Food Research International 136 (2020) 109595

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Food Research International

journal homepage: www.elsevier.com/locate/foodres

Prebiotic potential of pulp and kernel cake from Jerivá (Syagrus T

romanzoffiana) and Macaúba palm fruits (Acrocomia aculeata)
Amanda Cristina Andradea, Júlia Fernanda Urbano Marinhoa, Angélica Cristina de Souzab,
Talita de Sousa Tavaresc, Disney Ribeiro Diasd, Rosane Freitas Schwanb,
⁎
Cleiton Antônio Nunesd, , Sabrina Carvalho Bastosa
a
Lavras Federal University, Department of Nutrition, Federal University of Lavras, University Campus, Post Office Box 3037, 37200-900 Lavras, Minas Gerais, Brazil
b
Lavras Federal University, Department of Biology, Federal University of Lavras, University Campus, Post Office Box 3037, 37200-900 Lavras, Minas Gerais, Brazil
c
Lavras Federal University, Department of Chemistry, Federal University of Lavras, University Campus, Post Office Box 3037, 37200-900 Lavras, Minas Gerais, Brazil
d
Lavras Federal University, Department of Food Science, Federal University of Lavras, University Campus, Post Office Box 3037, 37200-900 Lavras, Minas Gerais, Brazil

A R T I C LE I N FO A B S T R A C T

Keywords: The jerivá (Syagrus romanzoffiana) and the macaúba (Acrocomia aculeata) are palm trees of the Arecaceae family,
Arecaceae widely distributed in tropical and subtropical areas of Latin America, which have a low production cost and high
Byproduct productivity throughout the year. Due to the high content of lipids, their fruits have been used for oil extraction,
Fructooligosaccharide which generates byproducts such as the pulps and the kernel cakes, a nutritionally rich byproduct that can be
Dietary fibers
added into human food and, may have prebiotic potential. Therefore, the objective of this work was to char-
Prebiotic
Antioxidant
acterize and evaluate the prebiotic potential of jerivá pulp (JP), macaúba pulp (MP), jerivá kernel cake (JC) and
macaúba kernel cake (MC). For this, the fruits characterization was carried out through proximate composition,
phenolic compounds content, and antioxidant activity, besides evaluating the antimicrobial and fermentative
capacity of Bifidobacterium lactis, Lactobacillus casei, and Lactobacillus acidophilus against Escherichia coli. Jerivá
and macaúba pulps and kernel cakes presented high levels of dietary fiber (20.45% JP, 37.87% JC, 19.95% MP
and 35.81% MC) and high antioxidant activity, especially JP, which also showed the high values found for ABTS
and DPPH (2498.49 µMTrolox·g−1 fruit and 96.97 g fruit·g−1 DPPH, respectively), has a high total phenolic
content (850.62 mg GAE·100 g−1). Also, JP promoted a better growth of probiotic strains and a more relevant
pH reduction when compared to the commercial prebiotic FOS. However, MP, JC, and MC were also able to
favor the growth of the strains. Probiotic microorganisms were able to use JP, MP, JC, and MC and produced
short-chain fatty acids such as lactic, propionic, butyric, and acetic acid, capable of promoting health benefits.
Therefore, the byproducts from jerivá and macaúba oil extraction have characteristics that indicate their pre-
biotic potential, and maybe interesting components to increase the nutritional value of foods.

1. Introduction
The jerivá (Syagrus romanzoffiana) and the macaúba (Acrocomia
aculeata) are palm trees of the Arecaceae family, widely distributed in
tropical and subtropical areas of Latin America (Moreira et al., 2013;
del Río et al., 2016). These species are popularly used in landscaping,
and they have a low production cost and high productivity throughout
the year (Coimbra & Jorge, 2011; Colombo, Berton, Diaz, & Ferrari,
2018).
The jerivá fruit can be globose or oval with approximately 3 cm of
diameter. The pulp is fleshy, fibrous, and sweet with yellow or orange
coloration. The inner part has a rigid endocarp that surrounds an oily
almond (Moreira et al., 2013; Santos & Salomão, 2017). The macaúba
fruits are globose and have 3–5 cm in diameter, with smooth epicarp,
fibrous yellow mesocarp with a sweet flavor and a characteristic aroma,
and an endocarp that can internally have up to four endosperms per
fruit (Bazzo, de Carvalho, Carazzole, Pereira, & Colombo, 2018;
Colombo et al., 2018).
Jerivá and macaúba fruits have a high nutritional value, high-
lighting the fiber content in both pulp and almond (Coimbra & Jorge,
2011; Lescano et al., 2018). Despite this, jerivá has no relevant com-
mercial application yet and is little used in human food, resulting in
large amounts of leftover fruits (Silva, Siqueira, Damiani, & Vilas Boas,
2016; Carvalho, Rodrigues, & Lima, 2019). Recently, due to the high

