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LWT - Food Science and Technology 65 (2016) 543e548

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The impact of onion juice on milk fermentation by Lactobacillus

Sha Li a, b, Chengjie Ma a, b, *, Guangyu Gong a, Zhenmin Liu a, Chao Chang c, Zhiping Xu a, b
State Key Laboratory of Dairy Biotechnology, Technology Center of Bright Dairy & Food Co., Ltd., 1518 Jiangchang Road (W), Shanghai 200436, China
Wuhan Bright Dairy Co., Ltd., 1 Zhangbai Road, Wuhan 430040, China
College of Food Science and Engineering, Wuhan Polytechnic University, 68 Xuefu Road (S), Changqing Garden, Wuhan, 430023, China

a r t i c l e i n f o a b s t r a c t

Article history: The aim of this study was to investigate the influence of onion juice on the fermentation of milk by
Received 4 March 2015 Lactobacillus acidophilus. The onion juice significantly stimulated the growth and acidification of the
Received in revised form bacterial strain L. acidophilus NCFM. The viable cell counts in onion-supplemented fermented milk were
12 August 2015
higher than that of the control sample and were maintained during cold storage. We considered the
Accepted 14 August 2015
Available online 17 August 2015
whole constituents of onion juice such as polyphenols, sulfur compounds, fructans, and minerals
together to play the stimulatory roles and result in this beneficial effect for L. acidophilus viability during
fermentation and storage. After the milk was fermented by L. acidophilus NCFM, the antioxidant capacity
Lactobacillus acidophilus
decreased greatly in the control and onion-supplemented fermented milk. The results suggested that it
Onion juice was very necessary and crucial to scavenge radical for L. acidophilus growth. The onion juice was slightly
Viable cell count beneficial to enhancing the antioxidant capacity of fermented milk. The higher cell numbers, the less
Antioxidant capacity fermentation time, the better antioxidant capacity, and more abundant flavor components were achieved
Flavor compound by onion-supplemented fermentation by L. acidophilus, demonstrating the potential for industrial
© 2015 Published by Elsevier Ltd.

1. Introduction Talwalkar & Kailasapathy, 2003). Ng, Yeung, and Tong (2011)
found that the toxic oxygenic metabolites produced by yogurt
Lactobacillus acidophilus NCFM is a common commercial bac- starter cultures were critical factors in impairing the survival of
terial strain used in the manufacturing of dairy products L. acidophilus NCFM. Because of this, there are an increasing num-
(Kailasapathy, Harmstorf, & Philips, 2007). Research has shown that ber of researchers attempting to produce fermented milk only with
it is capable of protecting the host by improving lactose digestion, L. acidophilus and to maintain or promote the viability of
preventing or lessening the impact of diarrhea, improving blood L. acidophilus throughout the product shelf life by making the
lipid chemistry, stimulating an immune response, and potentially environment more favorable to L. acidophilus. Hervert-Hern andez,
killing cancer cells as they develop (Sanders & Klaenhammer, Pintado, Rotger, and Gon ~ i (2009) found that grape pomace
2001). To realize the health benefits of L. acidophilus, an adequate phenolic extract induced a significant biomass increase of
number of viable cells must be delivered at the time of consump- L. acidophilus growth. More recently, Oliveira, Perego, Oliveira, and
tion (Pescuma, He bert, Mozzi, & de Valdez, 2010). However, the Converti (2011) found that inulin could improve the growth of
viable cells of probiotics significantly decrease during cold storage L. acidophilus in fermented skim milk.
because of acid accumulation, interaction with starter cultures, Some researchers have found that a major part of phytochemi-
levels of dissolved oxygen and hydrogen peroxide, and storage cals are not absorbed in the small intestine, but that they can
conditions (Donkor, Henriksson, Vasiljevic, & Shah, 2006; interact with colonic microbiota, stimulating the growth of lactic
acid bacteria (LAB) and having antimicrobial activity against many
pathogens (Scalbert & Williamson, 2000). Najgebauer-Lejko, Sady,
Grega, and Walczycka (2011) reported that the addition of tea
* Corresponding author. State Key Laboratory of Dairy Biotechnology, Technology
Center of Bright Dairy & Food Co., Ltd., 1518 Jiangchang Road (W), Shanghai 200436, extract containing polyphenols had a positive effect on yogurt
China. starter microflora. Additionally, Michael, Phebus, and Schmidt
E-mail address: (C. Ma).
0023-6438/© 2015 Published by Elsevier Ltd.
544 S. Li et al. / LWT - Food Science and Technology 65 (2016) 543e548

