu et al. (2007b)
treated Brassica rapa with 1.4 mg L
1
ozonated water,
which degraded approximately 27–34% of cyperme-
thrin, methyl parathion, parathion and diazinon after
15 min. Increasing the ozonated water concentration to
2.0 mg L
1
increased the degradation rates to 30–54%.
Clearly, a higher concentration of applied ozone will
improve the degradative effects on pesticide residues,
thus increasing the removal of their toxicity.
Several studies have investigated the relation
between ozone treatment duration and the degradation
rates of pesticide residues. Savi et al. (2015) employed
Table 1 The mechanism of ozonation of several major classes of pesticides
Type of pesticide Name of pesticide Chemical formula Mechanism of ozonation
Insecticide Parathion
O
N+
O
O
P
S
O
O
For parathion, ozone oxidised P=StoP=O. Five ozonation
byproducts were detected and one of the byproducts was
identified as paraoxon (Wu et al., 2007a)
Diazinon
N
N O
P
O
S
O
For diazinon, ozone oxidised P=StoP=O. Six ozonation
byproducts were detected and one of the byproducts was
identified as diazoxon (Wu et al., 2007a)
Herbicide Bromoxynil
OH
Br B
r
CN
Bromoxynil is a phenol derivative with a cyano group attached,
which is halogenated in the two meta-positions. Bromoxynil
has a hydroxyl substituent in the para-position making it more
water soluble. The oxidation of bromoxynil may occur through
direct attack by electrophilic addition and through indirect attack
by free radicals. It is suggested that the bromoxynil decomposition
pathway may occur via hydroxylation and debromination
(Chelme-Ayala et al., 2010)
Trifluralin
N
CF
3
NO
2
O
2
N
CH
3
CH
3
Trifluralin is an herbicide with two N-propyl groups. The oxidation
of trifluralin by O
3
may occur through direct attack by electrophilic
addition and through indirect attack by free radicals. The results
showed that oxidation by O
3
may proceed by two main
mechanisms: hydroxylation and dealkylation
(Chelme-Ayala et al., 2010)
©2018 Institute of Food Science and Technology International Journal of Food Science and Technology 2018
Use of ozone to remove pesticides from food S. Wang et al.5
60 lmol mol
1
gaseous ozone to store wheat grains
for 60, 120 and 180 min, and deltamethrin residues
were degraded by 67.5%, 88.1% and 89.8%, respec-
tively, which showed an increasing trend. Ikeura et al.
(2013a) treated green persimmon leaves with
2.0 mg L
1
of continuously bubbling ozonated water
for 5, 10 and 15 min, and the quantity of fenitrothion
residues decreased to 67%, 60% and 44%, respectively.
The residues of benomyl also fell to 85%, 62% and
50%, respectively, manifesting a similar trend. There-
fore, there is a positive correlation between the degrada-
tive effects of ozone treatment on pesticide residues and
treatment time. Nonetheless, the degradation rate with
ozonated water significantly decreases with increasing
ozone concentration and contact time in an actual oper-
ation. This may be attributed to the instability of ozone
dissolved in water, which escapes into the environment
within a few minutes. Furthermore, pesticides may have
gradually infiltrated inside food.
The next question raised is what is the optimal
ozone concentration and treatment duration so as to
maximise the degradative effects of ozone on pesticide
residues. de Souza et al. (2018) used response surface
methodology to determine the optimal factors
required for the degradation of difenoconazole and
linuron in carrots. When the concentration of gaseous
or aqueous ozone was 5 or 10 mg L
1
and exposure
time was approximately 120 min, ozone treatment
mediated the degradation of pesticide residues by
more than 80%.
Effect of types of foods on the degradation of
pesticide residues
According to the current utilisation status of pesti-
cides, the pesticide residues remaining in foods such as
vegetables and fruits pose a major threat for consumer
health. The detection rate of pesticide residues in leafy
vegetables has increased over the years. Furthermore,
leafy vegetables also comprise a majority of vegetables
that people prefer to consume in their daily lives.
