Fuel 144 (2015) 9095

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Fuel
journal homepage: www.elsevier.com/locate/fuel

The mass transfer of sugar in sweet sorghum stalks for solid-state

fermentation process
Yueying Mao a,b,c, Jihong Li a,b,c,, Shizhong Li a,b,c,, Sandra Chang a,b,c, Gang Zhao a
a

Institute of Nuclear and New Energy Technology, Tsinghua University, Beijing, Peoples Republic of China
Beijing Science and Technology New Innovations Development Base Project, Beijing, Peoples Republic of China
c
MOST-USDA Joint Research Center for Biofuels, Beijing, Peoples Republic of China
b

h i g h l i g h t s
 A modied kinetic model was developed to describe the sugar transfer of sweet sorghum.
 The modied kinetic model was the rst related to the structure of sweet sorghum stalks.
 The modied kinetic model was well tted to the extraction process.

a r t i c l e

i n f o

Article history:
Received 11 November 2014
Received in revised form 3 December 2014
Accepted 8 December 2014
Available online 20 December 2014
Keywords:
Solid state fermentation
Kinetic model
Sweet sorghum
Sugar

a b s t r a c t
Solid-state fermentation of sweet sorghum stalk is a cost-effective technology for bioethanol production.
Sugar transfer from the interior of sweet sorghum plant cell to the surface is one of the key factors affecting the fermentation process because the system takes place in the absence of free water. Mass transfer of
sugar from the interior of the sweet sorghum to the surface of substrates is mainly driven by the sugar
concentration gradient. A mass transfer model based on three steps process was developed. Taking into
consideration of the different tissue structures of sweet sorghum stalks, a two simultaneous rst-order
kinetic model of sugar transfer with two parameters characterizing the tissue structure difference was
developed to describe the sugar transfer process in sweet sorghum. Solid-liquid extraction experiments
were used to gather experimental kinetics data of sugar transfer. Four factors impacting the mass transfer
of sugar including particle sizes, stirring speed, temperature, and osmotic pressure were investigated. The
results showed that the newly modied model tted well the kinetics of sugar transfer in different
varieties of sweet sorghum. This model could be helpful in optimizing solid state fermentation of sweet
sorghum stalks. Moreover, the kinetic model with the added structural parameters based on difference in
plant tissue structure can also be used to describe the extraction of any active substance from types of
feedstocks with similar chemical compositions and biomass structures.
2015 Elsevier Ltd. All rights reserved.

1. Introduction
The depletion of fossil fuel and environmental concerns has
focused worldwide attention on research for energy crops suitable
for ethanol production [13]. Sweet sorghum is attractive as a nonfood feedstock for biofuel production because it is easily adaptable
to diverse climate and soil conditions [4,5]. It is a C4 plant
characterized by high photosynthetic efciency, high fermentation

Corresponding authors at: Institute of Nuclear and New Energy Technology,

Tsinghua University, Beijing, Peoples Republic of China. Tel./fax: +86 10 8019 4050.
E-mail addresses: maoyy12@mails.tsinghua.edu.cn (Y. Mao), tjlijh@mail.
tsinghua.edu.cn (J. Li), szli@tsinghua.edu.cn (S. Li), sandrahchang@gmail.com
(S. Chang).
http://dx.doi.org/10.1016/j.fuel.2014.12.023
0016-2361/ 2015 Elsevier Ltd. All rights reserved.

sugars and high yield of green biomass (with 2030 dry tons/ha). It
has low requirements for fertilizer, high efciency in water usage
(1/3 that of sugarcane and 1/2 that of corn), and a short growth
period of 120150 days [6].
Solid-state fermentation (SSF) has become a promising technology to convert biomass into bioethanol due to its relatively simple
process, low energy consumption and low wastewater production
[5,7]. However, the SSF process has limits due to its particular
operational conditions [8]: it is a heterogeneous system without
free water, and growth of contaminated microorganisms.
The performance of SSF is affected by many factors, such as particle size, temperature, stirring speed and moisture [8]. In the SSF
technology, each individual sweet sorghum particle could be
regarded as a single fermentation unit. The mass transfer of sugar

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Y. Mao et al. / Fuel 144 (2015) 9095

in each unit is critical for optimization of the production process.