⁎
Corresponding author.
E-mail address: cleiton.nunes@ufla.br (C.A. Nunes).

https://doi.org/10.1016/j.foodres.2020.109595
Received 6 March 2020; Received in revised form 22 July 2020; Accepted 23 July 2020
Available online 28 July 2020
0963-9969/ © 2020 Elsevier Ltd. All rights reserved.
A.C. Andrade, et al.
lipid content of its almond, jerivá has been studied to obtain oil
(Magalhães, Tavares, Gomes, & Nunes, 2020; Santos & Salomão, 2017).
On the other hand, macaúba has greater commercial relevance due to
its lipid content (50–70%), especially the almond (Bazzo et al., 2018;
Montoya, Motoike, Kuki, & Couto, 2016).
The oil obtained from jerivá and macaúba almonds have attractive
characteristics for the industrial sector, including the food, cosmetics,
pharmaceutical, and biodiesel industries (Magalhães, Tavares, & Nunes,
2020; del Río et al., 2016). However, the process of oil extraction
generates a large volume of remaining solids, such as the kernel cake, a
byproduct with high nutritional value (Sadh, Duhan, & Duhan, 2018;
Venkatesagowda, Ponugupaty, & Dekker, 2015).
Fruit byproducts are known to be natural sources of nutrients and
various bioactive compounds; therefore, they may have potential use as
functional ingredients (Albuquerque et al., 2019). According to Duarte
et al. (2017), fruits and their byproducts are components with prebiotic
potential due to their high carbohydrate content, especially fiber. In
this context, the kernel cake, as well as jerivá and macaúba pulps, can
be inserted into human food as significant sources of nutrients and
bioactive compounds.
According to Gibson et al. (2017), prebiotic is a substrate selectively
used by host microorganisms that can promote health benefits to the
individual. Prebiotics are used by microorganisms as a source of energy
in the fermentation process to produce metabolites such as short-chain
fatty acids (among them acetic, propionic, and butyric). These acids
may promote beneficial effects, such as inhibiting the proliferation of
pathogenic bacteria, increasing mineral bioavailability, preventing
colon cancer and gastrointestinal infections, boosting the immune
system, altering lipid metabolism by lowering cholesterol, and reg-
ulating intestinal transit time (Galdeano, Cazorla, Lemme-Dumit, Vélez,
& Perdigón, 2019; Gibson et al., 2017; Tsai et al., 2019).
Despite these benefits, most commercially available prebiotics are
expensive, restricting purchasing and consumption by most of the po-
pulation. However, new sources of prebiotic ingredients have been
studied lately, especially the natural components of the food matrix
rarely used in human food (Duarte et al., 2017). This way, pulps, and
cakes from jerivá and macaúba, which have high fiber content, should
be investigated as substrates with prebiotic potential. Therefore, the
objective of this work was to characterize the pulp and the kernel cake
from jerivá and macaúba regarding their physicochemical character-
istics, chemical composition, and prebiotic potential.
2. Material and methods
2.1. Sampling
The fruits of jerivá and macaúba were harvested in the mature stage
(fall fruits) in the region of Lavras – MG, Brazil, and transported to the
laboratory.
First, the fruits (Syagrus romanzoffiana and Acrocomia aculeata) were
sanitized in running water and disinfected with sodium di-
chloroisocyanurate (Startclor®) according to the manufacturer's re-
commendations. Then the macaúba was subjected to peeling and
pulping. Since the jerivá had no hard skin, it was directly subjected to
pulping, which was performed manually using a stainless steel knife.
The endocarps were broken in a hydraulic press (Marcon®), and the
almonds removed with a spatula, which was subjected to oil extraction
at room temperature using a screw press (Home Up Gourmet Yoda®).
From this process, the byproducts, called kernel cakes, were obtained.
The macaúba and jerivá pulps and kernel cakes were vacuum-
packed in plastic bags and wrapped in aluminum foil to protect from
light and frozen (−18 °C) for storage.
The samples, previously liquefied, were frozen at −20 °C for 24 h
and dehydrated in a lyophilizer (L101, Liotop®) for 72 h. Finally, the
pulp and kernel cakes were stored in glass containers and protected
from light and moisture at room temperature.
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Food Research International 136 (2020) 109595
2.2. Characterization of jerivá and macaúba pulp and kernel cake
The analyses were performed in triplicate for jerivá pulp (JP),
macaúba pulp (MP), jerivá kernel cake (JC) and macaúba kernel cake
(MC).
2.2.1. Physical and chemical characterization
The samples were evaluated separately for moisture, lipid (ether
extract), protein, and ashes, according to AOAC (2012). Soluble and
insoluble dietary fibers were determined by the gravimetric-enzymatic
method with the enzymes ɑ-amylase, protease, and amyloglucosidase,
using the total dietary fiber kit (Sigma®). Total dietary fiber was ob-
tained by the sum of soluble and insoluble dietary fibers (AOAC, 1997).
The carbohydrate content was determined by difference (Diaz-Vela,
