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DOI: 10.1111/jfpp.14026
ORIGINAL ARTICLE
1
Tecnológico Nacional de México, Instituto/
Tecnológico de Durango, Departamento Abstract
de Ingenierías Química y Bioquímica. Blvd. The effect of dehydrated apple‐based snack supplemented with Agave fructans on
Felipe Pescador 1830 ote. Colonia Nueva
Vizcaya., Durango, Dgo., Mexico short‐chain fatty acids (SCFA) production in mice was evaluated. Animals were ran‐
2
Unidad de Investigación Biomédica del domly divided into three groups (n = 8): Control group (CG), oligofructose (OG), and
Instituto Mexicano del Seguro Social,
Agave fructans (AG). After 24 days of treatment (stage 1), AG and OG showed el‐
Durango, Dgo., Mexico
3
Food Research Department, School of
evated levels of acetate (10 µmol/g for both treatments), propionate (2.4 µmol/g for
Chemistry, Universidad Autónoma de both treatments), and butyrate (1.5 and 3.2 µmol/g for OG and AG, respectively)
Coahuila, Saltillo, Mexico
4
compared with the CG. After 42 days of treatment (stage 2), AG had higher concen‐
Departamento de Biotecnología y
Bioquímica, Centro de Investigación y trations of acetate (20.8 µmol/g), propionate (2.1 µmol/g), and butyrate (5.5 µmol/g);
de Estudios Avanzados del IPN, Unidad whereas, OG only exhibited higher levels of acetate (16.8 µmol/g) and butyrate
Irapuato, Apartado Postal 629, C.P. 36821,
Irapuato, Gto., Mexico (5.6 µmol/g) in comparison with the controls. Dehydrated apple‐based snack supple‐
mented with Agave fructans exhibits a prebiotic effect increasing SCFA production
Correspondence
Mercedes G. López, Departamento de in mice.
Biotecnología y Bioquímica, Centro de Practical applications
Investigación y de Estudios Avanzados del
IPN, Campus Guanajuato, Apartado Postal Dehydrated fruit‐based snacks are generally perceived by consumers as healthy
629, Irapuato, Gto., 36500 Mexico. products with acceptable sensory attributes. They have a prolonged shelf life and
Email: mercedes.lopez@cinvestav.mx
Claudia I. Gamboa‐Gómez, Unidad de may be consumed directly or cut into small parts for use in confectionery and bakery.
Investigación Biomédica del Instituto In addition, the products derived from fruits plus prebiotics can enhance the ben‐
Mexicano del Seguro Social, Delegación
Durango. 34067, Durango, Mexico. eficial effect on health and increase their consumption. This study opens up some
Email: clau140382@hotmail.com commercial potential and technical challenges of using prebiotic‐based supplements.
Funding information
Strengthening and Development of
Scientific and Technological Infrastructure
Program, Grant/Award Number: 253333
and 224651; Mexican National Council of
Science and Technology (CONACYT), Grant/
Award Number: 55354
1 | I NTRO D U C TI O N metabolic disorders. In this regard, there is a growing interest for
functional foods which provides an additional benefit to health
Currently, western countries are characterized by changes in life‐ (Ozen, Pons, & Tur, 2012). However, one important factor to be con‐
style associated to an increase on the consumption of fast food and sidered for functional food to be accepted by the consumer are the
unhealthy snacks, with a consequent increase in the incidence of way in which it is offered (González‐Herrera et al., 2016). Dehydrated
J Food Process Preserv. 2019;00:e14026. wileyonlinelibrary.com/journal/jfpp © 2019 Wiley Periodicals, Inc. | 1 of 8
https://doi.org/10.1111/jfpp.14026
|
2 of 8 GONZÁLEZ‐HERRERA et al.
fruit‐based snacks are generally perceived by consumers as healthy having slight mechanical damage, deformed, among others) were
products with acceptable sensory attributes. In addition, it has been used for dehydrated apple‐based snack preparation. The tested
reported that are good carrier for nutraceuticals such as probiotics commercial prebiotics were: Agave fructans from Agave tequilana
and prebiotics (Rêgo, Freixo, Silva, Gibbs, & Teixeira, 2013). These Weber (90% inulin and 10% glucose/fructose/sucrose content.