Therefore, the problem of pesticide residues on leafy
vegetables should arouse our keen attention. The main
factors in the relationship between ozone treatment
and types of foods are the differences in contact area,
structure of tissue and compactness. Generally, ozone
treatment is more effective in the degradation of pesti-
cide residues in vegetables than in fruits. This is
because the leaves of most vegetables are thin and
have a larger surface area for ozone to interact with
adequately. In contrast, fruits have a thick pericarp,
which makes it difficult for ozone to penetrate the cuti-
cle or epidermis to reach the centre. Therefore, the
ozone is likely to be inactivated at the surface itself.
There was a study comparing ozone treatment
between fruits and vegetables. Ikeura et al. (2011b)
Table 2 Summary of the degradation of pesticide residues in food by O
3
Food Type and toxicity of pesticides Treatment conditions
Reduction
levels (%) References
Maize grains Pirimiphos-methyl, low toxicity 0.86 mg L
1
ozone gas, 60 min >91% de Freitas et al. (2017)
Wheat grains Pirimiphos-methyl, low toxicity 60 lmol mol
1
ozone gas, 30 min ~71.1% Savi et al. (2016)
Strawberries Chlorpyrifos, moderate toxicity 1 mg L
1
ozone water, 5 min 75.1% Lozowicka et al. (2016)
Wheat grains Deltamethrin, moderate toxicity 60 lmol mol
1
ozone gas, 180 min 89.8% Savi et al. (2015)
Strawberries Difenoconazole, low toxicity 0.8 mg L
1
ozone gas, 60 min 95% Heleno et al. (2014)
Red persimmon
leaves
Fenitrothion, moderate toxicity
Benomyl, low toxicity
2mgL
1
bubbling ozone
microbubbles solution, 15 min
60%
50%
Ikeura et al. (2013a)
Chinese white
cabbages
Chlorothalonil, low toxicity
Chlorfluazuron, low toxicity
250 mg h
1
ozone gas
production rate, 15 min
77%
75%
Chen et al. (2013)
Loaded seeds Imidacloprid, low toxicity 100 mg L
1
ozone gas, 32 min 95% Bourgin et al. (2013)
Citruses Chlorothalonil, low toxicity
Tetradifon, low toxicity
Chloropyrifos ethyl, moderate toxicity
10 mg L
1
ozone water, 5 min 100%
98.6%
94.2%
Kusvuran et al. (2012)
Lettuces Fenitrothion, moderate toxicity 2 mg L
1
ozone microbubbles
solution, 10 min
67% Ikeura et al. (2011a)
Table grapes Pyraclostrobin, low toxicity
Pyrimethanil, low toxicity
Cyprodinil, low toxicity
Fenhexamid, low toxicity
10 mL L
1
ozone gas, 60 min 100.0%
83.7%
75.4%
68.5%
Gabler et al. (2010)
Vegetable
(Brassica rapa)
Diazinon, high toxicity
Parathion, high toxicity
Methyl-parathion, high toxicity
Cypermethrin, moderate toxicity
1.4 mg L
1
ozone water, 30 min 60–99% Wu et al. (2007a,b)
©2018 Institute of Food Science and TechnologyInternational Journal of Food Science and Technology 2018
Use of ozone to remove pesticides from food S. Wang et al.6
used 2.0 mg L
1
ozonated water to degrade fenitroth-
ion in lettuce, cherry tomatoes and strawberries for
10 min. The removal rates were 58%, 35% and 25%,
respectively, indicating that ozone treatment was more
effective in lettuce than in cherry tomatoes or strawber-
ries. Another study compared ozone treatment of
leaf and root vegetables. Yang et al. (2013) determined
that the percentage of residual acephate, diazinon,
malathion, chlorpyrifos, quintiofos and triazophos ran-
ged from 26.4 to 65.2% in Brassica chinensis L. and
22.7–75.4% in cucumbers after aqueous ozone treat-
ment for 30 min. It was concluded that there was no
significant difference between outcomes of ozone treat-
ment on leaf and root vegetables. In future studies, it
would be interesting to investigate whether there is a
link between ozone treatment and the various types of
different foods. This research may increase our knowl-
edge of whether this technology is more suitable for
degrading pesticide residues in specific types of foods.
