Lentil Starch Content and its Microscopical Structure
as Influenced by Natural Fermentation
Cristina Sotomayor and
Juana Frias Madrid (Spain), Jozef Fornal
and Jaga Sadowska, Olsztyn (Poland),
Gloria Urbano, Granada (Spain) and
Concepcion Vidal-Valverde, Madrid (Spain)
Lentil seeds (Lens culinaris var. vulgaris, cultivar Magda-20) were
allowed to ferment naturally at different lentil flour concentrations
(79 g/L, 150 g/L and 221 g/L) and temperatures (28 °C, 35 °C and
42 °C). During fermentation, samples were taken at 24 h intervals. The
changes in starch content in all samples were studied. Scanning electron microscopy (SEM) was used to investigate changes in samples fermented for 96 h at two different concentrations (79 g/L and 221 g/L) and
two different temperatures (28 °C and 42 °C). A considerable decrease
in starch content was observed at 0 h of fermentation, defined as the
time when the lentil flour was completly suspended at the established
temperature. Once fermentation began, flour concentration and temperature modified starch content. Fermentation brought about a general decrease in starch content and a 32–37 % dry matter content was found in
the samples after 96 h. Microscopical studies showed that endocorrosion, i.e., breakdown starting from the center of starch granules, was the
main pattern observed during lentil fermentation.
1 Introduction
that fermented lentil flour is an excellent source of protein
and that natural fermentation removed a high amount of
trypsin inhibitor activity, tannins, α-galactosides and phytic
acid. Although most studies reported on natural fermentation
have been related to protein quality and the elimination of
some antinutritional factors, the full potential of natural fermentation on legumes is still unknown.
The present work investigates the modification in starch
content and starch’s microscopical structure that occurs during natural fermentation of lentils at different times, temperatures and concentrations of flour.
Dry lentils seeds are a good source of high quality protein,
vitamins, and a balanced range of minerals. They are also an
excellent source of complex carbohydrates and dietary fibres
[1]. Lentil seeds, which are highly accepted in most parts of
the world, provide one of the best means of fighting malnutrition among people in developing countries [2]. In several
countries, reduction in the consumption of legumes in general, and lentils in particular, has been related to the presence
of antinutritional factors in these legumes. Cheap methods
are required to improve nutritional quality, by either removing antinutritional compounds or by raising the levels of nutritional enhancers.
Traditional methods such as germination and fermentation tend to improve the nutrient quality of foods. Fermentation is generally achieved by native microflora. Fermented
food is a widely exploited source of valuable protein. Among
the legumes, soybeans have been extensively used for this
purpose [3], although other legumes such as beans and
chickpeas are also occasionally used [4]. Fermentation is
associated with many chemical changes that enhance
organoleptic response, contents of free sugars and vitamins,
as well as bioavailability of minerals [5, 6], and results in the
breakdown of some of the antinutritional endogenous compounds [7–11]. Ikenebomeh [12] found that the levels of reducing sugars and soluble nitrogen in African locust bean
gum increased dramatically as a result of natural fermentation. Beuchat et al. [13] proposed peanuts and cowpeas as
acceptable substrates for the preparation of natto-like products. In lentils, Ragaee et al. [14] observed that natural fermentation for 4 days at 32 °C increased the availability of
total amino acids and improved in-vitro protein digestibility.
These authors [15] also reported a good consumer acceptance of products formulated from fermented lentils, while
Mahaja and Chauhan [16] noted that natural fermentation
improved the HCl-extractability of minerals including calcium, magnesium and copper in pearl milled flour. VidalValverde et al. [8, 17] have also shown that natural fermentation of lentils caused an increase in vitamin content and an
improvement in the available starch:total starch ratio. Tabera
et al. [9], Frias et al. [10] and Kozlowska et al. [11] reported
152
Starch/Stärke 51 (1999) Nr. 5, S. 152–156
2 Materials and Methods
2.1 Sample preparation
Lentil seeds (Lens culinaris var. vulgaris, cultivar Magda20, from Albacete, Spain, harvested in 1992), were finely
ground in a ball mill and sieved; the 0.050–0.250 mm fraction was collected to carry out the fermentation experiments
as described in previous papers [9–11]. The flour was suspended aseptically in tap water at concentrations and temperatures shown in Tab. 1, which is based on a 22 complete
factorial design with three replicate centerpoints [18]. The
lentil flour was allowed to ferment naturally for 4 days without aeration in a stirred fermentor (Infors ISF-100, Infors
AG, Switzerland) using only the microorganisms that were
present on the seeds. Zero time, which was defined as the
time when the flour was completely suspended while stirring
at the controlled temperature, occurred 10–40 min after
Tab. 1. Experimental conditions for the selected natural fermentation
batches of lentils.