latter are defined as non‐digestible carbohydrates that are selec‐ American Foods, Jalisco, México), citric acid, glucose, fructose, and
tively fermented allowing specific changes in the composition and/ sucrose from Sigma Aldrich (St. Louis, MO.), and oligofructose (93%
or activity of the microbiota resulting in health benefits to the host oligofructose and 7% glucose/fructose/sucrose content. Raftilose
(Gibson et al., 2010). Non‐digestible carbohydrates are the main en‐ P95 Beneo e Orafti, Tienen Belgium) donated by MEGAFARMA S.A.
ergy and carbon source for colonic microorganisms, which have the de C.V. México. This latter was used as an active control.
capacity to hydrolyze particularly polysaccharides complex leading
to production of several metabolites that influence host metabolism
2.2 | Dehydrated apple‐based snack preparation
(Gill et al., 2006). The most‐studied non‐digestible carbohydrate is
oligofructose, which avoids the digestive process in the upper gas‐ Dehydrated apple‐based supplement snack with Agave fructans
trointestinal tract reaching the large intestine to be fermented to from Agave tequilana or oligofructose were performed accord‐
organic acids in the colon by the saccharolytic resident microbiota ing to the methodology described by González‐Herrera et al.
(Kolida, Tuohy, & Gibson, 2002). Accordingly, oligofructose provides (2016). Briefly, samples of 220 g of apples were washed, slice, and
energy for other bacteria, bowel epithelium, and peripheral tissues grounded for six minutes using a kitchen blender (“Oster” mod.
(Conlon & Bird, 2014). Moreover, Agave fructans are reserve carbo‐ 004093 NPO, México City, México). In this step, a solution of the
hydrates from Agave tequiliana. These are a highly branched complex corresponding prebiotics (Agave fructans or oligofructose) was
structure formed by links β (2‐1) and β (2‐6) and different ranging de‐ added (diluted in 50 ml of a solution of citric acid, 10 g/L). Heat
grees of polymerization from 3 to 30 monosaccharide units (Arrizon, treatment (75°C for 10 min) was applied. After, 200 g of each for‐
Morel, Gschaedler, & Monsan, 2010). This structure makes fructans mulation were poured in 20 × 35 cm metal trays lined with cel‐
resistant to hydrolysis by human digestive enzymes and may be fer‐ lophane paper (3 mm of thickness). Samples were allowed to cool
mented only by colonic microflora producing short‐chain fatty acids down at room temperature for 2 hr up to 27°C before their drying
(SCFA) which are the main bacterial metabolites (Franco‐Robles & process. Apple matrices with prebiotics were dried using a dryer
López, 2015). SCFA are a subset of saturated fatty acids with six (“POLINOX,” mod. SEM‐2, México City, México) at 60°C for 5 hr
or less carbon molecules (e.g., acetate, propionate, and butyrate). with an air velocity of 2 m/s. The final concentration of prebiotic,
These are produced by acidogenesis, acetogenesis, and homoaceto‐ moisture, thickness, and hardness were 15 g of prebiotic/100 g
genes bacterial processes (Zhang et al., 2018). Besides, SCFA may be per dehydrated apple‐based snack, 150–180 g/kg, 0.5 mm, and
further re‐captured for energy recovery which might later be used 4.0 N, respectively.
as a raw substrate for other microorganism reactions (Wang et al., Dehydrated apple‐based snack was vacuum packed in high‐den‐
2018). sity polyethylene bags and stored at room temperature.
The SCFA exhibit cellular and molecular mechanisms includ‐
ing inhibition of histone deacetylases and activation of G‐protein‐
2.3 | Animals and experimental design
coupled receptors, and their deficiency may be related with some
diseases such as allergies, asthma, several types of cancers, autoim‐ The protocol was approved by the animal ethics committee of the
mune diseases, metabolic diseases, and neurological diseases (Tan TECNM/Instituto Tecnológico de Durango, Durango, México and all
et al., 2014). experiments on animals were performed in accordance with the ani‐
Furthermore, although it has been suggested a prebiotic po‐ mal care and use protocol of the Norma Oficial Mexicana NOM‐062‐
tential of Agave fructans and oligofructose (Crispín‐Isidro, Lobato‐ ZOO‐1999, as recommended by National Institutes of Health (NIH),
Calleros, Espinosa‐Andrews, Alvarez‐Ramirez, & Vernon‐Carter, 2002 Guidelines.