Effects of a variety of pesticides on the
degradation of pesticide residues
Gabler et al. (2010) fumigated table grapes with highly
concentrated (10 000 lLL
1
) ozone gas for 60 min,
and the amounts of residues of pyraclostrobin, pyri-
methanil and cyprodinil in the grapes decreased by
significantly different amounts (100.0%, 83.7% and
75.4%, respectively). Two years later, Karaca et al.
(2012) repeated this experiment with a reduced concen-
tration of gaseous ozone (0.3 lLL
1
), and their
results showed that the degradation rates of pyri-
methanil, boscalid, cyprodinil and iprodione still dif-
fered (51.6%, 46.2%, 34.7% and 23.9%, respectively).
Longitudinal comparison of these two studies reveals
the relationship between ozone concentration and pes-
ticide residues, whereas a horizontal comparison
uncovers the relation between the type of pesticide and
ozone treatment.
In general, ozone reacts mostly with pesticides that
contain reducing groups, such as nitrogen, sulfur,
double bonds and aromatic rings. It also undergoes
reactions with nucleophile functional groups such as
-OH, -NH
2
. Pesticides with similar chemical structures
can also manifest similar characteristics. Chemicals in
organic pesticides tend to be more complex and less
water-soluble than those in inorganic pesticides
(Debost-Legrand et al., 2016). The systemic volatility,
water solubility and adsorbability of pesticides
directly affect the degradation of residues in food. In
other words, the efficacy of ozone treatment varies
depending on specific chemical structures and physic-
ochemical properties of the pesticides involved. From
the literature, it can be concluded that ozone treat-
ment is more effective in degrading organophosphate
pesticides than pyrethroid pesticides. For example,
Savi et al. (2016) found that the amounts of residues
of bifenthrin (a pyrethroid pesticide) in wheat grains
diminished by only approximately 37.5% after
180 min of exposure to 60 lmol mol
1
ozone gas. By
contrast, at the same ozone concentration, pirimiphos-
methyl (an organophosphate pesticide) residues could
be significantly decreased by ~71.1% within 30 min. In
addition, Kusvuran et al. (2012) found that all chlor-
othalonil residues adsorbed onto the orange matrix are
completely removed after 5 min by aqueous ozone,
indicating that ozone treatment is most effective
against this fungicide, and even results in complete
degradation, which is due to the fact that chlorothalo-
nil is a non-endogenous pesticide, it is only absorbed
on the surface of food and can be removed by rinsing
with ozone water. Conversely, ozone is less effective in
degrading some endogenous pesticides, mainly because
they can diffuse in food. Theoretically, the pesticide
residues remaining after reaction with ozone are those
pesticides that have penetrated into the food.
Effects of the level of pollution by pesticide
residues on their degradation
Food contaminated with greater quantities of pesti-
cides exhibit higher rates of pesticide residue degrada-
tion and higher removal efficiencies. In other words,
the efficiency of ozone-mediated degradation of pesti-
cide residues is higher at elevated concentrations of
pesticide residues than at low concentrations. This
phenomenon is related to the degradation kinetics of
pesticides. When there is a large amount of pesticide
residue in food, the target of ozone decomposition is
greater, which fits to the pseudo first-order kinetic
model (Debabrata & Sivakumar, 2018), naturally
increasing the degradation rate. Nevertheless, the
amount of residual pesticide is small at a low concen-
tration, the solution is non-saturated and the amount
of ozone that can be decomposed is certain; this situa-
tion leads to the retention of decomposition rates. Xu
et al. (2012) confirmed this point of view well. They
treated cucumbers from two groups, one with high
levels of pesticide residues (approximately
10 mg mL
1
) and the other with low levels of pesticide
residues (approximately 1 mg mL
1
) with ozonated
water for 7 min. The degradation rates of phoxim
were 63% and 14.77%, those of methamidophos were
41.5% and 32.1%, those of trichlorfon were 40.73%
and 20.13%, those of omethoate were 40.52% and
26.8%, those of dimethoate were 37.1% and 24.7%,
those of cypermethrin were 36.76% and 20.9%, those
of dichlorvos were 36.6% and 19.6%, and those of
deltamethrin were 14.2% and 8.45%, respectively.
