Food Chemistry 209 (2016) 144153

Contents lists available at ScienceDirect

Food Chemistry
journal homepage: www.elsevier.com/locate/foodchem

Effect of pectins on the mass transfer kinetics of monosaccharides, amino

acids, and a corn oil-in-water emulsion in a Franz diffusion cell
Mauricio Espinal-Ruiz, Luz-Patricia Restrepo-Snchez, Carlos-Eduardo Narvez-Cuenca
Departamento de Qumica, Facultad de Ciencias, Universidad Nacional de Colombia, AA 14490 Bogot DC, Colombia

a r t i c l e

i n f o

Article history:
Received 4 November 2015
Received in revised form 17 March 2016
Accepted 13 April 2016
Available online 16 April 2016
Keywords:
Pectin
Methoxylation degree
Diffusion
Viscosity
Franz diffusion cell

a b s t r a c t
The effect of high (HMP) and low (LMP) methoxylated pectins (2% w/w) on the rate and extent of the mass
transfer of monosaccharides, amino acids, and a corn oil-in-water emulsion across a cellulose membrane
was evaluated. A sigmoidal response kinetic analysis was used to calculate both the diffusion coefficients
(rate) and the amount of nutrients transferred through the membrane (extent). In all cases, except for
lysine, HMP was more effective than LMP in inhibiting both the rate and extent of the mass transfer of
nutrients through the membrane. LMP and HMP, e.g., reduced 1.3 and 3.0 times, respectively, the mass
transfer rate of glucose, as compared to control (containing no pectin), and 1.3 and 1.5 times, respectively,
the amount of glucose transferred through the membrane. Viscosity, molecular interactions, and flocculation were the most important parameters controlling the mass transfer of electrically neutral nutrients,
electrically charged nutrients, and emulsified lipids, respectively.
2016 Elsevier Ltd. All rights reserved.

1. Introduction
There is a growing interest among consumers about the nutritional, therapeutic, and functional properties of foods consumed in
the diet (Mohamed, 2014). The current trend of consumers is based
on the consumption of foods with functional components beneficial
for human health, such as phytosterols, polyphenolics, anthocyanins, carotenoids, and dietary fibres (Bigliardi & Galati, 2013).
In recent years, dietary fibre has received important attention from
the food industry and consumers due to the health benefits associated with the consumption of dietary fibre-rich foods (Brownlee,
2014). Dietary fibre components possess distinctive physicochemical and structural characteristics determining their functionality,
and they can be categorized as either insoluble or soluble dietary
fibres (Phillips, 2013). The consumption of insoluble dietary fibre
has been associated with increasing bulkiness of the digesta content
and improvement of the gastrointestinal tract (GIT) mobility
(Edwards, Johnson, & Read, 1988), whereas the consumption of
soluble dietary fibre has been associated with a wider variety of
physiological functions, such as control of postprandial glycemic
and lipid response (Pasquier et al., 1996), decrease of blood lipid
and glucose levels (Ye, Arumugam, Haugabrooks, Williamson, &
Hendrich, 2015), inhibition of the GIT enzyme activities (EspinalRuiz, Parada-Alfonso, Restrepo-Snchez, & Narvez-Cuenca, 2014),
Corresponding author.
E-mail address: cenarvaezc@unal.edu.co (C.-E. Narvez-Cuenca).
http://dx.doi.org/10.1016/j.foodchem.2016.04.046
0308-8146/ 2016 Elsevier Ltd. All rights reserved.

control of the rate and extent of lipid digestion (Espinal-Ruiz,

Parada-Alfonso,
Restrepo-Sanchez,
Narvaez-Cuenca,
&
McClements, 2014a, 2014b; Espinal-Ruiz, Restrepo-Snchez,
Narvez-Cuenca, & McClements, 2016), increase of the viscosity of
the GIT content (Edwards et al., 1988; Elleuch et al., 2011), and
retardation of the mass transfer process of nutritional compounds
to be absorbed by enterocytes (Fabek, Messerschmidt, Brulport, &
Goff, 2014; Srichamroen & Chavasit, 2011). Among the aforementioned properties of soluble dietary fibre, the ability to modulate
the viscosity of the GIT content stands out because this feature is
related to the control of the mobility of nutrients and their further
digestion and absorption (Fabek et al., 2014).
The functional properties of soluble dietary fibres (e.g., gums,
mucilages, and pectins) rely on their ability to gel into hydrated
three-dimensional networks and their subsequent increasing of
viscosity, determining their potential to exert physiological effects
along the GIT, specifically through the stomach and small intestine
(Brownlee, 2014). The proposed mechanism by which viscosity
may induce physiological responses includes increasing of luminal
bulk (Ye et al., 2015) and inhibiting of nutrient diffusion across the
unstirred water layer (UWL) of the mucosal membrane (Fabek
et al., 2014; Gunness, Flanagan, Shelat, Gilbert, & Gidley, 2012).
Viscous soluble fibres may hinder the mass transfer process of
nutritional compounds from the lumen to the UWL of the mucosal
membrane by reducing the mixing between them and reducing the
time available for intestinal absorption by enterocytes (Fabek et al.,
2014; Gunness et al., 2012). Therefore, an increase in digesta

