Date received: 12/7/2021
Date accepted: 13/10/2021
Introduction
The green asparagus (Asparagus officinalis L.) is a vegetable widely consumed by its turgid texture and high nutritional value.
Freshly harvested spears are very susceptible to senescence, mainly related to their
high respiration rate. They undergo several physiological changes during storage,
such as transpiration, chlorophyll degradation, and total phenols changes (1). Usually, the spears present a high quantity of phenolic compounds, being the flavonoids
with the greater antioxidant activity potential (2). Microorganisms easily contaminate the vegetables at various points during the production,
handling, and packing process. Therefore, eliminating microorganisms during postharvest
processing is vital to assure microbial safety (3).
Various postharvest treatments have been studied to prolong the quality of fruits
and vegetables, including chemical disinfectants such as sodium hypochlorite (chlorine)
and ozone, which are highly effective in reducing microorganisms’ load (4). Ozone in the water or gas phase is an interesting alternative because it is an
effective disinfectant recognized for its high oxidizing potential on the microbial
cell membrane. The disinfecting effect of ozone is approximately 150% more effective
than the commercial disinfectant known as chlorine (5).
Ozone has been generally recognized as a safe disinfectant approved by the United
States Food and Drug Administration (FDA) (6). Ozone application has gained increasing commercial interest as a postharvest technology
to control spoilage in fruits and vegetables, especially because it leaves no residue
in the treated product (7).
The quality of fruits and vegetables is evaluated mainly from the sensory, nutritional,
and microbiological aspects. Consumers often quickly assess the sensory quality in
retail stores and consider attributes such as appearance, color, and texture as a
priority. Impairment of these properties would influence the product’s shelf life
and purchase intent, particularly when these attributes fall below the acceptable
level (8).
Response surface methodology (RSM) has been commonly used for optimizing, designing,
developing, and improving processes where a response or responses are affected by
several variables (9). It is a technique of statistical and mathematical methods to assess numerous factors
and their interactions established on the fit of a polynomial model. It must depict
the behavior of the dependent variable to make statistical predictions to optimize
the response (10). The correct experimental design must be selected to designate which treatments
should be done in the experimental region being studied. For this purpose, experimental
designs for quadratic response surfaces, such as three-level factorial, central composite
(CCD), and Box-Behnken (BBD), should be applied (11). We have reviewed some RSM studies published in fresh food industry processes, such
as green pepper (12), french beans (13), chinese cabbage (10), onion (14), broccoli (15), spinach (16).
The objective of the current study is to determine through the response surface methodology
the concentration of gaseous ozone and storage time, which allows obtaining the minimally
processed green asparagus with the highest content of phenols and overall appearance,
and lowest microbial count.
Materials and methods
Material
The research material was green asparagus spears variety UC157 F1, purchased from
Chao province (coordinates 08°32′25″ S and 78°40′39″ O), department of La Libertad,
Perú. The green asparagus (maximum 07 hours after being harvested) showed no physical
damage (bumps, bruises, etc.) and were free of pests and any strange odor. According
to NTP 011.109:2008 (17), they were classified with AB tip quality and 14-20 mm caliber.
Minimum process treatment
Spears were washed by aspersion with potable water to remove surface impurities and
immersed in a chlorine dioxide solution at 100 ppm for 5 min at room temperature.
Afterward, they were cut to a length of 17 cm, considering the measure from the tip
to the base. The excess humidity was eliminated. The spears were conditioned in trays
of expanded polystyrene with a weight of 150 g ± 3 g, and then transferred to the
treatment chamber, where the gaseous ozone generated was injected by an ozonification
machine (Ozonomatic brand, model OZ-500) with a flow rate of 500 mg/h and through
a 7 mm diameter hose, subjecting them to different concentrations between 0 - 10 ppm,
during 20 min, controlled by using a digital gaseous ozone meter (Crowcon brand, model
Gasman O3, range 0-100 ppm, sensitivity ± 0.1 ppm). Finally, the trays with spears
were removed from the chamber and covered with polyvinyl chloride (PVC) film and stored
in a refrigeration chamber with temperature control for 28 days at 1 °C ± 0.1°C and
85-90% ± 2% relative humidity (usual storage conditions in the commercialization of
asparagus), control performed with a thermohydrometer (Fluke brand, Model 971).
