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Food Quality and Safety, 2018, 2, 83–87
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Research Paper
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Research Paper
Fermentation of groundnut brittle by
Lactococcus lactis produces γ-amino butyric
acid and enhances nutritional quality and safety
Vibhuti Batra,* Hitashi Lomash** and Abhijit Ganguli***
*Food Innovation Unit, SE Enterprises, Baddi, HP, India
**Amity University, Gurgaon, India.
***Department for Management of Science and Technology Development and Faculty of Applied Sciences, Ton Duc
Thang University, Ho Chi Minh City, Vietnam
Correspondence to: Abhijit Ganguli, Department for Management of Science and Technology Development and Faculty of
Applied Sciences, Ton Duc Thang University, Ho Chi Minh City, Vietnam. E-mail: abhijit.ganguli@tdt.edu.vn
Received 29 September 2017; Revised 15 January 2018; Editorial decision 31 January 2018.
Abstract
Objectives: The study aimed to evaluate the anti-nutrient reductions and γ-amino butyric acid
(GABA) enrichments of chikki (peanut brittle), a popular of traditional snack food, using Lactococcus
lactis subsp. lactis.The nutritional, storage, and sensorial analysis in order to understand the safety
and functionality of chikki following fermentation were attempted.
Materials and Methods: Partial fermentations of chikki were carried out using overnight grown
culture of L. lactis samples.The fermented chikki were further analysed for GABA and anti-nutrients.
The antioxidant profile, protein, and sugar were also analysed.The storage studies were carried on
up to 2 months for functional property evaluations.
Results: Fermentations at 37°C, pH of 5, with 1% inoculum and incubation for 24 h were optimal
conditions, and resulted in the GABA concentration of 816 mg/g, respectively, and the GABA
concentration did not change significantly (P > 0.05) upon storage for upto a period of 2 months.
Analysis of the fermented chikki revealed a slightly higher level of phenolic, flavonoid, protein, and
sugar contents as compared to those which were not subjected to fermentation.The results of sensorial
analysis showed an overall general acceptability on a 5-point hedonic scale to be 8.5 ± 0.01 (before
storage) and 8.03 ± 0.01 (after storage).The fermented chikki also possessed antioxidant properties
and significantly (P < 0.05) low levels of phytates with complete reductions of other anti-nutrients.
Conclusions: Traditionally prepared/manufactured chikki lacks GABA, possesses notable levels of
anti-nutrients with lower phenolics, flavonoids, as well as antioxidants. Our study suggested a simple
preparation of GABA could enrich the popular ethnic snack through fermentation by L. lactis subsp.
lactis. The developed snack is acceptable, economical with good shelf life, and has substantially
reduced levels of anti-nutrients originating from groundnuts affording consumer safety.
Key words: γ-amino butyric acid; anti-nutrients; ethnic snack; Lactococcus lactis.
Introduction
Groundnuts (Arachis hypogaea) or peanut is a legume which is widely
grown as one of food crops. Groundnut seed contains 44%–56% oil
and 22%–30% protein on a dry basis, and is a rich source of minerals
(P, Ca, Mg, and K) and vitamins (E, K, and B group) (Savage and
Keenan, 1994). Groundnut proteins are increasingly becoming impor-
tant food and feed sources in developing countries. The groundnut
seeds have several uses as whole seeds or processed to peanut butters,
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2. oil soups, stews, and other products. The groundnut chikki is a popu-
lar ethnic snack in the Western countries, and made by variant of the
peanut brittles. They are widely consumed in both rural and urban
South Asia. The roasted peanuts (A. hypogaea) and jaggery, the con-
centrated products of date, cane juice, or palm sap without separation
of molasses and crystals are used for making chikki. Because of their
acceptability among all age groups, long shelf life, and taste, they are
considered as good products for fortification and nutritional improve-
ment. The groundnuts provide considerable amounts of mineral ele-
ments as supplements to meet the dietary requirements of humans and
farm animals (Asibuo et al., 2008).The presence of anti-nutrients such
as tannin, phytic acid, and trypsin inhibitors necessitates the process-
ing of enable adequate nutritional benefits. The contribution of lactic
acid bacteria (LAB) in designing and developing functional non-dairy
foods presents interesting prospects and has begun to be exploited for
redesigning traditional foods with enhanced benefits. The many ben-
efits of LAB range from enhancing the shelf life and safety of foods,
improving food textures, and contribute to the nutritional value of
food products through removal or reduction of anti-nutrients without
changing of pleasant sensory profile.