Unfortunately, the mass transfer of sugar in this system has not
been studied.
Although no free water was observed in the SSF technology,
mass transfer of sugar occurred in particles with water moisture
above 70% [9]. In each particle unit, the sugar diffusion is driven
by the sugar gradient between the interior and exterior of the particle. Because the apparent mass transfer of sweet sorghum sugar
was originated from the adduct of each micro unit, the kinetic of
sugar transfer in SSF process of sweet sorghum was investigated
by solid-liquid extraction experiments. In the present paper,
various factors impacting the sugar transfer from sweet sorghum
cells to the surface in SSF were studied. These factors included
particle size, stirring speed, osmotic pressure and temperature.

concentration, C1 = C1/C1, C1 was the nal solute concentration

in the solution due to the broken and surface cells alone,
C2 = C2/C1, C2 was the nal solute concentration in the solution
due to the intact cells alone, k1 (min1) was the rate constant for
broken and surface cells and k2 (min1) was the rate constant for
the intact cells.

2.5. Statistical analysis

The model parameters were determined by non-linear
regression to the experimental data using data analysis software
Origin 8.5(Origin Lab Corporation, USA).

3. Results and discussion

2. Materials and methods

3.1. Model of sugar transfer in the solid-state fermentation of sweet

sorghum

2.1. Sweet sorghum

Two sweet sorghum varieties were used. Chuntian # 1 was harvested in Cangzhou, Hebei. H110 was harvested in Shijiazhuang,
Hebei. Leaves and husks were removed from the fresh stalks by
hand and the stalks were stored at ambient temperature with bacteriostatic agent for long-term storage. All sweet sorghum were
gifted by the Institute of Millet of Hebei Academy of Agriculture
and Forestry. The sweet sorghum stalks without the bark were
cut into cylinder with heights of 2, 4, 6, 8, 12, 16 mm. The diameter
of cylinder was about 22 2 mm.
2.2. Analytical method
Total sugar contents (glucose, fructose and sucrose) were analyzed by owing injection analyzer (FIA) (AA3, SEAL, Germany).
Thirty grams of sweet sorghum particles were stirred in a blender
with 300 mL distilled water at room temperature for 2 min. The
mixture was sonicated for 15 min. The clear supernatant liquid
was used to measure the concentration of sugar. The experiments
were carried out in triplicates.
2.3. Solid-liquid extraction experiments
A beaker with 300 mL water was preheated for 30 min in a water
bath at the experimental temperature. The sweet sorghum particles
(20 g) were added to the beaker, incubated at the stated experiment
temperature until the end of the extraction experiments. The beaker
was sealed with a piece of plastic lm to avoid water lost during the
experiment. One mL of solution was taken out to determine the
sugar concentration at the indicated times. Experimental conditions
were varied as stated with six particle sizes (2, 4, 6, 8, 12 and 16 mm),
four stirring speeds (100, 250, 500 and 750 Rpm), four kinds of osmotic pressure (1.2, 1.4, 1.9, 2.2  103 KPa) and ve temperatures (20,
30, 40, 50 and 60 C). All experiments were repeated in triplicates.
Extraction kinetics of sugar from sweet sorghum was monitored
by sugar concentration in the solution.
2.4. Kinetic model

