Use of ozone in sanitation and storage of fresh fruits and vegetables

Abstract

The following study focuses on the efficiency of ozone sanitation in the food industry with specific reference to fresh fruits and vegetables. Recent research findings including mechanisms of action, artificial synthesis, sanitation food efficiency and effects, application with different preservation techniques, as well as pros and cons have been reported. In particular, ozone reduces microbial spoilage and weight loss of apple.Onions treated with ozone showed that mould and bacterial counts were greatly reduced without any change in their chemical composition. Ozone treatments carried out on tomatoes did not affect their colour, sugar content, acidity and antioxidant capacity while it reduced the amount of aflatoxins when applied to peanuts. Red peppers, strawberries and cress treated with ozone showed a reduction in the microbiological population. In addition to many other examples it is also reported that the phenolic and flavonoid content of pineapples and bananas increased significantly when exposed to ozone for up to 20 minutes. While considering limitations and contraindication in ozone use, it has been pointed out that ozone is a highly instable and corrosive gas and due to its short life span, ozone must be generated on site as storage is not possible. In conclusion ozone appears to be a more effective biocide than other substances due to its high reactivity and its strong oxidant power. However, it is necessary to determine the safety limits of exposure to ozone in order to prevent damage on food and human health.

Full text

Journal of Food, Agriculture & Environment, Vol.11 (3&4), July-October 2013
585
www.world-food.net
Journal of Food, Agriculture & Environment Vol.11 (3&4): 585-589. 2013
WFL Publisher
Science and Technology
Meri-Rastilantie 3 B, FI-00980
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e-mail: info@world-food.net
Use of ozone in sanitation and storage of fresh fruits and vegetables
Letizia Carletti
1
, Rinaldo Botondi
2
, Roberto Moscetti
1
, Elisabetta Stella
1
, Danilo Monarca
1
, Massimo
Cecchini
1
and Riccardo Massantini
2
*
1
Dipartimento di scienze e tecnologie per l’Agricoltura, le Foreste, la Natura e l’Energia (DAFNE). Università degli studi della
Tuscia Via S. C. De Lellis 01100 Viterbo Italia.
2
Dipartimento di Innovazione dei sistemi Biologici, Agroalimentari e Forestali
(DIBAF). Università degli studi della Tuscia Via S. C. De Lellis 01100 Viterbo Italia. e-mail: massanti@unitus.it,
lcarletti@unitus.it, rbotondi@unitus.it, rmoscetti@unitus.it, elistella@unitus.it, monarca@unitus.it, cecchini@unitus.it
Abstract
The following study focuses on the efficiency of ozone sanitation in the food industry with specific reference to fresh fruits and vegetables. Recent
research findings including mechanisms of action, artificial synthesis, sanitation food efficiency and effects, application with different
preservation techniques, as well as pros and cons have been reported.
In particular, ozone reduces microbial spoilage and weight loss of apple.Onions treated with ozone showed that mould and bacterial counts were
greatly reduced without any change in their chemical composition. Ozone treatments carried out on tomatoes did not affect their colour, sugar
content, acidity and antioxidant capacity while it reduced the amount of aflatoxins when applied to peanuts. Red peppers, strawberries and cress
treated with ozone showed a reduction in the microbiological population. In addition to many other examples it is also reported that the phenolic
and flavonoid content of pineapples and bananas increased significantly when exposed to ozone for up to 20 minutes. While considering
limitations and contraindication in ozone use,
it has been pointed out that ozone is a highly instable and corrosive gas and due to its short life
span, ozone must be generated on site as storage is not possible.
In conclusion ozone appears to be a more effective biocide than other substances due to its high reactivity and its strong oxidant power. However,
it is necessary to determine the safety limits of exposure to ozone in order to prevent damage on food and human health.
Key words: Ozone, sanitation, fresh fruits and vegetables, foods, conservation techniques, IV range products, lightly processed foods.
Introduction
The increasing demand for sanitation as a means for controlling
infection and disease in food and the need for reducing the
emission of polluting substances have made researchers search
for safe and new sanitizing methods. Ozone has proved to be
suitable for this purpose.
The term “ozone” comes from the Greek word “ozein” which
means “to give off odour”.
