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98 Najafi and Shaban
Int. J. Biosci. 2015
RESEARCH PAPER OPEN ACCESS
The effect of pretreatment of ozone and citric acid on quality
of fresh-cut lettuce (Lettuce sativa L.) preserved into modified
atmosphere packaging (MAP)
Farzaneh Najafi*, Safoora Shaban
Department of Plant Scinece, Faculty of Biological Sciences, Kharazmi University, Tehran, Iran
Key words: Iceberg lettuce, microbial load, modified atmosphere, ozonated water.
http://dx.doi.org/10.12692/ijb/6.1.98-108
Article published on January 05, 2015
Abstract
In this study, the effect of three levels of citric acid (0, 0.5 and 1 g l-1) and three levels of ozonated water (0, 0.6
and 1 ppm) and the interaction of these two treatments on microbial load and qualitative features of fresh-cut
iceberg lettuce were studied. After treatment, microbial load and qualitative features of cut lettuce were
evaluated in modified atmosphere packaging (5% O2 + 5% CO2 + 90% N2) in four different storage times (3, 6, 9
and 12 days). The effects of these treatments were also compared with percidine (concentration 1 ml to 1200 ml
in water). After treatment, fresh-cut lettuce pieces were stored at 4C with relative humidity 75% for 12 days. The
results showed that the total count of microorganisms and the weight loss percentage were increased by
increasing the storage time, whereas parameters such as surface color, vitamin C and polyphenol oxidase activity
were decreased. In lettuces treated with different concentrations of citric acid, the lowest total count of
microorganisms was related to 1 g lˉ¹ citric acid concentration and also treatment with 1 ppm ozonated water
concentration. In total, treatments of citric acid and ozonated water, especially in high concentrations and
interaction of these treatments resulted in better preservation of qualitative features and reduced microbial load
of fresh-cut lettuces during storage time.
* Corresponding Author: Farzaneh Najafi [email protected]
International Journal of Biosciences | IJB |
ISSN: 2220-6655 (Print) 2222-5234 (Online)
http://www.innspub.net
Vol. 6, No. 1, p. 98-108, 2015
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Int. J. Biosci. 2015
Introduction
There is a growing use of Modified Atmosphere
Packaging (MAP) today aimed to improve the quality
of freshly cut produce and to prolong shelf-life. The
use of this method for packaging freshly cut fruits and
vegetables helps preserve their quality and increase
their storage life (Artes et al., 2007). This method
reduces the respiration rate, the chemical and
biochemical reaction rates and the growth rate of
pathogenic microorganisms in freshly cut fruits and
vegetables and thus increases their shelf-life ( Coles et
al., 2009; Regaert et al., 2007).
A big issue presenting itself in the freshly-cut produce
industry is finding ways to reduce microbial
contamination and to maintain the reduction up to
the point when the consumer gets it to their mouth.
To reduce the microbial load of these produce,
various antimicrobial agents such as ozonated water
and organic acids are used. Using ozone is
recommended as an alternative to traditional
disinfectants due to its efficiency in low
concentrations and during short exposure times and
due to its way of decomposition into non-toxic
compounds. The antimicrobial action of ozone is due
to the strong oxidizing properties of ozone molecules
or the materials produced from its decomposition,
such as hydroxyl radicals, which rapidly react with
intracellular enzymes, nucleic materials and their cell
constituents, fungal spore coats or viral capsids
(Khadre et al., 2001). Organic acids, particularly
citrate, lactate, and acetate, have antimicrobial
properties (Artes et al., 2007). They are therefore
used to deactivate foodborne pathogens in fresh
produce. Organic acids act fast and destroy a wide
range of bacteria. Citric acid prevents the
discoloration of fruits and vegetables through its
inhibiting effects on the action of this enzyme; it is
therefore extensively used on freshly processed fruits
and vegetables (Olmez and Kretzschmar, 2009).