Totosaus, Cruz-Guerrero, & Pérez-Chabela, 2013) and the total energy
value calculated according to the proposed by Osborne and Voogt
(1978), applying the protein and carbohydrate conversion factors of
4 kcal·g−1 and 9 kcal·g−1for lipids.
The pH and total soluble solids content were also determined. For
this, the samples were homogenized in a ratio of 1:9 and filtered on
filter paper (Silva et al., 2016). The pH reading was taken using a digital
pH meter (Digimed®) (AOAC, 2012), while soluble solids were read
using a portable hand-held refractometer, and the results were ex-
pressed as °Brix (AOAC, 2012).
2.2.2. Total phenolic compounds content and total antioxidant activity
The sample extracts were assayed in triplicate according to the
methodology of Whaterhouse (2002) with adaptations for total phe-
nolics and total antioxidant activity analysis.
The phenolic content was determined by the Folin-Ciocalteu
method, according to Whaterhouse (2002). For the analysis, 0.5 mL of
each extract, 2.5 mL of Folin-Ciocalteu solution (10%), and 2 mL of
sodium carbonate solution (4%) were used in triplicate test tubes.
Subsequently, the tubes were vortexed and kept at rest for 2 h in the
dark. The absorbance reading was taken on a Spectrum® − 2000UV
(720 nm) spectrophotometer and the total phenolic content calculated
using a gallic acid standard curve. Results were expressed as mg gallic
acid equivalent per 100 g of sample (mg GAE·100 g−1).
Total antioxidant activity was determined by three methods: β-
carotene/linoleic acid system, ABTS, and DPPH.
The total antioxidant activity obtained by the β-carotene/linoleic
acid system (adapted from Rufino et al. (2006)) was performed by
adding 0.4 mL of each extract and 5 mL of the β-carotene/linoleic acid
system solution. Data collection (470 nm) was taken after 2 h of mixing.
The spectrophotometer was calibrated with hydrogen peroxide, and the
results were expressed as oxidation protection percentage.
The antioxidant activity using ABTS method was determined by the
addition of 30 µL of each extract into the test tube with 3 mL of the
ABTS radical solution. The tubes were vortex homogenized and read at
734 nm after 6 min with ethyl alcohol as blank. Results were expressed
as µM Trolox·g−1 whole fruit (Rufino et al., 2007b).
The 2,2-diphenyl, 1-picrylhydrazyl (DPPH) radical scavenging
method was performed according to Brand-Williams, Cuvelier, and
Berset (1995), adapted by Rufino et al. (2007a). First, 0.1 mL of each
sample extract was added to test tubes containing 3.9 mL of DPPH ra-
dical solution, which were then homogenized. Methyl alcohol was used
as a blank. Spectrophotometer readings (515 nm) were taken at 10-
minute intervals until stabilization. Results were expressed as EC50 g of
the whole fruit·g−1 DPPH (Duarte-Almeida, Maurício, Santos,
Genovese, & Lajolo, 2006).
2.3. Determination of prebiotic potential
2.3.1. Microorganisms and inoculum production
Lyophilized bacteria Bifidobacterium lactis BLC1, Lactobacillus casei
BGP93, and Lactobacillus acidophilus LA3 (Lyofast®, Sacco®, Brazil) were
A.C. Andrade, et al.
used as probiotic microorganisms, whereas enteropathogenic
Escherichia coli (EPEC) INCQS 00181 (CDC 055) was used as a pathogen
control. Probiotic cultures were activated in MRS broth (DeMan,
Rogosa, and Sharpe) and the pathogen in TSB (Tryptic Soy Broth). Both
were incubated in BOD (Biochemical Oxygen Demand) at 37 °C ± 1 °C
for 18 h. Subsequently, the inoculum was homogenized, and, for pro-
biotics, 5 mL was removed from the aliquot and added in 90 mL of MRS,
while for E. coli 3 mL was removed and added in 200 mL of TSB.
The bacterial cell population was estimated by turbidimetry. Thus,
spectrophotometer (Spectrum® SP-2000UV) absorbance readings at
620 nm for probiotics and 600 nm for pathogens were taken until the
absorbance equivalent to an approximate cell concentration of 108
CFU·mL−1 was achieved.
2.3.2. In vitro antimicrobial activity
The antimicrobial activity of the samples was qualitatively de-
termined by the agar diffusion technique per well using the probiotics
B. lactis, L. casei and L. acidophilus, and the pathogen E. coli (adapted
from Marinho, da Silva, Mazzocato, Tulini, & Favaro-Trindade, 2019).
In a Petri dish (150 mm), with media MRS-agar for probiotics and
TSA (Tryptic Soy Agar) for the pathogen, five 8 mm wells were pre-
pared. Subsequently, 200 µL of the inoculum (108 CFU·mL−1) was in-
dividually added to the agar surface and spread with Drigalski's loop.
The samples (JP, MP, JC, and MC) were diluted with distilled water
(1:10) and added (40 µL) in triplicate to the wells. Also, 40 µL of the
negative control (C−) consisting of sterile distilled water and 40 µL of
tetracycline solution (100 mg·mL−1) as a positive control (C+) was
added. Plating was performed in duplicate for each sample tested and
incubated at 37 °C ± 1 °C.
The probiotics were kept for 72 h and pathogens for 24 h in aero-
biosis, except for B. lactis that was incubated in an anaerobic condition
using anaerobic generators (Probac®). After incubation time, the oc-
currence of inhibition halos was evaluated.
2.3.3. Fermentation
Fermentation was performed with probiotics and pathogens ac-