Analytical techniques
Total phenol content
2 g of sample was homogenized under darkness in 80% aqueous ethanol for 2 h, at room
temperature, and centrifuged at 4200 rpm for 15 min; the supernatant was evaporated
in an oven at 40 °C. The residues were dissolved in 5 mL of distilled water, extracting
100 μL that was diluted with 3 mL of distilled water, and then 0.5 mL of Folin-Ciocalteau
reagent was added. After 3 min, 2 mL of 20% (w/v) sodium carbonate solution was added,
and the resulting material was vigorously mixed. The color absorbance developed after
1 h was measured in a visible light spectrophotometer (Thermo Electron Corporation,
model Spectronic Genesys 6) at 765 nm, using gallic acid as standard. The results
were expressed as mg gallic acid/g sample (1, 18).
Overall appearance
It was determined following the method of Albanese et al. (2007) with modifications
by the author. Thirty untrained panelists, aged between 25 - 45 years and habitual
consumers of green asparagus were selected for the test. The criteria to be evaluated
were: spear shape based on entire terminal buds and completely closed bracts; color
according to the degradation of chlorophyll (less intense); spear firmness according
to the lignification that was observed when applying pressure to the touch; dehydration
of the shoot that referred to a wrinkled product; and rot damage that was evidenced
by the tissue softness. All participants involved in the evaluation were thoroughly
informed about the characteristics of the product to be evaluated. The factors mentioned
were responsible for the loss of freshness in asparagus. A structured hedonic scale
of 9 points was used, where 1: I dislike it very much, 0: I neither like it nor dislike
it, and 9: I like it very much. The evaluation was carried out in a single session,
in an environment with natural lighting, and the average of the values was reported
(19)
Total count of viable mesophilic aerobic bacteria, psychrophiles, and molds
10 g of the sample were aseptically separated and homogenized in 90 mL of 0.1% peptone
water. A series of dilutions were prepared in 9 mL of peptone water with 1 mL of aliquot.
In duplicate, the count of viable mesophilic aerobic and psychrophilic bacteria was
determined using the plate count agar (PCA) and standard methods agar. The plates
were incubated at 35 °C for 48 h for viable mesophilic aerobic bacteria and 7 days
at 7 °C for psychrophilic bacteria. Count molds were evaluated on pink flare red agar
(RBRM) and incubated at 28 °C for 5 days. Results were reported in CFU/g (1, 19).
Statistical analysis
A central composite rotational design (CCRD) of the response surface methodology (RSM)
technique was adopted to optimize the quality characteristics in fresh green asparagus.
The design was chosen for this study because it was suitable for modeling quadratic
response surfaces methodology. Two variables (ozone concentration and storage time)
known to influence fresh vegetable production were investigated. The ranges of these
variables are shown in Table 1. The model terms were calculated for multiple regression analysis, while analysis
of variance (ANOVA) was used to assess the model terms' significance. The experimental
design and the accompanying statistical analysis were performed using Minitab 19 program.
With the same data and choosing the factors considered to be the most important in
the quality of the asparagus, as a complement to the design, the desirability function
(FD) was built, which determined the ozone concentration and storage time values that
optimize the overall appearance, viable mesophilic aerobic bacteria count, and phenol
content.
Table 1
Central composite rotational design of the response surface methodology
|
Treatment
|
Ozone concentration (codified)
|
Storage time (codified)
|
Ozone concentration (ppm)
|
Storage time (days)
|
|
1
|
-1
|
-1
|
0
|
0
|
|
2
|
1
|
-1
|
10
|
0
|
|
3
|
-1
|
1
|
0
|
30
|
|
4
|
1
|
1
|
10
|
30
|
|
5
|
-1.4142
|
0
|
0
|
15
|
|
6
|
1.4142
|
0
|
10
|
15
|
|
7
|
0
|
-1.4142
|
5
|
0
|
|
8
|
0
|
1.4142
|
5
|
30
|
|
9
|
0
|
0
|
5
|
15
|
|
10
|
0
|
0
|
5
|
15
|
|
11
|
0
|
0
|
5
|
15
|
Results
Table 2 presents the results of total phenol content, overall appearance, and microbiological
counts based on the RSM's central rotating composite design treatments. Its behavior
was modeled as a function of ozone concentration and storage time.