(2010) found that plant extracts possessing antioxidant capacity pH end point) was reached. After samples were stirred at 500 rpm
extended the longevity of Lactobacillus delbrueckii subsp. bulgaricus for 5 min, they were stored at 4  C.
during storage.
Onions (Allium cepa L.) are one of most widely consumed veg- 2.3. Determination of titratable acidity
etables in Europe (mainly in UK, Holland and Spain) and Asia
countries (mainly in China, India and Japan). Onion adequately The titratable acidity (TA) of fermented milk samples was
processed could be useful in the food industry to be added to foods determined according to Yang et al. (2012) on day 1 and after 14
due to the increasing demand by consumers for substituting syn- days of cold storage.
thetic compounds by natural substances as functional food in-
gredients. Compounds of inherently natural origin would be widely 2.4. Enumeration of L. acidophilus
accepted by consumers in the market (Jang, Sanada, Ushio, Tanaka,
& Ohshima, 2002). There is an increasing interest in onions due to A standard plate count was used to enumerate viable
their high level of phytochemicals. Among these, flavonoids, fruc- L. acidophilus cells according to Ng et al. (2011) with slight modi-
tans, and organosulfur compounds are considered important fications. Fermented milk samples were serially diluted using
contributing factors to antioxidant activity (Siddiq, Roidoung, Sogi, sterile saline to achieve 20 to 200 colonies on MRS (de Man, Rogosa
& Dolan, 2013). For these reasons, the onion has been widely and Sharpe) agar plates. L. acidophilus was cultured under anaer-
researched for its antioxidant functions and antimicrobial proper- obic conditions (Bugbox Anaerobic System, Ruskinn, Bridgend,
ties against pathogenic microorganisms (Albishi, John, Al-Khalifa, & United Kingdom) with a mixture of 95% N2 and 5% CO2 at 37  C for
Shahidi, 2013; Lee, Jung, & Kim, 2012). The onion may exert a 72 h.
double positive effect on fermented milk production, on the one
hand stimulating LAB and inhibiting pathogenic bacteria, and on 2.5. Determination of antioxidant capacity (AOC)
the other hand improving nutritional values and health effects.
However, the stimulatory role of onions on LAB, and especially For the determination of the AOC of non-fermented milk or
L. acidophilus, has rarely been investigated. In addition, organo- fermented milk, the diphenyl picrylhydrazyl (DPPH) method ac-
sulfur compounds have a distinct flavor and are identified as the cording to Najgebauer-Lejko et al. (2011) was used in this study. It is
characteristic flavor compounds in onions (Gyawali et al., 2006). a simple, sensitive, and widely used method to measure the radical
Adding onion juice to milk, therefore, may provide the benefit of scavenging activity of all the antioxidant substances (including
adding flavor to fermented milk. protein, glutathione, lipoic, etc.) present in the examined sample.
In this study, onion juice was added to milk to investigate the The amount of sample required to decrease the initial DPPH con-
effects of onion juice on the growth of L. acidophilus NCFM. The centration by 50% (EC50) was calculated. Antioxidant capacity was
antioxidant capacity and flavor compounds of fermented milk were given as AOC, the reciprocal of EC50. The AOC was calculated rela-
also evaluated. tive to the AOC of Trolox, an analog of vitamin E, and expressed as
mmol/TEg of sample.
2. Materials and methods
2.6. Determination of volatile compounds
2.1. Preparation of onion juice
The fermented milk containing 60 g/kg onion juice and the
The fresh onion (commercially available) was cleaned and cut control fermented milk were chosen for the detection of volatile
into pieces, and then mixed with same amount of sterile distilled compounds.
water by weight. The initial onion juice was extracted from the Headspace solid-phase micro-extraction (SPME) was used to
mixture using a Philips juicer (HR 1861, Philips China Investment extract volatile compounds from the fermented milk samples ac-
Co., Ltd., Zhuhai, China), and then centrifuged (10,000  g, 10 min). cording to Li et al. (2014). The fiber used for manual extraction was
The supernatant was filtered to obtain the final onion juice used in DVB/CAR/PDMS (Supelco, Bellefonte, PA, USA).
the experiment. This juice was refrigerated at 4  C until use. Analysis of the volatile compounds was performed using an
Agilent 7890 (II) gas chromatograph (Agilent Technologies, Santa
2.2. Preparation of fermented milk Clara, CA, USA) coupled to an Agilent 5975 series mass selective
detector. The SPME fiber was inserted into the injection port that
The fermented milk was prepared according to Lucey (2004) was held at 250  C, and the compounds were thermally desorbed
with slight modifications. Onion juice (0, 20, 60, and 100 g/kg) for 4 min under split (1:10) conditions (Welty, Marshall, Grün, &
was added into fresh cow's milk, and distilled water, respectively at Ellersieck, 2001). A DB-Wax column 30 m  0.25 mm  0.25 mm
100, 80, 40, and 0 g/kg, was added into the onion juice to stan- (Agilent Technologies, Santa Clara, CA, USA) was used to separate
dardize the levels of protein and fat. The mixtures were stirred with the volatile compounds. The temperature of the column was held at
a stirrer RW20 (IKA, Staufen, Germany) at 600 rpm for 5 min at 45  C for 5 min, ramped up by 10  C/min to 80  C, and then further
65  C, and then homogenized under high pressure (18 MPa) at 65  C heated to 240  C at the rate of 5  C/min. The carrier gas was helium
and heat-treated at 95  C for 90 min immediately in order to kill all (1 mL/min). The mass spectrometer was run in the electron impact
the microorganisms, bacterial spores and fungal spores in milk and mode at 70 eV. The mass scan range was 25e400 m/z (Condurso,
onions due to low growth activity of L. acidophilus in milk. Cooled to Verzera, Romeo, Ziino, & Conte, 2008).
37  C, samples (each sample of two replicates) were inoculated
with L. acidophilus NCFM (Danisco, New Century, KS, USA) at 2.7. Statistical analysis
5  106 CFU/g. A set of samples were maintained at 37  C in an MIR-
253 incubator (Sanyo, Osaka, Japan). Another set of samples were All data were reported as the mean or mean ± standard devia-
monitored automatically (recorded every 5 min) during milk tion. Physicochemical experiments were carried out in triplicate. The
acidification for pH using a Cinac system (Alliance Instruments, data was analyzed with ANOVA using Statistica 9.2 software (Stat
Mery-Sur-Oise, France), and the corresponding sample were Soft, Inc., Tulsa, OK, USA). The comparison between means was
removed to terminate fermentation until a pH of 4.50 ± 0.03 (the carried out using the Tukey's significant difference test (p < 0.05).
S. Li et al. / LWT - Food Science and Technology 65 (2016) 543e548 545