In contrast to liquid fermentation, there is no continuous liquid

phase in SSF. SSF involves the growth of microorganisms on moist
substrates in the absence of free water, which makes the system
quite different from submerged fermentation (SmF) [13]. In particles with water moisture above 70%, sugar transfer from the interior of sweet sorghum plant cell to the surface is driven by sugar
concentration gradient. The schematic diagram of sugar transfer
in a sweet sorghum particle was shown in Fig. 1. From the microscopic view, the sugar transfer from the interior to the surface of
substrates through the plant cell membrane is driven by the concentration gradient. The sugar transfer from each particle takes
places in three steps. The rst one is the sugar migration from
the interior to the exterior of the plant cell. The second is moving
into the interface between the solid substrate, the plant cell wall,
and the liquid phase on the surface of the plant cell. This interface
is dened as the liquid membrane. The third is dissolving into the
bulk liquid phase on the surface. However, it is so thin liquid lm.
Although the system seems to be complex, the kinetic parameter is
described by a simple diffusion model because the driven force of
the entire system is sugar concentration gradient.
The yeast, Saccharomyces cerevisiae, grows in the thin liquid lm
at the particle surface and reproduces asexually by budding. It does
not extend into the gaseous region or inside of substrate like other
fungi [14]. Fermentable sugars are extracted continuously from
sweet sorghum substrate and consumed simultaneously by yeast.
In SSF, sugar consumption by the propagation and metabolism
of yeast creates the concentration gradient, which drives the
continuously sugars diffusion to the surface of the particles. In this

Sugar solution
Liquid membrane
Sweet sorghum cells

Sugar
Yeast

2
1

The kinetic models used in this study is list below.

Two simultaneous rst-order kinetic model was described by
the following equation [1012]:

C  C 1 1  ek1 t C 2 1  ek2 t

where C = C/C1, C was the solute concentration in the solution

during the extraction process, C1 was the equilibrium solute

Fig. 1. Structure of SSF systems at the microscopic scale and local mass transport
processes for sweet sorghum fermentation process. The processes occurring are 1,
sugar transferring from the interior of plant cell to the surface of substrates; 2, sugar
diffusion through liquid membrane and consumed by yeast. 3, bulk liquid phase
diffusion.

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Y. Mao et al. / Fuel 144 (2015) 9095

paper we modeled the mass transfer of sugar from sweet sorghum

cells to the surface by rst-order model of diffusion.

C  C 1 1  ek1 t C 2 1  ek2 t

3.2. The structure of sweet sorghum stalks

The stem bark and pith of sweet sorghum stalks are quite distinct in their chemical and the structure composition [15]. They
also have different machinability [16]. Stem bark and vascular
bundles have long and exible lignocellulosic bers, while the
pith has relatively loose bers and contain more parenchymal
cells. We hypothesize that the different structure of stalk maybe
affect the mass transfer of sugar, so the sweet sorghum stalks
was separated in to two zones according to the distinct morphological features. Base on the distinct density of the cell in the
sweet sorghum stalks, we separated the sweet sorghum stalk into
two zones.
The diagram was shown in Fig. 2, with the two zones marked as
A and B. The percentage of Zone A and B tissues was determined by
measuring the sugar concentration and weight of each zone. In
order to test our hypothesis, the extraction experiment was conducted for each zone. In Fig. 3 it was observed the mass transfer
rate of Zone A and B was quite different. This result approved
our previous hypothesis. Therefore the sugar transfer rate in the
sweet sorghum stalks could not be regarded as if the entire stalk
is homogeneous. Based on results from tissue measurements of
the sweet sorghum stalks, two simultaneous rst-order kinetic
model was developed. The equation of this model was listed as
follows.

Fig. 2. The cross section of sweet sorghum stalks (Zone A refers to the compact
structure with green color due to containing chloroplasts in the stalk. Moreover, the
vascular bundles in this zone are smaller and the tissue structure is dense. Zone B
refers to the soft structure with white color in the stalk. The vascular bundles in this
zone are bigger and the tissue structure is sparse). (For interpretation of the
references to colour in this gure legend, the reader is referred to the web version of
this article.)