The molecule has a pungent and characteristic odour and at
high levels of concentration it is blue at ordinary temperatures
1
.
At the level of concentration at which it is normally used, the
colour is not noticeable
2
.
Ozone was first discovered by the German researcher Christian
Friedrich Schönbein in 1839, even if as early as 1783,Van Marum
indicated the presence of a strange pungent smell of gas in
proximity of equipment capable of conducting electrical
discharge
3
.
In 1902 Cologne used ozone to disinfect frozen beef in order
to prolong its shelf life. In 1904, De la Coux noticed the ample
opportunities of using ozone in gelatine, casein and albumin
production plants
3
. It was first used commercially in 1907 for
disinfecting the municipal water supply in Nice and then in St.
Petersburg in 1910 for the same purpose. In 1928 it was used
for disinfecting eggshells and between 1953 and 1956 it was
acknowledged as an effective method for sterilising food
containers
3
.
In 1995 and 1996, Japan, France and Australia made laws which
permitted the use of ozone in the food industry. In 2001 the U.S.
Food and Drug Administration (FDA) modified the regulation
in such a way to allow the use of both aqueous and gaseous phases
in food treatment, conservation and transformation
3
.
The main physical and thermodynamic properties of pure ozone
are reported in Table 1.
As it is an unstable gas, the average life of ozone is about 20
min, depending on the temperature
1
. The molecule is generally
more stable in the gas phase than in the aqueous phase
5
.
In pure water, it degrades rather rapidly in oxygen. This
degradation is faster in impure solutions
6
. Rice
5
states that the
solubility of ozone in water is 13 times higher than the solubility
of oxygen in temperatures ranging from 0-30°C. The lower the
temperature, the higher the level of solubility of ozone. In fact
at high temperatures, the stability and effectiveness of ozone
Molecular weight 47.9982 g/mol
Density 0.001962 g/cm
3
Dielectric constant 1.002
Boiling point -111.9 ± 0.3°C
Melting point -192.5 ± 0.4°C
Critical temperature -12.1°C
Critical pressure 54.6 atm
Table 1. Major physical properties of pure ozone
2
.
Received 8 June 2013, accepted 27 October 2013.

586 Journal of Food, Agriculture & Environment, Vol.11 (3&4), July-October 2013
are reduced
7
.
This study reports the effect of ozone treatments on the main
fruits and vegetables and on some fresh-cut products.
Mechanisms Of Action
The bactericidal effect of ozone was studied and documented
on a wide variety of organisms, including Gram positive and
Gram negative bacteria as well as spores and vegetative cells.
Ozone is efficient against Venezuelan equine encephalomyelitis
virus, hepatitis A, influenza A, vesicular otitis virus, and
infectious bovine rhino-tracheitis virus as well as several strains
of bacteriophage
2
.
In the case of virus and bacteria, as well as protozoa and insects,
ozone acts through the catalytic oxidation of proteins and lipo-
saccharides destroying their structure. Ozone oxidizes the
organic matter of bacterial membranes, weakening cellular walls
and causing cell damage and the consequent death of the cell.
This distinguishes ozone from chlorine and other oxidant or non-
oxidant biocides which must be transferred through membranes
in order to interfere with cellular enzymatic or non enzymatic
activities and therefore perform biocide activity
8
. Ozone
treatments can cause death of cells due to the effect of nucleic
acid destruction
9
. Ozone has a short life span in water and in air,
so it is safer than other food additives, as no residues remain in
the food
9
. Khadre and Yousef
10
compared the effects of ozone
treatment to the effects caused by hydrogen peroxide treatment
on Bacillus spores of food origin and ozone proved to be more
efficient than hydrogen peroxide. When compared to chlorine
and hypochlorous acid, the potential of ozone is from 1.5 to 3000
times greater than the other two respectively
11
. Ikeura et al.
12
analyzed
the efficiency of ozone efficacy in removing pesticides from
vegetables by using gas in the form of micro-bubbles in rinsing
water. The effectiveness varies according to method used for
producing the micro-bubbles: production by means of
decompression is more efficient than production by gas-water
circulation. This could be due to a greater number of micro-bubbles
which can infiltrate into the vegetables.