3. Results and discussion are shown in Fig. 3. All onion juice supplemented samples con-
tained significantly higher levels of L. acidophilus than the control
3.1. Effects of onion juice addition on acidification of L. acidophilus sample (p < 0.05). Moreover, the viable cell counts of L. acidophilus
increased as the content of onion juice increased. In addition, there
The pH values of samples during fermentation are shown in was a significant decrease in viable cell counts of L. acidophilus
Fig. 1. With low levels (60 g/kg) of onion juice added, there was an during storage when the content of onion juice was less than 20 g/
increase in acidification rates with increasing onion juice content. kg (p < 0.05), while the fermented milk containing 60 g/kg or
However, when the content of onion juice reached 60 g/kg, the higher of onion juice had no significant decrease in viable cell
maximum acidifying rate occurred. The results showed that addi- counts of L. acidophilus during cold storage (p > 0.05). Hence, the
tion of onion juice into fresh cow's milk exerted a stimulatory effect onion juice had positive effects on the growth and maintenance of
on fermentation. L. acidophilus viability.
A possible explanation for the stimulatory effect was that Several studies had confirmed the decrease in viability of pro-
L. acidophilus possessed the ability to utilize compounds supplied biotics attributable to acid accumulation, interaction with starter
by onion juice during growth, such as phytochemicals, poly- cultures, levels of dissolved oxygen and hydrogen peroxide, and
saccharides, vitamins, and/or minerals. Hervert-Herna ndez et al. storage conditions (Donkor et al., 2006; Talwalkar & Kailasapathy,
(2009) found that grape polyphenols induced a significant 2003). Adding onion juice not only promoted the production of
biomass increase of L. acidophilus during growth in liquid culture acid but also increased the viable cell counts, which indicated that
media. However, not all plant extracts that were able to inhibit acid accumulation was not an important factor contributing to the
pathogenic bacteria could stimulate fermentation by LAB. Yang loss of L. acidophilus NCFM cell viability during storage. In general,
et al. (2012) found that ginger juice would inhibit the growth of L. acidophilus does not possess a sufficient scavenging mechanism,
Streptococcus thermophilus and Lactobacillus bulgaricus and could so the intracellular accumulation of toxic oxygenic metabolites
reduce the production of lactic acid. such as superoxide anion and hydroxyl radical can lead to its death
The TA values of samples during cold storage are illustrated in (Gilliland & Speck, 1977; Talwalkar & Kailasapathy, 2003). Ng et al.
Fig. 2. The TA of all samples increased over the 14 days of storage. (2011) also reported that L. acidophilus does not possess a catalase,
The more onion juice that was added into the milk base, the an enzyme hydrolyzing H2O2 into water and oxygen, so that
significantly higher (p < 0.05) the TA of the sample was after hydrogen peroxide might be an important factor resulting in the
storage. However, there was not a significant difference (p > 0.05) loss of cell viability of L. acidophilus NCFM.
in TA when the onion juice content was higher than 60 g/kg. These Onion is rich in antioxidant phenolic constituents such as
results indicated that adding onion juice may promote the pro- quercetin 3,40 -diglucoside, quercetin, and kaempferol that are
duction of acid even at high acid concentrations and low considered important contributing factors to antioxidant activity
temperatures. (Albishi et al., 2013). These compounds might scavenge hydrogen
According to previous studies, L. acidophilus possesses several peroxide and protect L. acidophilus during the fermentation and
mechanisms to counteract acid stress (Altermann et al., 2005; storage. Hervert-Hern andez et al. (2009) found polyphenols pos-
Azcarate-Peril, Altermann, Hoover-Fitzula, Cano, & Klaenhammer, sessing antioxidant functions had a stimulatory effect on
2004). Kullen and Klaenhammer (1999) reported that the F1F0- L. acidophilus, and a possible explanation for this would be that
ATPase system maintaining the pHi was an important mechanism L. acidophilus was able to use these compounds as substrates. On
for promoting survival in the presence of accumulating organic the other hand, onions are a source of fructooligosaccharides, sulfur
acids. compounds, vitamins, and minerals (Rolda n, Sanchez-Moreno, de
Ancos, & Cano, 2008; Verde Mendez, Rodriguez Rodriguez, Diaz
3.2. Effect of onion juice addition on viable cell counts of
L. acidophilus