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viscosity, arising from the soluble dietary fibre consumption, might

influence the processes occurring during the nutrient digestion and
adsorption (Espinal-Ruiz, Parada-Alfonso, Restrepo-Sanchez,
Narvaez-Cuenca, & McClements, 2014a, 2014b).
Among the different sources of soluble dietary fibre available,
pectin is a polysaccharide obtained from fruits and vegetables and
it is widely used in the pharmaceutical and food industries for its
thickening, gelling, and texturing properties (Maxwell, Belshaw,
Waldron, & Morris, 2012). Pectin is a biopolymer, mainly formed
from galacturonic acid (GalA) units joined in chains by a-D-(1,4)
glycosidic linkages. Three pectic structures [homogalacturonan
(HG), rhamnogalacturonan-I (RG-I), and rhamnogalacturonan-II
(RG-II)] have been isolated and structurally characterized
(Mohnen, 2008). HG corresponds to the linear chain of a-(1,4) GalA
units in which the carboxyl group (ACOO
) of GalA moieties can be
partially esterified with methanol (methoxylated), forming the
carbomethoxyl group (ACOOCH3). An important characteristic of
HG is the methoxylation degree, defined as the percentage of
carboxyl groups which have been methoxylated. If more than 50%
of the carboxyl groups are methoxylated, the pectin is called high
methoxylated pectin (HMP), and if less than that methoxylation
degree, it is called low methoxylated pectin (LMP). RG-I is a pectic
structure containing a linear backbone of the disaccharide [?4)-aD-GalA-(1?2)-a-L-Rha-(1?], where Rha corresponds to rhamnose,
and RG-II consists of a HG backbone substituted with side branches,
consisting of twelve different types of monosaccharides in up to
twenty different linkages (Maxwell et al., 2012). The most abundant
pectic structure is HG that comprises 65% (mol/mol) of pectin,
whereas RG-I and RG-II comprise 25 and 10% (mol/mol), respectively (Yapo, 2011). It is important, however, to stress that the ratios
of HG, RG-I and RG-II may vary greatly, depending on both the
source and the extraction method (Mohnen, 2008). Many functional
properties of pectin (e.g., viscosity, solubility, as well as waterholding, texturing, and gelling capacities) are dependent on its
structural parameters such as molecular weight, methoxylation
degree, and the distribution pattern of methoxylation within the
GalA chains (Mohnen, 2008; Ryden, MacDougall, Tibbits, & Ring,
2000; Yapo, 2011). In previous studies, we have demonstrated that
pectin inhibits the activity of some digestive enzymes (EspinalRuiz, Parada-Alfonso, Restrepo-Snchez, & Narvez-Cuenca, 2014)
and interferes with the digestion process of emulsified lipids
(Espinal-Ruiz, Parada-Alfonso, Restrepo-Sanchez, Narvaez-Cuenca,
& McClements, 2014a, 2014b; Espinal-Ruiz et al., 2016) by interacting with several GIT components, such as digestive enzymes, bile
salts, and electrolytes (Espinal-Ruiz, Parada-Alfonso, RestrepoSanchez, Narvaez-Cuenca, & McClements, 2014a, 2014b).
Although studies regarding the mass transfer control of some
nutritional compounds (e.g., glucose and bile salts) have been carried out by using different sources of dietary fibres, no information
is currently available concerning the influence of pectins on the
mass transfer process of the primary nutritional compounds consumed in the diet or produced after the digestion process, such
as monosaccharides, amino acids, and lipids. The objective of this
study was, therefore, to determine the effect of HMP and LMP on
the rate and extent of the mass transfer process of the main nutritional compounds consumed in the diet or obtained after the
digestion process, e.g. monosaccharides, amino acids, and lipids
(represented by a corn oil-in-water emulsion). The mass transfer
profiles of monosaccharides, amino acids, and a corn oil-in-water
emulsion in the absence (control) or presence of pectins (LMP or
HMP) reported a possible interaction mechanism between pectin
and the evaluated nutritional compounds. These results might lead
to the design, formulation, and fabrication of functional foods
developed to control postprandial blood concentrations of the
monosaccharides, amino acids, and lipids consumed in the diet.

2. Materials and methods

2.1. Chemicals and materials
D-(+)-Glucose, D-(+)-galactose, D-(
)-fructose, and D-(
)-ribose
were purchased from Panreac Qumica SLU (Barcelona, Spain).
L-lysine, L-glycine, L-aspartic

acid, L-tyrosine, ninhydrin monohydrate, Tween 80, and a dialysis tubing cellulose membrane
(cut-off 14 kDa) were purchased from Sigma-Aldrich Chemical
Company (St Louis, MO, USA). Corn oil was purchased from a commercial food supplier (Grasco LTDA, Bogot DC, Colombia) and
stored in darkness at room temperature until used. The manufacturer reported that the corn oil contained approximately 14, 35,
and 51% (w/w) of saturated, monounsaturated, and polyunsaturated fatty acids, respectively. Commercial powdered LMP was
donated by TIC Gums Inc. (Belcamp, MA, USA) and was used without further purification, with methoxylation degree and average
molecular weight previously reported as 30% (mol/mol) and
130 kDa, respectively (Espinal-Ruiz et al., 2016). Commercial powdered HMP (Genu Citrus Pectin USP/100) was donated by CP Kelco
Co. (Lille Skensved, Denmark) and was also used without further
purification, with methoxylation degree and average molecular
weight previously reported as 71% (mol/mol) and 181 kDa, respectively (Espinal-Ruiz et al., 2016). All other chemicals were
purchased from Merck KGaS (Darmstadt, Germany). Deionized
water was used to prepare all solutions. Franz diffusion cells
(Fig. 1) were fabricated by Siliser LTDA (Bogot DC, Colombia).
The volumes of the donor and receptor compartments were 3
and 17 mL, respectively. The effective area of mass transfer (A)
was 1.33 cm2.
2.2. Sample preparation
LMP and HMP stock solutions (4% w/w) were prepared separately by dispersing 2 g of powdered pectins into 48 g of deionized
water. These solutions were stirred at 1000 rpm overnight at room
temperature to ensure complete dispersion and dissolution. LMP
and HMP solutions were then adjusted to pH 7.0 by using 0.1 M
NaOH.
A monosaccharide stock solution (280 mM of each compound)
was prepared by dissolving together glucose, galactose, fructose,
and ribose in deionized water. These monosaccharides were
selected because of their nutritional relevance and because they
are monosaccharides composing digestible carbohydrates the most
(Asp, 1996). The monosaccharide stock solution (2.5 mL) was then

a
c

b
f

e
Fig. 1. Structural design of a Franz diffusion cell. Donor compartment with a
nominal volume of 3 mL (a), receptor compartment with a nominal volume of 17 mL
(b), position for a semipermeable cellulose membrane (c) with an effective area of
mass transfer (A) of 1.33 cm2 (diameter of 1.30 cm), sampling port (d), magnetic stir
bar (e), thermostatted chamber at 37 C (f), water inlet (g), and water outlet (h).