100
80
Permeability. %

Two simultaneous rst-order kinetic model was described by

the following equation:

where C1 and C2 were related to the percentage of Zone A and B in

the stalks respectively.
The values of C1 and C2 were conrmed by the sugar concentration and weight of the zones. Different varieties of the sweet sorghum have different values. In this paper, two varieties of sweet
sorghum Chuntian #1 and H110 were investigated.
First, the kinetic model of the sweet sorghum was studied using
Chuntian #1. In order to conrm the value of C1 and C2, we selected
30 stalks to test the sugar concentration and weight in the two
areas. The result was that 75.24% of the stalks weight and sugar
was contributed from zone A, and the rest from zone B. So the
parameters C1 and C2 in the two simultaneous rst-order model
were substituted by the values obtained from structure analysis
of sweet sorghum stalks. The equation could be modied as follows
when we studied the mass transfer of the sugar using the sweet
sorghum sample of Chuntian 1#:

C  0:25  1  ek1 t 0:75  1  ek2 t

Various factors impacting the sugar transfer in SSF of sweet sorghum were studied by the modied model in the following
sections.
3.3. Effect of particle size
The impact of different particle sizes 2, 4, 6, 8, 12, 16 mm of
sweet sorghum stalks in sugar transfer was investigated. The sugar
extraction curves for different sweet sorghum stalk particle sizes
were shown in Fig. 4(a). As can be seen, the smaller particle sized
stalk reach the equilibrium faster. A similar observation was
reported by Goula AM [17], who studied the ultrasound-assisted
extract oil from pomegranate seeds observed that smaller particle
size shortened the extraction time to achieve the highest yield. As
particle size decreased the mass transfer distance shortened thus
with the shorter distance less time was needed. In addition, smaller size also meant that more surface area was exposed to the
solvent.
The mass transfer parameters of the sugar in the sweet sorghum
stalks was calculated by the modied two simultaneous rst-order
kinetic model. Because the sample was Chuntian #1, the value C1
and C2 used in this equation was 0.250.75. The results were
shown in Table 1 and Fig. 4(a). The results demonstrate that this
model tted the data very well. All the R2 of the t curve were
greater than 0.99 with exception of the 16 mm which also had a
high R2 value of 0.964. Moreover, the parameter k1 and k2 describing the extraction rate decreased with the increase of particle size.
The results demonstrated that the modied kinetic model tted
the data from the sugar transfer in the sweet sorghum very well.
3.4. Effect of stirring speed

60

40
B
A
Whole stalks

20
0
0

100

200

300

400

Extraction time, min

Fig. 3. The extraction kinetic of A, B and the whole stalks.

The effect of stirring speed on the kinetics of the sugar transfer

in sweet sorghum was studied using 2 mm samples of Chuntian #1
at 30 C. A series of stirring speeds of 100, 250, 500, 750 Rpm were
investigated. The results, as seen in Fig. 4(b), shows that increasing
stirring speed accelerated the extraction rate. This was attributed
to the fact that the sugar on the surface of the particles could diffuse into the solution more quickly under stirring, and generated a
large concentration gradient at the local surface of the particles.
The tting results of the modied kinetic models with different
stirring speeds were shown in Table 2. The modied kinetic model
showed an excellent t to the experimental data. The rate constant

93

100

100

80

80

Permeability ( %)

Permeability , %

Y. Mao et al. / Fuel 144 (2015) 9095

2mm
4mm
6mm
8mm
12mm
16mm
fitting of 2 mm
fitting of 4 mm
fitting of 6 mm
fitting of 8 mm
fitting of 12 mm
fitting of 16 mm

60

40

20

0 rpm
100 rpm
250 rpm
500 rpm
750 rpm
fitting of 0 rpm
fitting of 100 rpm
fitting of 250 rpm
fitting of 500 rpm
fitting of 750 rpm

60

40

20

0
0

200

400

600

800

1000

50

100

Extraction time, min

150

200

250

300

350

Extraction time, min

(a)

(b)