Ozone Generation
Oxygen molecules are ruptured, producing oxygen fragments
which join other oxygen molecules to produce ozone, O
3
13
. In
another process of ozone formation, oxygen floats upward into
the atmosphere and in turn is converted into ozone through
ultraviolet radiation
14
.
Ozone can be generated artificially by means of the corona
discharge; air or O
2
passes through a high voltage electric field.
In this case the stable molecule of oxygen is broken and splits
into two oxygen radicals which react with each other to form
ozone. The formation of Ozone produced by electrical discharges
on a gas is based on the lack of homogeneity of the corona
discharge in the air and in oxygen. There are many micro-
discharges distributed in space through which ozone is produced:
every single micro-discharge only lasts a few nanoseconds and
is greater (2.5-3 times) in the air than in pure oxygen. In order
to create corona discharge an electrical potential of at least
5000V is required. The typical range within which the reactions
are carried out is between 5000 V (with a frequency of 1000
Hz) and 16000 V (with a frequency of 50 Hz)
3
.
The first ozone generator was developed in the United States
in 1888 by Fewsn to deodorize gas pestilential. In Germany in
1902, Siemens and Halske built the first ozone generator for
treating water.
Use Of Ozone In Food Hygiene
Ozone is a strong oxidant which is efficient for controlling
bacteria, molds, protozoa and viruses
15
. In 1997, ozone was
declared a GRAS product (Generally Recognized As Safe) by a
team of experts from FDA
17
. This denomination soon caused an
increase in research concerning the use of ozone in the food
industry. Ozone can be used for various purposes such as cleaning
surfaces or equipment and disinfecting water for recycling
8, 17
.
The effectiveness of disinfectants varies according to the type
of product, the surface to be treated and the specific
characteristics of the microorganisms
14
. In addition, the
susceptibility of microorganisms to ozone varies according to
the physiology of the tissue, temperature, moisture, the pH level
and the presence of additives such as acids, soaps and sugars
19
.
The effectiveness of the various types of treatment can be seen
in Table 2. Other proven positive effects of the use of ozone
concern the purification of micotoxins
19
and pesticide residuals
20
and for the control of classified microbes in the field of biological
risk
21
. Leesch and Tebbets
22
demonstrated that ozone is effective
for controlling the presence of arthropods, like in the case of
grape fumigation with high doses of ozone to control spider
populations belonging to the black widow spider species which
are often found in boxes of grape exported from California.
Ozone can be used as a sanitizer in the form of a gas or
dissolved in water. When ozone is utilized as a gas, the length of
exposition is longer (1-4 h) than ozone dissolved in water (1-10
minutes)
3
.
Ozonated water is a good alternative to traditional sanitizers
because it is effective at a low concentration
13
. Artes et al.
23
reported several studies in which the efficacy of ozonated water
was successfully tested by inoculating targeted specific
microorganisms on pure cell suspensions or on the food surface
and treating these surfaces with O
3
. Singht et al.
24
and Kim et al.
8
demonstrated the controlling action of ozone on some
pathogens: Staphylococcus aureus, Salmonella typhimurium,
Bacillus cereus, Enterococcus faecalis, Pseudomonas
aeruginosa, Pseudomonas fluorescens, Leuconostoc
mesenteroides, Yersinia enterocolica, Listeria monocytogenes,
Escherichia coli, Candida albicans, Zygosaccharomyces and
Aspergillus niger spores.
The Effect of Ozone Treatment On Fresh And Fresh-cut
Fruit And Vegetables
More recently, there has been a growing interest in the evaluation
of ozone treatments during the processing and storage of fruits
and vegetables
25, 26
.
Microbial contamination of fruit and vegetables can occur at
various stages from the farm to the table. The propagation of
microorganisms occurs during growth in the field, harvesting,
post-harvest handling and transportation, storage, processing and
marketing for human consumption.
Beuchat
27
showed that treatment with ozone seems to have a
beneficial effect in extending the storage life of fresh non-cut
commodities such as broccoli, cucumber, apples, grapes,
oranges, pears, raspberries and strawberries by reducing

Journal of Food, Agriculture & Environment, Vol.11 (3&4), July-October 2013
587
microbial populations and through ethylene oxidation. Treatments
on apples with ozone resulted in a reduction of weight loss and
spoilage.
Onions treated with ozone during storage showed a
considerable decrease in mould and bacterial counts without
causing any change in their chemical composition and sensory
quality
28
.