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M. Espinal-Ruiz et al. / Food Chemistry 209 (2016) 144153

mixed with either 2.5 mL of deionized water (control) or 2.5 mL of

4% (w/w) pectin stock solutions (LMP or HMP), to obtain monosaccharide working solutions containing 140 mM concentrations of
each monosaccharide and 2% (w/w) pectin. Monosaccharide working solutions were then adjusted to pH 7.0 by using 0.1 M NaOH. In
previous studies we demonstrated that pectin is able to modulate
several digestive processes at this concentration (Espinal-Ruiz,
Parada-Alfonso, Restrepo-Snchez, & Narvez-Cuenca, 2014;
Espinal-Ruiz, Parada-Alfonso, Restrepo-Sanchez, Narvaez-Cuenca,
& McClements, 2014a, 2014b; Espinal-Ruiz et al., 2016). In addition, because fruits and vegetables present typical pectin concentrations (around 20% w/w dry basis) and, based on the dilution
process upon transit in the mouth, stomach and small intestine,
the pectin concentration in the small intestine is expected to be
around 2% (w/w) (Baker, 1997; Fukunaga et al., 2003).
Amino acid stock solutions (4 mM of each compound) were
prepared by separately dissolving lysine, glycine, aspartic acid, or
tyrosine in deionized water. These amino acids were selected
because they are part of the majority of the food proteins
(Bidlingmeyer, Cohen, Tarvin, & Frost, 1987) and because of the
differences in their electrical characteristics: glycine (neutral),
aspartic acid (anionic), lysine (cationic), and tyrosine (neutral and
aromatic). Each amino acid stock solution (2.5 mL) was then mixed
separately with either 2.5 mL of deionized water (control) or
2.5 mL of 4% (w/w) pectin stock solutions (LMP or HMP), to obtain
amino acid working solutions containing 2 mM concentrations of
each amino acid and 2% (w/w) pectin. Each amino acid working
solution was then adjusted to pH 7.0 by using 0.1 M NaOH.
A stock emulsion (20% w/w) was prepared by mixing together
20 g of corn oil and 80 g of buffered emulsifier aqueous solution
[5 mM phosphate buffer, pH 7.0, containing 2.5% (w/w) Tween
80] for 5 min, using an Ultra-Turrax homogenizer (Speed
35000 min
1; Model Miccra D-9; ART Prozess & Labortechnik
GmbH & Co. KG; Mllheim; Germany). Corn oil was selected as a
lipid model because it is one of the most consumed oils in Colombia (SIC, 2011) and because we have established, in previous studies, that corn oil-in-water emulsions can be extensively flocculated
upon addition of pectin (Espinal-Ruiz, Parada-Alfonso, RestrepoSanchez, Narvaez-Cuenca, & McClements, 2014a, 2014b; EspinalRuiz et al., 2016). A dilution was prepared by mixing 10 g of stock
emulsion with 90 g of buffer solution, pH 7.0, to obtain a diluted
emulsion containing 2% (w/w) corn oil. Finally, the diluted emulsion (2.5 mL) was mixed with either 2.5 mL of deionized water
(control) or 2.5 mL of 4% (w/w) pectin stock solutions (LMP or
HMP), to obtain working emulsions containing 1% (w/w) corn oil
and 2% (w/w) pectin samples. Each working emulsion was then
adjusted to pH 7.0 by using 0.1 M NaOH.
2.3. Effect of pectins on the mass transfer kinetics of monosaccharides,
amino acids and a corn oil-in-water emulsion in a Franz diffusion cell
17 mL of deionized water (adjusted to pH 7.0 by using 0.1 M
NaOH) were transferred to the receptor compartment of the Franz
diffusion cell (Fig. 1), and incubated at 37 C for 15 min. Then, 3 mL
of the thermostatted working solutions (37 C) containing
monosaccharides, amino acids, or the corn oil-in-water emulsion,
with the absence (control) or presence of pectin samples (LMP or
HMP), were transferred separately to the donor compartment.
The Franz diffusion cell was thermostatted at 37 C throughout
the experiment. At times 0, 2, 4, 6, 8, 10, 24, 26, 28, 30, 32, 34,
and 48 h, an aliquot of 500 lL was collected from the receptor
compartment and then, 500 lL of deionized water (adjusted to
pH 7.0 and thermostatted to 37 C) were added immediately to
reconstitute the total volume of the cell. Samples collected from
the Franz diffusion cell over time were analyzed for their monosaccharide, amino acid or emulsion contents, as described below.