100

100

80

80

Permeability , %

Permeability , %

20 C
30 C
40 C
50 C
60 C
fitting of 20 C
fitting of 30 C
fitting of 40 C
fitting of 50 C
fitting of 60 C

60

40

20

50

100

150

200

250

300

1.2x10 KPa
3

1.4x10 KPa

60

1.9x10 KPa
3

2.2x10 KPa
3

fitting of 0x10 KPa

3

fitting of 1.2x10 KPa

40

fitting of 1.4x10 KPa

3

fitting of 1.9x10 KPa

3

fitting of 2.2x10 KPa

20

0
0

0x10 KPa

350

400

Extraction time, min

0
0

50

100

150

200

250

300

350

400

Extraction time (min)

(c)

(d)

Fig. 4. The effect and tting results of particle size (a), stirring speed (b) temperature (c) and osmotic pressure (d) during sugar extraction from sweet sorghum.

Table 1
The tting results of the modied kinetic model with different particle sizes.
h (mm)

k1 (min1)

k2 (min1)

R2

Permeability

2
4
6
8
12
16

0.12
0.093
0.059
0.040
0.033
0.026

0.013
0.0087
0.0067
0.0044
0.0029
0.0017

0.997
0.998
0.997
0.994
0.997
0.964

97.4
90.6
91.7
93.1
90.4
85.9

h is the sweet sorghum cylinder height.

Table 2
The tting results of the modied kinetic model with different stirring speeds.
Rpm

k1 (min1)

k2 (min1)

R2

Permeability

0
100
250
500
750

0.12
0.15
0.18
0.34
0.38

0.014
0.015
0.018
0.019
0.021

0.988
0.992
0.998
0.996
0.982

96.8
96.6
99.7
99.9
98.7

Rpm is the stirring speed: revolutions per minute.

k1 and k2 increased with increasing stirring speeds. Moreover,

compared with the results of particle size, the value of k1 and k2
both increased one order of magnitude. The results suggested that

stirring promoted the diffusion of the sugar to increase the

concentration gradient. So this provided further evidence that the
essential driving force for transfer of sugar in the sweet sorghum
was concentration gradient.
3.5. Effect of temperature
The effect of temperature on the kinetics of the sugar transfer in
the sweet sorghum was studied using 2 mm samples of Chuntian
#1. A series of temperatures of 20, 30, 40, 50, 60 C were investigated. The results were shown in Fig. 4(c). The results showed that
increasing temperature accelerated the extraction rate. This was
attributed to the fact that the increasing temperature promoted
the molecular diffusion of sugar. This result also conrmed that
our kinetic model, which was based on the diffusion, was accurate.
The tting results of the modied kinetic models with different
temperature were shown in Table 3. The tting results showed a
good t for the experimental data (R2 > 0.9). Moreover, the value
of k1 and k2 increased with the increase of temperature at the same
extent. Again the data pointed to a difference in concentration
gradient as the driving force for sugar transfer.
Under the same conditions, the other kinetic model generally
used in the extraction, such as rst order kinetic model [18] was
not a good t to the experimental data. The results were shown

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Y. Mao et al. / Fuel 144 (2015) 9095

Table 3
The tting results of the modied kinetic model with different temperatures.
T (C)

k1 (min1)

k2 (min1)

R2

Permeability

20
30
40
50
60

0.089
0.12
0.24
0.28
0.38

0.0064
0.011
0.013
0.019
0.025

0.961
0.980
0.993
0.993
0.994

85.5
95.6
96.7
99.1
99.5

is appropriate to describe the sugar transfer in different varieties

of sweet sorghum. For modeling extraction of active substance in
plants, the specic tissue structure of the different plants is problematic for researchers. The kinetic model based on taking into
consideration of different tissue structure is signicant to studying
the extraction kinetic of active substance from different plants.
4. Conclusion