Furthermore, LAB have been exploited for generating bioactive
molecules such as γ-amino butyric acid (GABA) in both dairy and non-
dairy products. GABA, a non-protein inhibitory neurotransmitter, is
primarily produced from irreversible α-decarboxylation of L-glutamic
acid, catalyzed by glutamic acid decarboxylase (GAD), which has been
found in bacteria, plants, and animals. Currently, GABA is used consid-
erably in pharmaceuticals, and massively as a major active constitute
in foods, such as gammalone, cheese, gabaron tea, and shochu. The
GABA intake can regulate sensations of pain and anxiety, and lipid
levels in serum (Miura et al., 2006). Consumption of GABA-enriched
foods can inhibit cancer cell proliferation (Park et al., 2007), and
improve memory and the learning abilities. The existence of the gdh
gene in LAB which is responsible for the production of glutamic acid
can facilitate production of functional foods rich in bioactive molecules
such as GABA. There have been long and safe histories of the produc-
tion of fermented foods and beverages by LAB, which can accumulate
high amounts of GABA (Leroy and de Vuyst, 2004). Especially, the
productions of GABA by LAB have been extensively explored during
the manufacture of black raspberry juice, kimchi, soymilk, cheese, and
other dairy products (Kim et al., 2009). GABA producing LAB also
protected foods by controlling the food spoilage pathogens by secret-
ing bacteriocins (Dhakal et al., 2012).
No reports on the evaluated anti-nutrient reductions or GABA
enrichment of chikki, the popular ethnic groundnut snack con-
sumed by all sections of population, thus far. We supposed that the
fermentative productions of GABA which requires glutamic acid
abundant in peanuts could be a possibility for producing GABA
in chikki under in situ conditions, using probiotic LAB. This was
based on our previous findings on the GABA producing capabilities
of Lactococcus lactis subsp. lactis. Besides, the strain of L. lactis has
been previously examined for its potential in degrading several anti-
nutrients in Vigna mungo (Varsha et al., 2014); therefore, simultane-
ous removal or reduction of anti-nutrients in the groundnut could
be also assessed. Consequently, the present study was designed to
understand the nutritional, sensory properties, and anti-nutrient
profile of groundnut chikki subjected to fermentation by L. lactis.
Materials and Methods
Microorganism and culture conditions
The L. lactis subsp. lactis (GenBank accession number JN618456)
previously characterized by Bhanwar et al. (2013) was used
throughout present study. The strains were routinely grown in De
Man Rogosa and Sharpe (MRS) agar at 37°C. The inoculums were
prepared by overnight growth of the microorganism in MRS medium
at 37°C with shaking (120 rpm). Purity was confirmed periodically
by gram staining and microscopic observation. All media compo-
nents were purchased from Difco (UK). Chemicals and reagents were
of highest analytical grade; standards were purchased from Sigma
(MO, USA).
Formulation of fermented chikki
Jaggery and peanuts were purchased from local supermarket. The
pre-weighed components were crushed, jaggery was heated at a
temperature of 40°C, and culture (L. lactis) (1%) was added with
gradual stirring. After addition of peanuts, the mixture was allowed
to solidify in moulds held at room temperature for 2 h, later stored
in air-tight containers (Babuskin et al., 2015). Sensory analysis was
carried out including mouth feel, consistency texture, colour appear-
ance, smell, taste, and overall acceptability on 5-point hedonic scale
by a panel of 10 trained judges.