The viable cell counts of L. acidophilus in samples during storage

Fig. 2. The titratable acidity of samples during storage: , day 1; D day 7; Q day 14;
bars with different letters denote significant differences (p < 0.05) among the samples
with different contents of onion juice added. Error bars with different letters denote
Fig. 1. Changes in the pH of samples added of onion juice (0 g/kg, 20 g/kg, 60 g/kg, and significant differences (p < 0.05) among the samples with different contents of onion
100 g/kg) during fermentation. juice added and among the different storage periods.
546 S. Li et al. / LWT - Food Science and Technology 65 (2016) 543e548

and control samples are given in Table 1. Twenty-three compounds,

consisting of 4 alcohols, 5 aldehydes, 5 carboxylic acids, 3 ketones,
and 6 sulfur compounds, were identified in the 4 samples.
As seen in Table 1, propanal, 2-methyl-2-butenal, and 6 sulfur
compounds that had been identified as main volatile compounds of
onions were detected in both the fermented sample (60 g/kg onion
juice) and its control sample (60 g/kg onion juice, not fermented by
L. acidophilus). Moreover, comparing the sulfur compound contents
in the two samples, most sulfur compounds had significantly
decreased after fermentation (p < 0.05). The results confirmed that
L. acidophilus was able to utilize these compounds from onion juice
to supply energy to L. acidophilus during growth.
Acids produced in fermentation are the major components
causing the sour taste of fermented milk (Tamime & Robinson,
2007). Many carboxylic acids were detected in the fermented
milk samples. However, none of them was detected in the control
samples (not fermented by L. acidophilus). Previous studies have
shown that butanoic acid and hexanoic acid were produced by
lactose fermentation, and that hexanoic acid could also be formed
Fig. 3. The viabilities of L. acidophilus in samples after storage: , day 1; D day 7; Q by lipolysis of free fatty acids (Ott, Fay, & Chaintreau, 1997). In
day 14; bars with different letters denote significant differences (p < 0.05) among the
addition, comparing the contents of acids in the two fermented
samples with different contents of onion juice added. Error bars with different letters
denote significant differences (p < 0.05) among the samples with different contents of milk samples, there were more carboxylic acids in the fermented
onion juice added and among the different storage periods. sample with 60 g/kg of onion juice added. The stimulatory effect of
onion juice on producing acid observed in this investigation by
Romero, Matallana Gonzalez, & Torija Isasa, 2008), which might might be attributed to flavonoid, fructans and minerals, consistent
also account for the positive effects of its addition to milk. Babu, with the result of acidification of L. acidophilus.
Mital, and Garg (1992) reported that the addition of tomato juice Flavonoids are one of the abundant phenolic-type bioactive
to skimmed milk stimulated the growth of L. acidophilus because of compounds commonly found in vegetables and fruits, which been
sugars and minerals present in the juice. Sharma et al. (2013) re- categorized as flavonoid, flavanol, flavanone, flavone, anthocyani-
din, and isoflavon (Wach, Pyrzyn  ska, & Biesaga, 2007). The total
ported that Mnþ-metabolite complexes could protect essential
enzymes from oxidative damage. Therefore, it is probable that the flavonoid concentration was obtained at 89.6 mg/kg fresh onions by
whole constituents of onion juice such as fructans, polyphenols, summing the concentrations corresponding to all the identified
flavonoids (Rodríguez Galdo n, Rodríguez Rodríguez, & Díaz
sulfur compounds, and minerals together played the stimulatory
role and resulted in this beneficial effect for L. acidophilus viability Romero, 2008). Fructans such as oligosaccharides and fructooligo-
during fermentation and storage. saccharides are the other bioactive compounds in onion with the
total concentration of about 18 mg/kg of fresh weight (Rodríguez
Galdo n, Tasco
 n Rodríguez, Rodríguez Rodríguez, & Díaz Romero,
3.3. Antioxidant capacity of fermented milk 2009), which with falvonoids show a variety of pharmacological
effects in stimulating the metabolism of microbial cells, including
The AOCs of samples are presented in Fig. 4. It is noteworthy that L. acidophilus (China et al., 2012; Kaplan & Hutkins, 2000). Several
the AOC decreased significantly (p < 0.05) after the milk was fer-
mented by L. acidophilus NCFM (for example, AOC ¼ 0.783 before
fermentation vs. AOC ¼ 0.545 after fermentation in the control fer-
mented milk; AOC ¼ 0.836 before fermentation vs. AOC ¼ 0.578 after
fermentation in the fermented milk containing 60 g/kg onion juice).
It is possible that some antioxidant compounds were consumed and
considerable oxygenic metabolites were produced simultaneously
as L. acidophilus NCFM grew in milk. The results confirmed that it
was very necessary to scavenge radical for L. acidophilus growth. The
AOC of fermented milk containing onion juice was slightly higher
than that of control fermented milk (p < 0.05), which suggested that
antioxidants in onions might played a certain role in growth and
maintenance of L. acidophilus NCFM viability.
Some previous studies have confirmed that the high level of
antioxidant activity in onions was attributable to their flavonoid
constituents, namely quercetin, kaempferol, myricetin, and cate-
ndez et al. (2009) inferred
chin (Siddiq et al., 2013). Hervert-Herna
that L. acidophilus may be able to use polyphenols possessing
antioxidant functions as substrates. Hence, adding onion juice into
a milk base would be an effective method to increase the AOC of
fermented milk and to maintain the viability of L. acidophilus.
Fig. 4. The antioxidant capacity (AOC) of samples: , before fermentation; D day 1; G
day 7; Q day 14; bars with different letters denote significant differences (p < 0.05)
3.4. Volatile flavor compounds among the samples with different contents of onion juice added. Error bars with
different letters denote significant differences (p < 0.05) among the samples with
The volatile compounds detected in the fermented milk samples different contents of onion juice added and among the different storage periods.
S. Li et al. / LWT - Food Science and Technology 65 (2016) 543e548 547

Table 1
Results of volatile compounds analysis of four samples, showing the averaged peak areas (in arbitrary unit  1000).