Table 2
Experimental results applying the central composite rotational design.
|
Ozone concentration (ppm)
|
Storage time (days)
|
Total phenols content (mg/g sample)
|
Mold count (CFU/g)
|
Psychrophilic bacteria count (CFU/g)
|
Mesophilic bacteria count (CFU/g)
|
Overall appearance (points)
|
|
0
|
0
|
18.73
|
0
|
0
|
6,696
|
9.0
|
|
0
|
15
|
16.22
|
714
|
68,593
|
31,289
|
6.8
|
|
0
|
30
|
13.90
|
1,569
|
195,667
|
62,261
|
5.1
|
|
5
|
0
|
19.78
|
0
|
0
|
2,819
|
9.0
|
|
5
|
15
|
18.39
|
337
|
28,839
|
10,573
|
7.9
|
|
5
|
30
|
15.79
|
826
|
128,350
|
27,731
|
7.2
|
|
10
|
0
|
19.90
|
0
|
0
|
2,613
|
9.0
|
|
10
|
15
|
18.42
|
78
|
19,267
|
3,814
|
7.9
|
|
10
|
30
|
16.35
|
260
|
87,495
|
7,538
|
7.4
|
|
5
|
15
|
18.02
|
404
|
29,813
|
11,205
|
8.1
|
|
5
|
15
|
18.27
|
385
|
31,964
|
10,176
|
8.1
|
Table 3 presents the models and lack of fit for phenols, overall acceptability, mold, psychrophilic
bacteria, and viable mesophilic aerobes counts.
Table 3
Models and lack of fit for phenols, overall acceptability, mold, psychrophilic bacteria,
and viable mesophilic aerobes counts.
|
Variable
|
Equation
|
R2 (%)
|
P value
|
Lack of fit
|
|
Phenols
|
y=18.578 + 0.4207 ozone - 0.1239 time - 0.02907 ozone*ozone - 0.001164 time*time +
0.00427 ozone*time
|
98.76
|
0.000
|
0.469
|
|
Overall appearance
|
y=8.974 + 0.032 ozone - 0.2228*time - 0.00316* ozone*ozone + 0.00187 time*time + 0.00667
ozone*time
|
95.05
|
0.001
|
0.996
|
|
Molds
|
y=7.9 - 12.61 ozone + 44.64 time + 1.323 ozone*ozone + 0.2226 time*time - 4.363 ozone*time
|
99.09
|
0.000
|
0.577
|
|
Psycrophiles
|
y=2534 - 3835 ozone + 2345 time + 399 ozone*ozone + 134.3 time*time - 360.6 ozone*time
|
99.47
|
0.000
|
0.074
|
|
Mesophiles
|
y=7642 - 2599 ozone + 1345 time + 225.5 ozone*ozone + 14.94 time*time - 168.8 ozone*time
|
99.51
|
0.000
|
0.054
|
Figure 1 presents contour and response surface methodology of (a) total phenol content and
(b) overall appearance for ozone concentration and storage time.
Figure 1
Contour and response surface methodology of (a) total phenol content and (b) overall
appearance for ozone concentration and storage time
Figure 1a shows that the initial application with gaseous ozone between concentrations of
6 to 10 ppm generated an increase in total phenols content. Then, a decrease of these
compounds was observed until the end of storage, consistently reporting higher values
in the ozonated samples (16-17 mg/g sample) compared to the control sample (not ozonated).
The analysis of variance showed that the quadratic model presented a significant effect
(p<0.05), high coefficient of determination (R2 = 98.76%), and lack of fit p > 0.05, which explains a good fixation of the model
data (Table 3).
Figure 1b shows that gaseous ozone concentrations of 6 to 10 ppm and storage time of 20 to
25 days produced the highest overall perception with acceptable levels of 6 to 8 points
in the asparagus spears than samples treated at lower concentrations, including not
ozonated. The analysis of variance showed that the quadratic model presented a significant
effect (p<0.05), high coefficient of determination (R2 = 95.05%), and lack of fit p > 0.05, which explains a good fixation of the model
data (Table 3).
Figure 2 presents contour and response surface methodology blanket for microbiological counts
of (a) molds, (b) psychrophilic bacteria, and (c) viable aerobic mesophilic bacteria
for ozone concentration and storage time.
Figure 2
Contour and response surface methodology blanket for microbiological counts of (a)
molds, (b) psychrophilic bacteria, and (c) viable aerobic mesophilic bacteria for
ozone concentration and storage time
Figures 2a, b, c show that gaseous ozone concentrations of 6 to 10 ppm and final storage (20
to 25 days) generated the lowest microbial counts (5 x 102, 4 x 103, and 1 x 104 CFU/g for molds, psychrophilic, and viable mesophilic aerobic bacteria, respectively)
compared, with the samples treated at a lower concentration, including the control.
The analysis of variance showed that the quadratic model presented a significant effect
(p<0.05) for microbial counts; high coefficient of determination (R2 = 99.09, 99.47 and 99.51%, respectively) and in all cases, a lack of fit p > 0.05,
which explains a good fixation of the model data (Table 3).
Figure 3 presents the optimization of quality characteristics in fresh green asparagus.