Determination of GABA contents
To determine GABA contents, 18 g of the groundnut chikki samples
were extracted with 40 ml of distilled water for 2 h in water bath at
85°C. The samples extracts were then centrifuged at 12 000 rpm for
10 min at room temperature. The resulted supernatant was filtered
and described using thin-layer chromatography (TLC) as described
by Cho et al. (2007), spectrophotometrically by the method of Zhang
and Bown (1997). The GABA productions were confirmed by HPLC
method (Rossetti and Lombard, 1996). Incubation time (8, 16, 24,
48, 72 h), inoculum sizes (1%–5%), and pH (3.5–5.5) were opti-
mized for maximizing productions of GABA by L. lactis in chikki.
Texture, nutritional analysis, and storage stability
The GABA-enriched chikkis were analysed for their textures objec-
tively by following triple beam snap method using a texturometer
TA.XT-Plus (Stable Micro-Systems, UK) as described by Babuskin
et al. (2015). The total protein contents (Lowry et al., 1951), fol-
lowed by total sugars (Dubois et al., 1956), and the total flavo-
noid contents by using a modified colorimetric method (Zhishen
et al., 1999). Functional analysis included reducing power by
the Fe3+-Fe2+ transformation in the presence of the fractions as
described by Fejes et al. (2000). The total polyphenol contents were
determined by Folin–Ciocalteau reagent method and the total anti-
oxidant capacity by phosphomolybdate method using ascorbic acid
as the standard (Prieto et al., 1999).
The fermented chikkis were stored in air-tight containers at
ambient temperature (28°C), and their GABA contents were com-
pared before and after storage for 2 months. The sensory quality of
chikkis was evaluated by a panel of 10 trained judges by grading on
sensory analysis and overall acceptability. The scores were given on a
5-point hedonic scale where 1 represents worst and 5 represents best.
Analysis of anti-nutritive factors
Tannin and cyanide contents in the fermented chikkis were deter-
mined by the method of Association of Official Analytical Chemists
(AOAC) (Miura et al., 2006). Oxalates were determined by using
the method of Talpatra et al. (1948). For determining trypsin
inhibitor activity, the method of Kakade et al. (1969) was used.
Haemagglutinin activity was analysed by the method described by
Liener et al. (1996).
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3. Statistical analysis
All data analysis were performed using SPSS version 20.0 (SPSS Inc.,
USA), at a Type I error rate of 0.05 (Spielberg et al., 1970); ‘t’-tests,
correlations, and ANOVA were used for verification of study.
Results and Discussion
Cell viability and GABA contents
The strain of L. lactis has been reported as a potential GABA pro-
ducer with probiotic attributes (Bhanwar et al., 2013). However, the
judgment of its viability was deemed important since GABA produc-
tions may be envisaged with growth and utilization of glutamate in
peanuts, the cell viability in the formulated matrix was the direct
correlation to its metabolic capability of glutamate conversion to
GABA during storage (Figure 1). The GABA concentrations in the
fermented chikkis increased with time and were reached to the maxi-
mum yields after 24 h (Figure 1). The highest GABA concentration
in the fermented chikkis was 816 mg/g, respectively, and neither
increased following 24 h nor significant (P 0.05) decreases were
observed upon further storage at 28°C for up to 2 months.
Effects of time, temperature, and inoculum size on
GABA productions of chikkis
The optimum conditions for GABA productions were 37°C at 24 h
with 1% inoculum size. The highest amount of GABA was obtained
at a pH 5.0. After stored up to 2 months, there was no change in pH
value, and in concurrence with the previous reports stated that the
highest GABA productions by LAB usually occurred in the range of
4.0–5.0.(Cho et al., 2007). The GABA yields decreased with increas-
ing inoculum size (Figure 2). Higher inoculum sizes may have led
to overcrowding of microbial cells resulted in the lesser in nutrient
acquisition and consequently reduced cell growth and GABA pro-
ductions in the semi-solid matrixes. The optimal temperature was
37°C and was similar to that earlier reported for GABA production
reported by Bhanwar et al. (2013) (Figure 3). A temperature range of
25–40°C has been suggested for high GABA production.