Contents of monosaccharides, amino acids, and the corn oil-inwater emulsion were corrected by the dilution factor introduced
at each sampling time.
2.4. Analysis of monosaccharides, amino acids, and the corn
oil-in-water emulsion contents
2.4.1. Analysis of monosaccharides
Monosaccharide samples collected from the receptor compartment were analyzed by a high performance liquid chromatograph
coupled to a refractive index detector. An UHPLC+ Focused Dionex
Ultimate 3000 liquid chromatograph (Thermo Scientific Inc.,
Waltham, MA, USA) equipped with an ion-exchanger resin column
(MetaCarb Ca Plus column, 300  7.8 mm  9 lm, Agilent Technologies, Santa Clara, CA, USA) was used. The column was operated
at 70 C and at a flow rate of 0.5 mL min
1 with deionized water
(adjusted to pH 7.0) as eluent. Monosaccharide samples were
centrifuged (18000g; 20 min; 4 C) and then 10 lL of the clear
supernatant was injected into the column. Monosaccharides
eluting from the column were detected by using a Shodex RI-101
refractive index detector (Showa Denko Corporation, Tokyo, Japan)
thermostatted at 35 C and the area under the curve for each
monosaccharide signal was measured. The amount of monosaccharides transported through the cell was determined by using an
external standard method (direct interpolation of the area under
the curve in the calibration line for each monosaccharide). Calibration lines were obtained at concentrations ranging from 2 to
20 mM for each monosaccharide (n = 10; r2 = 0.995, 0.998, 0.999,
and 0.990 for glucose, galactose, fructose, and ribose, respectively).
2.4.2. Analysis of amino acids
Amino acid samples collected from the receptor compartment
(500 lL) were mixed with 500 lL of ninhydrin solution [2% (w/v)
prepared in 100 mM citrate buffer pH 4.0] and then incubated at
92 C (boiling water) for 10 min to generate the ninhydrin
chromophore (Ruhemanns purple) (Friedman, 2004). The mixtures were cooled to room temperature and then the absorbance
was recorded at 570 nm with a Genesys 10uv Spectrophotometer
(Thermo Scientific Inc., Waltham, MA, USA). The amount of amino
acids transported through the cell was determined using an external standard method (direct interpolation of the absorbance at
570 nm in the calibration line for each amino acid). Calibration
lines were obtained at concentrations ranging from 35 to 350 lM
for each amino acid (n = 10; r2 = 0.997, 0.989, 0.992, and 0.995
for glycine, aspartic acid, lysine, and tyrosine, respectively).
2.4.3. Analysis of the optical turbidity of the corn oil-in-water
emulsion
The optical turbidity (absorbance at 600 nm) of the emulsion
samples collected from the receptor compartment was measured,
using a Genesys 10uv Spectrophotometer (Thermo Scientific Inc.,
Waltham, MA, USA) at room temperature. The amount of the
emulsion transported through the cell was determined, using an
external standard method (direct interpolation of the absorbance
at 600 nm in the calibration line). A calibration line was obtained
at concentrations of the corn oil-in-water emulsion ranging from
0.02 to 0.20% (w/w) (n = 10; r2 = 0.998).
2.5. Apparent viscosity of pectin solutions
Pectin solutions (2% w/w) for apparent viscosity measurements
were prepared by dissolving 400 mg pectin samples (LMP or HMP)
in 19.6 g of 25 mM NaCl aqueous solution with gentle stirring for
18 h at room temperature. Then, pectin solutions were centrifuged
(3000g; 15 min; 4 C) to expel the entrapped air bubbles.
Afterwards, pectin solutions were stored at 4 C overnight before

M. Espinal-Ruiz et al. / Food Chemistry 209 (2016) 144153

147

measurements. The apparent viscosity measurements of pectin

solutions were determined, using an Ares Discovery HR-1 Rheometer (TA Instruments Inc., New Castle, DE, USA) with a parallel plate
geometry, with a diameter of 40 mm and a gap of 1 mm. Samples
were placed in a temperature-controlled Peltier plate and allowed
to equilibrate at 25 C for 5 min prior to conducting the measurements. All apparent viscosity measurements were performed using
a series of fixed shear rates that consecutively increased from 0.002
to 10 s
1 and recorded at 25 C. The Power Law Model (Eq. (1)) was
used to analyze the rheological profiles of pectin samples
(Marcotte, Taherian Hoshahili, & Ramaswamy, 2001) by calculating
both the K and n values, as follows:

as the ratio of C and CMax. The integration of this first-order

non-linear differential equation leads to Eq. (3), as follows:

g K c_ n

where A corresponds to the effective area of the mass transfer

process.

where g is the apparent viscosity, c_ is the shear rate, K is the

consistency index (which corresponds to the apparent viscosity of
a fluid behaving as Newtonian), and n is the flow index (which
indicates the degree of deviation from Newtonian behaviour).
2.6. Emulsion characterization
2.6.1. Microstructure
The microstructure of the emulsions was characterized by
optical microscopy. An optical microscope (C1 Digital Eclipse,
Nikon Co., Tokyo, Japan) with a 60 objective lens was used to
capture images of the emulsions. A small aliquot of the emulsions
(5 lL) was transferred to a glass microscope slide and covered with
a glass cover slip. Then, the cover slip was fixed to the slide, using
sealing resin (Ted Pella Inc., Redding, CA, USA) to avoid evaporation. Next, a small amount of immersion oil (Type A, Nikon Co.,
Melville, NY, USA) was placed on the top of cover slip. All optical
microscopy images were recorded by using the instrument
software (EZ CS1 version 3.8, Nikon Co., Melville, NY, USA).
2.6.2. Particle size distribution
The particle size distribution of emulsions was measured, using
a dynamic light scattering instrument (Zetasizer Nano ZSP,
Malvern Instruments Ltd., Worcestershire, United Kingdom).
Refractive indices of 1.467 (corn oil) and 1.333 (water) were used
for the calculations of the particle size distribution. Particle sizes
were reported as particle size distribution profiles [volume fraction
(%) vs. particle diameter (nm)].
2.7. Kinetic model
A sigmoidal response kinetic model (Eq. (2)) was used to fit the
experimental data of the mass transfer profiles of monosaccharides, amino acids, and a corn oil-in-water emulsion through the
Franz diffusion cell. Both the effective diffusion coefficients
(the rate of the mass transfer process) and the maximum amount
of the compound transferred through the Franz diffusion cell
(the extent of the mass transfer process), in the absence (control)
or presence of 2% (w/w) HMP or LMP were calculated. This model
represented by Eq. (2) assumes that the rate of the mass transfer
process is directly proportional to the concentration of the nutritional compound to be transferred across the membrane
(Edwards et al., 1988), as follows:



dC
C
kC 1

dt
CMax

where C is the concentration of the nutritional compound transferred at time t, k is the steepness of the curve, and CMax is the maximum observable value for C. The relative transfer percentage
[RT (%)] of the nutritional compound can be conveniently expressed

RT%

1
C
 100% 1 expkt1=2
t
 100%
CMax

where RT (%) corresponds to the relative transfer percentage of the

nutrient and t1/2 represents the time in which the 50% of the total
concentration of this nutrient has been transferred across the membrane. The effective diffusion coefficient (DEff) was defined as
follows:

