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Corresponding author. ABSTRACT
TEL: +52(443)-3142152, Ext. 201;
FAX: +52(443)-3142152, Ext. 201; The aim of this work was to characterize the mucilage extracted from six species
EMAIL: hedu65@hotmail.com of Opuntia. The species studied were as follows: O. atropes, O. tomentosa,
O. hyptiacantha, O. streptacantha y O. joconostle and O. ficus-indica. The first step
Received for Publication December 6, 2013
was to find the best extraction conditions to obtain an unaltered chemical
Accepted for Publication February 7, 2014
structure of mucilage. The mucilages were characterized using high-performance
doi:10.1111/jfpe.12084 liquid chromatography and Fourier transform infrared spectroscopy techniques.
The optimal conditions employed to obtain the mucilage were: ratio of
cladodes : ethanol solution at 50% of 1:1 (w/v), temperature of 22C and precipita-
tion of mucilage with a solution of ethanol 96%, at a ratio of 1:4 (v/v). Mucilage
from all species studied had a high content of soluble dietary fiber, ranging from
51.79 to 67.51%. In decreasing order, sugars found in the mucilages were:
L-arabinose (26.83–35.36%), D-galactose (21.59–45.48%), D-xylose (12.23–
17.05%), uronic acids (5.59–13.91%), D-glucose (5.18–16.21%) and L-rhamnose
(1.41–5.40%).
PRACTICAL APPLICATIONS
This research presents an optimization method for the extraction of mucilage five
wild species of cactus based on temperature and time of extraction and solvent
ratio: sample used. Mucilages were characterized chemically and by chromato-
graphic and Fourier transform infrared spectroscopy techniques and were com-
pared with the species mucilage Opuntia ficus-indica, the species most
commercially studied. The mucilage obtained can be used for commercial pur-
poses as additives in the food industry.
Journal of Food Process Engineering 37 (2014) 285–292 © 2014 Wiley Periodicals, Inc. 285
MUCILAGE FROM WILD SPECIES OF OPUNTIA S. RODRÍGUEZ-GONZÁLEZ ET AL.
Authors Gal Ara Xyl Rha Uronic acids Glu Fru Fuc Man
a
McGarvie and Parolis (1981) 18.4 42.4 24.5 6.4 8.4
Trachtenberg and Mayer (1981)a 40.1 24.6 22.2 13.1
Nobel et al. (1992)a 21 42 22 7 8
Medina-Torres et al. (2000)a 17.92 46.68 23.45 6.76 5.19
Matsuhiro et al. (2006) + + + + +
Cárdenas et al. (2008)a 7 6 1 0.6 85.4
Ginestra et al. (2009) + + + + + + + +
Ribeiro et al. (2010) + + + + + +
Ara, arabinose; Fru, fructose; Fuc, fucose; Gal, galactose; Gluc, glucose; Man, manose; Ram, rhamnose; Xyl, xylose.
a
Expressed as percentage.
A molecule of mucilage from O. ficus-indica can contain O. ficus-indica. The mucilages from the wild species of
more than 30,000 sugar subunits or residues (McGarvie and Opuntia could be used as potential ingredients in the food
Parolis 1981; Gibson and Nobel 1990; Medina-Torres et al. industry.
2000). It is a polysaccharide with a reported molecular
weight of 2.3 × 104 to 4.3 × 106 Daltons (Trachtenberg and
MATERIAL AND METHODS
Mayer 1982; Medina-Torres et al. 2000). Mucilage repre-
sents about 14% dry basis in nopal cladodes (Ginestra et al.
Materials
2009). The sugars found in mucilage are arabinose (35–
40%), galactose (20–25%), rhamnose (7–8%), xylose (20– The studied species O. atropes, O. hyptiacantha, O. joconostle,
25%) and uronic acids (7–8%) (Gibson and Nobel 1990). O. streptacantha, O. tomentosa and O. ficus-indica grown in
According to McGarvie and Parolis (1981), a hypothetical the Morelia area (Michoacán State, México) were harvested
model of the mucilage from O. ficus-indica consists of alter- in May of 2011. Cladodes (pads) had two ages at the time of
nating rhamnose and galacturonic acid residues, attached to collection.
the side chains composed of three galactose residues.