Incubation time required can vary from 24 to 72 h for GABA
production (Kim et al., 2008), the production usually declines on
account of lowering of pH following in liquid cultures. Besides,
the availability of the GABA substrate at appropriate times (strain
variable) may also influence the rapid conversion; a slow release of
glutamate from peanut matrices is expected in this case. Moreover,
in semi-solid matrices, the inhibitory effect of pH effect is not antici-
pated immediately; therefore, GABA production continued una-
bated for a longer time in chikki. The physiologically appropriate
temperature for optimal growth in conjunction with other cultural
factors favoured high GABA production in chikki.
Measurement of texture and compositional analysis
Texture values of the fermented chikkis were 7.06 ± 0.18 for freshly
prepared and 6.1 ± 0.11 (results not shown), respectively, after
2 months storage. Compositional analysis revealed a slightly ele-
vated phenolic, flavanoid, protein, and sugar contents as compared
to those lacking cultures (Table 1). A slightly lower reducing ability
as compared to standard was observed; however, these differences
remained insignificant (P 0.05).
Storage, stability, and sensorial analysis
The GABA concentrations in the fermented chikkis increased
slightly for up to 24 h (Table 2). The sensorial analysis resulted
as the overall general acceptability of the fermented chikkis on
a 5-point hedonic scale to be 8.5 ± 0.01 (before storage) and
8.03 ± 0.01 after 60 days storage. The results suggested an overall
acceptability of the fermented snacks in comparison to the unfer-
mented chikkis (Table 3).
Figure 1. Determination of cell viability and γ-amino butyric acid (GABA)
concentration. The cell viability (CFU/g) and GABA conc. (mM/g) of
Lactococcus lactis in chikki.The blue bars indicate GABA conc. before storage
and red bars indicate GABA conc. after storage. Data are means ± SD from
three independent experiments.
Figure 2. Effect of inoculum size on γ-amino butyric acid (GABA) production.
Data are means ± SD from three independent experiments.
Figure 3. Effect of temperature on γ-amino butyric acid (GABA) production
in chikki. Temperature (°C) on GABA concentration (mM/g) in fermented
chikki before and after 2 months storage. Data are means ± SD from three
independent experiments.
Fermentation of Groundnut Brittle by Lactococcus Lactis, 2018, Vol. 2, No. 2 85
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4. Role of fermentation on the peanut anti-nutrients
The effects of L. lactis fermentation process on oxalate, cyanide,
trypsin inhibitory activity, tannin, and phytates are presented in
Table 4. Trypsin inhibitor activity, cyanide, oxalate, and tannin con-
centrations were completely removed following fermentation. The
haemagluttination activities could not be detected. However, the
complete removal of phytates was not observed.
Discussion
GABA is known to reduce pain, slow heartbeat, decrease anxiety, and
induce calm (Fang et al., 2014). Therefore, natural addition/presence
of GABA is preferred over the addition of chemical counterpart since
consumers prefer naturally occurring substances. Moreover, the
fermentation could help to reduce the cost of the foods due to the
omission of chemical addition of GABA and also render foods with
better taste (Li et al., 2008). The L. lactis strain used in this study,
has been reported to survive and produce high levels of y amino
butyric acid (226.220 mg/100 g) in other food matrices (Bhanwar
et al., 2013). Therefore, due to the ability of L. lactis to survive in the
solid food matrixes and produce GABA, it was selected as a potent
strain for snack food development. Cell viability was not affected
during fermentation of the groundnut jaggery mixture. However,
the growth rates were lower as could be expected, in the semi-solid
matrix (Figure 1). The maximum GABA concentration was achieved
after 24 h of storage but did not differ significantly (P 0.05) upon
further storage. The optimum conditions of room temperature with
1% inoculum size and pH 5.0 did not alter the GABA concentra-
tions. Sensorial and storage ability after 2 months did not change
significantly. These results suggested that the fermented chikki would
be functionally stable and acceptable for up to 2 months, and in
agreement to those reported by Babuskin et al. (2015).
