Chemical Characterization of Tomato Juice
Fermented with Bifidobacteria
Jong-Ho Koh, Youngshik Kim, and Jun-Hyun Oh
C: Food Chemistry
Abstract: The objective of this research was to characterize the chemical properties of tomato juice fermented with
bifidobacterial species. Tomato juice was prepared from fresh tomatoes and heated at 100 ◦ C prior to fermentation.
Bifidobacterium breve, Bifidobacterium longum, and Bifidobacterium infantis were inoculated in tomato juice and kept at 35
to 37 ◦ C for up to 6 h. Fructooligosaccharide (FOS) was added to tomato juice prior to fermentation. The analyses
for brix, total titratable acidity (TTA), pH, color, and lycopene content were conducted to characterize tomato juices
fermented with bifidobacterial species. Heat treatment of tomato juice did not cause any significant changes in brix, pH,
and TTA. Only the redness of tomato juice was significantly increased, as the heating time increased to 30 min. The
tomato juices fermented with B. breve and B. longum exhibited significant decreases in pH (3.51 and 3.80, respectively)
and significant increases in TTA (13.50 and 12.50, respectively) (P < 0.05). B. infantis did not cause any significant change
in the chemical properties of tomato juice. The addition of FOS further improved the fermentation of tomato juice by
bifidobacterial species. The lycopene contents of tomato juice were significantly increased from 88 to 113 μg/g by heat
treatment at 100 ◦ C (P < 0.05), however did not exhibit any significant change after fermentation with bifidobacterial
species.
Keywords: bifidobacteria, fermentation, juice, tomato
Introduction
Tomato is one of major vegetables widely consumed around
the world. The heath benefits of tomatoes are attributed to the
abundant antioxidant components present in tomatoes (Giovannucci 1999; Willcox and others 2003; Ramandeep and Savage
2005), such as lycopene and provitamin A (Rodriguez-Amaya
and Tavares 1992; Mayeaux and others 2006), ascorbic acid (Hanson and others 2004), vitamin E (Lee and others 2000), and other
flavonoids (Dewanto and others 2002). Tomatoes are consumed
mainly as fresh or processed products. In 1999, approximately 17.6
pounds of fresh tomatoes and 72.8 pounds of tomato products
were consumed annually per capita in the United Sates (Willcox and others 2003). Tomatoes are processed for wide ranges of
products such as canned and sun-dried tomatoes, ketchups, pastes,
purees, salads, sauces, soups, and juice products, supplying significant sources of vitamins and minerals to the consumers (Tsen and
others 2008). Tomato products are playing an important role in
supplying lycopene to the consumers; more than 80% of dietary
lycopene consumed in the United States come from a wide variety
of tomato products (Willcox and others 2003).
Among tomato products, tomato juices are well recognized as
healthy beverages (Yoon and others 2004). In fact, tomato juices
as well as tomato paste and sauces are the main contributors of
dietary lycopene, accounting for 25% total daily lycopene intake
MS 20091137 Submitted 11/16/2009, Accepted 3/15/2010. Author Koh is with
Dept. of Bio-Food Technology, Korea Bio Polytechnic College, 315-1, Chaewoon-Ri,
Ganggyeong-Eup, Nonsan, Chungnam 320-905, South Korea. Authors Kim and
Oh are with Dept. of Plant Science and Technology, Sangmyung Univ., 300 AnseoDong, Dongnam-Gu, Cheonan, Chungnam 330-720, South Korea. Direct inquiries
to author Oh (E-mail: [email protected]).
C428
Journal of Food Science r Vol. 75, Nr. 5, 2010
in Canadian population (Rao and others 1998). There are extensive efforts to enhance the functionality of tomato juice products
with the trials of introducing value-added components or healthimproving compounds to tomato juice products (Anese and others
1999). One recent effort in improving the functionality of tomato
juice products is to utilize lactic acid bacteria (LAB) to ferment
tomato juice as probiotics (Yoon and others 2004; Tsen and others
2008; Cagno and others 2009). Although the probiotic products
are usually marketed in the forms of fermented dairy products,
fruit or vegetable juices may serve as good media for cultivating
probiotics (Yoon and others 2004; Wang and others 2009).