Continuous ozone exposure to 0.3 ppm (v/v) inhibited the
growth of fungi and spores on ‘Elegant Lady’ peaches during
storage
29
. The authors also observed a reduction of grey mould
in ‘Thompson Seedless’ table grapes.
Treatments on whole and fresh-cut Thomas tomatoes, stored
for a long time at high concentrations (7µL L
-1
), show how ozone
efficiently reduced bacterial and fungal population
30
.
Gonzales-Barrio et al.
31
analyzed the induction of antioxidant
accumulation in white table grapes (var. ‘Superior’) after ozone
treatments at different concentrations (3.88 and 1.67 gh
-1
) for
1, 3, and 5 h during storage at 22°C.
Fresh-cut salad, washed with ozonated water and packed in
ozone, showed an extension of shelf life
32
.
Tzortzakis et al.
33
demonstrated that low-level ozone-enrichment
(0.1 µmol mol
-1
) during storage at 13°C, reduces spore production
in Botrydiscinerea and lesion development in tomatoes,
strawberries, table grapes and prunes.
Tzortzakis et al.
34
report that ozone treatments between 0.005
and 5.0 µmol mol
-1
reduce fungal lesion development due to
Alternaria alternate and Colletotrichum coccodes.
Tiwari et al.
35
investigated the main effects and interaction of
ozonation on orange juice colour degradation. The ozonation of
organic dyes causes loss of colour because of the oxidative
fission of the chromophores due to attack on conjugated double
bonds. Similarly the chromophore of conjugated double bonds
of carotenoids is responsible for the colour of orange juice.
Carotenoid pigments which are responsible for the yellow,
orange or red colour in orange juice contain one or more aromatic
rings. The ozone and hydroxylradicals (OH
-
) generated in the
aqueous solution may open these aromatic rings and lead to a
partial oxidation of substances such as organic acids, aldehydes,
and ketones.
Rodoni et al.
15
evaluated the effect of short-term gaseous ozone
treatment (10 µL/L; 10 min) on the quality of tomato fruits. The
treatments did not modify fruit colour, sugar content, acidity, or
antioxidant capacity but reduced fruit damage by 27% after 9 days
of storage at 20°C (Fig. 1). They also reduced weight loss and
aided the accumulation of phenolic compounds (Fig. 2). The study
shows that short-term treatments with ozone are also effective in
Applications Treatment Micro-organism Results
2 ppm ozone gas at atmospheric
pressure, 22° C and 77% HR for 4 h
E.coli, S. liquefaciens, S. aureus, L.
innocua, Rhodorotura rubra
Reduction ranging from 7.56 to 2.41 log values Stainless steel surfaces
2 ppm ozone gas in biolaerosol
chamber at 20°C and 50% HR for 1 h
Micrococcus luteus 2-3 log reduction
Stainless steel surfaces in the presence
of UHT milk
2 ppm ozone gas at atmospheric
pressure, 22°C and 77% H.R. for 4 h
E.coli, S. liquefaciens, S. aureus, L.
innocua, Rhodorotura rubra
Reduction ranging from 5.64 to 1.65 log
Equipment, walls, floors, drains, tables
and conveyors, previously well-cleaned
Ozonated water, 3.0-3.5 ppm Trichophyton mentagrophytes, S.
cholerasuis,S. aureus, Ps. aeruginosa,
Campylobacter jejuni, L.
monocytogenes, Aspergillus flavus,
Brettanomyces bruxellensis, E. coli
4-6 log reduction
Table 2. Treatments with ozone and relatives effects
4, modified
.
Control
O
3
Damaged fruits (%)
Time at 20°C (d)
Figure 1. Ozone treatment effects on tomatoes damage. The asterisk
indicates significant differences compared to control (P≤0.05)
15
.

588 Journal of Food, Agriculture & Environment, Vol.11 (3&4), July-October 2013
reducing the softening of tomato fruits.
Alothman et al.
36
studied the effect of ozone treatments (8±0.2
ml/s for 0, 10, 20, and 30 min) on the total phenol, flavonoid,
and vitamin C content of fresh-cut honey pineapple, ‘pisang mas’
bananas and guava demonstrating that the total phenol and
flavonoid content of pineapple and banana increased significantly
when exposed to ozone for more than 20 min. An opposite trend
was observed for guava. The ozone treatment significantly
decreased the vitamin C content of all three fruits.