Many scientists have investigated the microbial-load-
reducing effect of antimicrobial agents such as
ozonated water and organic acids on the quality of
produce and found the highest total count of
microorganisms to pertain to bacteria, which are
often responsible for spoiled vegetables. Ozone is
known to change the permeability of bacterial cell
membrane and to destroy them. Akbas and Olmez,
2007 demonstrated that immersion treatment with
chlorine, citric acid and ozonated water effectively
helps reduce microflora in freshly cut iceberg lettuce,
and that immersion in organic acids has a greater
antimicrobial effect on lettuce microflora and storage
life compared to ozone or chlorine treatments (Akbas
and Olmez, 2007). In one study, researchers showed
that a combined ozone and citric acid treatment has a
greater effect on reducing the population of
pathogens in iceberg lettuce compared to single
treatments (Yuk et al., 2007). It's found that, when
using antimicrobial compounds, ozonated water has
great effects on destroying both gram positive and
gram negative bacteria in food (Restaino et al.,1995).
Immersion of iceberg lettuce in a 0.5% solution of
citric or lactic acid for 2 minutes can be as effective in
reducing microbial populations in freshly cut iceberg
lettuce as treatment with 100 ppm chlorine (Olmez
and Akbas, 2009).
Bacteria counts in spinach, lettuce and strawberry
treated with 0.05 ppm concentration of ozone and
stored at low temperatures for 7 days decreased by
30% to 50% (Kader et al., 1989). Salmonella
populations decreased in carrots treated with lemon
juice, vinegar and a combination of both (Sengun and
Karapinar, 2004). Uyttendaele et al., 2004 reported a
significant reduction in Psychrotrophic natural flora
in minimally-processed vegetables such as chopped
carrots, lettuce and pepper after treatment with a 2%
lactic acid for just 1 minute.
Being a salad vegetable, lettuce is consumed by a lot
of people. The present study thus investigated the
means of preserving the freshness of freshly cut
lettuce without sacrificing its nutritional quality and
also assessed the effect of proper doses of permitted
disinfectants (treatments with ozone and citric acid
separately and in combination) on increasing shelf
life and reducing microbial load of this produce for
supply to consumers.
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Int. J. Biosci. 2015
Materials and methods
Iceberg lettuce was provided in the spring of 2011
from farms in Karaj and transferred to the cold
storage and stored for 24 hours at 4°C. Damaged and
unhealthy lettuce leaves were separated and the
remaining leaves were rinsed with water and when
the surface moisture dried, they were chopped
uniformly with a sharp knife and were kept in a cold
storage after treatment.
Treatments
In this study, fresh-cut lettuce pieces were immersed
in ozonated water treatment in three levels (0, 0.6
and 1 g l-1) for 10 minutes and in citric acid in three
levels (0, 0.5 and 1 g l-1) for 5 min. Then they were
packed using polypropylene package with modified
atmosphere of 5% O2 + 5% CO2 + 90% N2 and were
kept in the cold storage. In this study, a group of
fresh-cut lettuce was treated with percidine (by a ratio
of 1 to 1200) and considered sham group. An
ozonated water generator (Ozone EUF model
MHP1H) was used to produce ozonated water at
needed concentrations.
Packing
Two-hundred grams of chopped lettuce was packaged
using Henkelman vacuum packaging machine (model
200A) under modified atmosphere (5% O2 + 5% CO2
+ 90% N2). Then lettuce packages were moved to cold
storages at temperature of 4°C with relative humidity
75%. The treated lettuce was sampled to assess the
factors in four stages, each stage including three days
in the cold storage.
Evaluated characteristics
Weight Loss
In all samplings, the plant fresh weight was measured
by a balance with 0.1 g accuracy and was obtained by
the following formula and reported as weight loss
percent (Saini et al., 2001).
Weight loss percent =
×
100.
Discoloration
The discoloration during the storage time was
measured based on parameters L*, a*, and b* (degree
of color transparency) by using a chromameter
(Konica Minolta CR-403, Japan) and chroma (purity
of color) and hue were calculated from the following
formula (Bernalte et al., 2003).
h0 =
c = 1/2
Vitamin C
For measuring vitamin C, titration with iodine and
potassium iodide and starch solution was used. Five
ml filtered lettuce juice was mixed with 20 ml
distilled water, and 2 ml starch solution 1% was added
to it. The resulting solution was titrated with iodine
and potassium iodide and the value of vitamin C was
obtained by the following formula (Saini et al., 2001).
C = (0.88 × V) / 5 × 100.
