Effect of fermentation on the nutritive value of maize

Abstract

The effects of fermentation on protein, in vitro protein digestibility (IVPD), amino acid, total phenolics, phytic acid and colour values of four maize cultivars (two bi‐colour waxy corn and two super sweet corn), namely Jing Tian Zi Hua Nuo NO. 2, Jing Tian NO. 3, Bright Jean and Su Ke Hua Nuo 2008, were determined and compared with those of their unfermented counterparts. Results showed that fermentation caused significant increase in protein (43.5% largest increase), most kind of amino acid (131.5% largest increase in lysine content) and total phenolic content (23.4% largest increase), but significant reduction in phytic acid content (24.3% largest reduction) of four maize cultivars. The IVPD of four maize cultivars, except Suke2008, did not change significantly. Colour values of two waxy corn were resulted in the increase in a‐values and reduction in L‐values.

Full text

Original article
Effect of fermentation on the nutritive value of maize
Li Cui
1,2
, Da-jing Li
1,2
& Chun-quan Liu*
1,2
1 Institute of Farm Product Processing, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China
2 Engineering Research Center for Agricultural Products Processing, National Agricultural Science and Technology Innovation Center
in East China, Nanjing 210014, China
(Received 21 July 2011; Accepted in revised form 1 November 2011)
Summary The effects of fermentation on protein, in vitro protein digestibility (IVPD), amino acid, total phenolics,
phytic acid and colour values of four maize cultivars (two bi-colour waxy corn and two super sweet corn),
namely Jing Tian Zi Hua Nuo NO. 2, Jing Tian NO. 3, Bright Jean and Su Ke Hua Nuo 2008, were
determined and compared with those of their unfermented counterparts. Results showed that fermentation
caused significant increase in protein (43.5% largest increase), most kind of amino acid (131.5% largest
increase in lysine content) and total phenolic content (23.4% largest increase), but significant reduction in
phytic acid content (24.3% largest reduction) of four maize cultivars. The IVPD of four maize cultivars,
except Suke2008, did not change significantly. Colour values of two waxy corn were resulted in the increase
in a-values and reduction in L-values.
Keywords Fermentation, in vitro protein digestibility, maize, phytic acid, total phenolic content.
Introduction
Maize is an excellent source of carbohydrate, but its
protein quality is relatively poor because it is deficient in
the essential amino acids lysine and tryptophan (Paulis,
1982). Owing to nutritional importance of maize,
significant efforts have been made to improve its protein
quality. Fermentation is an inexpensive and simple
method for improving the nutritive value of maize-based
foods and reducing their antinutritional factors (Mbu-
gua, 1988). Chelule et al. (2010) reported that tradi-
tional amahewu fermentation may improve the protein
and amino acid yield. Amahewu is a sour maize-based
fermented gruel or beverage consumed mainly by the
indigenous people of South Africa. It is not clear
whether fermentation of four Chinese maize cultivars
based on the technique used in amahewu, and the maize,
the yeast, the wheat flour and the environment that were
from China can result in the same beneficial effects.
Therefore, the objective of this study was to evaluate the
effect of the fermentation on the protein quality of four
Chinese maize cultivars by assessing contents of protein,
amino acid, total phenolics and phytic acid and in vitro
protein digestibility (IVPD) of the raw and fermented
maize. The four types of maize cultivars (Jing Tian Zi
Hua Nuo NO.2, Jing Tian NO.3, Bright Jean and Su Ke
Hua Nuo 2008) were chosen based on their agricultural
importance. These all cultivars are popularly grown in
Jiangsu Province, China. Briefly, they can be described
as follows: Jing Tian Zi Hua Nuo NO. 2 (J2) – a
bi-colour waxy corn, selected by Beijing Yanhejin
Agricultural Science and Technology Development
Center, with purple and white kernels; Su Ke Hua
Nuo 2008 (S) – a bi-colour waxy corn, selected by
Institute of Food Crops, Jiangsu Academy of Agricul-
tural Sciences, with blue and white kernels; Jing Tian
NO. 3 (J3) – a super sweet corn, selected by Nanjing
Vegetables (Flower) Scientific Institute, China, with
yellow kernels; Bright Jean (B) – a super sweet corn,
selected by KNOWN-YOU Seed CO., Ltd, Kaohsiung,
Taiwan, with yellow kernels.