Batches
Temperature (°C)
Concentration (g/L)
F1
28
79
F2
42
79
F3
28
221
F4
42
221
F5
35
150
© WILEY-VCH Verlag GmbH, D-69451 Weinheim, 1999
0038-9056/99/0505-0152$17.50+.50/0
placing the mixture in the fermentor. Samples were collected
daily and freeze-dried for analysis.
2.2 Determination of starch content
500 mg of raw and fermented samples were suspended in
50 mL of 80 % ethanol, boiled under reflux for 15 min,
cooled and filtered through a no. 4 sintered glass funnel. The
residue was extracted two additional times and washed with
distilled water until a negative Mölisch’s test was obtained
[19]. The residue was used for starch determination using a
procedure based on total enzyme digestion of starch to glucose [20]. Glucose content was measured by the method of
Dalquist [21].
2.3 Scanning electron microscopy
Scanning electron microscopy was performed on raw
lentils and on lentils fermented for 96 h at 79 g/L and 28 °C
(F1), at 79 g/L and 42 °C (F2), at 221 g/L and 28 °C (F3), and
at 221 g/L and 42 °C (F4). Lyophilized flour particles were
placed on double-stick adhesive tape mounted on aluminium
stubs. The samples were subjected to a nitrogen stream to remove unattached particles and then coated with carbon and
gold in a vacuum evaporator JEOL JEE 4X. Scanning electron micrographs were taken on ILFORD film using a JEOL
JSM 5200 microscope operated at an accelerating voltage of
5 and 10 kV.
2.4 Statistical analysis
Multifactor analysis of variance using multiple range test
was applied to the data using Statgraphics Statistical Graphics System Software, rel. 5.
3 Results and Discussion
3.1 Effect of fermentation on starch content
Tab. 2 shows the starch content in raw and fermented
lentils at different concentration and temperature conditions.
The starch content in raw lentil seeds was 51 % of dry matter
(d.m.). This value is in the range of data reported in the literature [1, 2, 22–24]. The sample preparation, i.e., the time required to reach the selected fermentative temperature for the
lentil flour suspension (0 h), sharply affected the starch content. Starch content decreased drastically during this step,
and starch retentions between 58–75 % were observed. During this sample preparation step, lentil flour concentration
and temperature strongly influenced the drop in starch content. The largest decreases in starch concentration were observed at the highest temperature, i.e., 42 °C (F2 and F4), be-
ing maximum at the lowest concentration, 79 g/L (F2). During the soaking process used for the sample preparation,
some metabolic reactions take place which affect carbohydrate content [25]. Therefore, this sample preparation step
might modify lentil starch content, and it could be influenced
by concentration and temperature conditions.
After 24 h of fermentation, an increase in starch content
was obtained compared to that found at 0 h; no significant
differences (p ≤ 0.05) within fermentative batches were
found (Tab. 2). A longer fermentation time (48 h) led to a further reduction in starch content in the batches with the minimum lentil flour concentration, irrespective of temperature
(F1 and F2). No significant differences occurred (p ≤ 0.05) in
the fermentation experiments carried out at the highest concentration, irrespective of temperature (F3 and F4). However,
a noticeable increase in starch content was found for those
centerpoints carried out at 150 g/L and 35 °C (F5; Tab. 2).
After 72 h of fermentation, an increase in starch content was
achieved in the batches fermented at the lowest concentration (F1 and F2), reaching levels found for fermentation
experiments performed at the highest concentration (F3 and
F4). The starch content increased sharply in batches fermented at a concentration of 150 g/L and 35 °C (F5; 89 % retention). The combined effects of temperature and concentration were more pronounced after 96 h of fermentation.
Starch content suffered a general decrease after 96 h, whereas retentions ranging from 63 % to 73 % were obtained; only
significant differences (p ≤ 0.05) within fermentation conditions at 96 h carried out at the lowest concentration and the
highest temperature were found (32 % starch d.m.).
No information has been found about the effect of fermentation of legumes on their starch content. The results
presented in this paper show that during the natural fermentation procedure fluctuations in starch content of lentils were
observed. These changes could be partly related to the effect
of fermentation in other lentil constituents. Kozlwoska et al.
[9], who worked with the same set of samples, reported a
gradual decrease in the inositol phosphates content during
natural fermentation of lentils for 96 h and maximum reductions were found at a concentration of 79 g/L. Tabera et al.
[9] reported a slight increase in protein content during natural fermentation of lentils. These authors also observed a noticeable decrease in trypsin inhibitor activity (TIA), although
maximum TIA reductions (63 %) were reached at the lowest
concentration (79 g/L) and the highest temperature (42 °C).