Probiotic microorganisms are defined as live microorganisms
that confer a health benefit on the host, when administered in
adequate amounts (Sindhu and Khetarpaul 2004; Corrêa and others 2008). Microorganisms from several selected bacterial genera
such as Lactobacillus are currently utilized as probiotics, however
the members of genus Bifidobacterium are also believed to possess
probiotic activities (Ouwehand and others 2002). Bifidobacteria
are gram-positive procaryotes that naturally inhabit the gastrointestinal tract of humans and other warm-blooded animals (Leahy
and others 2005). Bifidobacteria possess health-improving properties by maintaining improved intestinal microflora, reducing serum
cholesterol, inhibiting the growth of potential pathogens, stimulating the immune responses, and exhibiting anticarcinogenic activity ( Jeon and others 2002). Recently, as the market for functional
food grows, probiotic products are gaining a great attention by the
consumers.
Nonetheless, there is very limited information on the probiotic
potentials of bifidobacteria in vegetable juices such as tomato juice.
Regarding the probiotic potentials of bifidobacteria, coconut flan
(Corrêa and others 2008) and noni juice (Wang and others 2009)
were used for fermentation with the mixture of both LAB and
bifidobacteria. However, there is no research on the fermentation
R
C 2010 Institute of Food Technologists
doi: 10.1111/j.1750-3841.2010.01632.x
Further reproduction without permission is prohibited
of tomato juice with bifidobacteria alone. Therefore, the objective Analysis of lycopene
of this research was to characterize the chemical properties of
The extraction and analysis of lycopene from tomato was contomato juice product fermented with bifidobacteria species.
ducted following the general procedures described by Kozukue
and Friedman (2003). The homogenized tomato juice (2 g) was
mixed with 10 mL 6% pyrogallol in ethanol, and 8 mL 60% KOH
Materials and Methods
was added into the mixture under nitrogen gas. The mixture was
saponificated at 70 ◦ C and cooled down to room temperature. The
Materials
concentration of ethanol was adjusted to possess approximately
Fresh raw tomatoes (Lycopersicon esculentum) were purchased
30% (v/v) using 2% NaCl solution. Lycopene was extracted from
from local markets and farms. Bifidobacteria selected in this retomato juice using a mixed solvent (hexane:acetone:methanol =
search were Bifidobacterium breve, Bifidobacterium longum, and Bifi50 : 25 : 25, v/v/v) in the presence of BHT as an antioxidant. The
dobacterium infantis isolated from the commercial probiotic prodhexane layer containing lycopene was separated from the mixture,
ucts manufactured by Mediogen Co. (Chungbuk, South Korea).
and recovered several times. The optical density was measured at
The bifidobacterial culture was cultivated and maintained in ei470 and 502 nm using a spectrophotometer (UV/VIS Lambda35,
ther MRS broth or MRS agar (Difco Laboratories, Detroit, Mich.,
Perkin Elmer, Waltham, Mass., U.S.A.). Total lycopene content
U.S.A.). Fructooligosaccharide (FOS) was obtained from Samyang
was calculated from the optical density based on a standard curve
Genex Co. (Incheon, South Korea). Lycopene standard (L9879
obtained from lycopene standard (Sigma, St. Louis, Mo., U.S.A.).
obtained from tomatoes) were purchased from Sigma Co. (St
Figure 1 represents the spectral profiles of lycopene standard (A)
Louis, Mo., U.S.A.). The other chemical reagents and solvents
and the standard curves obtained at selected wavelengths (B and
used in this research were analytical grades and high-performance
C).
liquid chromatography (HPLC) grades.