The results of our study indicated that the fermented
chikki (1500 mg), consumed once a day (Recommended Daily
Allowance (RDA) of GABA for anxiety is 500–1800 mg) may be
able to relieve stress. However, clinical studies are necessary to estab-
lish this. The possibility of enriching foods with GABA is an active
area and has been explored in many food products like brown rice
(0.0001 g/l), yogurt (0.000425 g/l), cheese (0.000383 g/g), GABA
tea (0.019 g/l), and kimchi (26.8 g/l) with various LAB L. buchneri,
L. delbrueckii, and L. acidophilus.
The groundnut was chosen for present study, and based on the
formulating the snack on account of the inherent nutritional ben-
efits besides the high glutamic acid in peanuts which would not
necessitate any external addition, for instance, of Mono-sodium
Glutamate (MSG) to ensure GABA production. Besides, groundnut
is a good source of vitamin E, magnesium, fibre, polyphenols, vita-
min B-6, proteins, and unsaturated fats. Recent studies have indicated
that groundnuts have potential to improve age-related impairments
in cardiometabolic health and cognitive function increase with ageing
(Coates et al., 2016). Jaggery (unrefined sugar made from sugar cane
or palm) contains iron, magnesium, potassium, manganese, protein
besides fructose, sucrose, and glucose and adds to the sweetness as
well as nutrition. Apart from germination, roasting, cooking which
enable reduction in anti-nutrients important for enabling the aforesaid
nutritional benefits, fermentation has been advocated as a practical
method for significantly removing anti-nutrients. We observed a com-
plete reduction of tannin in the fermented chikkis after 24 h. Varsha
et al. (2014) reported tannase activity of L. lactis, the extracellular
Table 2. Stability of γ-amino butyric acid (GABA) concentration
(mM/g) in fermented chikki at ambient temperature during its
production and following storage for 60 days
Time (h) Kinetics of GABA conc.
during fermentation of
chikki
GABA conc. in chikki
after fermentation
during storage
0 1.03 ± 0.20 2 days: 8.80 ± 0.13
4 2.03 ± 0.11 7 days: 8.76 ± 0.31
8 4.36 ± 0.31 10 days: 8.87 ± 0.23
12 5.12 ± 0.22 15 days: 9.0 ± 0.66
16 6.08 ± 0.85 30 days: 8.96 ± 0.73
20 7.13 ± 0.77 45 days: 8.94 ± 0.65
24 8.16 ± 0.92 60 days: 8.07 ± 0.73
Figures in parenthesis indicate SD ± mean.
Table 3. Sensory scores of fermented chikki before and after
storage at ambient temperature
Attributes Before storage After storage
Mouth feel 8.6 ± 0.01 8.1 ± 0.01
Taste 8.5 ± 0.01 7.9 ± 0.01
Smell 8.9 ± 0.01 8.5 ± 0.01
Consistency 7.5 ± 0.01 7.2 ± 0.01
Texture 8.9 ± 0.01 8.3 ± 0.01
Colour and appearance 8.8 ± 0.01 8.2 ± 0.01
Overall acceptability 8.5 ± 0.01 8.03 ± 0.01
Values with different letters in the same column differ significantly (P, 0.05).
Values are expressed as mean ± SD P 0.001 when compared with
standard.
Scores were assigned numerical values from 1 (extremely weak) to 5
(extremely strong).
Table 4. Anti-nutrients before and after fermentation in chikki. ND,
not detected.
Antinutrients
analysed
Chikki
(before fermentation)
Chikki
(after fermentation)
Tannin 31.66 ND
Phytate 21.89 mg/100 g 9.71 mg/100 g
Oxalate 137 mg/100 g ND
Trypsin inhibitor 79.67 TUI/mg ND
Cyanide 4.6% ND
Haemagluttination 179 Hg ND
Results are average of three independent replicates.