Compound Averaged peak area  1000

Sample 1 Sample 2 Sample 3 Sample 4

d b c
Hexanol 62.6 ± 1.2 109.4 ± 3.5 73.9 ± 1.5 132.8 ± 4.8a
Heptanol 29.6 ± 0.8d 311.8 ± 5.6b 42.1 ± 1.7c 697.8 ± 7.2a
Octanol 113.9 ± 4.7b 119.2 ± 2.8b 93.2 ± 1.7c 129.8 ± 1.5a
Furanmethanol ND 166.2 ± 3.3a ND 171.3 ± 4.2a
Propanal ND ND 353.1 ± 5.8a 98.7 ± 1.8b
Hexanal 219.5 ± 3.5c 421.5 ± 7.6a 68.1 ± 0.6d 335.6 ± 4.4b
Octanal 136.2 ± 1.7c 264.2 ± 3.8a 32.4 ± 0.4d 189.1 ± 1.4b
Benzaldehyde 240.0 ± 5.2c 659.3 ± 6.9a 86.1 ± 1.1d 310.7 ± 1.5b
2-methyl-2-butenal ND ND 6999.9 ± 32.1a 5656.6 ± 28.7b
Propanoic acid ND ND ND 107.5 ± 1.8
Butanoic acid ND 724.4 ± 7.8b ND 790.6 ± 8.9a
Hexanoic acid ND 2821.5 ± 24.4b ND 3247.4 ± 28.9a
Octanoic acid ND 829.9 ± 8.9b ND 1341.2 ± 10.2a
Decanoic acid ND 92.4 ± 1.3b ND 190.5 ± 2.1a
Heptanone 3262.5 ± 30.1c 3060.1 ± 33.5d 6160.1 ± 37.6a 4341.0 ± 31.5b
Nonanone 3464.4 ± 28.9a 1334.9 ± 11.8d 2163.2 ± 21.6b 1475.5 ± 19.9c
Undecanone 847.0 ± 7.5a 212.8 ± 4.3d 624.9 ± 6.7b 368.1 ± 5.7c
Dimethyl disulfide ND ND 3266.1 ± 41.2a 1725.7 ± 31.5b
Methyl propyl disulfide ND ND 1803.4 ± 15.6a 1581.4 ± 14.3b
Methyl propenyl disulfide ND ND 123.4 ± 1.9b 237.1 ± 2.1a
Dimethyl trisulfide ND ND 2256.2 ± 22.5a 1832.9 ± 11.5b
Dipropyl trisulfide ND ND 255.0 ± 1.3a 123.4 ± 0.9b
2, 4-Dimethyl thiophene ND ND 2239.7 ± 22.5a 2158.8 ± 18.4b

All values are mean of three replications ±SD. Different superscript letters in the same row indicate significant differences at P < 0.05. ND: not detected. Sample 1: 0 g/kg onion
juice & not fermented; Sample 2: 0 g/kg onion juice & fermented; Sample 3: 60 g/kg onion juice & not fermented; Sample 4: 60 g/kg onion juice and fermented.

other interesting studies concerning the ability of L. acidophilus to and slightly enhancing the antioxidant capacity of fermented milk.
growth in the presence of fructans. Rendo  n-Huerta, Juarez-Flores, This study showed a potential application of adding onion juice to
Pinos-Rodríguez, Aguirre-Rivera, and Delgado-Portales (2011) re- the fermented milk production process.
ported that the lower pH values of the medium and the higher cell
counts were achieved in vitro growth of L. acidophilus with fructans Acknowledgments
of Cichorium intybus, Helianthus tuberosus and Agave angustifolia
spp. tequilana. Pehrson, Mancilha, and Pereira (2014) reported that This work was supported by National High Technology Research
L. acidophilus strain grew well in the medium containing fructans as and Development Program of China (2011AA100901), and the Na-
main carbohydrate sources, which a cellular viability significantly tional Key Technologies Program of China (2013BAD18B01) during
higher in this group than in the negative control. the 12th Five-Year Plan Period.
Alcohol, aldehyde, and ketone are also important to the flavor of
fermented milk. Comparing the alcohol and ketone contents in the References
two fermented milk samples, there were more of these compounds
in the fermented sample with 60 g/kg of onion juice added, but the Albishi, T., John, J. A., Al-Khalifa, A. S., & Shahidi, F. (2013). Antioxidative phenolic
aldehyde content was the opposite: more was found in the control constituents of skins of onion varieties and their activities. Journal of Functional
Foods, 5, 1191e1203.