cording to the methodology adapted from Diaz-Vela et al. (2013) and
Marinho et al. (2019). In the tests, different substrates were used as a
carbon source to evaluate their effect on the growth of microorganisms.
For this, the MRS and TSB culture media (Table 1) were prepared
without a carbon source at pH 7.0 ± 0.5.
First, the media were placed in sterile 50 mL polypropylene vials, in
triplicate. In the fermentative medium, 2% of one of the evaluated
carbon sources samples (JP, MP, JC, and MC) in lyophilized form was
individually added. As a positive control, 2% glucose (GLC) broth was
used, and as a comparison model, 2% of the commercial fructooligo-
saccharide (FOS) prebiotic was used. Both were solubilized in distilled
water and sterilized by filtration on nylon filters (0.22 µm). Control (C)
consisted only of culture medium without carbon source. Finally,
strains (stock suspension of 108 CFU·mL−1) were inoculated at a ratio of
1:9 in the sample, reaching a final concentration of approximately 107
CFU·mL−1 to start the fermentative test.
Table 1
Composition of MRS and TSB without carbon source.
MRS TSB
Peptone 10 g Casein Peptone 17 g
Meat extract 10 g Soy Peptone 3g
Yeast extract 5g Sodium Chloride 5g
Bibasic Sodium Phosphate 3.76 g Potassium Phosphate 2.5 g
Manganese Sulfate Monohydrate 0.1 g –
Magnesium sulfate 0.204 g – as modification of the bacterial metabolites that are beneficial for in-
Tween 80 1g – testinal mucosa metabolism, physiology, and health (Blachier,
Total 30.06 g 27.5 g
The final volume of 1000 mL of distilled water.
3
Food Research International 136 (2020) 109595
After inoculum addition, the tubes were incubated in BOD at
37 °C ± 1 °C in the anaerobic atmosphere using anaerobic generator
systems (Probac®). Fermentation was carried out for 36 h, and 2 mL of
each vial was removed every 12 h for viable cell count, pH, and short-
chain fatty acid (SCFA) determination.
2.3.3.1. Viable cell count. Quantification of viable cells was performed
by the drop plate technique, adapted from Herigstad, Hamilton, and
Heersink (2001). From 2 mL of sample, 100 µL were taken, added in
900 µL of sterile peptone water (0.1%), and serial decimal dilutions
were performed. For counting, 100 µL of duplicate diluted samples
were inoculated on the surface of MRS agar (probiotics) and TSA
(pathogenic) media.
Plates were incubated at 37 °C ± 1 °C for 48 h for probiotics and
24 h for the E. coli. Besides, the B. lactis strain was incubated in anae-
robic jar (Probac®). Plates were made in duplicates, and the results
were expressed as log CFU·mL−1.
2.3.3.2. pH. The pH was monitored at 0, 12, 24, and 36 h of
fermentation and 2 mL were taken each time, homogenized, and read
in digital pH meter (Digimed®) with duplicate reading (AOAC, 2012).
2.3.3.3. Determination of metabolites. Samples were taken after
fermentation and were centrifuged (4 °C at 6000g for 10 min),
supernatants were acidified to pH 2.1 and then filtered through nylon
membrane (0.22 µm). Samples were stored in a vial (−20 °C) until the
time of analysis (Silva et al., 2017 with adaptations).
The organic acids (lactic, acetic, propionic and butyric) were de-
termined in duplicate by high-performance liquid chromatography
(HPLC) using a Shimadzu model LC-10Ai chromatograph (Shimadzu
Corp., Japan) equipped with a dual detection system, which consists of
a UV–Visible detector (SPD 10Ai, Shimadzu) and a refractive index
detector (RID − 10Ai, Shimadzu). A Shimadzu ion exclusion column
(Shim-pack SCR − 101H, 7.9 mm × 30 cm) was used at 50 °C, and a
perchloric acid solution at pH 2.1 was used as eluent at a flow rate of
6 mL.min−1. Acids were detected by absorbance at 210 nm (Alves, de
Oliveira, Nunes, Dias, & Schwan, 2011). Acids were identified by
comparing their retention times with certified standard retention times,
and their concentrations were determined using external calibration,
comparing different concentrations and peak areas for each compound
standard (Freire, Ramos, & Schwan, 2017). Data were obtained through
LCSolution® software.
2.4. Statistical analysis
Physical and chemical characterization, total phenolic content, an-
tioxidant activity, and organic acids results were compared by analysis
of variance (ANOVA), followed by Tukey test using Sensomaker soft-
ware (Pinheiro, Nunes, & Vietoris, 2013). The differences were con-
sidered significant when p ≤ 0.05.
3. Results and discussion
3.1. Physical and chemical characterization
Jerivá and macaúba kernel cakes showed statistically higher protein
content than pulps (Table 2). Plant proteins, as present in the samples,
are known to be less digestible compared to animal protein, and in-
complete digestion in the small intestine allows a residual amount of
protein and peptides to reach the colon. Thus, there may be a mod-
ification of the microbial composition and its metabolic activity, as well
Beaumon, Portune, Steuer, & Audebert, 2019).
The samples (MP e MC) presented same lipid contents (Table 2),
whereas for the JP, the lowest value, 0.45%, was observed. Coimbra
A.C. Andrade, et al. Food Research International 136 (2020) 109595