Preparation and fermentation of tomato juice
The purchased fresh tomatoes were stored in the box at room
temperature for further maturation. The tomatoes were washed
with tap water to remove soil and other impurities, dried at room
temperature prior to use, and treated with steam for 3 to 4 min for
easy peeling. The tomato fruit was ground and filtered through
a pulper (AG-5500, Angel Juicer Co, Pusan, South Korea) with
a sieve (0.8 to 1.1 mm pore size) to separate tomato juice and
cake containing peel and seed. The tomato juice was homogenized using a D-500 homogenizer (Hauser, Berlin, Germany) for
10 min. The tomato juice was then heated at 100 ◦ C for selected time periods (5, 30, 60, 90, and 120 min) prior to fermentation. The selected concentrations of FOS (0.25% and 0.50%)
were added to tomato juice prior to fermentation. The starter
of bifidobacterial species was activated in the MRS media for
overnight to possess approximately 109 CFU/mL before inoculation to tomato juice. The cultured bifidobacteria (5%, v/v) were
finally inoculated into the tomato juice in 250 to 500 mL flasks.
The fermentation of tomato juice was performed anaerobically in
the dark for up to 6 h in a shaking incubator with a shaking rate
of 120 rpm at 35 to 37 ◦ C.
Characterization of fermented tomato juice
The solid contents of tomato juice were determined by the
standard AOAC method (AOAC 1997). The recovery rate was
expressed as the percentage calculated from the ratio of the weight
of tomato juice obtained after each processing step and the weight
of the fresh tomatoes. The total titratable acidity (TTA) of tomato
juice was determined by the standard AOAC method, and expressed as % lactic acid (AOAC 1997). The pH was directly measured in the tomato juice using a pH meter (Seven Easy S20,
Metter Toledo, Greifensee, Switzerland). The total sugar content
expressed as brix of tomato juice was determined using a refractometer (ABBE DR-A1, Atogo, Tokyo, Japan). The Hunter color
scale of L ∗ , a∗ , b∗ values of tomato juice was measured using a
CM-3500d Minolta Chromameter (Minolta Camera Co., Osaka,
Japan). The light source was illuminant C, and the white plate
(CR-A43; L ∗ = 96.86, a∗ = −0.02, and b∗ = 1.99) provided by
the manufacturer was used for calibration and background.
Statistical analysis
Each experiment was performed 3 times in duplicates. Data
were analyzed using the general linear models procedure in SAS
software program (Statistical Analysis System Inst. Inc., Cary, N.C.,
U.S.A.). Multiple mean comparisons among the samples were
carried out by Duncan’s multiple range tests at 5% significance
level (P < 0.05).
Results and Discussion
Solid content and recovery rate
of tomato juice
Approximately 840 g tomato juice was obtained after steaming
1000 g fresh tomato juice at 100 ◦ C for 5 min, exhibiting an
increase of solid contents of tomato juice from 4.5% to 4.7%
(w/v) (Table 1). The tomato juice was then further concentrated
to possess the solid content approximately 9.3% prior to use for
fermentation.
Chemical characterization of tomato
juice prior to fermentation
The brix, pH, TTA of tomato juice heated at 100 ◦ C for 30
to 120 min were not significantly different, when compared to
the tomato juice heated at 100 ◦ C for 5 min (control) (Table 2).
Regarding the color properties, the lightness (L ∗ value) and yellowness (b∗ value) of tomato juice were not significantly changed,
however, the redness (a∗ value) was significantly changed by the
heating time (P < 0.05). As the heating time increased until
60 min, the redness of tomato juice also significantly increased,
however, decreased after 60-min heating. The red color of tomatoes is known mainly due to the large lycopene contents in
tomatoes (Mayeaux and others 2006). The significant changes of
lycopene contents in tomatoes during storage and processing such
as drying, paste, or juice processing were reported by several researchers (Dewanto and others 2002; Hackett and others 2004;
Seybold and others 2004; Mayeaux and others 2006). Dewanto and
others (2002) reported that the lycopene contents in cooked tomatoes after heating for 2, 15, and 30 min at 88 ◦ C were increased to
3.11, 5.35, and 5.32 mg/g, respectively, as compared to 2.01 mg/g
in raw tomatoes. Therefore, the significant increase in red color of
Vol. 75, Nr. 5, 2010 r Journal of Food Science C429
C: Food Chemistry
Tomato juice fermented by bifidobacteria . . .