Materials and methods
Samples and their preparation
Based on the technique used in amahewu, each type
meal of four maize cultivars were separated into three
equal portions, respectively. Each portion (80 g) was
homogenised in 1500 mL of cold tap water with 10 g
sodium chloride. It was stirred continuously for about
15 min, while boiling. The porridge was then cooled.
Yeast (Angel Yeast Co., Ltd, Hubei, China) 0.8 g and
wheat flour (Nanjing Tongheng Flour Co. Ltd, Jiangsu,
*Correspondent: E-mail: liuchunquan2009@163.com
International Journal of Food Science and Technology 2012, 47, 755–760 755
doi:10.1111/j.1365-2621.2011.02904.x
2012 The Authors. International Journal of Food Science and Technology 2012 Institute of Food Science and Technology

China) 8 g were added, and the entire mixture was made
up to one litre with water. All samples were fermented at
5C for 3 days. Fermentation was considered ready
when the pH range was 3–4. After fermentation, the
samples were freeze-dried and stored at 4 C before
analysis. An unfermented control sample was prepared
as described before, omitting the inoculation step.
Chemical analysis
Crude protein and in vitro protein digestibility
Crude protein was determined by the micro-Kjeldahl
method (AOAC, 1975). IVPD was carried out according
to Yousif and El-Tinay (2000). Dried sample 1 g was
placed in a 50-ml centrifuge tube, 15 mL of 0.1 N HC1
containing 15 mg of pepsin (1:3000; Sigma, Shanghai,
China) was added and the tube was incubated at 37 C for
3 h. The suspension was then neutralised with 0.5 N
NaOH (ca. 3.3 mL) and then treated with 36 mg of
trypsin (1:250; Sigma) in 15 mL of 0.2 mphosphate buffer
(pH = 8.0), and the mixture was then gently shaken and
incubated at 37 C for 24 h. After incubation, the sample
was treated with 10 mL of 10% trichloroacetic acid and
centrifuged at 1028 gfor 30 min at room temperature.
Nitrogen in the supernatant was estimated using the
Kjeldahl method. Digestibility was calculated using the
formula:
Protein digestibility% = (nitrogen in supernatant ⁄
nitrogen in sample) *100
Amino acids
Each dried sample (ca. 0.5 g) was thoroughly mixed with
5mHCl (25 mL). Samples were hydrolysed for 24 h at
110 C. Two millilitres of sample of the supernatant was
filtered, concentrated to dryness under reduced pressure,
redissolved in 1 mL of acid water (0.005 mHCl) and
finally filtered through a membrane (membrane filter,
pore size 0.45 lm; Millipore, Bedford, MA, USA). Then,
the HITACHI L-8900 Amino acid analyzer (Hitachi
High-Technologies Corporation, Tokyo, Japan) was
used to analyse the free amino acid composition of a
20-lL sample. The solvents used to elute the sample were
a mixture of sodium acetate (0.14 m), trimethylamine
(0.05%) and 60% acetonitrile. The signal was detected at
the wavelength of 254 and 440 nm. Each amino acid was
identified using the authentic amino acid (Sigma) and
quantified by the calibration curve of the authentic
compound.
Phytic acid
Phytic acid stock solutions were prepared with
1.0 mg mL
)1
phytic acid sodium salt hydrate from rice
(Sigma). Ferric solution was prepared by dissolving
0.3 g FeCl3 and 3 g 5-sulphosalicylic acid in distilled
water and the volume was made to 1000 mL. For the
analysis, 0.2 g of samples was extracted with 3 mL of
0.01 mHCl at 4 C overnight, and 2.5 mL of this extract
was pipetted out into a test tube fitted with a ground-
glass stopper. Two millilitres of Ferric solution was
added into it. The test tube was then covered with a
stopper and shook for 5 min. After 20 min, the absor-
bance was immediately measured at 500 nm against
distilled water.