Table 2
Proximate composition (%), total energy value (TEV) (kcal·100 g−1), pH and soluble solids (°Brix) of jerivá and macaúba pulp and kernel cake (whole matter).
Parameters JP JC MP MC

d b c
Moisture 44.34 ± 0.36 8.51 ± 0.13 37.96 ± 0.12 3.52 ± 0.21a
Protein 2.97 ± 0.06a 18.46 ± 0.06b 2.87 ± 0.01a 27.83 ± 0.02c
Lipids 0.45 ± 0.08a 20.67 ± 0.10b 28.63 ± 0.44c 28.31 ± 0.32c
Carbohydrates 29.45 ± 0.33d 11.58 ± 0.20c 9.68 ± 0.32b 1.02 ± 0.31a
Total dietary fiber 20.45 ± 0.00b 37.87 ± 0.00d 19.95 ± 0.00a 35.81 ± 0.00c
Soluble fiber 6.92 ± 0.00c 1.54 ± 0.00a 10.68 ± 0.00d 3.21 ± 0.00b
Insoluble fiber 13.53 ± 0.00b 36.34 ± 0.00d 9.26 ± 0.00a 32.60 ± 0.00c
Ashes 2.34 ± 0.03b 2.91 ± 0.02c 0.97 ± 0.11a 3.52 ± 0.03d
TEV 133.77 ± 0.54a 306.18 ± 0.48b 307.01 ± 0.80b 369.57 ± 0.09c
pH 5.28 ± 0.06a 5.95 ± 0.02b 6.47 ± 0.05c 6.61 ± 0.04d
Soluble solids 7.83 ± 0.28c 2.66 ± 0.28b 3.00 ± 0.00b 2.00 ± 0.00a

The values are the means of triplicate determination. ± indicates the standard deviation of the mean. a–dDifferent lowercase letters on the same line indicate a
significant difference (p ≤ 0.05) between values based on the Tukey test. JP: jerivá pulp; JC: jerivá kernel cake; MP: macaúba pulp; MC: macaúba kernel cake.

Table 3
Total phenolics and antioxidant activity (β-carotene, DPPH, and ABTS) of jerivá and macaúba pulp and cake (whole matter).
Parameters JP JC MP MC

Total phenolics (mg GAE·100 g−1) 850.62 ± 4.68c 265.54 ± 4.68b 262.41 ± 7.63b 215.53 ± 2.8a
β-carotene (% Protection) 97.00 ± 0.43b 95.13 ± 0.7ab 94.05 ± 0.05a 99.38 ± 0.65c
ABTS (µMTrolox·g−1 fruit) 2498.49 ± 186.7c 1314.87 ± 29.78b 735.35 ± 20.13a 898.0 ± 66.2a
DPPHEC50 (g fruit·g−1 DPPH) 96.97 ± 3.74a 331.80 ± 3.95c 290.86 ± 7.68b 296.94 ± 5.4b

The values are the means of triplicate determination. ± indicates the standard deviation of the mean. a–cDifferent lowercase letters on the same line indicate a
significant difference (p ≤ 0.05) between values based on the Tukey test. JP: jerivá pulp; JC: jerivá kernel cake; MP: macaúba pulp; MC: macaúba kernel cake.