Tomato juice fermented by bifidobacteria . . .
C: Food Chemistry
Figure 1–The spectral profile of lycopene standard (A), and the standard curves at 470 nm (B) and 502 nm (C).
Table 1–Solid content and recovery rate of tomato juice during
selected process steps.
Processing step
Fresh tomatoes
Processed tomato juice after steaming at
100 ◦ C for 5 min
Processed tomato juice concentrate after
steaming at 100 ◦ C for 5 min
Solid
content
(%)
Recovery
rate
(%)
4.5
4.7
100.0
84.0
9.3
83.0
tomato juice until 60 min-heating in this study was presumably
due to the increase in lycopene content of tomato juice caused by
heating effects. The significant decrease in redness of tomato juice
after 30 min-heating might be resulted from the degradation of
lycopene during a severe heat treatment as reported by Mayeaux
and others (2006).
C430 Journal of Food Science r Vol. 75, Nr. 5, 2010
Chemical characterization of tomato juice fermented with
selected bifidobacterial species
The brix, pH, TTA, and color of tomato juice fermented with
selected bifidobacterial species are summarized in Table 3. The pH
of tomato juice was significantly decreased by the fermentation
with B. breve and B. longum (P < 0.05), indicating that these 2
bifidobacterial species could grow in tomato juice. The growth
of both B. breve and B. longum resulted in a significant increase in
TTA of the tomato juice (P < 0.05). In addition, the fermentation
of tomato juice with B. breve and B. longum significantly increased
the L ∗ , a∗ , and b∗ values of tomato juice (P < 0.05). However,
since there were no significant changes of pH and TTA in tomato
juice inoculated with B. infantis, it was assumed that B. infantis did
not grow in the tomato juice.
The probiotic properties of LAB in tomato juice were reported
by several investigators (Yoon and others 2004; Tsen and others
2008). The viable cell counts of LAB in tomato juice reached
1 × 109 to 9 × 109 CFU/mL after 72 h-fermentation, simultaneously reducing the pH of tomato juice to 4.1 or below, and
increasing the acidity to 0.65% or higher (Yoon and others 2004).
Tsen and others (2008) also reported that the fermentation of
tomato juice was significantly improved by using k-carrageenan
immobilized with Lactobacillus acidophilus, exhibiting better L. acidophilus growth during the k-carrageenan mobilized fermentation
than during the free cell fermentation. Both research groups suggested that the probiotic tomato juice fermented with LABs could
serve as a healthy beverage alternative to fermented dairy products,
specifically for vegetarians or consumers allergic to dairy products.
There is very limited information on the probiotic properties
of bifidobacteria alone in the literature. Most investigators focused
on the probiotic effects from the combination of both LAB and
bifidobacteria. Corrêa and others (2008) reported the probiotic
potentials of coconut flan supplemented with B. lactis in the presence of Lactobacillus paracasei. Recently, Wang and others (2009)
reported the combined probiotic effects of both B. longum and
Lactobacillus plantarum in fermented noni juice. The results in this
research demonstrated the potential probiotic effects of selected
bifidobacterial species in tomato juice, suggesting that bifidobacterial species such as B. breve and B. longum could be used for
tomato juice fermentation.
Chemical characterization of tomato juice fermented
with bifidobacteria with the addition of FOS
Yoon and others (2004) observed a rapid reduction in sugar contents of tomato juice as LAB fermentation progressed, indicating
that LAB consumed sugar to promote tomato juice fermentation.