DEff kA

2.8. Data analysis

All experiments were performed at least three times, using
freshly prepared solutions. Apparent viscosity measurements of
pectin solutions were performed in quadruplicate. Averages and
standard deviations were calculated from these replicated
measurements. Statistical analysis was performed by using
STATGRAPHICS Centurion XVI version 16.1.11 for Windows.
A Fishers least significance difference (LSD) test was conducted
to detect any significant differences among the pectin samples. A
p-value <0.05 was considered as statistical significance.
3. Results
3.1. Mass transfer profiles of monosaccharides
Pectins, especially HMP, were able to inhibit both the rate and
extent of the mass transfer process of monosaccharides through
the Franz diffusion cell. Fig. 2 shows the mass transfer profiles of
monosaccharides [glucose (Fig. 2a), galactose (Fig. 2b), fructose
(Fig. 2c), and ribose (Fig. 2d)]. Both the rate and extent of the mass
transfer process of monosaccharides through a Franz diffusion cell
in the absence (control) or presence of pectin (LMP or HMP) were
characterized by calculating DEff and maximum RT (%) values,
respectively (Table 1). The maximum RT (%) value is related to
the amount of nutrients which can be effectively transferred
through the cellulose membrane (the extent of the mass transfer
process), whereas the DEff value is related to the rate at which
the mass transfer process occurs. The RT (%) values increased with
time and tended towards a plateau after 36 h for each of the tested
monosaccharides (Fig. 2). When a pectin sample (LMP or HMP) was
added, all of the tested monosaccharides diffused more slowly than
the control (Table 1, DEff), reaching a lower maximum RT (%) value
[Table 1, maximum RT (%)]. The inhibitory effect of the mass transfer process was higher with HMP than LMP. For example, for the
diffusion of glucose (Fig. 2and Table 1), DEff values were
1.44  10
5, 1.14  10
5, and 0.48  10
5 cm2 s
1 for control,
LMP, and HMP, respectively; and the maximum RT (%) values were
94.7, 71.5, and 63.3 for control, LMP, and HMP, respectively. Similar trends were observed for galactose (Fig. 2b), fructose (Fig. 2c),
and ribose (Fig. 2d).
3.2. Mass transfer profiles of amino acids
As observed with the mass transfer of monosaccharides, the
rate and the extent of amino acids transported towards the Franz
diffusion cell were reduced by the presence of pectins, with a
higher effect of HMP towards glycine, aspartic acid, and tyrosine,
and a higher effect of LMP towards lysine. Fig. 2 shows the mass
transfer profiles of amino acids [glycine (Fig. 2e), aspartic acid

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M. Espinal-Ruiz et al. / Food Chemistry 209 (2016) 144153

a.

100

b. 100

Control

Control

LMP

HMP

80

Relative transfer (%)

80

Relative transfer (%)

LMP

HMP

60

40

60

40

20

20

0
0

12

24

36

48

12

c.

100

d. 100

Control

Relative transfer (%)

Relative transfer (%)

60

40

48

36

48

36

48

60

40

20

0
0

12

24

36

48

12

f.

100

Control

100

Control

LMP

LMP

HMP

HMP

80

Relative transfer (%)

80

24

Time (h)

Time (h)

Relative transfer (%)

36

HMP

80

60

40

20

60

40

20

0
0

12

24

36

48

Time (h)

g. 100

h. 100

Control

24

Control
LMP

HMP

HMP

80

Relative transfer (%)

80

12

Time (h)

LMP

Relative transfer (%)

48

LMP

HMP

20

e.

36

Control

LMP

80

24

Time (h)

Time (h)

60

40

20

60

40

20

0
0

12

24

Time (h)

36

48

12

24

Time (h)

Fig. 2. Effect of low (LMP) and high (HMP) methoxylated pectins on the mass transfer kinetics of glucose (a), galactose (b), fructose (c), ribose (d), glycine (e), aspartic acid (f),
lysine (g), and tyrosine (h) through a Franz diffusion cell. Control corresponds to the sample without addition of pectin. Points correspond to experimental data and lines
correspond to fitted data according to Eq. (3).

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M. Espinal-Ruiz et al. / Food Chemistry 209 (2016) 144153

Table 1
Effect of low (LMP) and high (HMP) methoxylated pectins on the effective diffusion coefficient (DEff) and the maximum relative transfer percentage [maximum RT (%)] of
monosaccharides, amino acids, and a corn oil-in-water emulsion through a Franz diffusion cell. Control corresponds to the sample without addition of pectin. Different letters
indicate significant differences. Lowercase letters indicate significant differences of the same compound among treatments (Control, LMP, and HMP; comparison between
columns), and uppercase letters indicate significant differences of the same treatment among the type of compound (comparison within columns) at the p < 0.05 level.
Compound

Maximum RT (%)