Total phenolics and colour values
Total phenolics were measured as gallic acid equivalents
(GAE) from a gallic acid standard curve. Each dried
sample (100 mg) was thoroughly mixed with 70%
ethanol. Samples were sonicated for 60 min at 20 kHz.
Followed by centrifugation (10 000 rpm, 30 min), the
supernatant was used in the estimation. One millilitre of
the sample extract was transferred to a test tube, and
1 mL of 95% ethanol, 7.75 mL of distilled water and
0.25 mL of Folin-Ciocalteu phenol reagent (Sigma) were
added. After an incubation period of 5 min, 1.5 mL of
20% Na
2
CO
3
was added, mixed well and kept in the
dark for an hour. Then, the samples were vortexed, and
the absorbance was measured at 760 nm using a UV
spectrophotometer (Beijing Purkinje General Instru-
ment Co., Ltd., Beijing, China). The total phenolic
content was assessed by plotting the gallic acid calibra-
tion curve and expressed as milligrams of GAE per gram
of dried example. The Hunter colour L*, a*, b* values
were determined using a colour difference meter (WSC-
S; SHENGUANG, Shanghai Precision Scientific
Instrument Co., Ltd., Shanghai, China).
Statistical analysis
Results were reported as mean ± SD for three replica-
tions. In all experiments, one-way analysis of variance in
combination with Tukey’s test for individual compari-
sons was performed. All statistical calculations were
made at the P< 0.05 level using 2005 SAS (Version 9.1;
SAS institute Inc., Cary, NC, USA).
0
5
10
15
20
25
J3 J2 S B
Protein content (% weight)
Before After
Figure 1 Effect of fermentation on protein content.
Effect of fermentation on total phenolic content, phytic acid content L. Cui et al.756
International Journal of Food Science and Technology 2012 2012 The Authors
International Journal of Food Science and Technology 2012 Institute of Food Science and Te chnology

Results and discussion
Effect of fermentation on protein and amino acids content
Fermentation significantly (P< 0.05) increased the
protein content for all cultivars (Fig. 1). Increase in
J3, J2, S and B was 40.6%, 43.5%, 29.7% and 35.2%,
respectively. From these results, it seems that all four
maize cultivars’ fermentation yields a positive protein
return. This is in agreement with earlier work that
demonstrated increased levels of protein in amahewu
produced in the presence of yeast (Chelule et al., 2010).
Azoulay (1978) also reported 15–30% increase in
protein content as a result of maize fermentation, with
an appropriate yeast such as Candida tropicalis. Ony-
ango et al. (2004) found that the increase in protein
content after fermentation was attributable to a
decrease in carbon ratio in the total mass. Micro-
organisms utilise carbohydrates as an energy source and
produce carbon dioxide as a by-product. This causes the
nitrogen in the fermented slurry to be concentrated, and
thus, the proportion of protein in the total mass
increases. The amino acid profile is important in
evaluating the nutritive quality of protein. The amino
acid yield followed a trend similar to that for proteins.
Majority of amino acid content significantly (P< 0.05)
increased after fermentation (Table 1). Increase in
essential amino acids was highest in sample J2
(79.2%), followed by samples B (72.6%), J3 (69.3%)
and S (53.2% increase), respectively. Lysine and tryp-
tophan (not measured) are the most limiting amino
acids in maize (Paulis, 1982). After fermentation, lysine
levels of four cultivars increased significantly
(P< 0.05). Increase in J3, J2, S and B was 126.5%,
117.9%, 93.8% and 131.5%, respectively. This is in
agreement with earlier work that demonstrated in-
creased levels of lysine in fermented maize (Hamad &
Fields, 1979; Umoh & Fields, 1981).