In fact, a large number of bifidobacteria isolated from human and
animal origins was able to ferment and degrade complex carbohydrates, mainly D-galactosamine, D-glucosamine, amylose, and
amylopectin (Crociani and others 1994). FOS contains oligosaccharides that are smaller than complex carbohydrates, and is well
known as a substrate for microflora in the large intestine, increasing the overall gastrointestinal tract health (Yun 1996). The main
health-improving effects of FOS are believed to attribute to the
prebiotic effects of FOS (Yun 1996; Alles and others 1997; Xu and
others 2003). Therefore, it was hypothesized that FOS might not
only promote the fermentation process with bifidobacteria, but
also provide the additional prebiotic effects to fermented tomato
juice. The addition of 0.50% FOS into tomato juice resulted in a
significant reduction in pH and increase in TTA of tomato juice
after 6-h fermentation (P < 0.05), as compared to the addition of
0.25% FOS, indicating that FOS could promote the fermentation
with B. breve (Figure 2). The color properties of tomato juice with
the addition of FOS are also presented in Table 4. When 0.50%
FOS was added, the a∗ and b∗ values of fermented tomato juice
were significantly increased (P < 0.05). Xu and others (2003)
also reported that FOS enhanced the growth of lactic acid bacteria such as Bifidobacterium and Lactobacillus, however, inhibited
the growth of E. coli in the small intestine and colon in chicken.
FOS also exhibited 83% apparent fermentability in the colon, and
significantly increased the fecal weight, when fed to the patients
with large bowel disease (Alles and others 1997).
The addition of FOS in tomato juice might also improve the
taste of tomato juice fermented with bifidobacteria. Although an
extensive sensory evaluation was not conducted in this research,
the preliminary sensory test implied that the tastes and off-flavors
of the tomato juice were apparently improved by the fermentation
with bifidobacterial species and the addition of FOS into tomato
juice (data not presented). Therefore, FOS could be recommended
to use for the improvement of tomato juice fermentation with
bifidobacteria.
Lycopene content of fermented tomato juice
The lycopene contents of fresh tomato and tomato juices are
presented in Table 5, exhibiting comparable amounts reported by
Rao and others (1998). The lycopene content of tomato juice
after heating at 100 ◦ C for 5 min was significantly increased from
88 to 113 μg/g (P < 0.05). Although there are still controversies on the changes in lycopene contents caused by heating, it
was reported that the lycopene contents could be increased after heat processing, especially when processed at relatively low
temperature such as approximately 80 to 90 ◦ C (Thompson and
others 2000). Dewanto and others (2002) also reported that the
lycopene contents of raw tomatoes were significantly increased by
heating at 88 ◦ C for selected times. Our results also supported
the increase in lycopene contents in processed tomato juice, also
evident from the significant increases in redness in color (P < 0.05)
(Table 2).
However, the lycopene content of fermented tomato juice was
not significantly different from the lycopene contents of unfermented tomato juice, indicating that bifidobacterial fermentation
did not cause any adverse effects on lycopene content in tomato
juice. Therefore, it was thought that the fermentation of tomato
juice with bifidobacteria would not affect the health benefits of
lycopene in tomato juice.
Table 2–Effects of heating time at 100 ◦ C on brix, pH, TTA, and color of tomato juice.
Color
Heating time (min)
5
30
60
90
120
Brix (◦ )
pH
4.4 ± 0.1
4.6 ± 0.1a
4.6 ± 0.2a
4.6 ± 0.1a
4.6 ± 0.1a
a
4.35 ± 0.03
4.35 ± 0.04a
4.35 ± 0.02a
4.35 ± 0.03a
4.35 ± 0.04a
a
TTA (%)
L∗
6.5 ± 0.2
6.5 ± 0.1a
6.5 ± 0.3a
6.5 ± 0.2a
6.5 ± 0.1a
32.53 ± 0.18
32.85 ± 0.21a
33.44 ± 0.35a
32.74 ± 0.29a
32.54 ± 0.24a
a
a∗
a
b∗
11.19 ± 0.15
12.72 ± 0.24b
13.84 ± 0.29a
12.93 ± 0.21b
12.87 ± 0.17b
b
24.25 ± 0.27a
26.06 ± 0.13a
26.45 ± 0.21a
27.33 ± 0.27a
27.73 ± 0.24a
Different letters within the column indicate significant differences between the means (P < 0.05).