sample. Aldehyde is labile and has a high level of activity. When the Altermann, E., Russell, W. M., Azcarate-Peril, M. A., Barrangou, R., Buck, B. L.,
fermented milk was supplemented with onion juice having McAuliffe, O., et al. (2005). Complete genome sequence of the probiotic lactic
considerable antioxidant substances, part of the aldehyde might acid bacterium lactobacillus acidophilus NCFM. Proceedings of the National
Academy of Sciences USA, 102, 3906e3912.
have been reduced to alcohol or other compounds. Overall, adding Azcarate-Peril, M. A., Altermann, E., Hoover-Fitzula, R. L., Cano, R., &
onion juice into milk increased the volatile compounds in fer- Klaenhammer, T. R. (2004). Identification and inactivation of genetic loci
mented milk and changed their flavor compounds profile. involved with lactobacillus acidophilus acid tolerance. Applied and Environmental
Microbiology, 70, 5315e5322.
Babu, V., Mital, B. K., & Garg, S. K. (1992). Effect of tomato juice addition on the
growth and activity of Lactobacillus acidophilus. International Journal of Food
4. Conclusion Microbiology, 17, 67e70.
China, R., Mukherjee, S., Sen, S., Bose, S., Datta, S., Koley, H., et al. (2012). Antimi-
The onion juice significantly stimulated the growth and acidi- crobial activity of Sesbania grandiflora flower polyphenol extracts on some
pathogenic bacteria and growth stimulatory effect on the probiotic organism
fication of L. acidophilus NCFM. The maximum acidifying rate was Lactobacillus acidophilus. Microbiological Research, 167, 500e506.
observed for when 60 g/kg of onion juice was added to the fer- Condurso, C., Verzera, A., Romeo, V., Ziino, M., & Conte, F. (2008). Solid-phase
mented milk sample. Probably, the whole constituents of onion microextraction and gas chromatography mass spectrometry analysis of dairy
product volatiles for the determination of shelf-life. International Dairy Journal,
juice together played the stimulatory roles and resulted in this 18, 819e825.
beneficial effect for L. acidophilus viability. During cold storage, not Donkor, O. N., Henriksson, A., Vasiljevic, T., & Shah, N. P. (2006). Effect of acidifi-
only did adding onion juice promote the production of acids by cation on the activity of probiotics in yoghurt during cold storage. International
Dairy Journal, 16, 1181e1189.
L. acidophilus NCFM, but it also exerted a positive effect on the
Gilliland, S. E., & Speck, M. L. (1977). Instability of Lactobacillus acidophilus in yogurt.
maintenance of L. acidophilus NCFM viability. Hence, rather than Journal of Dairy Science, 60, 1394e1398.
the accumulation of lactic acid, the accumulation of toxic oxygenic Gyawali, R., Seo, H., Lee, H., Song, H., Kim, D., Byun, M., et al. (2006). Effect of
metabolites may be the main reason for impaired survival of geirradiation on volatile compounds of dried welsh onion (Allium fistulosum L.).
Radiation Physics and Chemistry, 75, 322e328.
L. acidophilus NCFM during storage. Onion juice was beneficial to Hervert-Hern andez, D., Pintado, C., Rotger, R., & Gon ~ i, I. (2009). Stimulatory role of
shortening the fermentation time, enriching the flavor components grape pomace polyphenols on Lactobacillus acidophilus growth. International
548 S. Li et al. / LWT - Food Science and Technology 65 (2016) 543e548