Effect of fermentation on
in vitro
protein digestibility
Because maize possesses lower protein digestibility owing
to the interference by various antinutrients such as phytic
acid, total phenolic content and trypsin inhibitor activity
(Onyango et al., 2004), IVPD may be substantially
increased if the level of phytic acid and total phenolic
content is significantly reduced. Our results showed that
fermentation decreased phytic acid but increased total
phenolic content (Figs. 3 and 4). Thus, the net effect of the
changes of these two antinutrients may be important in
determining the direction in which the IVPD will change.
After fermentation, the IVPD of four maize cultivars,
except Suke2008, did not change significantly (P> 0.05)
(Fig. 2). These results are in disagreement with other
studies where it has been reported that fermentation
improves digestibility of cereals. Hamad & Fields (1979)
showed that natural fermentation of whole corn meal
increased the protein quality that was measured by %
relative nutritive value. Yousif & El-Tinay (2000) also
reported that the IVPD of naturally fermented corn
dough increased from 74.9% for the control to 93.5% for
24-h dough. It gradually decreased to 64.8% after 24 h.
The IVPD of four maize cultivars may be not necessary to
be improved by fermentation because the IVPD of four
Table 1 Effect of fermentation on amino acids content (% of dried sample) (mean ± SD, n=3)
B F*B S FS J2 FJ2 J3 FJ3
Thr
†
0.487 ± 0.032
à
0.752 ± 0.067
†
0.431 ± 0.034
à
0.616 ± 0.047
†
0.383 ± 0.032
à
0.649 ± 0.034
†
0.558 ± 0.061
à
0.888 ± 0.053
†
Val
†
0.614 ± 0.041
à
1.054 ± 0.097
†
0.584 ± 0.054
à
0.882 ± 0.067
†
0.506 ± 0.042
à
0.918 ± 0.067
†
0.716 ± 0.052
à
1.198 ± 0.087
†
Ile
†
0.427 ± 0.034
à
0.751 ± 0.064
†
0.436 ± 0.064
à
0.684 ± 0.054
†
0.384 ± 0.031
à
0.694 ± 0.035
†
0.510 ± 0.041
à
0.866 ± 0.067
†
Leu
†
1.219 ± 0.092
à
1.968 ± 0.156
†
1.462 ± 0.213
à
2.149 ± 0.187
†
1.240 ± 0.091
à
2.150 ± 0.170
†
1.445 ± 0.098
à
2.305 ± 0.170
†
Phe
†
0.453 ± 0.037
à
0.809 ± 0.087
†
0.464 ± 0.032
à
0.800 ± 0.067
†
0.432 ± 0.034
à
0.806 ± 0.078
†
0.592 ± 0.061
à
0.995 ± 0.074
†
Lys
†
0.375 ± 0.012
à
0.868 ± 0.079
†
0.308 ± 0.024
à
0.597 ± 0.074
†
0.268 ± 0.041
à
0.584 ± 0.034
†
0.419 ± 0.034
à
0.949 ± 0.086
†
His
†
0.312 ± 0.024
à
0.507 ± 0.065
†
0.410 ± 0.021
à
0.545 ± 0.054
†
0.307 ± 0.032
à
0.508 ± 0.044
†
0.317 ± 0.042
à
0.514 ± 0.034
†
Arg
à
0.472 ± 0.059
†
0.522 ± 0.061
†
0.342 ± 0.017
à
0.479 ± 0.044
†
0.307 ± 0.031
à
0.524 ± 0.045
†
0.417 ± 0.037
à
0.605 ± 0.053
†
Met
à
0.216 ± 0.018
à
0.384 ± 0.042
†
0.238 ± 0.019
à
0.344 ± 0.032
†
0.205 ± 0.017
à
0.361 ± 0.023
†
0.229 ± 0.009
à
0.399 ± 0.021
†
Asp
à
0.768 ± 0.056
à
1.245 ± 0.094
†
0.767 ± 0.087
à
1.050 ± 0.095
†
0.637 ± 0.071
à
1.043 ± 0.090
†
0.882 ± 0.057
à
1.445 ± 0.087
†
Ser
à
0.516 ± 0.032
à
0.873 ± 0.088
†
0.553 ± 0.064
à
0.813 ± 0.054
†
0.469 ± 0.036
à
0.833 ± 0.067
†
0.625 ± 0.043
à
1.023 ± 0.085
†
Glu
à
2.268 ± 0.112