Measurement of polyphenol oxidase activity
One gram of lettuce tissue was pulverized in a mortar
with 6 ml sodium phosphate buffer (pH 6.5) and 1 mg
polyvinylpyrrolidone and the resulting mixture was
centrifuged (12000 rpm, 4C, 20 min). The reaction
mixture contained 0.2 ml catechol in addition to 2.7
ml sodium phosphate buffer (0.1 M) plus 0.1 ml
extract. The absorption was read every 10 seconds for
100 seconds at wavelength 420 nm (Huang et al.,
2009).
Evaluation of microbial load
Microbial load was evaluated during storage time
once every three days.
Sample preparation methods
The sample was prepared under a sterile hood. First,
the surface of the package was cut with a sterile knife
and 10 g of the sample was taken with forceps and
placed in a sampling container containing 90 ml
sterile normal saline and the sampling container was
capped. The container was left for 10 minutes so that
microbial load of the plant could be transferred into
the solution. This container had a dilution of 1/10
with 90 ml of normal saline and 10 g of sample plant.
After ensuring homogeneity of the initial dilution of
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Int. J. Biosci. 2015
1/10, serial dilutions were prepared according to
standard protocols (Microbiology of Food and Animal
Feeding Stuffs. No.8923).
Sterilization of culture medium and containers and
tools needed
After normal saline was prepared and weighed in
glass containers and test tubes, glass containers were
capped and test tubes were plugged with cotton, and
then tightly wrapped in aluminum foil. Also, when the
culture media were prepared, they were covered with
cotton and then wrapped tightly in aluminum foil.
After normal saline and the culture media were
prepared, they were sterilized with other equipment
in an autoclave at 121°C for 20 min.
Instructions for culturing and total count of
microorganisms
First, 1 ml of the dilutions (in this experiment, the
dilutions 1/100, 1/1000, 1/10000 were cultured) was
poured into the sterile empty plates by a sampler and
then 15-20 ml of nutrient agar culture medium
sterilized at temperature of 45-50°C was added to
sterile plate containing the desired dilution. After
solidification of the culture medium, the plates were
tightly sealed with parafilm and then the plates were
placed in an incubator upside down at 30°C for 72
hours. After 72 hours, the plates were removed from
the incubator, and the total colony counts, including
bacteria and molds on each plate were counted by
using the following formula (Microbiology of Food
and Animal Feeding Stuffs. No. 5272).
The number of colonies in one gram or one ml of the
sample (cfugˉ¹ or ml) = The total number of colonies
× 1/dilution × 1/volume used.
Experimental design and statistical analysis
A factorial experiment was designed with 3 replicates
in a completely random model. Data were analyzed by
SPSS software programs and the means were
compared with Duncan multiple range test at P≤0.05
level.
Results and discussion
Weight Loss
Weight loss percentage had an increasing trend with
increasing storage time (Fig. 2 and Fig. 3). The results
also show that among different concentrations of
citric acid, treatment of 0.5 g l1- acid had the lowest
weight loss percentage and among various
concentrations of ozone, the lowest weight loss
percentage was related to 1 ppm ozone concentration
(Fig. 1). Weight loss is very important as it is
associated with economic issues and generally weight
loss more than 5% can reduce the market value of
fruits and vegetables (Brown and Bourne, 2002). In
general, evaporation, transpiration and respiration of
products after harvest and imbalance of vapor
pressure in the product tissues and the air inside the
package lead to weight loss and more weight loss over
time (Baldwin et al., 1995). In addition to treatments,
propylene packaging and also the use of modified
atmosphere are the most important factors in
preventing weight loss. Less water vapor permeability
of the package causes less weight loss percentage (Esti
et al., 2002). Weight loss in the used propylene
packaging was small due to low permeability to water
vapor, no steam escapes and the relative increase of
humidity inside the package. The use of modified
atmosphere was also effective in preventing weight
loss (Serrano et al., 2005). Lettuce stored in
propylene packaging at 5C showed 28% weight loss
after 7 days of storage (Allende et al., 2004).
Fig. 1. The effect of interaction of ozone and citric
acid on weight loss of fresh-cut lettuce.
Hue (h0)
The amount of hue indicator decreased with
increasing storage time (Fig. 5 and Fig. 6). Also
treatment with citric acid and ozone led to better
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Int. J. Biosci. 2015
maintenance of hue in storage time and treatment
with percidine compared to treatment with ozone and
citric acid showed smaller amounts of hue (Fig. 4).
The amount of hue represents the actual color
parameter which is obtained by calculation a* and b*.