2015; Gibson et al., 2010), the prebiotic impact in vivo of dehydrated Female C57BL/6 mice (Rismart SA de CV, México City, México),
apple‐based snack supplemented with fructans from Agave tequil‐ 12 weeks old, were housed in a light and temperature‐controlled
iana on SCFA concentrations has not been investigated. Thus, the room (12–12 hr light–dark cycle; 25 ± 1°C). Mice were randomly di‐
aim of the present study was to evaluate the effect of Agave fruc‐ vided into three groups of eight animals each. (1) Control group (CG):
tans‐based supplement on SCFA production in C57BL/6 mice. dehydrated apple‐based snack without prebiotic (3.9 g/kg of body
weight per day). (2) Agave fructans group (AG): 3.9 g of dehydrated
apple‐based snack supplemented with Agave fructans/kg of body
2 | M ATE R I A L S A N D M E TH O DS
weight per day, and (3) oligofructose group (OG): 3.9 g of dehydrated
apple‐based snack supplemented with oligofructose/kg of body
2.1 | Materials
weight per day.
Representative samples of “Red delicious” apples from Canatlán The doses used were equivalent to 1 g/day in humans, which
Durango, Mexico with low commercial value (smaller than standard, represent 0.2% of fiber recommended per day by the WHO
GONZÁLEZ‐HERRERA et al. |
3 of 8
Washing period
humans to the animal model was carried out according to the for‐
1.1 ± 0.02
0.8 ± 0.02
1.0 ± 0.02
19.5 ± 0.5
mula reported by Reagan‐Shaw, Nihal, and Ahmad (2008).
Groups were fed with a base diet (proteins 23%, lipids 4.5% [1%
saturated fat], and carbohydrates 64%) for seven weeks. Diets and
water were provided ad libitum to all groups. After one week of ac‐
0.9 ± 0.02
1.1 ± 0.01
1.0 ± 0.01
19.2 ± 0.4
Stage 2 climatization, treatments were administered during six weeks using
oral via to the corresponding groups. Body weight was measurement
weekly; food and water intake were assessed daily.
1.0 ± 0.03
1.7 ± 0.02
1.2 ± 0.01
18.5 ± 0.3
Stage 1
2.4 | Sample collection
Oligofructose group
1.3 ± 0.01
1.1 ± 0.01
stage), at 24 (stage 1) and 42 days (stage 2) after treatment, as well at
Washing period Basal state
14.8 ± 0.5
0.8 ± 0.01
18.0 ± 0.8
2.5 | Bacterial enumeration
Sample of feces (100 mg/ml) were serially diluted 10‐fold with an‐
1.0 ± 0.02
1.1 ± 0.01
1.0 ± 0.01
17.7 ± 0.6
1.2 ± 0.01
1.3 ± 0.01
1.0 ± 0.01
14.0 ± 0.5
2.6 | Sample preparation
One ml of formic acid (1%) was added to 40 mg of each feces sam‐
ple, followed by a mixing for 2 min using an Ultra‐Turrax homog‐
Note: Values are expressed as mean ± standard error (n = 7).
1.4 ± 0.03
0.9 ± 0.02
0.8 ± 0.02
17.6 ± 0.8
enizer (IKA, Lab. Equip., Staufen, Germany) to extract the SCFA. The
Stage 2
1.0 ± 0.02
1.1 ± 0.01
Then, 500 μl of ethyl acetate was added, and vortex mixing (1 min).