These results indicate that the degradation rates of
pesticide residues were higher in the group exposed to
high pollution levels than those in the group exposed
©2018 Institute of Food Science and Technology International Journal of Food Science and Technology 2018
Use of ozone to remove pesticides from food S. Wang et al.7
to low pollution levels. Further studies are needed to
fully understand this relationship between ozone treat-
ment and pollution levels of pesticide residues because
there is little research in this area.
Effects of environmental factors on ozone-
mediated degradation of pesticide residues
Ozone-mediated degradation of pesticide residues in
food is affected by surrounding environmental factors.
Theoretically, lowered temperatures will increase the
solubility of ozone thus improving the degradation
rate of pesticide residues. Nonetheless, the reaction
rate of ozone decomposition that yields hydroxyl radi-
cals will slow down when the water temperature is
low. These relative contributions may compensate for
each other. Thus, lowering of temperature is not suffi-
cient for a significant improvement. Ikeura et al.
(2013b) demonstrated that fenitrothion in lettuce and
cherry tomatoes is efficiently degraded when ozone
water temperature is controlled at approximately
30 °C. In addition, increasing humidity and decreasing
pH will augment the efficiency of the aqueous ozone
(Karaca & Velioglu, 2007). Hwang et al. (2001) indi-
cated that the most rapid rate of mancozeb degrada-
tion is at pH 7.0.
Effects of ozone treatment of pesticide residues
on the quality of food
Kechinski et al. (2012) investigated the effect of ozone
treatment on the quality of food. They dipped
papayas in 4 mg L
1
ozonated water for 1–2 min and
preserved the fruit under constant conditions of
25 °C for 10 days. The results showed that low con-
centrations of ozone did not change the macroscopic
appearance of the fruit. Similarly, Heleno et al.
(2015) demonstrated that 2 mg L
1
gaseous ozone
has no significant effect on the quality parameters of
table grapes. In addition, organic acids, soluble sug-
ars, lycopene and other micronutrients in food are
not affected by low concentration ozone treatment
(Tzortzakis et al., 2007; Ali et al., 2014). Chen et al.
(2014) treated peanuts with 6.0 mg L
1
ozonated gas
for 30 min to test whether there was an effect on the
nutritional value. Eventually, no significant difference
was observed between ozone-treated and untreated
samples. Furthermore, ripening induced protein car-
bonylation in kiwifruit, but this effect was depressed
by ozone treatment (Minas et al., 2012). It was
demonstrated that appropriate levels of ozone treat-
ment inhibited cellular respiration intensity, reduced
the production of ethylene and enhanced the activity
of some antioxidant enzymes (Boonkorn et al., 2012).
These changes delayed the ripening and senescence of
fruit and controlled tissue metabolism and surface
browning of food, improving the storage period and
shelf life.
However, ozone treatment for a prolonged period is
likely to affect the sensory properties of food, to alter
surface morphology, lead to spoilage, discolouration,
weight loss and undesirable odours (Isikber &
Athanassiou, 2015), and to cause plants to yellow, wilt
or die. For example, green loss in fruits and vegetables
can be explained by the decomposition of chlorophyll
in cells, while colour darkening may be caused by phe-
nol oxidation and bacterial decay. If the concentration
of ozone during treatment is inappropriate, it will
damage the cells, leading to the leakage of cell inclu-
sions, decreased levels of total chlorophylls, carote-
noids and carbohydrates, and increased concentrations
of 1-aminocyclopropane-1-carboxylic acid (ACC).