Table 1. Nutritional analysis of fermented chikki and non-
fermented chikki
Nutritional analysis Fermented chikki Chikki (non-fermented)
Total flavanoids (g/ml of
catechol)
0.528 ± 0.01 0.378 ± 0.01
Total protein (g/ml of BSA) 0.0010 ± 0.01 0.0006 ± 0.01
Total sugar (g/ml of glucose) 0.0004307 ± 0.01 0.0004016 ± 0.01
Reducing power 2.089 ± 0.01 2.022 ± 0.01
Total antioxidant activity
absorbance at 695 nm
2.43 ± 0.05 2.12 ± 0.05
Values are expressed as mean ± SD P 0.001 when compared with standard.
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5. tannase produced by this strain being thermostable. The efficacy of
other LAB such as Lactobacillus plantarum as tannase producer has
been reported. However, the applications of strain with the objec-
tive of reducing tannin in food legumes have not been reported. The
reduction of trypsin inhibitor level therefore may be useful to improve
nutritional quality with respect to protein digestibility. Phytate, tan-
nin, and oxalate interfere with impair digestion and impair bioavail-
ability of essential minerals. Amongst methods suggested for reducing
anti-nutrients, the germination demonstrated high reduction of anti-
nutrients in groundnut seeds. Fermentation of groundnuts for a tem-
peh-like product was reported by Bhavanishankar et al. (1987), with
enhanced levels of free lysine and methionine and Protein Efficiency
Ratio (PER). The extracellular peptidases of Lactococcus have been
ascribed in several degradative reactions during food fermentations,
and are responsible for degradation of the trypsin inhibitors (Leroy
and de Vuyst, 2004). Similar studies have reported on the reductions
in trypsin inhibitors during natural lactic acid fermentation of cere-
als (Ejigui et al., 2005). Trypsin inhibitor is important for reducing
protein digestibility, pancreatic hypertrophy, and poor growth perfor-
mance in rats, mice, and chicks. The role of LAB in oxalate degrada-
tion has been reported. However, the role of phytate degradation by
this strain remains elusive and requires detailed investigations, since
in vitro experiments (using purified anti-nutrients) failed to produce
conclusive results for phytate (results not shown).
The fermented chikkis exhibited slightly higher levels of phenolic,
flavonoid, protein, and sugar contents as compared to those lacking
culture. It was plausible that fermentation may have caused release
of bound flavonoids and polyphenols resulting in slightly elevated
levels. The biomass of L. lactis attributed to the small increment in
the total proteins observed similar to those reported by in case of
chikki prepared using extracts. To the best of our knowledge, this is
the first report of production of GABA (816 mg/g) by L. lactis in the
traditional fermented peanut snack foods with decreased anti-nutrient
levels. Peanuts/groundnuts and jaggery are both economical and can
be conveniently used for fermentation of groundnut brittles/chikkis.
Furthermore, there were no significant (P 0.05) differences found
in the sensory properties. The GABA concentrations and antioxidant
profile of the chikki that prepared from L. lactis prior and following
storage period at ambient temperature were observed. These findings
may contribute to enhancing the health benefits by contributing to the
safety and elevating the nutritional value of the traditional fermented
chikki. Based on these findings, the commercial viability of the newly
designed chikki should be evident following clinical studies.
Conclusions
A partially fermented ethnic peanut brittles or chikkis was developed
using a probiotic strain of L. lactis subsp. lactis. The L. lactis strain
could ferment the peanut (5.348 g/100 g glutamic acid) and jaggery
basic mixture, resulting in GABA concentration of 816 mg/g, anti-
oxidant properties, and significantly low levels of phytate with com-
pleted reduction of other anti-nutrients. Moreover, the developed
chikki possessed antioxidant properties, was shelf stable at ambient
temperature for up to 2 months. The newly modified ethnic snack,
following clinical trials, may offer an affordable and acceptable solu-
tion in terms of cognition and safety.
Acknowledgements
The authors wish to thank TDTU, Ho Chi Minh City, Vietnam for financially
supporting this work.
Conflict of interest statement. None declared.
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