Figure 3
Optimization of quality characteristics in fresh green asparagus.
The contours of the RSM were obtained using the superposition technique; as a result,
the region of interest that determines the optimal area corresponded to a concentration
of 10 ppm of gaseous ozone up to 25.9 days of storage, indicating characteristics
of 16.99 mg/g sample of phenols; 7.61 points in general appearance, and 5.3 x103 CFU/g sample of viable aerobic mesophilic bacteria.
Discussion
Ozone concentration effect and storage time on total phenol content
The results obtained can be explained due to the activation reaction that ozone treatments
produce in the defense mechanisms before the onset of oxidative stress and the changes
in the activity of enzymes that participate in the synthesis of polyphenolic compounds
such as phenylalanine aminolyase (PAL) (20, 21). The increase in phenolic compounds can be attributed to the modification of the
cell wall during exposure to ozone; this modification can increase the extraction
and release capacity of conjugated phenolic compounds (22). Tabakoglu and Karaca (2018) indicated that storage vegetables at low temperatures
with gaseous ozone application can increase the phenols’ content (23). Yeoh et al. (2014) suggested that the increase in total phenols, due to the initial
application of gaseous ozone, may produce the inhibition of enzymes such as polyphenol
oxidase (PPO) and peroxidase (POD), which often cause oxidation of these compounds
in freshly cut fruits and vegetables (24). Gutierrez et al. (2018) associated that fresh-cut leafy vegetables in contact with
gaseous ozone played an important role in protecting plant tissues against biotic
and abiotic oxidative stress because it promotes the synthesis of phenolic compounds
(25).
The positive effect of gaseous ozone treatment on the content of phenolic compounds
was also observed in bell pepper (26), green and red bell pepper (27), and rocket (28).
Ozone concentration effect and storage time on overall appearance
The product’s visual quality is important because any color alteration can be recognized
as a symptom of senescence. Likewise, there are studies with the application of ozone
in the disinfection of fruits and vegetables that do not harm the original quality
of the vegetables despite observing slight changes of color. The application of gaseous
ozone could prevent the deterioration of the product and increase its shelf life (29). The overall appearance represents all the visible food attributes and can be a
fundamental element in purchasing the vegetable (30).
Similar results with exposure to gaseous ozone were found in strawberries (31), lettuce (32), bell pepper strips (33), pomegranate (30), and coriander (34).
Ozone concentration effect and storage time on microbial inactivation
The ozone inactivates microorganisms by the progressive oxidation of vital cellular
components because it breaks the cell wall, achieving its disintegration. Gram-negative
bacteria (E. coli, viable aerobic mesophilic bacteria, psychrophilic bacteria, total coliforms, etc.)
are more susceptible to ozone because they possess thin layer peptidoglycan. An external
membrane made of lipoproteins and polysaccharides, which are easily oxidized (35). Yeoh et al. (2014) indicated that microorganisms could be affected by temperature,
concentration, duration of exposure to ozone, and biological factors, such as the
type and composition of vegetables and the type and microbial load (24). Sheng et al. (2018) mentioned that the effect of ozone could be attributed to the
fact that it interferes with the diffusion of nutrients on the surface of the cut
vegetable, inhibiting the growth of bacteria, molds, and yeasts (36). Gutiérrez et al. (2018) indicated that ozone treatments effectively extended the
shelf life of different vegetables, reporting that ozone treatments between 0.15-5.0
ppm succeeded in reducing the growth of bacteria and molds (25). Variations in the results could suggest that molds, yeasts, and spore-forming bacteria,
due to their sensitivity, require increasing ozone concentrations and longer exposure
times for inactivation, which is one of the main parameters governing the effectiveness
of ozone (37).
Similar behaviors were found in products like lettuce, parsley, and spinach (35), tomato strips (38), fresh-cut lettuce leaves (39), green asparagus (40), lettuce, and green bell pepper (37).
Optimization
The technique of RSM contours superposition was used to optimize the independent variables,
such as phenol content, general appearance, and count of viable mesophilic aerobic
bacteria. They are considered important for maintaining the quality of green asparagus
spears during the logistics and marketing chain and their antioxidant activity (Figure 3).
Conclusions
This research showed that the application of gaseous ozone at 10 ppm was not only
a great disinfectant agent, but it was also a functional postharvest technology that
maintains the quality characteristics, such as overall appearance and total phenols
content of the minimally processed green asparagus spears, allowing a shelf life of
26 days at 1 ° C.
Acknowledgment
The authors thank the Antenor Orrego Private University for the support provided by
its Food Science and Technology Laboratories to carry out the experimental part of
the research.
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