Introduction
Diets rich in tropical fruits have been associated with reduce develop of some
diseases. An essential part of a healthy diet is the consumption of fruits, because
it has been demonstrated that fruits can be an important source of some compounds
known as bioactive compounds (BC) such as phenolic compounds (PC). Guava
(Psidium guajava) and soursop (Annona
muricata) are two tropical fruits that are a source of dietary fiber
and PC, and the combination of these components may have an additive and/ or
synergistic effect in healthy properties (Ajila &
Prasada Rao, 2013; Liu, 2003;
Quirós-Sauceda et al.,
2014). Guava and soursop are mainly consumed fresh, but also they are
consumed as processed products, mainly as purees due to the consumers increase the
demand of processed products that are easily accessible, ready to eat and provide
health benefits (Pérez-Beltrán et
al, 2017). Most studies are focused only in the
quantification of PC from plant foods; while other studies highlight the effect of
the combination or addition of fruit ingredients to processed foods to increase the
content of BC that improve their functional properties (Blancas-Benítez, de Jesús Avena-Bustillos, Montalvo-González,
Sáyago-Ayerdi & McHugh, 2015a; Kristl, Slekovec, Tojnko, & Unuk, 2011).
However, despite of the fact that the PC have shown important biological properties,
including their strong in vitro antioxidant capacity (Abderrahim et al, 2015; Tang et al, 2015), their
simple chemical identification and in vitro assessments can not
necessarily is taken as a direct prediction of their real potential effect on human
health. The simple quantification of PC do not include an assessment of the
bioaccessibility of BC (Rein et
al., 2013), since a compound can only exert health benefits
if it remains available for absorption after all the phases involved in the
gastrointestinal digestion process have taken place (Espín, García-Conesa, & Tomás-Barberán, 2007; Rein et al., 2013). The scientific literature
contains several studies where the BC content of guava and soursop have been
determined (Coria-Téllez, Montalvo-Gónzalez, Yahia,
& Obledo-Vázquez, 2018; Jiménez-Escrig, Rincón, Pulido, & Saura-Calixto, 2001; Onyechi, Ibeanu, Nkiruka, Eme, & Madubike,
2012; Rojas-Garbanzo, Zimmermann,
Schulze-Kaysers, & Schieber, 2017; Soares, Pereira, Marques, & Monteiro, 2007). However, there are no
reports on the bioaccessibility of the PC presents in processed fruit products like,
purees. Thus, the aim of this work was to determine, using an in
vitro digestion procedure, the in vitro
bioaccessibility and release kinetics of PC from guava and soursop pulp.
Materials and methods
Sample preparation
Guava (Psidium guajava L.) and soursop (Annona
muricata L.) fruits were acquired from a local market in Tepic,
Nayarit. The fruits were used in maturity stage they were transported to the
Laboratorio Integral de Investigación en Alimentos, and were processed
immediately to produce the purees. The guava was used only seedless, while
soursop fruit was used the pulp without peel and seeds. The samples were
homogenized (Ultraturrax, T25, IKAworks, Wilmington, NC) and were freeze-dried
(Labconco Model 77522020, Kansas, USA) ground, sieved and stored hermetically
for later use in analysis.
In vitro digestion model and bioaccessibility percentage
(%) in guava and soursop pulp
Freeze-dried guava and soursop pulps were submitted to an in
vitro digestion model adapted from the methodology proposed by
Saura-Calixto, García-Alonso, Goñi, &
Bravo (2000) with some modifications (Blancas-Benítez, Pérez-Jiménez, Montalvo-González, González-Aguilar &
Sáyago-Ayerdi, 2018) (Figure 1).
Firstly, the samples were subjected to an enzymatic hydrolysis process with
pepsin (300 mg/mL, P-7000, Sigma Aldrich) (37 °C, 1 h) (Step 1,
gastric fraction-GasF), pancreatin (5 mg/mL, P-1750, Sigma Aldrich) (37 °C, 6 h)
and α-amylase (120 mg/mL, A-6255, Sigma Aldrich) (37 °C, 16 h) (Step
2, intestinal fraction-IntF). After the hydrolysis, samples were
centrifuged (Step 3) to separate the soluble and insoluble
indigestible fractions. The supernatants were dialyzed (D9652, 12-14 KDa, Sigma
Aldrich, 48 h) to simulate passive absorption (Step 4). After
dialysis, the PC associated with the soluble indigestible fraction (SIF) was
determined (Step 5). The residue, after samples were centrifuged
was used to determine the PC associated with insoluble indigestible fraction
(IIF) after an organic extraction (Pérez-Jiménez
et al., 2008) (Step 6). Both the PC
associated with the SIF and IIF correspond to the non-bioaccesible PC fraction.