and Jorge (2011), when evaluating the pulp and almond of jerivá and The pH and soluble solids influence the sweetness and acidity,
macaúba, obtained a higher content for JP (7.48%) and similar content contributing to the sensory quality of fruits and their products
for MP (28.94%). Regarding the lipid content in almonds (56.37% for (Milošević, Milošević, & Mladenović, 2016). The fruits have low acidity
jerivá and 46.06% for macaúba), the authors found higher values than (Table 2), which may favor their sensory characteristics. Regarding the
the kernel cakes, as expected, since the cake is a byproduct obtained soluble solids content, it was observed an expressively high content for
from the extraction of almond oil. However, high lipid contents were JP, being JC and MP statistically similar, and the lowest soluble solids
retained in the kernel cakes. content was found in MC samples. Due to these characteristics, the
JP presented the highest carbohydrate content (Table 2), followed samples could be used in the development of new products without
by JC and MP. Carbohydrates are essential components to be de- compromising the technological and sensorial aspects.
termined as they include reducing sugars (such as glucose and fructose),
non-reducing sugar (sucrose), starches, and cellulose, which play a key
3.2. Total phenolic compounds content and total antioxidant activity
role in fruit flavor and structure (Pomares-Viciana, Martínez-
Valdivieso, Font, Gómez, & Del Río-Celestino, 2018). Another critical
The content of phenolic compounds (Table 3) ranged from 215.53
factor is that carbohydrate composition influences probiotic growth.
(MC) to 850.62 (JP) mg GAE·100 g−1 of fruit. According to the clas-
Simple carbohydrates (mono and disaccharides) are more readily me-
sification by Vasco, Ruales, and Kamal-Eldin (2008), JC, MP, and MC
tabolized by microorganisms (Charoensiddhi, Conlon, Vuaran, Franco,
samples can be classified as having a medium phenolic concentration
& Zhang, 2016; Nor et al., 2017).
(100–500 mg GAE·100 g−1), while JP has a high concentration
Total dietary fiber amount was high for all samples, but higher
(> 500 mg GAE·100 g−1). In general, all samples can be considered
values were obtained for JC and MC (Table 2). Both have high insoluble
good sources of phenolic compounds for presenting at least 100 mg
fiber content (36.34% for JC and 32.60% for MC), despite the low so-
GAE·100 g−1 (Vasco et al., 2008).
luble fiber content. On the other hand, the pulps presented considerable
The antioxidant activity of plant products can be assayed by
amounts of soluble and insoluble fiber. The carbohydrates composition
methods such as β-carotene, which quantifies products formed in lipid
of fiber fractions is important to understand the jerivá and macaúba
peroxidation, and DPPH and ABTS, related to radical scavenging.
byproducts as prebiotics. Further studies envisioning to isolate carbo-
Therefore, a single method would not quantify the antioxidant effect at
hydrate fractions and determine its compositions, to find out any oli-
all, and more than one method should be used to provide a complete
gosaccharide’s structures present in macaúba and jerivá fruits, will help
characterization of the samples (Schiassi, Souza, Lago, Campos, &
to elucidate those oligosaccharides, if present, as prebiotics.
Queiroz, 2018).
According to the World Health Organization, it is recommended to
Despite an average phenolic content had been found for JC, MP and
consume at least 25 g per day of dietary fiber (WHO, 2003). However,
MC samples, according to Vasco et al. (2008), high antioxidant activity
according to McGill, Fulgoni, and Devareddy (2015), most of the po-
was observed for all samples by the β-carotene method (Hassimotto,
pulation of all age groups do not consume the WHO’s guidance. Thus,
Genovese, & Lajolo, 2005), since they have more than 70% oxidation
the fruit pulp and cake with low cost and high availability can be
inhibition (Table 3). Besides, the ABTS method also indicated high
considered excellent sources of dietary fiber. Also, dietary fibers are
antioxidant activity of the samples (> 100 µM Trolox·g−1) (Souza,
potentially substrates with prebiotic effects, as they are resistant to
Pereira, Queiroz, Borges, & Carneiro, 2012), with JP presenting the
digestion and absorption of the small intestine and can reach the colon
highest antioxidant activity, while MP and MC showed no statistically
and be fermented by beneficial microorganisms (Duarte et al., 2017).
difference antioxidant activity.
Hence, regular consumption of jerivá and macaúba pulp and cake can
Regarding DPPH, the smaller the EC50, the higher the antioxidant
benefit human health.
capacity of the fruit (Brand-Williams et al., 1995). The results were