Control

LMP

HMP

Control

LMP

HMP

Monosaccharides
Glucose
Galactose
Fructose
Ribose

1.44 0.04a,B
1.44 0.04a,B
1.40 0.04a,B
3.91 0.41a,A

1.14 0.04b,A
1.18 0.04b,A
1.14 0.04b,A
1.11 0.11b,A

0.48 0.04c,A
0.48 0.04c,A
0.48 0.04c,A
0.52 0.04c,A

94.7 0.9a,A
94.5 0.7a,A
96.0 1.6a,A
80.4 0.8b,B

71.5 2.4b,B
68.5 1.6b,B
67.4 1.5b,B
86.1 3.8a,A

63.3 1.6c,B
62.4 3.7c,B
60.6 2.1c,B
86.0 1.7a,A

Amino acids
Glycine
Aspartic acid
Lysine
Tyrosine

3.83 0.04c,B
3.87 0.18a,B
4.06 0.04a,A
3.87 0.04b,B

4.65 0.15b,B
3.91 0.26a,C
0.59 0.07c,D
6.75 0.29a,A

5.24 0.04a,B
4.20 0.04a,C
3.54 0.15b,D
6.45 0.04a,A

87.8 3.3a,B
96.0 1.8a,A
90.8 1.2a,B
95.2 1.7a,A

17.2 1.3b,C
81.6 2.6b,A
7.0 0.7c,D
69.4 3.4b,B

10.6 0.7c,B
39.3 1.9c,A
40.2 2.7b,A
36.7 1.8c,A

3.43 0.15a

3.24 0.15a

82.9 1.9a

43.1 0.3b

6.8 0.1c

Lipids
Emulsion
1

DEff  105 (cm2 s
1)1

3.47 0.26a
5

Example: for Glucose (Control): DEff  10 (cm s

1

5

) = 1.44 should be read as DEff = 1.44  10

(Fig. 2f), lysine (Fig. 2g), and tyrosine (Fig. 2h)]. Although the mass
transfer profiles obtained for the amino acids were fairly similar to
those obtained for monosaccharides, a very important difference in
the mass transfer profiles of amino acids was observed: a sigmoidal
kinetic behaviour in the control and pectin-containing experiments. A lag time of approximately 10 h was observed for the mass
transfer process of each of the tested amino acids in both absence
(control) and presence of pectins (LMP and HMP). Before the lag
time (t < 10 h), no significant differences in the RT (%) values were
observed among pectin samples for each of the tested amino acids,
as compared to the control (the amount of amino acids transferred
through the membrane was less than 3% after 10 h in both absence
and presence of pectins). The RT (%) values increased with time and
tended towards a plateau after 36 h for each of the tested amino
acids (Fig. 2). When a pectin sample (LMP or HMP) was added,
different results for glycine, aspartic acid, and tyrosine were
observed, in comparison to lysine (Fig. 2g).
Upon addition of pectins, glycine, aspartic acid, and tyrosine
diffused faster (Table 1, DEff), but they reached a lower maximum
RT (%) value, as compared to the control [Table 1, maximum RT
(%)]. For example, for the diffusion of glycine (Fig. 2e and Table 1),
DEff were 3.83 x 10-5, 4.65 x 10-5, and 5.24 x 10-5 cm2 s-1 for control,
LMP, and HMP, respectively; and the maximum RT (%) values were
87.8, 17.2, and 10.6 for control, LMP, and HMP, respectively. Similar trends were observed for aspartic acid (Fig. 2f and Table 1) and
tyrosine (Fig. 2h and Table 1). These results indicate that pectins,
especially HMP, were able to inhibit the amounts of glycine, aspartic acid, and tyrosine that can be effectively transferred through
the Franz diffusion cell (the extent of the mass transfer process),
but they were not able to reduce the rate at which the mass transfer process occurred. In addition, it was observed that the inhibitory effect of the extent of the mass transfer process of glycine,
aspartic acid, and tyrosine through the Franz diffusion cell was
higher with HMP than with LMP. Opposite to the behaviour
observed for glycine, aspartic acid, and tyrosine, the effect of pectins towards the diffusion of lysine (Fig. 2g and Table 1) was quite
different. For this amino acid, DEff were 4.06  10
5, 0.59  10
5,
and 3.54  10
5 cm2 s
1 for control, LMP, and HMP, respectively;
and the maximum RT (%) values were 90.8, 7.0, and 40.2 for the
control, LMP, and HMP, respectively. These results indicate that
pectins, especially LMP, were able to inhibit both the amount of
lysine that can be effectively transferred through the Franz diffusion cell and the rate at which the mass transfer process of lysine

cm s

1

occurs. In addition, it was observed that the inhibitory effect of the

rate and extent of the mass transfer process of lysine through the
Franz diffusion cell was higher with LMP than with HMP.
3.3. Mass transfer profile of the corn oil-in-water emulsion
Pectins, especially HMP, were able to inhibit both the rate and
extent of the mass transfer process of the corn oil-in-water emulsion through the Franz diffusion cell. Fig. 3a shows the mass transfer profile of the corn oil-in-water emulsion through the Franz
diffusion cell. The mass transfer profile obtained for the emulsion
was fairly similar to those obtained for the monosaccharides: the
sigmoidal behaviour was not observed and the effect of pectins
on the rate and extent of the mass transfer process followed the
same order: Control > LMP > HMP. It was also observed that both
the rate and extent of the mass transfer process of the emulsion
were inhibited upon addition of pectins (DEff were 3.47  10
5,
3.43  10
5, and 3.24  10
5 cm2 s
1 for control, LMP, and HMP,
respectively and the maximum RT (%) values were 82.9, 43.1, and
6.8 for control, LMP, and HMP, respectively), the inhibitory effect
of the rate and extent of the mass transfer process of the emulsion
through the Franz diffusion cell being higher with HMP than with
LMP (Table 1).
4. Discussion
4.1. Mass transfer profiles of electrically neutral nutrients
The inhibition of both the rate and extent of the mass transfer
process of electrically neutral nutrients (monosaccharides, glycine,
and tyrosine) observed upon addition of pectins might be due to
the high viscosity of both LMP and HMP solutions as compared
to that of the control. The apparent viscosity profiles of 2% (w/w)
LMP and HMP solutions are shown in Fig. 4. Both LMP and HMP
solutions behaved as pseudoplastic non-Newtonian fluids because
the viscosity of the solutions decreased as the shear rate increased
(Sato, Oliveira, & Cunha, 2008). The apparent viscosity of HMP was
significantly higher than that of LMP, at low shear rates (below
0.01 s
1). In addition, the flow behaviour indices (n), for both
LMP and HMP solutions, were less than 1 (0.292 and 0.183 for
HMP and LMP, respectively), demonstrating that pectin solutions
behaved as non-Newtonian fluids [defined for Newtonian fluids,
n = 1 (Cross, 1965)]. Due to the high molecular weight of HMP

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M. Espinal-Ruiz et al. / Food Chemistry 209 (2016) 144153

a.

b.

100

Control

Control

LMP

LMP

HMP

HMP

Volume fraction (%)

Relative transfer (%)

80

15

60

40

10

20

0
0

12

24

36

48

Time (h)

10

100

1000

10000

Particle diameter (nm)

c.