Color analysis shows that immersion of fresh-cut
iceberg lettuce in chlorine, organic acids and
ozonated water does not have adverse effects on
lettuce color, however, changes in the color
parameters were associated with time as increased
value of a*, decreased value of b*, reduced green
pigments, decreased value of L* and the darkening of
color (Akbas and Olmez, 2007). According to Bolin et
al.,1991 reduction of chlorophyll in cells will increase
the value of a*. Reduced value of b* can be due to the
reduction of ß- carotene during the storage time
(Bolin et al., 1991). Results show that the reduction of
hue indicator during storage time occurred because of
discoloration (browning) of cuts due to enzymatic
activities.
Fig. 2. The effect of interaction of citric acid and
percidine in storage time (day) on weight loss of
fresh-cut lettuce.
Fig. 3. The effect of interaction of ozone and
percidine in storage time (day) on weight loss of
fresh-cut lettuce.
Color purity (chroma)
Purity of color decreased over storage time (Fig. 8 and
Fig. 9), which was relatively slow. Ozone treatment
resulted in better preservation of chroma during
storage time, whereas lower concentrations of citric
acid showed better color purity during the storage
time (Fig. 7).
Fig. 4. The effect of interaction of ozone and citric
acid on hue indicator.
Fig. 5. The effect of interaction of citric acid and
percidine in storage time (day) on hue indicator.
Brightness of fresh-cut lettuce (L*)
The color brightness indicator decreased because of
increased storage time (days) (Fig. 11 and Fig. 12). In
treatments used, lower concentrations of citric acid
and ozone caused better preservation of the color
brilliance during storage time and with increasing
concentrations of citric acid and ozone the brightness
of fresh-cut lettuce colors was decreased (Fig. 10).
Decreased value of L* may indicate the formation of a
dark part in the product, which can be attributed to
oxidation of phenolic compounds and microbial
wastes in the product during storage time (Akbas and
Olmez, 2007).
L* indicator in the stored products shows brightness
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Int. J. Biosci. 2015
of the color, and given that L* is reduced during
storage time, it can be concluded that over time the
surface color of fresh-cut lettuce darkens. The results
of this study are consistent with the results of Jandric
et al., 2010. According to this researcher, the
browning of cut surface due to enzymatic reactions
decreases the color brightness during storage time.
Fig. 6. The effect of interaction of ozone and
percidine in storage time (day) on hue indicator.
Fig. 7. The effect of interaction of ozone and citric
acid on color purity (chroma).
Vitamin C
The amount of vitamin C was reduced by increasing
storage time (Fig. 14 and Fig. 15) and in comparison
of treatments, 0.5 g lˉ¹ citric acid concentration and 1
ppm ozone preserved vitamin C better during storage
time (Fig. 13). Treatment with percidine was also
effective on vitamin C preservation after the other
treatments. One reason is that in the early days of
storage time, the amount of oxygen in the packaging
was higher and oxidation of ascorbic-citric acid
(vitamin C) was more than dehydroascorbic acid
citric. According to Agar et al. (1997), increased
concentration of carbon dioxide by more than 20%
can further destroy vitamin C. In this study, actually,
with the increase of storage time and product
respiration, levels of carbon dioxide are increased and
destroy vitamin C during storage time.
Fig. 8. The effect of interaction of citric acid and
percidine in storage time (day) on color purity
(chroma).
Fig. 9. The effect of interaction of ozone and
percidine in storage time (day) on color purity
(chroma).
It is said that the cut made in fresh-cut products will
induce an increase in ethylene production and the
ethylene can stimulate other physiological processes
such as the degradation of vitamin C etc. (Kader,
1985).
Fig. 10. The effect of interaction of ozone and citric
acid on Brightness (L*).
According to Zhang et al., 2005, increased
concentration of ozone leads to better preservation of
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Int. J. Biosci. 2015
vitamin C in fresh-cut celery. The reduced vitamin C
during storage time, especially under modified
atmosphere conditions was consistent with the results
of Beltran et al., 2005 and Zhang et al., 2005.
Fig. 11. The effect of interaction of citric acid and
percidine in storage time (day) on Brightness (L*).
Fig. 12. The effect of interaction of ozone and
percidine in storage time (day) on Brightness (L*).
Fig. 13. The effect of interaction of ozone and citric
acid on vitamin C content.