Frias et al. [10] reported that natural fermentation of lentils
brought about a general decrease in soluble carbohydrates.
These authors observed a sharp decline in soluble carbohydrate content after 24 h. These compounds are used as a
Tab. 2. Total starch content during natural fermentation of lentils.
Batch
Temp.
(°C)
F1
28
Conc.
(g/L)
79
Raw lentil
starch
conc.
(%)
51.47 ± 0.87
Fermentation time
0h
Starch conc.
24 h
Starch conc.
(%)
48 h
Starch conc.
(%)
a
34.64 ± 1.041
72 h
Starch conc.
(%)
36.66 ± 1.083
a
(%)
a
39.77 ± 1.482
96 h
Starch conc.
a
(%)
a
35.50 ± 1.3013ab
a
39.66 ± 2.622
F2
42
79
51.47 ± 0.87
30.02 ± 0.91
39.23 ± 0.901
36.02 ± 1.38a
40.05 ± 1.121
32.05 ± 1.46
F3
28
221
51.47 ± 0.87
36.35 ± 1.00ab
40.23 ± 1.261a
39.60 ± 1.841b
40.50 ± 1.121a
34.20 ± 1.82a
F4
42
221
51.47 ± 0.87
33.68 ± 0.62a
39.36 ± 1.021a
39.50 ± 1.001b
40.37 ± 1.281a
37.14 ± 1.43b
42.32 ± 1.46
46.87 ± 3.11
35.19 ± 1.19a
F5
35
150
51.47 ± 0.87
38.43 ± 4.381
b
39.81 ± 2.021
a
Values are the mean of 6 determinations ± standard deviation. Same superscript/subscript in the same column/row indicates no significant differences (p ≤ 0.05).
Starch/Stärke 51 (1999) Nr. 5, S. 152–156
153
source of energy and carbon during fermentation. Thus, the
gradual rise in starch content (on a percentage basic) noted at
the first stage (24 h) of lentil fermentation could be related
to the decrease in soluble carbohydrates. Once easily fermentable soluble carbohydrates were consumed, starch
could be degraded more extensively during the last stages.
This would account for the sharp drop in starch content
found mainly between 72 and 96 h of lentil fermentation.
Natural fermentation of lentils with a consistent decrease
in pH is characteristic for lactic acid microorganisms. With
acidification during fermentation profuse growth of lactic
acid bacteria occurs. Giraud et al. [26] reported that some
strains of Lactobacillus are able to break down raw starch
isolated from cassava (Manihot esculenta, var. Ngansa) by
alpha amylase enzymatic attack. They found that after 3 days
of fermentation 41 g of lactic acid were produced from 45 g
of starch. Reddy and Salunkhe (1980) reported that lactic
acid microorganisms involved in the natural fermentation
of lentils exhibit alpha amylase activity which could hydrolyse the starch content. During natural fermentation of lentils,
Villa [27] found the presence of Lactobacillus and Pediococcus strains to be predominant in fermented samples
which were involved in the degradation of storage compounds (carbohydrates) of lentil seeds. Umeta and Faulks
[28] fermenting two types of Tef (small seeded millet-like
cereal grain indigenous to Ethiopia) found that the starch
was utilised as the main energy source by the fermentation
organisms, resulting in a 9 % loss of starch in both types of
Tef. Vidal-Valverde et al. [8] observed a decrease in total and
available starch during lentil fermentation at a concentration
of 100 g/L and at 30 °C, although the relative availability of
the remaining starch (available starch:total starch ratio) improved after 96 h.
microstructure is shown in Fig. 2A. Starch granules were
characterized by having smooth surfaces with only few adhering protein particles. In the centre of Fig. 2 an open starch
granule, resulting from ball milling, is discernible. The granule evidently keeps the internal integrity, but a cavity in the
middle might be an evidence of structural changes during
fermentation. Fig. 2B shows an enlarged view of a broken
starch granule with a deep internal cavity showing very distinct lamellae on the cross-section. Fermentation conducted
A
B
3.2 Effect of fermentation of the ultrastructure of
starch granules
A scanning electron micrograph of unfermented lentil
flour is shown in Fig. 1. Starch granules of diameter ranging
from 3 to 30 µm and differing in shape from ovoid to spherical were the main components of the flour. On the surface of
granules numerous globular or irregular particles were distinguished which could be protein bodies or fragments of
protein matrix disrupted during milling.
The effect of lentil fermentation, performed at a concentration of 79 g/L and at 28 °C for 96 h (F1), on starch granules
C
Fig. 1. Scanning electron microscopy of unfermented lentil flour.