Journal of Food Microbiology, 136, 119e122. Rendo n-Huerta, J. A., Juarez-Flores, B. I., Pinos-Rodríguez, J. M., Aguirre-Rivera, J. R.,
Jang, M. S., Sanada, A., Ushio, H., Tanaka, M., & Ohshima, T. (2002). Inhibitory effects & Delgado-Portales, R..,E. (2011). Effects of different kind of fructans on in vitro
of 'enokitake' mushroom extracts on polyphenol oxidase and prevention of growth of Lactobacillus acidophilus, Lactobacillus casei and Bifidobacterium lactis.
apple browning. LWT-Food Science and Technology, 35, 697e702. African Journal of Microbiology Research, 5, 2706e2710.
Kailasapathy, K., Harmstorf, L., & Philips, M. (2007). Survival of Lactobacillus aci- Rodríguez Galdo  n, B., Rodríguez Rodríguez, E. M., & Díaz Romero, C. (2008). Fla-
dophilus and Bifidobacterium animalis ssp. lactis in stirred fruit yogurts. LWT- vonoids in onion cultivars (Allium cepa L.). Journal of Food Science, 73,
Food Science and Technology, 41, 1317e1322. C599eC605.
Kaplan, H., & Hutkins, R. W. (2000). Fermentation of fructooligosaccharides by lactic Rodríguez Galdo  n, B., Tascon Rodríguez, C., Rodríguez Rodríguez, E. M., & Díaz
acid bacteria and bifidobacteria. Applied and Environmental Microbiology, 66, Romero, C. (2009). Fructans and major compounds in onion cultivars (Allium
2682e2684. cepa). Journal of Food Composition and Analysis, 22, 25e32.
Kullen, M., & Klaenhammer, T. R. (1999). Identification of the pH-inducible, proton- Roldan, E., Sanchez-Moreno, C., de Ancos, B., & Cano, M. P. (2008). Characterisation
translocating F1F0-ATPase (atpBEFHAGDC) operon of Lactobacillus acidophilus of onion (Allium cepa L.) by-products as food ingredients with antioxidant and
by differential display: gene structure, cloning and characterization. Molecular antibrowning properties. Food Chemistry, 108, 907e916.
Microbiology, 33, 1152e1161. Sanders, M. E., & Klaenhammer, T. R. (2001). Invited review: the scientific basis of
Lee, B., Jung, J., & Kim, H. (2012). Assessment of red onion on antioxidant activity in Lactobacillus acidophilus NCFM functionality as a probiotic. Journal of Dairy
rat. Food and Chemical Toxicology, 50, 3912e3919. Science, 84, 319e331.
Li, S., Ma, C., Liu, Z., Gong, G., Xu, Z., Xu, A., et al. (2014). Flavour analysis of stirred Scalbert, A., & Williamson, G. (2000). Dietary intake and bioavailability of poly-
yoghurt with Cheddar cheese adding into milk. Food Science and Technology phenols. Journal of Nutrition, 130, 2073Se2085S.
Research, 20, 939e946. Sharma, A., Gaidamakova, E. K., Matrosova, V. Y., Bennett, B., Daly, M. J., &
Lucey, J. A. (2004). Cultured dairy products: an overview of their gelation and Hoffman, B. M. (2013). Responses of Mn2þ speciation in Deinococcus radiodurans
texture properties. International Journal of Dairy Technology, 57, 77e84. and Escherichia coli to geradiation by advanced paramagnetic resonance