17.4 ± 0.3
Stage 1
1.3 ± 0.01
1.5 ± 0.01
1.1 ± 0.01
Basal state
2.7 | Chemical derivatization
The derivatization reaction of feces extract was performed accord‐
ing the methodology described by Han, Lin, Sequeira, and Borchers
Fecal weight (g)
Food consump‐
sumption (ml)
(2015) with few modifications. Briefly, 20 μl were mixed with 10 μl
Water con‐
The mixtures were reacted at 40°C for 30 min. After reaction, the for column stabilization. Multiple reaction monitoring (MRM) data
mixtures were cooled on ice for 1 min before dilution with 960 μl were collected from 0 to 15 min. Negative ionization mode was
of aqueous acetonitrile (10%) (50:50). Solutions were injected into used for MS assays. Electron spray ionization (ESI) conditions were
the ultra‐performance liquid chromatography coupled with tandem as follows: capillary voltage 1.5 kV, 350°C of desolvation tempera‐
mass (UPLC‐MS/MS) instrument. ture, 2V for cone, 150°C of source temperature, desolvation and
cone gas 350 and 151L/h; nebulizer gas flow 7.0 Bar, and collision
gas 0.13 ml/min. For identification and quantification, a multiple
2.8 | Ultra‐performance liquid chromatography
reaction‐monitoring mode with standards (acetate acid, propionic
coupled with tandem mass spectrometry analysis
acid, and butyric acid from Sigma‐Aldrich, USA) was used. The
Acquity UPLC system (Waters Corp., Milford) coupled with a tan‐ UPLC and tandem Xevo TQ‐S triple quadrupole mass spectrome‐
dem Xevo TQ‐S triple quadrupole mass spectrometer (Waters ter control and data were processed using MassLinx v. 4.1 (Waters
Corp., Wexford) were used for sample analysis. The LC system Corp.) Software.
consisted of a sample manager (20°C) and a binary solvent man‐
ager. The column used to determine SCFA was an Acquity UPLC
2.9 | Statistical analysis
HSS C18 SB, 100 mm × 2.1 mm, 1.8 µm (Waters Corp., Wexford)
operated at 40°C. The elution profile included two solvents (LC‐ Data were expressed as mean values ± standard error (SE). Statistical
MS, both J.T. Baker): acidified water with 0.01% formic acid (sol‐ significance was determined by one‐way variance analysis (ANOVA)
vent A) and acetonitrile with 0.01% formic acid (solvent B), flow (p < 0.05) followed by the Tukey's test. Statistical analysis was made
rate was 0.350 ml/min: initial 85% A, 0–2 min, 45% A, 2–9 min, using the SigmaPlot software version 13.0 (Systat Software, Inc., San
0% A, 9–10 min, 0% A, 10–13 min, and 85% A (linear gradient) Jose, CA, USA).
F I G U R E 1 Bacterial concentrations (a: Bifidobacteria, b: Lactobacilli, c: Total coliforms, d: Gram‐positive cocci) in feces of mice treated with
Agave fructans (AG), oligofructose (OG), and dehydrated apple‐based snack without prebiotic as control (CG). Values are means of triplicate
determinations ± standard error. a,b,c Different letters are significantly different between groups for each stage (p ≤ 0.05) by Tukey's test
GONZÁLEZ‐HERRERA et al. |
5 of 8
F I G U R E 2 Short‐chain fatty acids contend (a: acetate, b: propionate, and c: butyrate) in feces of mice treated with Agave
fructans (AG), oligofructose (OG), and dehydrated apple‐based snack without prebiotic as control (CG). Values are means of duplicate
determinations ± standard error
|
6 of 8 GONZÁLEZ‐HERRERA et al.
(5.6 µmol/g) than the CG. Finally, after washing period, both inter‐ bacteria, and intestinal transit time (Cook & Sellin, 1998; Cummings
vention groups returned to basal conditions (Figure 2). et al., 1997; Roberfroid, 2005). In this regard, the significant effect
of AG on SCFA production may be related to the high degree of po‐
lymerization (DP23) of AG which leads to a slower fermentation in
4 | D I S CU S S I O N the caecum and proximal colon reaching the distal colon with few
structural changes, where the resident bacteria use these indigest‐
The present study demonstrated that the intake of dehydrated ible carbohydrates to produce high concentrations of SCFA (Hughes
apple‐based snack supplemented with Agave fructans improves the & Rowland, 2000) resulting in an acidic environment that favors
production of SCFA. In addition, the concentrations of bifidobacteria the maintenance and development of bacterial strains involved in
and lactobacilli were also increased by Agave fructans supplemented the synthesis of SCFA (Gibson, 1999; Gibson, Probert, Loo, Rastall,
apple‐based snack, while the concentrations of coliforms and cocci & Roberfroid, 2004; Huazano‐García & López, 2013). Hence, this
were reduced. mechanism could explain, at least in part, the beneficial effect of AG
In agreement with our results, Pompei et al. (2008) also observed in the reduction of coliforms and cocci.