The total soluble polyphenols (TSP) content of the different fractions GasF,
IntF, SIF, and IIF were determined, and the samples were analyzed by HPLC-DAD as
described below. The in vitro bioaccessibility percentage (%BA)
of PC was determined using Eq. 1:
Figure 1
Bioaccesibility of phenolic compounds in guava and soursop pulp
samples: Step 1 gastric fraction, Gas-F (Pepsine), Step 2 intestinal
fraction, Int-F (Pancreatine and amylase), Step 3 centrifugation to
separate supernatants and residues, Step 4 dialysis 24-48 h, Step 5
non-bioaccesible PC, associated to soluble indigestible fraction
(SIF), Step 6 non-bioaccesible PC, associated to insoluble
indigestible fraction (IIF).
Where PC-IntF= the PC released on the intestinal fraction, PC-SIF= the PC
associated with the IIF, and PC-IIF= the PC associated with the IIF.
In vitro release kinetics of PC in guava and soursop
pulp
The in vitro released kinetics of PC from guava and soursop pulp
were determined according to an in vitro digestion method
(Blancas-Benítez et al.,
2015b) Briefly, 300 mg of dried sample was weighed and combined with
10 mL of phosphate buffer (0.05 M, pH 1.5) and 0.2 mL of pepsin solution (300
mg/mL, P-7000, >250 units/mg, Sigma Aldrich). The solution was incubated at
37 °C for 1 h, afterwards, phosphate buffer (4.5 mL, 0.05 M, pH 6.9) was added,
and the samples were transferred to cellulose dialysis bags (D9652, 12-14 KDa,
Sigma Aldrich). One milliliter of pancreatic α-amylase (120 mg/mL, A-6255, 110
units/mg, A6255, Sigma) was added to each dialysis bag, the samples were
adjusted to a volume of 30 mL, and the dialysis tubes were sealed. The tubes
were placed in a glass vessel with 200 mL of phosphate buffer (0.05 M, pH 6.9)
that had previously been stabilized at 37 °C. The samples were incubated for 3 h
with continuous stirring. At 30 min intervals, 1 mL extract of the liquid
containing the dialyzed compounds were taken and used for the analysis of the
TSP using HPLC-DAD, as described in the following section. To calculate the
kinetic parameters of PC release during the in vitro digestion,
the final rate (Vf ) of PC release was determined according to
Eq. 2:
Where ΔC is the difference in concentration between the final and the initial PC
concentration, At is the time difference between a specific time and the initial
time, and Vf is the final rate of PC release during the
in vitro digestion (mg GAE/min).
Total soluble polyphenols (TSP) content in the guava and soursop pulp
digestion fractions
TSP contents were quantified in all digested fractions of guava and soursop from
the in vitro digestion assay and at each point in the release
kinetics assay; this analysis was conducted according to the method described by
Montreau (1972) with slight
modifications, 250 μL aliquots of each fraction (in vitro
digestion or kinetics assay) were mixed with 1000 μL of sodium carbonate (7.5%
w/v) and 1250 μL of Folin-Ciocalteu's reagent. Afterward, the absorbance of each
sample was measured at 750 nm using a 96-well microplate reader (Bio-Tek®,
Synergy HT, Winooski, VT, USA) with Gen5 software. Gallic acid was used as the
standard (0.0125-0.2 mg/mL, R2 > 0.9997), and the results were
expressed as mg of gallic acid equivalents (g GAE/100 g DW).
Identification of phenolic compounds (PC) by HPLC-DAD analysis on digested
fractions of guava and soursop pulp
The identification of the PC was carried out using an HPLC Agilent 1260 series
(Agilent Technologies, Santa Clara, CA, USA) equipped with a UV-Vis Diode Array
Detector (DAD). Samples were injected (10 μL, flow rate 0.4 mL/min in a
Poroshell 120 EC-C18 (4.6 mm χ 150 mm, particle size 2.7 μm) (Agilent
Technologies). The gradient elution was carried out using water containing 0.1%
trifluoracetic acid (Sigma Aldrich) as solvent A and acetonitrile (Sigma
Aldrich) as solvent B applied as follows: 0 min, 5% B; 10 min, 23% B; 15 min,
50% B; 20 min, 50% B; 23 min, 100% B; 25 min, 100% B; 27 min, 5% B, 30 min, 5%
B. DAD detection was performed at 280-320 nm. The data analysis was performed
using OpenLab CDS, ChemStation Edition software (Agilent Technologies, Santa
Clara, CA, USA). Characterization of the PC was based on retention time.
Antioxidant capacity (AOX)
All analyses of AOX were slightly modified to adjust in a microplate reader.