4
A.C. Andrade, et al.
similar to those forABTS (Table 3), where all samples evaluated had
scavenging effects against the DPPH radical. However, the highest an-
tioxidant activity was observed for JP (96.97 g fruit·g−1 DPPH), while
the antioxidant activities of MP and MC were similar and JCwas the
lowest one (331.80 g fruit·g−1 DPPH).
Based on these physical–chemical characteristics and proximate
composition, jerivá and macaúba pulps and kernel cakes can be useful
for technological applications, and the fruit can be fully utilized in
human nutrition.
3.3. In vitro antimicrobial activity
According to Balouiri, Sadiki, and Ibnsouda (2016), plant products
contain most of the discovered antimicrobial compounds, and among
them, polyphenols have been widely studied for their antimicrobial
activity. Thus, given the high concentration of phenolic compounds in
the samples (Table 3), the antimicrobial activity of jerivá and macaúba
pulps and kernel cakes was determined.
No sample showed inhibitory activity against the evaluated micro-
organisms. Thus, although the samples had high antioxidant activity,
the present bioactive compounds were not able to inhibit the growth of
E. coli, neither the probiotics as well. The antimicrobial effect of natural
sources changes according to species, variety, and plant parts
(Raybaudi-Massilia, Suárez, & Francisco, 2015). Therefore, the high
phenolic content is not directly associated with the inhibition of mi-
crobial growth. Another point to be considered is that in this analysis,
whole fruits were used and not their extract, and those fruits substrates,
especially cakes, have a high content of carbohydrates and proteins
(Table 2), which can favor the microbial growth. It is important to note
that polyphenols, oligosaccharides and other nutrients present in food
are not fully absorbed in the small intestine and will be available in the
colon lumen, favoring the beneficial microbiota and, consequently, the
host (Duda-Chodak, Tarko, & Sroka, 2015; Ozdal et al., 2016; Gibson
et al., 2017).
3.4. Prebiotic potential
Fermentation was monitored by microbial growth (log CFU·mL−1)
and pH changes for B. lactis, L. casei, L. acidophilus, and E. coli over 36 h
of fermentation, with evaluation every 12 h, as shown in Fig. 1.
Growth curves (Fig. 1) show a higher microbial growth rate in the
range between 0 h and 12 h. When evaluating the microbial activity of
the probiotic strains in the different substrates, it was noticed that the
substrates investigated for prebiotic potential were used as a carbon
source. Jerivá and macaúba byproducts were used by all the micro-
organisms tested and were relatively better than the growth observed in
the control culture medium. Among the byproducts, JP was the one that
most stimulated L. acidophylus growth and presented a higher result
compared to FOS in all tested microorganisms. E. coli can use prebiotics
as a carbon source (Schouler, Taki, Chouikha, Moulin-Schouleur, &
Gilot, 2009; Wang et al., 2020) and was also able to use jerivá and
macaúba byproducts (Fig. 1). When compared to FOS and GLC, the JP
substrate showed significantly superior behavior (p ≤ 0.05) to promote
microbial growth for all strains evaluated, except for L. casei, where JP
had similar GLC behavior (Table 4). This behavior may be due to fruit
composition (Tables 2 and 3), as JP has relevant soluble fiber and
carbohydrate contents, and soluble polysaccharides are more readily
and entirely used by probiotics (Nor et al., 2017). Besides, JP presented
higher content of phenolic compounds, which can also be consumed by
microorganisms.
MP presented similar behavior to JP for B. lactis and E. coli, i.e., it
provided growth superior to FOS, whereas, for L. casei, it promoted
growth almost equal to FOS. MP also provided higher growth than GLC
for B. lactis and E. coli, and similar for L. acidophilus (Table 4).
Overall, JC provided similar growth to FOS for the microorganisms
analyzed, except for L. casei, which was significantly higher (p ≤ 0.05).
5
Food Research International 136 (2020) 109595
Regarding MC, despite promoting lower growth than FOS for B. lactis
and L. acidophilus probiotics, it was the same for L. casei. MC also
promoted growth almost equal to GLC, except for L. casei, which was
lower (Table 4).
The pH of fermented substrates showed similar behavior regarding
the curves slope, with a pH reduction in all samples (Fig. 1). The most
substantial reduction was observed at time 12 h. As expected, it has
been found that pH is reduced with increasing bacterial growth due to
the production of different organic acids during the fermentation of
energy source substrates such as carbohydrates, proteins and even
polyphenols (Charoensiddhi et al., 2016; Gibson et al., 2017).
Another point that can be observed is that JP and GLC, in general,
were the samples that had the most considerable pH reductions
(Table 4). According to Diaz-Vela et al. (2013), bacteria prefer mono-
saccharides, which justifies the lower pH of these samples. JP had a
high carbohydrate content, of which probably most of it should be
simple carbohydrates due to its sweet taste and high soluble solids
content (Table 2).
Despite the acidifying capacity of E. coli in fermentation, the re-
duction in pH in the intestinal lumen by the fermentation process may
limit or inhibit the growth of pathogenic bacteria, such as E. coli and
other genera, and benefit the growth of some beneficial species (Fu
et al., 2018; Nor et al., 2017).
Components that are not fully digested or absorbed in the upper
gastrointestinal tract are exposed to fermentative activity by the gut
microbiota. Of this process, the major metabolites produced are short-
chain fatty acids (SCFA), the most abundant and important being acetic,
propionic, and butyric acids (Koh, de Vadder, Kovatcheva-Datchary, &
Backhed, 2016; Rocchetti et al., 2019). Given this and the most con-
siderable reduction in pH at time 12 h, organic compounds were
quantified at the beginning of the fermentation process (time 0 h) and
at time 12 h and represented as the total acids produced. The individual
concentration for each organic acid (lactic, acetic, propionic, and bu-
tyric) produced at time 12 h were also presented (Table 5).
Despite the differences in organic acid concentrations for each
sample, lactic acid was, in general, the most synthesized by the pro-
biotic strains, especially Lactobacillus. This genus is composed of
homofermentative species, and its main organic acid produced during
carbohydrate metabolism is lactic acid (Duarte et al., 2017). Besides,
this acid can be metabolized in the colon and converted to butyric and
propionic acid (Barroso et al., 2016).
Secondly, the acids with higher contents were propionate and
acetate. Propionic acid is associated with reduced lipogenesis and
cholesterol synthesis and is involved in activating G protein receptors
by releasing satiety hormones (Sáyago-Ayerdi, Zamora-Gasga, &
Venema, 2019). Acetic acid, on the other hand, can inhibit the growth
of enteropathogenic bacteria and is related to the microbiota-brain-cell
axis and can cross the blood–brain barrier and reduce appetite for a
central homeostatic mechanism (Holscher, 2017; Koh et al., 2016).
Despite the small amount, butyric acid was also produced during fer-
mentation. This acid is the main energy source of colonocytes and is
essential for maintaining tissue integrity through the apoptosis of DNA-
damaged cells (Charoensiddhi et al., 2016).
It was possible to observe that there was a significant increase in
acid concentration at 12 h for probiotic microorganisms (p ≤ 0.05),
corroborating the pH reduction (Fig. 1). This observation allowed to
infer that microorganisms were able to use the jerivá and macaúba
substrates and produce SCFA.
For E. coli, despite the pH reduction, there was a significant re-
duction of acids at 12 h (p ≤ 0.05), except for GLC, which did not show
a significant change in total acid production. This behavior can be ex-
plained by the production of higher amounts of other acids that were
not quantified in this study. Most of the microorganisms were able to
produce a high amount of organic acids in the presence of GLC.
However, it is interesting to note that glucose is rapidly absorbed when
ingested, while digestion resistant substrates such as complex
A.C. Andrade, et al. Food Research International 136 (2020) 109595