similar changes on bifidobacteria and lactobacilli in favor of fructans Because the proportions of SCFA can vary depending on diet,
compared with oligofructose. This could be due to the presence of microbiota composition, site of fermentation, and host genotype
agave fructans which have very complex molecular structures in‐ (Hamer et al., 2008), the microbiota modulation and SCFA produc‐
cluding highly branched and present a terminal glucose molecule tion could be a novel target in the prevention and/or treatment of
(graminans) or internal glucose (agavins) (Mancilla‐Margalli & López, several diseases. In this context, previous studies have indicated
2006). The branches in the Agave fructans result in terminal fruc‐ that specific SCFA may reduce the risk of developing some chronic
tose available for the fructosyltransferases of bacteria (Huazano‐ gastrointestinal disorders such as inflammatory bowel disease and
García & López, 2013) favoring the fermentation process of these colorectal cancer (Huda‐Faujan et al., 2010; Scheppach, Bartram, &
fructans. Richter, 1995). However, further research in this field is required in
In addition, an efficient fermentation process is characterized order to elucidate the biological mechanisms induced by prebiotic
by the decrease in pH promoting an acid environment (Huazano‐ therapy on humans.
García & López, 2013), which is highly beneficial for the growth
of bacteria such as bifidobacteria and lactobacilli but is detrimen‐
tal for the growth undesirable species such as coliforms and cocci 5 | CO N C LU S I O N S
(Márquez‐Aguirre et al., 2013; Pan, Chen, Wu, Tang, & Zhao,
2009). Results of the present study revealed that the dehydrated apple‐
The principal end products of fructans metabolism are SCFA based snack supplemented with Agave fructans increases the pro‐
(Cummings & Macfarlane, 1991). The production of SCFA is per‐ duction of SCFA by changes in the microbiota. Thus, Agave fructans
formed in the caecum and distal colon. These are rapidly absorbed supplement acts as nutraceutical and might be a new alternative for
and only from 5% to 10% are excreted in the feces; once absorbed, prevention or treatment of human diseases; however, future clinical
SCFA are metabolized mainly in the cells of the caecum‐colonic epi‐ trials are warranted in order to confirm our findings.
thelium for maintenance energy, by hepatocytes for gluconeogene‐
sis, and by muscle cells for generating energy (Van Loo, Coussement,
Leenheer, Hoebregs, & Smits, 1995). Nevertheless, although the AC K N OW L E D G M E N T S
concentrations of SCFA in feces are not the best method to mea‐ This project was financially supported by Strengthening and
sure the production rates, this evaluation is considered an accept‐ Development of Scientific and Technological Infrastructure Program
able indicator to evaluate the effect of fructans diet since a large (Grants No. 253333 and 224651) also CONACyT is acknowledged.
proportion is taken up by the colonic mucosa (Huazano‐García & SMGH thanks to the Mexican National Council of Science and
López, 2013). With this regard, we found that the intake of dehy‐ Technology (CONACYT) for the financial support during her doctor‐
drated apple‐based snack supplemented with Agave fructans or ate studies through the scholarship 55354.
oligofructose improves the production of SCFA in mice compared
with CG. The elevation of SCFA observed in both groups varies ac‐
cording to the type of prebiotic and treatment period. Interestingly, C O N FL I C T O F I N T E R E S T
in stage 1, OG showed a greater effect in butyrate concentrations in
The authors have declared no conflicts of interest for this article.
comparison with AG; however, this effect was similar in both groups
during stage 2. Several studies have reported that the production
of SCFA is affected by diverse factors such as the chemical com‐
ORCID
position of the substrate, the bacterial species composition of the
microbiota, the competitive and cooperative interactions between Claudia I. Gamboa‐Gómez https://orcid.org/0000-0002-2815-9406
GONZÁLEZ‐HERRERA et al. |
7 of 8
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