Ferric reducing antioxidant power (FRAP) assay was performed as was described by
Benzie & Strain (1996), modified
by Álvarez-Parrilla, de la Rosa, Amarowicz &
Shahidi (2010). FRAP solution 10:1:1 (v/v/v) dissolved in a sodium
acetate buffer (0.3 M; pH 3.6), TPTZ-HCl (10 mM, 40 mM), and ferric chloride
hexahydrated (20 mM) was warmed to 37 °C before mixing it with the samples.
Briefly, 24 μL of sample from the aqueous-organic extraction was mixed with 180
μL of FRAP solution and the absorbance was measured at 595 nm after 30 min using
microplate reader (Biotek, Synergy HT). Results were expressed as millimol of
trolox (6-hydroxy-2,5,7,8-tetramethylchromane-2-carboxylic) equivalents per gram
DW (mmoL TE/g DW). Radical-scavenging activity was determined by 2,2'-azinobis-
3-ethylbenzotiazoline-6-sulphonic acid (ABTS) radical assay as was described by
Re et al., (1999);
with some modifications. For this determination, ABTS (7 mM) was dissolved in
potassium persulphate (2.42 mM) and kept in the dark at room temperature for 14
h. The solution was adjusted with phosphate buffer at an absorbance of 0.70
(±0.02). Trolox was used as a standard and methanol as a blank. Samples of 10 μL
of extract were added in a microplate reader (Biotek, Synergy HT, Winooski, VT,
USA) of 300 μL of capacity and 280 μL of ABTS radical was added. Then, the
mixture was incubated at 37°C in the dark and the absorbance was measured after
6 min, at 734 nm. A calibration curve was prepared using an aqueous solution of
trolox as standard. The results are reported in mmoL TE/g DW.
Statistical analysis
All analyses were performed in triplicate; means values and standard deviations
from each determination were calculated. Statistical significance between guava
and soursop pulp was analyzed by t-student. Data were analyzed using the
software Statistic 8.0 Release for Windows (Stat Soft. Inc., Tulsa, OK, USA)
with a significance level of α=0.05.
Results and discussion
In vitro digestion and bioaccessibility percentage (%) in
guava and soursop pulp
Table I shows that the TSP of guava and
soursop pulp in gastric and intestinal stages of an in vitro
digestion. The PC in Gas-F from soursop pulp were higher than guava pulp.
Nevertheless in the IntF of the digestion an increase in the content of TSP
respect the GasF was observed from both pulps. This could be due to the partial
release of PP bound to the cell wall material of the plant food (Chandrasekara & Shahidi, 2012). It has
been reported that some PC present in plant foods, can be associated mainly with
carbohydrates which can decrease their bioaccesibility (Saura-Calixto, 2010). During intestinal digestion, a series
of enzymes, mainly some hydrolases responsible for the hydrolysis of
carbohydrates, could react with some links or interactions that exist between
carbohydrates and PC (González-Aguilar,
Blancas-Benítez, & Sáyago-Ayerdi, 2017; Blancas-Benítez et al., 2015b), which would
result in an increase in the concentration of PC in the samples, after
intestinal hydrolysis, a process that would occur when consuming any plant food,
and that can be observed in the guava and soursop pulps analyzed in this
study.