Polyphenol oxidase activity
As can be seen in Fig.17 and Fig.18, the activity of the
polyphenol oxidase reduced over time and compared
with the applied treatments, citric acid concentrations
(0.5 and 1 g lˉ¹) to the concentration of zero had the
lowest enzyme activity. However, in terms of the
numerical comparison, concentration 0.5 g lˉ¹
showed the lowest activity. In ozone treatment, 1 ppm
ozone concentration showed the lowest activity of
polyphenol oxidase during storage time (Fig. 16).
Enzymatic browning that can cause discoloration in
fruits and vegetables is the result of the activity of a
group of enzymes especially polyphenol oxidase that
has been reported in many plants. The results of
Zhang et al.,2005 showed that polyphenol oxidase
activity is reduced by treatment with ozonated water,
and higher concentrations of ozonated water have
more inhibitory effects on the activity of polyphenol
oxidase. The results of the present study are
consistent with the results of these researchers.
Fig. 14. The effect of interaction of citric acid and
percidine in storage time (day) on vitamin C content.
The results of the present study is consistent with the
results obtained by Rico et al., 2006 who found that
ozonated water (1 mg l-1 at 18-20°C) on fresh-cut
lettuce leads to enzymatic and non-enzymatic
browning.
Fig. 15. The effect of interaction of ozone and
percidine in storage time (day) on vitamin C content.
Total count of microorganisms
As can be seen in Fig. 19, among different
concentrations of ozone, 1 ppm ozone concentration,
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Int. J. Biosci. 2015
and among different concentrations of acid, 1 g lˉ¹
acid concentration had the greatest decrease in the
total count of microorganisms. Also, among the
interaction of different concentrations of citric acid
and ozone, the greatest decrease was related to the
interaction of 1 ppm ozone concentration in 1 g lˉ¹
citric acid. Total count of microorganisms is increased
over time (Fig. 20 and Fig. 21).
Fig. 16. The effect of interaction of ozone and citric
acid on polyphenol oxidase (PPO) activity.
Fig. 17. The effect of interaction of citric acid and
percidine in storage time (day) on polyphenol oxidase
activity.
The highest total count of microorganisms was
related to bacteria that usually spoil vegetables. Most
of these bacteria are gram-negative bacteria especially
Erwinia and Pseudomonas that destroy the tissue of
these products (Barriga et al., 1991). The results of
this study are consistent with the results of Akbas and
Olmez, 2007.
Zambre et al., 2010 in their study found that
treatment with ozone on tomatoes can reduce the
microbial load and increase the shelf life of tomatoes.
Ketteringham et al., 2006 also showed the reduction
of microbial population treated with ozonated water
on cut green pepper.
Fig. 18. The effect of interaction of ozone and
percidine in storage time (day) on polyphenol oxidase
activity.
Fig. 19. The effect of interaction of ozone and citric
acid on total count of microorganisms.
Fig. 20. The effect of interaction of citric acid and
percidine in storage time (day) on total count of
microorganisms.
Fig. 21. The effect of interaction of ozone and
percidine in storage time (day) on total count of
microorganisms.
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Int. J. Biosci. 2015
Francis and O'Beirne (2002) found that the solution
of 1% citric acid for 5 minutes can reduce mesophilic
bacteria on lettuce about 1.5 log CFU gˉ¹.
Conclusion
The results showed that the total count of
microorganisms and weight loss percentage were
increased by increasing the storage time, while
parameters such as surface color, vitamin C and
polyphenol oxidase activity were decreased. Among
the different concentrations of citric acid, the highest
preservation of vitamin C was related to 0.5 g lˉ¹
citric acid concentration. In treatment with different
levels of ozonated water, the highest preservation of
vitamin C was related to the treatment with 1 ppm
ozonated water concentration. In the lettuce treated
with different concentrations of citric acid, the lowest
total count of microorganisms was related to 1 g lˉ¹
citric acid concentration and also treatment with 1
ppm ozonated water concentration. In all treatments
used, the increased concentrations and the
interaction of these treatments resulted in better
preservation of qualitative features and reduced
microbial quality during storage time.
Acknowledgement
The authors thanks Dr. Y. Mostofi for his support and
guidance at Faculty of Agricultural Science and
Engineering of Tehran Univeristy, Karaj, Iran.
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