Arabinose and xylose sugars are branches on the galactose
Mucilage Extraction Procedures
side chains. In general, xylose appears to be joined to
arabinose, which is then bonded to galactose. Some galac- Three methods were evaluated for mucilage extraction. The
tose side chains have arabinose but not xylose, and some objective of testing by three methods was to find the best
have one xylose with two arabinose residues. The mucilage extraction conditions without causing damage to the native
from other species of the Opuntia is composed of the same structure of the mucilage. The methods are described as
sugar residues. However, the residues are present in different follows: (1) Fresh cladodes were mixed for 1 min in a
ratios than for the O. ficus-indica. Mucilage molecules tend blender with water in a ratio of 1:8 (w/v). Then, suspension
to be negatively charged, because hydrogen ions can dissoci- was maintained at 83C for 2 h. Afterwards suspension was
ate from their carboxylic part of the galacturonic acids centrifuged at 3,500 rpm for 15 min. The supernatant was
(Gibson and Nobel 1990). This is important, because some added with ethanol 96% in a ratio of 1:4 (v/v). Mucilage
physiochemical properties of the mucilage are dependent mass was separated by centrifugation at 3,500 rpm for
on the ionized form of the carboxylic group. According to 15 min (a method proposed by Zavala 2012). (2) Fresh
Cárdenas et al. (2008), the rheological properties, mainly cladodes were mixed for 1 min in a blender with water in a
the intrinsic viscosity of mucilage, are dependent on their ratio of 1:2 (w/v). Then, suspension was maintained at 83C
chemical composition, pH, sterification degree and the for 1 h. Following that, suspension was centrifuged at
presence of calcium ions. Mucilage is a compound of a low 3,500 rpm for 15 min. The supernatant was added with
degree of esterification (DE) (Cárdenas et al. 2008). ethanol 96% in a ratio of 1:4 (v/v). Mucilage mass was sepa-
Some authors studied the sugar composition of mucilage rated by centrifugation at 3,500 rpm for 15 min (a method
from O. ficus-indica normally using chromatography tech- proposed by Rodríguez 2010); and (3) Fresh cladodes were
niques (Table 1). The objective of this work was to charac- mixed for 1 min in a blender with ethanol solution 50% in a
terize the profile of the sugar composition of mucilage from ratio of 1:1 (w/v). Then, suspension maintained at 22C was
six species of Opuntia collected in Michoacán, México. Five centrifuged at 3,500 rpm for 15 min. The supernatant was
of the specimens studied were from wild species and were added with ethanol 96% in a ratio of 1:4 (v/v). Mucilage
compared with the species most studied in the world, mass was separated by centrifugation at 3,500 rpm for
286 Journal of Food Process Engineering 37 (2014) 285–292 © 2014 Wiley Periodicals, Inc.
S. RODRÍGUEZ-GONZÁLEZ ET AL. MUCILAGE FROM WILD SPECIES OF OPUNTIA
Chemical Composition
Moisture, ash, protein and fat content of mucilages were
determined by methods 925.45, 945.18, 955.04 and 920.39
of the AOAC (2005), respectively. The protein quantity was
calculated by multiplying the nitrogen content using the
Kjeldahl method by the coefficient 5.73. Total dietary fiber
(TDF), soluble fiber (SF) and insoluble fiber (IF) was
carried out using the method of Prosky et al. (1998). Total
available carbohydrates (Anthrone method) were deter-
mined according to the method reported in AOAC (1990).
Journal of Food Process Engineering 37 (2014) 285–292 © 2014 Wiley Periodicals, Inc. 287
MUCILAGE FROM WILD SPECIES OF OPUNTIA S. RODRÍGUEZ-GONZÁLEZ ET AL.
a–d Different letters in the same row are significant differences between means of species.
(P < 0.05) in all species. The main chemical component of average value of 37.3%. Calcium content was the predomi-
the six species of Opuntia was the TDF. The highest value of nant mineral in the mucilages. The highest calcium values
TDF was seen in the species O. hyptiacantha (73.01%) fol- were for O. atropes (7.44 g/100 g) and O. streptacantha
lowed by O. tomentosa (68.43%), O. streptacantha (67.44%), (6.87 g/100 g). The protein content found in the mucilages
O. joconostle (65.2%), O. atropes (57.71%) and O. ficus- ranged from 4.01% in O. atropes to 8.26% in
indica (57.23%). The TDF value obtained in this study was O. streptacantha. O. ficus-indica showed a value of 5.24%.