Table I
Polyphenols released during each of the stages of the in
vitro digestion, and bioaccesibility of polyphenols of
guava and soursop pulp.1
|
|
Guava pulp |
Soursop pulp |
|
TSP (g GAE per 100 g sample) |
|
|
|
Gastric fraction |
14.33 ± 0.17b
|
17.15 ± 0.28a
|
|
Intestinal fraction |
28.88 ± 0.59a
|
29.83 ± 1.0a
|
|
Phenolic compounds profile (%) |
|
|
|
Gallic acid |
77.02 ± 0.31b
|
83.5 ± 0.43a
|
|
Chlorogenic acid |
12.5 ± 0.21a
|
6.4 ± 0.11b
|
|
Coumaric acid |
5.5 ± 0.51 |
n.d. |
|
Hydroxycinnamic acid |
4.6 ± 0.12 |
n.d |
|
Caffeic acid |
n.d. |
10.1 ± 0.10 |
|
Non-bioaccesible PC (SIF) |
8.16 ± 0.17a
|
6.77 ± 0.10b
|
|
Phenolic compounds profile (%) |
|
|
|
Gallic acid |
59.5 ± 0.05b
|
30.94 ± 0.18a
|
|
Chlorogenic acid |
40.2 ± 0.23b
|
60.80 ± 0.11a
|
|
Caffeic acid |
n.d. |
9.83 ± 0.08 |
|
Non-bioaccesible PC (IIF) |
1.73 ± 0.67a
|
2.51 ± 0.34a
|
|
Gallic acid |
10.45 ± 0.22a
|
3.42 ± 0.31b
|
|
Chlorogenic acid |
87.50 ± 2.3a
|
78.93 ± 1.4a
|
|
Caffeic acid |
n.d. |
17.45 ± 0.46 |
|
Bioaccesible PC (%) |
67.69b
|
71.30a
|
The PC profile of guava and soursop pulp found on in vitro
digestion showed that gallic acid and chlorogenic acid were mainly detected in
both samples, although caffeic acid was detected only in soursop pulp. Also,
gallic acid and chlorogenic acid were the PC that was mostly found in SIF and
IIF, respectively from guava and soursop pulp. Although these two main compounds
are potentially absorbed in the intestine, a substantial percentage of them were
also found on the indigestible fractions, which can reach the colon. In the
colon this phenolic acids, because of its simple structure, may still be
absorbed on the large intestine, it has been previously documented on various
in vitro and in vivo models (Rui et al., 2014; Vetrani et al., 2016). All
these compounds have been previously identified in both guava and soursop fruit,
and they have been attributed beneficial effects for health (Coria-Téllez, Montalvo-González, Yahia &
Obledo Vázquez, 2018; Jiménez-Escrig,
Rincón, Pulido & Saura-Calixto, 2001; Onyechi, Ibeanu, Nkiruka, Eme & Madubike, 2012; Rojas-Garbanzo, Zimmermann, Schulze-Kaysers &
Schieber, 2017; Soares, Pereira,
Marques & Monteiro., 2007).
For the bioaccessibility determination was considerate the overall distribution
of the TSP content, the data showed that 67.69% of the TSP from the guava pulp
are bioaccessible, while 71.30% of TSP from soursop pulp. It is apparent that
soursop pulp has a higher bioaccessibility of PC than the guava pulp. This
suggests that soursop pulp PC are not bound to the food matrix, making them more
available for intestinal absorption than PC present in guava pulp (Bohn, 2014; Cuervo et al., 2014).
In vitro release kinetics of PC in guava and soursop
pulp
Figure 2 shows the release kinetics of PC
from guava and soursop pulp. The PC released did not showed statistical
difference with similar rate in the soursop pulp (0.10 mg GAe/ min) and the
guava pulp (0.09 mg GAe/min), during the first 30 min of digestion. The release
rate was similar after 150 min of digestion, without subsequent changes in
either pulps, These results may be related to those from Table I, where a higher bioaccessibility was found for
soursop pulp, it is apparent that the soursop pulp PC might have a low
interaction with the food matrix and they could be highly bioaccessible than the
PC presents in guava pulp.
Figure 2
In vitro release kinetics of total soluble
polyphenols of guava and soursop pulps
Figure 3 shows the different PC that was
identified through time of the in vitro digestion on each fruit
pulp. Gallic acid was the main compound found in the guava and soursop pulp. The
PC from both pulps remained constant throughout the 180 min of digestion. As
previously mentioned, gallic acid was the main compound detected, and its
percentage of detection increased during the in vitro
digestion. The same behavior was observed for chlorogenic, coumaric and
hydroxycinnamic acids in guava pulp; and for chlorogenic and caffeic acids in
soursop pulp. These results not only revealed the potential bioaccessibility of
PC, but the ratio with which these compounds could be released and absorbed in
the small intestine (Blancas-Benítez et
al., 2015b).
Figure 3
Phenolic compounds profile (HPLC-DAD) of guava (a) and soursop
(b) pulp digestion fractions. a) Gastric fraction, b) Intestinal
fraction c) After dialysis process Peak annotations; 1: Gallic acid,
2: Chlorogenic acid, 3: Coumaric acid, 4: Hydroxycinnamic acid, 5:
Caffeic acid.
Conclusions
The bioaccessibility of the PC was higher in the soursop pulp (71.30 %) than in the
guava pulp (67.69 %). The main PC identified were gallic acid in the guava pulp, and
chlorogenic acid in the soursop pulp. The release kinetics rate of PC was higher in
the soursop pulp than on the guava pulp. These results highlight that although the
guava pulp has a higher PC content than soursop pulp, not all of these PC will be
bioaccessible. The importance of the bioavailability analysis lies to indicate the
functional potential that fruit pulps can have. However further studies are required
to establish their in vivo effects after intake of ready to eat
foods like fruit pulp.
Acknowledgements
Francisco J. Blancas Benítez thanks the financial support from Consejo Nacional de
Ciencia y Tecnología, México (CONACYT) for the scholarship granted by NUM
378371.
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