Data from Iglesias et al. (2006) suggest that solute
leakage and lipid peroxidation in citrus plants in gas-
eous ozone-treated (65 nL L
1
) fruit were significantly
greater than those in an untreated control group. Of
note, ozone treatment may also trigger protective
mechanisms against oxidative stress in citrus fruits
(Thwe et al., 2015). In addition, high concentrations of
ozone on the surface of food may decrease the amount
of vitamin C (VC). One study revealed that adding
1% vinegar and lowering the water temperature in the
reaction system effectively reduces the loss of ascorbic
acid from food (Wu et al., 2014).
Current restrictions in application of ozone
treatment for pesticide residues
Although ozone treatment has many technical advan-
tages in the degradation of pesticide residues and its
efficacy is remarkable, there are still several limitations
to its practical application. For instance, ozone treat-
ment may generate ozonation byproducts and cause
secondary pollution. Further studies are necessary to
characterise and understand this unpredictable possi-
bility. Ozone is also likely to cause some damage to
human health and production equipment. Therefore, it
is necessary to investigate such a phenomenon further,
so that ozone treatment can be integrated into agricul-
tural production on a larger scale.
Byproducts of ozonation
The oxidation of pesticide residues may generate
ozonation byproducts. Compared to their parent pesti-
cides, intermediate ozonides may have the same or
greater toxicity (Battaglin & Fairchild, 2002; Ver-
straeten et al., 2002). This is because the degradation
of pesticide residues introduces polar chemical groups
into the molecular structure of parent pesticides, caus-
ing production of more polar byproducts. The increase
in polarity raises the water solubility and mobility, and
©2018 Institute of Food Science and TechnologyInternational Journal of Food Science and Technology 2018
Use of ozone to remove pesticides from food S. Wang et al.8
decreases the adsorption and volatility of these
byproducts, and they are often more difficult to
degrade than their parent pesticides. For example,
ozone easily attacks P=S groups in organophosphate
pesticides, generating compounds that contain P=O
bonds as major byproducts, which are released into
the environment and converted into forms that are
more mobile and toxic. That is, a thion form is con-
verted into an oxon form, which can be two- to three-
fold more toxic when compared with the source
pesticide (Evgenidou et al., 2006). It is no use remov-
ing the pesticide or reducing its concentration and gen-
erating by products with greater toxicity. Moreover,
organophosphate pesticides that contain oxon groups
are more difficult to degrade continuously by ozone.
Hydroxyl radicals with strong oxidisability may
degrade them only in a process of advanced oxidation.
Some research groups determined that the main
ozonation byproduct of parathion was paraoxon, and
the main ozonation byproduct of diazinon was
diazoxon. Paraoxon was present at trace levels and
unstable, while diazoxon was observed to be highly
stable, which indicates that paraoxon was readily
degraded by ozone solution. (Wu et al., 2007a).
Hydroxylation and debromination were the primary
pathways of degradation of bromoxynil (3,5-dibromo-
4-hydroxybenzonitrile). The former may lead to the
formation of 3,5-dibromo-2,4-dihydroxybenzonitrile,
and the latter may proceed via 3-bromo-4,5-hydroxy-
benzonitrile, 3-bromo-4-hydroxybenzonitrile, generating
4-hydroxybenzonitrile. Hydroxylation and dealkylation
were the major routes for trifluralin (a,a,a-trifluoro-2,6-
dinitro-N,N-dipropyl-p-toluidine) oxidation. Aromatic
hydroxylation may result in the formation of a,a,a-
trifluoro-4,6-dinitro-5-(dipropylamino)-o-cresol. The
formation of a,a,a-trifluoro-2,6-dinitro-N-dipropyl-p-
toluidine seemed to involve the mono-dealkylated
derivative of trifluralin. 2,6-dinitro-4-trifluoromethyaniline
may be the result of didealkylation. (Chelme-Ayala et al.,
2010). The ozone reaction products are totally different
species than the original molecule. Accordingly, degrada-
tion products should be comprehensively investigated.