à
3.315 ± 0.297
†
2.597 ± 0.211
à
3.567 ± 0.347
†
2.277 ± 0.197
à
3.622 ± 0.287
†
2.628 ± 0.314
à
3.829 ± 0.213
†
Gly
à
0.463 ± 0.033
à
0.800 ± 0.064
†
0.403 ± 0.032
à
0.629 ± 0.065
†
0.372 ± 0.025
à
0.666 ± 0.054
†
0.538 ± 0.041
àà
0.903 ± 0.075
†
Ala
à
1.111 ± 0.089
†
1.311 ± 0.099
†
0.938 ± 0.087
à
1.280 ± 0.097
†
0.764 ± 0.065
à
1.264 ± 0.099
†
1.191 ± 0.087
à
1.516 ± 0.092
†
Cys
à
0.128 ± 0.008
à
0.231 ± 0.017
†
0.139 ± 0.009
à
0.253 ± 0.014
†
0.137 ± 0.009
à
0.286 ± 0.014
†
0.132 ± 0.009
à
0.263 ± 0.042
†
Tyr
à
0.463 ± 0.035
à
0.710 ± 0.067
†
0.444 ± 0.054
à
0.682 ± 0.057
†
0.390 ± 0.021
à
0.712 ± 0.054
†
0.539 ± 0.034
à
0.876 ± 0.074
†
Pro
à
0.550 ± 0.012
à
0.945 ± 0.087
†
0.500 ± 0.064
à
0.776 ± 0.068
†
0.431 ± 0.036
à
0.775 ± 0.067
†
0.621 ± 0.045
à
1.068 ± 0.097
†
Means in the same row with different symbols are significantly different (P< 0.05).
*F, fermented.
†
Essential amino acid.
à
Nonessential amino acid.
Effect of fermentation on total phenolic content, phytic acid content L. Cui et al. 757
2012 The Authors International Journal of Food Science and Technology 2012
International Journal of Food Science and Technology 2012 Institute of Food Science and Technology

raw maize cultivars, ranged from 83.6% to 85.7%, will be
well enough.
Effect of fermentation on phytic acid
Phytic acid content of untreated four maize sample
was 476, 415, 379 and 387 mg per 100 g for J3, J2, S
and B, respectively. Fermenting of four maize sample
significantly (P< 0.05) reduced phytic acid content to
364 (23.6%), 392 (5.4%), 287 (24.3%) and 314 mg per
100 g (18.8% reduction) for J3, J2, S and B, respec-
tively (Fig. 3). Phytic acid content in untreated four
maize sample was found to be lower than 9.87 mg g
)1
DM in raw yellow maize (Ejigui et al., 2005),
7.1 mg g
)1
DM in Malawian white maize flour (Hotz
& Gibson, 2001) and 6.98 mg g
)1
DM in pounded
white maize flour (Hotz et al., 2001). These results
were similar to those observed for maize (Abedel-
Hady et al., 2005; Ejigui et al., 2005). Fermentation
reduced the phytic acid content also confirming the
study of Egounlety & Aworh (2003) who found the
reduction of 30.7% in soybean, 32.6% in cowpea and
29.1% in groundbean after fermentation with Rhizo-
pus oligosporus. After fermentation, the reduction in
phytic acid content may have partially been attributed
to the activity of phytase present in the microflora,
which hydrolyse phytate into inositol and orthophos-
phate (Ejigui et al., 2005). However, the optimum pH
for activity of cereal phytase ranges from 5.1 to 5.3
(Marfo et al., 1990). After 24-h fermentation, pH of
four maize sample was 5.50, 5.57, 5.43 and 5.39 for
J3, J2, S and B, respectively. After 48-h fermentation,
it was 4.01, 4.02, 3.97 and 3.90. Phytase was probably
denaturated or inhibited after 48-h fermentation. The
drop of pH to 4 contributed to the slow breakdown
of phytate, which may explain why all the phytate was
not removed.