Michael, M., Phebus, R. K., & Schmidt, K. A. (2010). Impact of a plant extract on the methods. Proceedings of National Academy of Sciences of the United States of
viability of Lactobacillus delbrueckii ssp. bulgaricus and Streptococcus thermo- America, 110, 5945e5950.
philus in nonfat yogurt. International Dairy Journal, 20, 665e672. Siddiq, M., Roidoung, S., Sogi, D. S., & Dolan, K. D. (2013). Total phenolics, antioxi-
Najgebauer-Lejko, D., Sady, M., Grega, T., & Walczycka, M. (2011). The impact of tea dant properties and quality of fresh-cut onions (Allium cepa L.) treated with
supplementation on microflora, pH and antioxidant capacity of yoghurt. Inter- mild-heat. Food Chemistry, 136, 803e806.
national Dairy Journal, 21, 568e574. Talwalkar, A., & Kailasapathy, K. (2003). Metabolic and biochemical responses of
Ng, E. W., Yeung, M., & Tong, P. S. (2011). Effects of yogurt starter cultures on the probiotics bacteria in oxygen. Journal of Dairy Science, 86, 2537e2546.
survival of Lactobacillus acidophilus. International Journal of Food Microbiology, Tamime, A. Y., & Robinson, R. K. (2007). Biochemistry of fermentation. In yoghurt
145, 169e175. science and technology (3rd ed., pp. 535e577). Cambridge, UK: Woodhead
Oliveira, R. P. S., Perego, P., Oliveira, M. N., & Converti, A. (2011). Effect of inulin as a Publishing Ltd.
prebiotic to improve growth and counts of a probiotic cocktail in fermented Verde Mendez, C. M., Rodriguez Rodriguez, E. M., Diaz Romero, C., Matallana
skim milk. LWT- Food Science and Technology, 44, 520e523. Gonzalez, M. C., & Torija Isasa, M. E. (2008). Comparison of the mineral and
Ott, A., Fay, L. B., & Chaintreau, A. (1997). Determination and origin of the aroma trace element concentrations between 'gazpacho' and the vegetables used in its
impact compounds of yogurt flavor. Journal of Agricultural and Food Chemistry, elaboration. International Journal of Food Sciences and Nutrition, 59, 660e670.
45, 850e858. Wach, A., Pyrzyn  ska, K., & Biesaga, M. (2007). Quercetin content in some food and
Pehrson, M. E. S. F., Mancilha, I. M., & Pereira, C. A. S. (2014). Mixture of short-chain herbal samples. Food Chemistry, 100, 699e770.
and long-chain fructans exert a positive effect on the growth of three poten- Welty, W. M., Marshall, R. T., Grün, I. U., & Ellersieck, M. R. (2001). Effects of milk fat,
tially probiotic Lactobacillus strains. European International Journal of Science cocoa butter, or selected fat replacers on flavour volatiles of chocolate ice
and Technology, 3, 72e78. cream. Journal of Dairy Science, 84, 21e30.
Pescuma, M., He bert, E. M., Mozzi, F., & de Valdez, G. F. (2010). Functional fermented Yang, G., Guan, J., Wang, J., Yin, H., Qiao, F., & Jia, F. (2012). Physicochemical and
whey-based beverage using lactic acid bacteria. International Journal of Food sensory characterization of ginger-juice yogurt during fermentation. Food Sci-
Microbiology, 141, 73e81. ence and Biotechnology, 21, 1541e1548.