Possible harm caused by ozone to the human
body
Ozone is a powerful oxidant that can react with almost
any biological tissue in the human body. Therefore,
this is a key point to consider when determining
whether there is a health threat to the human body
from the ozone used to degrade pesticide residues. For
safety reasons, the Food and Drug Administration
(FDA) defined the allowable exposure value of ozone
concentration as 0.05 ppm for 8 h. If operators inhale
excess ozone for a prolonged period, there will be
some negative health effects, such as stimulation of
(and damage to) mucous tissues of the eyes and of the
respiratory system to varying degrees, headaches, ver-
tigo, a burning sensation in the eyes and throat, cough
and other symptoms. For those with asthma, emphy-
sema, and chronic bronchitis, the negative effects of
ozone exposure are more pronounced. Fortunately, the
smell of ozone is distinctively irritating and can be
detected when ozone concentration is as low as
0.02 ppm. Thus, while ozone has been used around
the world for more than a century, there have been no
reported cases of death due to ozone poisoning.
Equipment requirements for ozone treatment
Ozone can corrode almost any metal in addition to
gold and platinum, but equipment containing fer-
rochrome will basically not be oxidised by ozone.
Accordingly, ferrochrome stainless steel containing
25% chromium is commonly used to make generators
and fill components for ozone treatment. Ozone also
has a strong corrosive effect on non-metallic materials,
including fairly stable materials such as plastic filter
plates made from polyvinyl chloride; therefore, over
time it will loosen, crack, or perforate ozone-filling
equipment. Ordinary rubber is not an effective sealing
material for ozone equipment, and instead, silicon rub-
ber or acid-resistant rubber that is highly resistant to
corrosion is necessary.
Prospects of application of ozone treatment to
pesticide residues
Today, with the inevitable recurrence of the pesticide
residue problem, the prospect of using ozone treatment
to degrade pesticide residues in food is certainly
strong. Ozone treatment has many advantages which
increases the applicability of this method. Ozone treat-
ment holds promise as a residual pesticide degradation
method because of the unique properties of ozone cou-
pled with the fact that it is free from the limitations of
traditional degradation methods and the fact that it
can guarantee the quality of food. To improve the
development and application of this technology in
food processing, it is necessary to carry out the degra-
dation of pesticide residues. Currently, there are many
studies on the reaction kinetics of degradation, but
there are only a few studies on the qualitative, quanti-
tative and toxicological evaluation of reaction byprod-
ucts. Therefore, the following can be areas of future
research in the development of ozone treatment for
degradation of pesticide residues in food: (i) improving
the efficiency of ozone treatment and degradation of
pesticide residues effectively, while maintaining the
quality of product, (ii) identifying the byproducts of
pesticide residue degradation and evaluating their toxi-
city. Due to the scarcity of research on byproducts of
©2018 Institute of Food Science and Technology International Journal of Food Science and Technology 2018
Use of ozone to remove pesticides from food S. Wang et al.9
pesticide residue degradation and the complexity and
chronicity of safety assessment, time is needed to solve
these problems. In addition, it is also necessary to
screen the degradation byproducts for their impact on
human health through toxicological studies in vivo and
in vitro, and (iii) finally, studying the mechanism of the
degradative action of ozone on the different types of
pesticide residues should help achieve accurate regula-
tion of product safety. This includes understanding the
reaction mechanisms of the molecular structures of
various degradation byproducts generated by ozone
treatment and modelling of the reaction kinetics. On
the basis of these data, it will be possible to predict
the change in concentration of pesticide residues and
their degradation byproducts to precisely regulate their
safety.
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