Effect of fermentation on total phenolic content
Data on the effect fermentation on total phenolic
content of four maize samples is shown in Fig. 4. In
contrast to phytic acid, polyphenol content signifi-
cantly (P< 0.05) increased after fermentation. The
total phenolic content of untreated four maize samples
was 0.98, 0.95, 0.91 and 0.96 mg GAE ⁄g for J3, J2, S
and B, respectively. Fermenting of four maize sample
significantly (P< 0.05) increased total phenolic con-
tent to 1.19 (22%), 1.17 (22.5%), 1.10 (21.6%) and
1.18 mg GAE ⁄g (23.4% increase) for J3, J2, S and B,
respectively. Similar trend was observed during the
fermenting process of four cereals, namely buckwheat,
wheat germ, barley and rye (
Dordevic
´et al., 2010).
Contrary to our study, total polyphenolic contents
were reported to decrease during natural lactic acid
fermentation in pearl millet, moth bean, maize and
lentil (Dhankher & Chauhan, 1987; Abedel-Hady
et al., 2005; Bhandal, 2008). The increase in total
phenolic content found in the fermented samples
could be due to the bound phenolics being liberated
during fermentation (Sosulski et al., 1982; Bartolome
& Gomez-Cordoves, 1999). The decrease in phenolic
compounds during fermentation could also be due to
Figure 2 Effect of fermentation on in vitro protein digestibility
(IVPD).
Figure 3 Effect of fermentation on phytic acid content.
0
0.2
0.4
0.6
0.8
1
1.2
1.4
J3 J2 S B
Total phenolic content (mg g–1)
Before After
Figure 4 Effect of fermentation on total polyphenol content.
Effect of fermentation on total phenolic content, phytic acid content L. Cui et al.758
International Journal of Food Science and Technology 2012 2012 The Authors
International Journal of Food Science and Technology 2012 Institute of Food Science and Te chnology

the acidic environment and the reduced extractability
of the phenolic compounds (Towo et al., 2006).
Effect of fermentation on Colour values
After fermentation, J2 and S had a darker red colour
(lower L-value and higher a-values), but there is no
change on the colour values of J3 and B (Table 2). It is
the same as the result of Cuevas-Rodriguez et al.
(2004), who found that fermentation of quality protein
maize (QPM) tended to a slightly darker colour and
suggest it may be attributed to the influence of mycelia
colour and the drying step. But we suggest that the
increase in total phenolic content promotes the inten-
sity of the red colour. Osman (2011) observed a
significant increase in tannin content of pearl millet
after fermentation. As the Folin-Ciocalteu method,
which was used to determine the total amount of
phenolic compounds, is nonspecific, it has limitations
when used in fermentation studies. The significant
increase in total phenolic content after fermentation in
present work may be partly attributed to the increase in
tannin content (Fig. 4). There were reports suspected
that tannin had copigmentation effect to purple sweet
potato anthocyanin (Zhu et al., 2006), and colour in
maize was determined by anthocyanins and other
pigments (Trujillo et al., 2009).
Conclusion
This study showed that increases in protein and amino
acid (including Lysine) yield do occur, as a result of
fermentation. Thus, fermentation could be regarded as
viable mean for improvement of the protein quality of
four Chinese maize cultivars.
Acknowledgments
This research was financially supported by Independent
Innovation of Agricultural Sciences in Jiangsu Province,
China (CX [11] 2067).
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†
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†
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†
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†
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†
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†
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†
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†
16.6 ± 2.33
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†
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†
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†
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†
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†
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†
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International Journal of Food Science and Technology 2012 2012 The Authors
International Journal of Food Science and Technology 2012 Institute of Food Science and Te chnology