Table 3–The brix, pH, TTA, and color of tomato juice fermented by selected bifidobacterial species.
Color
Bacterial species
No fermentation
B. breve
B. longum
B. infantis
◦
∗
Brix ( )
pH
TTA (%)
L
4.40 ± 0.15a
4.10 ± 0.21b
4.00 ± 0.26b
4.20 ± 0.11a
4.32 ± 0.11a
3.51 ± 0.12b
3.80 ± 0.15b
4.30 ± 0.21a
6.00 ± 0.21b
13.50 ± 0.33a
12.50 ± 0.28a
5.90 ± 0.17b
29.48 ± 0.20b
38.02 ± 0.31a
36.72 ± 0.19a
31.36 ± 0.25b
a∗
b∗
10.58 ± 0.31b
15.45 ± 0.27a
14.84 ± 0.19a
11.61 ± 0.21b
21.63 ± 0.31b
26.29 ± 0.18a
25.23 ± 0.11a
22.32 ± 0.29b
Different letters within the column indicate significant differences between the means (P < 0.05).
Vol. 75, Nr. 5, 2010 r Journal of Food Science C431
C: Food Chemistry
Tomato juice fermented by bifidobacteria . . .
Tomato juice fermented by bifidobacteria . . .
B
A
12.0
4.35
0.25%
10.0
Total Titratable Acidity (%)
0.25%
4.30
0.50%
pH
C: Food Chemistry
4.25
4.20
4.15
0.50%
8.0
6.0
4.0
2.0
4.10
0.0
4.05
0
2
4
0
6
2
4
6
Incubaon me (h)
Incubaon me (h)
Figure 2–The changes of pH (A) and TTA (B) in tomato juice during fermentation with B. breve in the presence of selected concentrations of FOS.
Table 4– The color properties of tomato juice fermented with
bifidobacterial species in the presence of FOS.
Bifidobacteria
B. breve
B. longum
FOS
content
(%)
L∗
0.25
0.50
0.25
0.50
24.33 ± 0.33
24.95 ± 0.24b
24.35 ± 0.21b
26.80 ± 0.15a
Color
a∗
b
b∗
15.36 ± 0.25
19.36 ± 0.29a
15.88 ± 0.31b
21.98 ± 0.19a
b
14.21 ± 0.23b
16.37 ± 0.31a
14.69 ± 0.41b
20.06 ± 0.21a
Different letters within the column indicate significant differences between the means
(P < 0.05).
Table 5– The lycopene content in tomato juice fermented with
B. breve.
Processing step
Fresh whole tomatoes
Tomato juice after steaming at 100 ◦ C for 5 min
Tomato juice fermented by B. breve
Lycopene
content
(μg/g)
88.0 ± 4.86b
113.0 ± 4.21a
112.1 ± 4.17a
Different letters within the column indicate significant differences between the means
(P < 0.05).
Conclusions
This research demonstrates that tomato juices can be fermented
with selected bifidobacterial species alone such as B. breve and
B. longum as probiotic microorganisms. The addition of sugars
such as FOS into tomato juice promoted the fermentation process, and presumably improved the tastes and off-flavors of fermented tomato juice. During fermentation, the lycopene contents
in tomato juice were not affected by the growth of bifidobacterial species. Therefore, this research suggests that the tomato juice
fermented with bifidobacteria can be developed as a potential probiotic product, and may benefit the consumers searching for an
alternative beverage to replace fermented dairy products.
Acknowledgments
This research was carried out with the support of RegionSpecific Agriculture Development Project of Rural Development
Administration (RDA), Republic of Korea.
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