Treatments carried out with ozonated water on red peppers,
strawberries and cress showed a reduction in the microbiological
population (0.5-1.0 log cycle
-1
). This reduction is even more
evident when the treatment is combined with a scalding process
37
.
Ozone treatments on kiwi brought about an interruption in the
production of ethylene and in the induction of the antioxidant
activity
38
.
Alencar et al.
39
reported that peanuts treated with ozone showed
a total aflatoxin reduction (about 3 log cycle
-1
) and a B1 aflanoxine
and internal fungal population reduction.
Kechinsky et al.
40
observed that ozone treatments with wax
and thermal-therapeutic treatments with water led to fungal
absence and disinfection on papaya.
Limits And Contraindications Of Ozone Use
Ozone is an efficient sanitizer, but has some limitations when
used on food. Moreover, due to its short life span, ozone must
be generated on site as storage is not possible
14
. Ozone is a
highly instable and corrosive gas. The decomposition of ozone
requires elaborate processes depending on the types of radicals
formed in solution and on several types of organic matter in
medium that induce, promote or inhibit the reaction chain
9
. In
addition, low doses of ozone, which can inactivate pure microbial
cultures, can be inefficient against viruses, spores and cysts.
Perez et al.
25
reported the loss of aroma which is typical of
strawberries treated with ozone during conservation, due to
changes in the ratio between soluble solids and organic acids.
The changes may be due to degradation of saccharose and
glucose.
Kim et al.
9
observed modifications in the surface color of
some fruits and vegetables such as peaches and carrots, a
decrease in the amount of ascorbic acid in broccoli florets and
thiamin in wheat flour, and lipid oxidation affecting the sensory
quality of grains and crushed spices. Ozone in air, at
concentrations higher than 0,1 ppm, has a strong odor which
causes irritations of the nose, throat and eyes. Exposure to a high
concentration of ozone may have mutagen effects and cause death
due to acute toxicity. After 1-2 hours of exposure to ozone at a
concentration of 0.65 ppm concentration, an acceleration in the
respiration rate was observed in test dogs. Exposure to 0.02 ppm
ozone concentrations for 4-6 weeks caused distension of the lung
in young rats
41
. Ozone concentrations higher than 0.02 ppm cause
various levels of damage to the respiratory system according to
the duration of exposure
42
. It is important to establish safety
limits for the treatment of food, find efficient systems for detecting
and destroying ozone when there are high levels of concentration
of the gas and carry out regular medical checkups on workers
subject to chemical risk. In humans, ozone mainly effects and
damages the respiratory system. Symptoms of intoxication are
headache, weakness, loss of memory, increase in frequency of
bronchitis and high muscle tension
43
.
Use Of Combined Preservation Methods
Several studies analysed the use of combined preservation
methods with ozone treatments.
Sharma
15
mentioned hydrostatic pressure, UV and H
2
O
2
.
The application of pressure aids the penetration of the
sanitizers into the inaccessible cracks and crevices of foods,
thus enhancing microbial decontamination without
compromising quality. The main advantage of applying
hydrostatic pressure includes uniform transmission of pressure,
regardless of the size and shape of sample.
The use of ozone in combination with initiators such as UV or
H
2
O
2
can result in advanced oxidation processes that are highly
effective against the most resistant microorganisms.
Conclusions
Ozone is a more efficient biocide than other chemical substances
due to its high reactivity and strong oxidant power. Therefore it
is widely used to decontaminate food, mainly fruits and vegetables
despite its instability. The identification of the most efficient
applications and their implementation at industrial level have been
a slow process. This may be due to the fact that high capital
investment and operational costs are required for ozone treatments
44
.
Further studies must be carried out on ozone treatment with the
aim of finding a valid alternative to the chemical decontamination
of fresh or cut-fresh fruits and vegetables. It is necessary to find
food products for which ozone treatment is qualitatively effective
and find synergies with other solutions like UV ray, hydrostatic
pressure and sonication. In the future, ozone treatment will be
considered a suitable post harvest operation for removing chemical
and biological contaminants and improving the conservation as
well as for recycling water.
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