similar (57.83%) to that documented by Rodríguez (2010) Sepúlveda et al. (2007) report an average protein value of
for O. ficus-indica. Most of the TDF corresponded to the SF 7.3% for O. ficus-indica, meanwhile Rodríguez (2010)
fraction. The O. hyptiacantha had the highest value of SF reports a value of 6.69%, and both values were slightly
(67.51%) and did not show a significant difference lower than our results. The fat content was as much as 0.2%
(P < 0.05) as compared with O. joconostle (65.12%) and or lower in the mucilage extracted from the six species of
O. tomentosa (64.04%), and only presented a partial differ- Opuntia studied. Total carbohydrates obtained in this study
ence (P < 0.05) with respect to the O. streptacantha was as follows: O. atropes 18.67%, O. ficus-indica 14.67%,
(61.07%) and O. atropes (57.69%) species. The O. ficus- O. joconostle 9.82%, O. tomentosa 8.21%, O. hyptiacantha
indica species had the lowest SF value (51.79%). This result 6.25% and O. streptacantha 1.62%.
was similar to the SF value (56.80%) reported by Rodríguez
(2010) for the O. ficus-indica species. The IF values in the
TLC
mucilage species were as follows: 6.37%, 5.50%, 5.43%,
4.03%, 0.08% and 0.03%, respectively, for O. streptacantha, Table 3 shows the monosaccharides, uronic acids and the
O. hyptiacantha, O. ficus-indica, O. tomentosa, O. joconostle mucilage detected by TLC. The presence of free monosac-
and O. atropes. The ash content for the mucilages varied charides (mainly D-xylose) was observed in the methods of
from 10.82% (O. hyptiacantha) to 15.13% (O. ficus-indica). Rodríguez (2010) and Zavala (2012). The temperature,
In general, the ash content in O. ficus-indica obtained in this extraction time and ratio of cladodes : water used by
study was similar to that documented by Rodríguez (2010), Rodríguez (2010) and Zavala (2012) could have hidrolyzed
who reported 11.91%; however, our results are different the native structure of mucilages during the extraction
from those found by Sepúlveda et al. (2007), who report an process releasing some monosaccharides and uronic acids.
TABLE 3. DETERMINATION OF SUGARS AND URONIC ACIDS IN MUCILAGE EXTRACTED FROM SIX SPECIES OF OPUNTIA (%)
Species of Opuntia
Opuntia Opuntia Opuntia Opuntia Opuntia Opuntia
Sugar tomentosa atropes hyptiacantha joconostle streptacantha ficus-indica
L-arabinose 33.50ab 34.36a 32.82ab 26.83c 30.43b 35.36a
D-galactose 21.59d 26.75c 30.83b 45.48a 31.83b 27.26c
D-xylose 16.02a 16.62a 17.05a 12.23c 14.04b 16.32a
D-glucose 16.21a 9.05c 6.03de 7.13d 11.81b 5.18e
L-rhamnose 2.58c 1.44e 1.41e 4.09b 5.40a 1.93d
Uronic acids 11.80b 11.76b 11.84b 5.59d 8.26c 13.91a
Different letters in the same row are significant differences between means in species.
288 Journal of Food Process Engineering 37 (2014) 285–292 © 2014 Wiley Periodicals, Inc.
S. RODRÍGUEZ-GONZÁLEZ ET AL. MUCILAGE FROM WILD SPECIES OF OPUNTIA
The differences in the processes employed by Rodríguez and Trachtenberg and Mayer (1981), and is different
(2010) and Zavala (2012) were as follows: Rodríguez (2010) from those reported by McGarvie and Parolis (1981),
used a ratio of cladodes : water of 1:2 (w/v) and the extrac- Medina-Torres et al. (2000), Habibi et al. (2004), and
tion time was 1 h. Meanwhile, Zavala (2012) used a ratio Majdoub et al. (2010) for mucilage from O. ficus-indica.
cladodes : water of 1:8 (w:v) and an extraction time of 2 h. The differences in sugar composition in mucilages reported
Both methods employed 83C to extract the mucilage. On by different authors for O. ficus-indica could vary, depend-
the other hand, in the modified method, neither the pres- ing on the source and conditions of extraction, location
ence of free monosaccharides nor uronic acids was observed and other environmental factors such as age of the
only the presence of mucilage. This method uses a ratio cladodes, climatic conditions and soil where the Opuntia
cladodes : ethanol at 50% of 1:1 at a temperature of 22C, grow – as was indicated by Cárdenas et al. (1997), Ribeiro
and no extraction time was used. For this reason, we used et al. (2010), Majdoub et al. (2010) and Guevara-Arauza
the mucilage extracted from modified method to character- et al. (2012).
ize their sugars profile by gas chromatogram. Statistical analysis shows a highly significant effect
(P < 0.001) on the species depending on sugar content. The
D-galactose content in mucilage obtained from O. joconostle
Gas Chromatogram
(45.48%) was higher (P < 0.05) than the other Opuntia
The chromatograms (Fig. 2) showed the presence of species. The lowest value corresponded to O. tomentosa
D-galactose, L-arabinose, L-rhamnose, D-xylose, D-glucose (21.59%). The highest value of glucose was observed
and uronic acids, in all samples of mucilages extracted, using in O. tomentosa (16.21%) (P ≤ 0.05), followed by O.