Control

LMP

HMP

Fig. 3. Effect of low (LMP) and high (HMP) methoxylated pectins on the mass transfer kinetics of a corn oil-in-water emulsion through a Franz diffusion cell (a). Points
correspond to experimental data and lines correspond to fitted data according to Eq. (3). Particle size distribution of a corn oil-in-water emulsion in presence of LMP and HMP
(b). Microstructure of a corn oil-in-water emulsion observed by optical microscopy in presence of LMP and HMP (c). The scale bars corresponds to 20 lm. Control corresponds
to the emulsion without addition of pectin.

15000
HMP

Apparent viscosity (mPa s)

LMP

10000

5000

0
0.001

0.01

0.1

Shear rate

10

(s-1)

Fig. 4. Rheological profiles (apparent viscosity versus shear rate) measured at 25 C

of 2% (w/w) low (LMP) and high (HMP) methoxylated pectin solutions prepared in
25 mM NaCl. Pectin solutions were thermally stabilized at 25 C for 5 min prior to
analysis. Points correspond to experimental data and lines correspond to fitted data
according to Eq. (1).

(181 kDa) compared to that of LMP (130 kDa), the consistency

index (K) of HMP (281 mPa s) was significantly higher than that
of LMP (62 mPa s).
The non-Newtonian behaviour of pectin solutions originates
from the presence of macroscopic network structures which
are characteristic of the hydration process of pectin molecules
(Lfgren, Walkenstrm, & Hermansson, 2002). Viscous fibres of
hydrophilic nature, such as pectins, have been reported to
create complex networks by the entanglements of hydrated

chains of pectin, producing viscous solutions (Ryden et al.,

2000). The formation of these complex hydrated networks is
commonly related to the capacity of pectin molecules to embed
nutritional compounds, thereby limiting their further mobility
(Zsivanovits, MacDougall, Smith, & Ring, 2004). Therefore, the
retardation of the rate and extent of the mass transfer process
of electrically neutral nutrients (monosaccharides, glycine, and
tyrosine) through the Franz diffusion cell was higher with
HMP than with LMP, probably due to the higher viscosity of
HMP than LMP.
It is important to consider that amino acids can be electrically
charged, depending on the pH, and this electrical charge will
determine their potential to interact with other charged species
(such as pectin). The net electrical charge for glycine and tyrosine
was calculated by using the relative distribution of their charged
species at pH 7.0. For glycine, the neutral specie (charge 0,
+
NH3CH(H)COO
) has a relative abundance of 99.8%, and for
tyrosine, the neutral specie (charge 0, +NH3CH(CH2uOH)COO
)
has a relative abundance of 99.4%. These calculations confirm that
both glycine and tyrosine are neutral amino acids at pH 7.0.
Because of the neutral structures of glycine and tyrosine at pH
7.0, the electrostatic interactions between them and pectin were
not significant. Therefore, the viscosity of the pectin solutions
might be the parameter governing the retardation of the mass
transfer process of all the studied electrically neutral nutrients.
For electrically neutral nutrients, however, other structural parameters, such as hydrophobicity and molecular size, might be
involved in the interactions with pectins. For example, in previous
studies we showed that the carbomethoxyl group (ACOOCH3) of
HMP is able to interact through hydrophobic interactions with
tyrosine (Espinal-Ruiz, Parada-Alfonso, Restrepo-Snchez, &
Narvez-Cuenca, 2014). In addition, we also demonstrated that,

M. Espinal-Ruiz et al. / Food Chemistry 209 (2016) 144153

151

Fig. 5. Molecular mechanisms governing the interaction between pectin and nutritional compounds (monosaccharides, amino acids, and emulsified lipids) and its effect on
the mass transfer kinetics of them through the Franz diffusion cell (highly schematic). The mass transfer process of monosaccharides and neutral amino acids (glycine and
tyrosine) is controlled by the viscosity of the pectin solutions, whereas the mass transfer process of charged amino acids is controlled by both viscosity and repulsive (aspartic
acid) and attractive (lysine) electrostatic interactions between them and pectin. Finally, pectin induces flocculation of lipid droplets by depletion attraction and therefore,
their mobility is reduced.

the higher the molecular size of the pectin (e.g., molecular weight
and hydrodynamic radius), the higher is the viscosity of the
solution (Espinal-Ruiz et al., 2016).
4.2. Mass transfer profiles of electrically charged amino acids
We suggest that the mass transfer process of electrically
charged amino acids (aspartic acid and lysine) can be influenced
by both the viscosity of the pectin solutions and the electrostatic
interactions between each charged amino acid and the surface
electrical charges of LMP and HMP. It is well known that pectin
molecules are anionic in nature (Mohnen, 2008) because of the
spontaneous ionization of the carboxyl group in aqueous solution
ACOOH H2 OACOO
H3 O . The surface electrical charge of
the pectins tested in this study were previously characterized
(Espinal-Ruiz et al., 2016). LMP has a higher surface negative
charge (f =
47.5 mV at pH 7.0) than has HMP (f =
28.2 mV at
pH 7.0) because a higher fraction of the carboxyl groups (ACOO
)
of LMP remain free than those of HMP (Espinal-Ruiz et al., 2016).
Furthermore, the electrical net charges of aspartic acid and lysine
at pH 7.0 are
1 and +1, respectively (Moore, 1985).
We suggest, therefore, that the repulsive electrostatic interactions between the carboxyl group of aspartic acid (Fig. 2f) and
the carboxyl groups of LMP prevented aspartic acid molecules from
being trapped in the structural network of LMP, and therefore, the
extent of the mass transfer process of aspartic acid through the
Franz diffusion cell was not significantly hindered upon addition
of LMP. In contrast, because of the lower surface negative charge
of HMP, as compared to that of LMP, the electrostatic interactions
between aspartic acid and HMP were not significant, and therefore,
the inhibition of the extent of the mass transfer process observed
for aspartic acid upon addition of HMP can be attributed to viscosity effects. Conversely, the attractive electrostatic interactions