S = starch granules, PB = protein bodies.
154
Fig. 2. Scanning electron microscopy of lentil flour fermented for 96 h
at a flour concentration 79 g/L at 38 °C (A and B) and at 42 °C (C).
PM = protein matrix, arrows and arrow heads indicate internal cavities
and lamellae, respectively.
Starch/Stärke 51 (1999) Nr. 5, S. 152–156
at higher temperature (42 °C; F2) did not change the microscopic aspect of the starch granules (Fig. 2C). The smooth
surface of some granules is covered by an adhering thin film
or thick fragments of the residual protein matrix. Single distinguishable protein bodies seem to form elongated strands.
Unfortunately, a partly broken starch granule was curtained
by some structural materials making the evaluation of the interior of the cavity difficult.
Fermentation conducted at a concentration of 221 g/L and
at 28 °C (F3) resulted in more visible changes in the microscopic picture of lentil flour components (Fig. 3A). The most
A
B
striking impression was the presence of a dense protein matrix with embedded, partly denatured protein bodies. Starch
granules or their fragments show an empty interior. Only one
starch granule from the microphotographs presented and
which is not covered by protein, shows the cavities that
could either be the effect of erosion or of shearing forces during milling. A micrograph of lentil flour fermented at 42 °C
is shown in Fig. 3B. Two open starch granules are discernible
of about 30 µm in diameter. The empty interior can be observed in both of them, but only the upper one apparently has
a slight lamella just under the enveloping layer. In the other
granule, minute external cavities can be observed in the
granule envelope, but they do not penetrate into the interior
of the granule. Fig. 3C shows an enlarged view of two starch
granules which were disrupted during fermentation, milling
and lyophilization. The internal structure of the starch granule is similar to that presented in Fig. 2B because of its
slightly marked lamellae. The bisected granule had some radially arranged shadows, possibly the structural elements of
the granule.
The changes in lentil starch during lentil fermentation
could probably be associated with different pH values, as reported by Frias et al. [10]. The pH values are 3.8 for lentils
fermented at a concentration of 79 g/L and 4.6 for those fermented at 221 g/L, which may cause either solubilization of
protein (pH 3.8) (Fig. 2A) or, according to Tovar and Asp
[29], precipitation (pH 4.6) of protein on the surface of starch
granules (Fig. 3A). Based on SEM observations, enzymatic
attack that starts from the periphery of the granule (exocorrosion) is not necessarily involved in the starch breakdown
during fermentation, as it has been described during germination [30, 31]. We are of the opinion that endocorrosion
rather than exocorrosion is the main attack pattern during
lentil fermentation. Endocorrosion has been previously reported by Planchot et al. [32] to occur in starch granules
from different sources treated in vitro by bacterial alpha
amylase. Giraud et al. [26] evidenced an enzymatic attack
studying changes in cassava starch granule structure during
fermentation with Lactobacillus plantarum A6 by SEM.
They also observed large cavities in granules with rough surface similar to those observed in the present investigation.
4 Conclusions
C
Natural fermentation of lentils is a good procedure to improve the nutritive value of lentils. Even under those conditions in which the lowest antinutritive factor content was
achieved (79 g/L and 42 °C) according to previous papers,
the starch retention is still high (62 %). These improvements
in the quality of fermented lentil flour could have wide applications in human nutrition. From microscopical studies,
endocorrosion seems to be the main reaction pattern observed in lentil starch granule after 96 h of natural fermentation.
Acknowledgments
This work has been supported by the Spanish Comision Interministerial de Ciencia y Tecnologia ALI96-0480 and by Copernicus Network
FU (Contract No. IC15 CT96 1007). The authors are indebted to Dr.
Tabera for providing the fermented lentil seeds. This study is part of the
Ph.D. Dissertation work of C. Sotomayor.
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Fig. 3. Scanning electron microscopy of lentil flour fermented for 96 h
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Addresses of Authors: C. Sotomayor, Ph.D., J. Frias, Ph. D. and
C. Vidal-Valverde*, Ph.D., Instituto de Fermentaciones Industriales
(CSIC), Juan de la Cierva 3, 28006 Madrid, Spain. J. Fornal, Ph.D. and
J. Sadowska, Ph.D., Polish Academy of Sciences, Division of Food
Science (IAR & FR), 10-718 Olsztyn 5, Poland. G. Urbano, Ph.D.,
Universidad de Granada, Facultad de Farmacia, Instituto de Nutrición,
Departamento de Fisiología, Cxampus Universitario de Cartuja s/n,
18071 Granda, Spain.
* Corresponding author.
(Received: February 24, 1999).
Starch/Stärke 51 (1999) Nr. 5, S. 152–156