in Supplementary Table 1. The rate constant kobs increased with the

increase of temperature. This meant that extraction rate increased
when the temperature rose. However, the value of kobs at 40 C was
the same as 50 C. This phenomenon was different compared with
what was reported in literature [19,20]. So the rst order kinetic
model could not adequately describe the sugar extraction from
sweet sorghum stalks in terms of temperature.
3.6. Effect of osmotic pressure
The effect of osmotic pressure on the kinetics of the sugar transfer in the sweet sorghum was studied using 2 mm samples of
Chuntian #1 at 30 C. The extraction solvent with different osmotic
pressure of 0, 1.2, 1.4, 1.9, 2.2  103 KPa were used. The extraction
data was shown in Fig. 4(d). The modied kinetic model was tted
to the data from different sugar concentrations in the solvent as
shown in Table 4. At high osmotic pressure, the kinetic model also
exhibited good t to the sugar transfer in the sweet sorghum. All
the R2 of the tting curves were more than 0.92. Moreover, the
value of k1 and k2 calculated by the model decreased as the osmotic
pressure increased. The results demonstrated that the modied
kinetic model tted the experimental data well.
Under the same conditions, the other kinetic model generally
used in the extraction, such as second order kinetic model [21],
did not t the experimental data well. The results were shown in
Supplementary Table 2. The tting results of second-order model
were poor, especially for the 2.2  103 KPa osmotic pressure. The
value of R2 was only 0.0282. At this condition, the second-order
model could not be used. This result revealed that the secondorder model was not a good model to describe the effect of osmotic
pressure on sugar extraction from sweet sorghum stalks.
3.7. Validation experiments with different varieties of sweet sorghum
In our two simultaneous rst-order kinetic model, the specic
difference in tissue composition was taken into consideration.
The model could be modied according to the analysis of the structure in Section 3.2. In order to validate the models predictive
capacity for different varieties of sweet sorghum, additional
extraction experiments were conducted for a different variety of
sweet sorghum, H110 at 2 mm and 30 C. The C1 and C2 were
determined using the method developed in Section 3.2 and the calculated values were 0.310.69 respectively. Using these specic
values of C1 and C2, the R2 value of the sugar transfer data tted
to the model was 0.959. This result demonstrated that our model

Table 4
The tting results of the modied kinetic model with different osmotic pressures.
Osmotic pressure
(103 KPa)

k1 (min1)

k2 (min1)

R2

Permeability

0
1.2
1.4
1.9
2.2

0.11
0.036
0.032
0.027
0.0086

0.010
0.0058
0.0028
0.0020
0.00089

0.998
0.985
0.929
0.945
0.959

94.2
85.1
63.6
55.8
40.1

A model for sugar transfer in particles of sweet sorghum in SSF

was developed. The kinetics of sugar transfer of sweet sorghum
was investigated by solidliquid extraction experiments. Based
on taking into consideration of tissue structure of sweet sorghum,
a specic kinetic model of two simultaneous one-order model
which has two parameters C1 and C2 describing the tissue difference was developed. The model tted the exaction data well under
different conditions. According to the model, relatively high temperature and stirring was benecial to promote the transfer of
the sugar from the interior to the exterior of the sweet sorghum
plant particle. Particle size was a key factor to the mass transfer
by decreasing the diffusion distance.
In addition, the model tted well when a different variety of
sweet sorghum was used. The model proved to be signicant in
studying the extraction of active substance from plants with specic structures. The parameters describing the tissue differences
could be modied according to the research system.
Acknowledgements
This work was supported by National High-tech R&D Program
(863 Program 2012AA101805), supported by International Scientic and Technological Cooperation Program (Grant No.
2012DFG61720, 2013DFA60470) of the Ministry of Science and
Technology of China, Beijing Science and Technology New Innovations Development Base Project.(Grant No. Z131109002813080).
We also appreciate the Institute of Millet of Hebei Academy of
Agriculture and Forestry kindly provided the sweet sorghum sample for our research.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.fuel.2014.12.023.
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