between the e-amino group of lysine (ANH+3) and the carboxyl

group of LMP (ACOO
) significantly promoted the entrapment of
lysine molecules in the structural network of LMP, and therefore,
both the rate and extent of lysine through the Franz diffusion cell
were significantly hindered upon addition of LMP. Moreover, our
results suggest that the electrostatic attractive interactions overcame the viscosity effects and consequently, the capacity of LMP
to inhibit the mass transfer process of lysine through the Franz
diffusion cell was higher than that of HMP (Table 1). We hypothesize that positive charges of lysine molecules play an important
role in controlling their interaction with pectins because lysine
was the only amino acid evaluated where the effect of LMP was
higher than HMP (Fig. 2g). In addition, we suggest that the lag
phase and the sigmoidal behaviour observed in the diffusion
profiles of all of the tested amino acids (Fig. 2) are attributable to
the strong electrostatic interactions between the ionizable groups
of the amino acids (ANH+3, ACOO
, and side chains) and the
cellulose molecules composing the membrane (Mahrenholz,
Tapia, Stigler, & Volkmer, 2010).
4.3. Diffusion profile of the corn oil-in-water emulsion
The mechanism by which pectin is able to retard the rate and
extent of the mass transfer process of the emulsion might be
related to the high capacity of HMP to flocculate the lipid droplets
of the emulsion as compared to LMP (Espinal-Ruiz et al., 2016). The
depletion interaction might be the driving force which promotes
the flocculation of the emulsified lipids, and it has been established
that this force, induced by polysaccharides, increases as the molecular weight of the polysaccharide increases (McClements, 2000).
Consequently, because the molecular weight of HMP (181 kDa) is
higher than that of LMP (130 kDa), the flocculation capacity of
HMP was greater than that of LMP. Therefore, the inhibition of

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M. Espinal-Ruiz et al. / Food Chemistry 209 (2016) 144153

the rate and extent of the mass transfer process of the emulsion
through the Franz diffusion cell was greater with HMP (6.8% of
the emulsion was transferred) as compared to 43.1% for LMP,
because of the higher capacity of HMP to flocculate the lipid
droplets composing the emulsion. The particle size distribution
analysis (Fig. 3b) indicated that the control emulsion (without
addition of pectin) contained small lipid droplets (the lipid droplet
diameter was around 300 nm) with a monomodal distribution
(only one peak was observed), suggesting that the lipid droplets
in the control emulsion were stable to aggregation (Fig. 3c,
Control). However, the multimodal distribution of the emulsions
containing LMP and HMP (Fig. 3b) indicated that pectins were able
to induce aggregation of the lipid droplets (Fig. 3c, LMP and HMP)
through a mechanism of flocculation [lipid droplet (flocs) diameters were 1100 and 1500 nm for LMP and HMP, respectively].
Therefore, it can be suggested that the inhibitory effect of the rate
and extent of the mass transfer process of the corn oil-in-water
emulsion through the Franz diffusion cell was higher with HMP
than LMP (Fig. 3a and Table 1), probably due to the high capacity
of HMP to flocculate the lipid droplets of the emulsion as compared
to LMP (Fig. 3b and c).
It is important to stress that our results show that the presence
of pectin affects the diffusion process of nutrients occurring in the
UWL of the intestinal mucosa (the rate at which the nutrient can
reach the receptor where it is absorbed), but they do not give information on how pectin is able to affect the nutrient-receptor interaction. In addition, it can be suggested that the chemical nature of
the nutritional compounds (monosaccharides, amino acids, and the
corn oil-in-water emulsion) to be transferred through the Franz
diffusion cell, as well as the chemical nature of the pectin sample,
will determine the mechanism by which the nutritional compound
is able to interact with pectin molecules (Fig. 5). For example, it
was observed that viscosity of the pectin solution was the most
important parameter, governing both the rate and extent of the
mass transfer process of monosaccharides and neutral amino acids
(glycine and tyrosine), whereas electrostatic interactions played an
important role, controlling the extent of the mass transfer process
of charged amino acids (repulsive for the interaction between pectin and aspartic acid, and attractive for the interaction between
pectin and lysine). Furthermore, the complex aggregated structures formed by the flocculation of emulsified lipids lead to complex interactions between them and pectin molecules,
flocculation being the most important parameter governing both
the rate and extent of the mass transfer process of the corn
oil-in-water emulsion. Because the molecular weight and
methoxylation degree of pectins are, nevertheless, often interdependent variables, it is necessary to have a large number of pectin
samples with different methoxylation degrees and molecular
weights to be able to discriminate the relative effect of each
parameter on the overall mass transfer kinetics efficiency of the
tested nutritional compounds.

5. Conclusions
Viscosity of pectin solutions and electrostatic interactions
between pectins and nutrients are proposed to be the main factors
influencing both the rate and extent of the mass transfer process of
nutrients across a cellulose membrane in a Franz diffusion cell. Our
results suggest that, the higher the viscosity of the pectin solution,
the higher is the inhibition of the rate and extent of the mass transfer of nutrients through the Franz diffusion cell. In addition, it was
established that HMP was more able than LMP to inhibit the extent
of the mass transfer process of all evaluated nutritional compounds, except for lysine, in which strong attractive electrostatic
interaction with LMP was the dominant factor governing its mass

transfer process. The inclusion of pectin in food formulations might

be an effective strategy for controlling the calorie intake by
limiting the digestion and absorption of nutritional compounds.
However, the formulation of foodstuffs with high pectin contents
must be done carefully in countries whose inhabitants are deficient
in minerals such as iron, calcium, and zinc, since the consumption
of pectin has been associated with a decreased bioavailability of
these minerals.

Acknowledgments
We are grateful to Departamento Administrativo de Ciencia,
Tecnologa e Innovacin de Colombia (COLCIENCIAS) and Vicerrectora Acadmica de la Universidad Nacional de Colombia for
providing a fellowship to Mauricio Espinal-Ruiz supporting this
work. We are also grateful to Vicerrectora de Investigaciones de
la Universidad Nacional de Colombia for funding the project
Efectos moleculares de la pectina sobre el metabolismo de lpidos y
carbohidratos (Cdigo Hermes 20610).

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