the modified method. We select only the chromatogram of streptacantha (11.81%) and O. atropes (9.05%). The lowest
two species because the chromatogram peaks of the sugars was observed in O. ficus-indica (5.18%). Some authors such
detected can be better observed. Our results agree with those as McGarvie and Parolis (1981) and Gibson and Nobel
obtained by Ginestra et al. (2009), Habibi et al. (2004), (1990) did not discover the presence of D-glucose in the
Majdoub et al. (2010) and Ribeiro et al. (2010). mucilage of O. ficus-indica. However, several authors did
The most abundant sugars contained in the mucilages document the presence of glucose (Habibi et al. 2004;
(in decreasing order, Table 3) were as follows: L-arabinose Ginestra et al. 2009; Majdoub et al. 2010 and Ribeiro et al.
(26.83–35.36%), D-galactose (21.59–45.48%), D-xylose 2010). The values of D-glucose obtained by these authors
(12.23–17.05%), uronic acids (5.59–13.91%), D-glucose are lower than our results. The higher values of L-rhamnose
(5.18–16.21%) and L-rhamnose (1.41–5.40%). This abun- (P < 0.05) correspond to the mucilage from O. streptacantha
dance order for all species of Opuntia obtained in our study (5.40%). The lowest L-rhamnose values (P < 0.05) were
was similar to the values documented by Nobel et al. (1992) found in O. hyptiacantha (1.41%) and O. atropes (1.44%).
Journal of Food Process Engineering 37 (2014) 285–292 © 2014 Wiley Periodicals, Inc. 289
MUCILAGE FROM WILD SPECIES OF OPUNTIA S. RODRÍGUEZ-GONZÁLEZ ET AL.
290 Journal of Food Process Engineering 37 (2014) 285–292 © 2014 Wiley Periodicals, Inc.
S. RODRÍGUEZ-GONZÁLEZ ET AL. MUCILAGE FROM WILD SPECIES OF OPUNTIA
rhamnose. The mucilage studied from wild species contains FOX, D.I., PICHLER, T., YEH, D.H. and ALCANTAR, N.A.
a higher content of FD and FS than the commercial species 2012. Removing heavy metals in water: The interaction of
O. ficus-indica. All species of Opuntia had low DE evidenced cactus mucilage and arsenate (As (V)). Environ. Sci. Technol.
by FTIR studies. For this reason, the mucilage of the five 46, 4553–4559.
wild species could also be exploited to produce hydro- GIBSON, C.A. and NOBEL, S.P. 1990. Special chemicals. In The
colloids of importance in the food industry. We recom- Cactus Primer pp. 198–199, First Harvard University Press,
mended studies of viscosity and emulsifying properties of Cambridge, MA.
mucilages from wild species to propose specific uses. GINESTRA, G., PARKER, L.M., BENNETT, N.R., ROBERTSON,
J., MANDALARI, G., NARBAD, A., LO CURTO, B.R.,
BISIGNANO, G., FAULDS, B.C. and WALDRON, W.K. 2009.
Anatomical, chemical, and biochemical characterization of
ACKNOWLEDGMENTS cladodes from prickly pear [Opuntia ficus-indica (L.) Mill]. J.
Agric. Food Chem. 57, 10323–10330.
This work was supported by the Coordinación de la
GUEVARA-ARAUZA, J.C., ORNELAS-PAZ, J.J.,
Investigación Cientifica. Universidad Michoacana de San PIMENTEL-GONZALEZ, D.J., ROSALES, M.S., SORIA,
Nicolás de Hidalgo (CIC-UMSNH), project 26.1, 2012. G.R.E. and PAZ, M.L.M.T. 2012. Prebiotic effect of mucilage
Sarahí Rodríguez González and Eder Zavala Mendoza wish and pectic-derived oligosaccharides from nopal (Opuntia
to thank CONACyT for the scholarship received for MSc ficus-indica). Food Sci. Biotechnol. 21, 997–1003.
studies. HABIBI, Y., HEYRAUD, A., MAHROUZ, M. and VIGNON,
M.R. 2004. Structural features of pectic polysaccharides from
the skin of Opuntia ficus-indica prickly pear fruits. Carbohydr.
Res. 339, 1119–1127.
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292 Journal of Food Process Engineering 37 (2014) 285–292 © 2014 Wiley Periodicals, Inc.