10.0 7.0
9.5 6.5
9.0 6.0

log CFU / mL
8.5 5.5
8.0 5.0

pH
7.5 4.5
7.0 4.0
6.5 3.5
6.0 B. lactis 3.0 B. lactis
0 0
0 12 24 36 0 12 24 36
Time (hours) Time (hours)

10.0 7.0
9.5 6.5
9.0 6.0
log CFU / mL

8.5 5.5
8.0 5.0

pH
7.5 4.5
7.0 4.0
6.5 3.5
6.0 3.0
L. casei L. casei
0 0
0 12 24 36 0 12 24 36
Time (hours) Time (hours)
10.0 7.0
9.5 6.5
9.0 6.0
log CFU / mL

8.5 5.5
8.0 5.0
pH

7.5 4.5
7.0 4.0
6.5 3.5
6.0
L. acidophilus 3.0 L. acidophilus
0 0
0 12 24 36 0 12 24 36
Time (hours) Time (hours)
10.0 7.0
9.5 6.5
9.0
log CFU / mL

6.0
8.5 5.5
pH

8.0 5.0
7.5 4.5
7.0 4.0
6.5 3.5
6.0 E. coli
E. coli 3.0

0 0
0 12 24 36 0 12 24 36
Time (hours) Time (hours)
Fig. 1. Microbial growth (log CFU·mL−1) and pH over time (36 h). C: control; GLC: glucose; FOS: fructooligosaccharide; JP: jerivá pulp; MP: macaúba pulp; JC: jerivá
kernel cake; MC: macaúba kernel cake.

carbohydrates can be used as a source of energy in fermentative pro- carbon source in the fermentation process, stimulating the growth of
cesses to produce SCFA (Chen, Tuo, & Dong, 2016; Koh et al., 2016). microorganisms and reducing the pH due to the production of SCFA. It
Therefore, JP, JC, MP, and MC substrates were generally used as a is noteworthy that the nutritional composition of fruits, high

6
A.C. Andrade, et al. Food Research International 136 (2020) 109595

Table 4
Microbial growth (log CFU·mL−1) and pH at time 12 h for the samples and microorganisms evaluated.
Parameters Samples B. lactis L. acidophilus L. casei E. coli

−1 a a b a
Log CFU·mL C 8.22 ± 0.06 7.91 ± 0.04 8.85 ± 0.06 8.79 ± 0.08
bc a
GLC 8.67 ± 0.17 7.78 ± 0.07 9.26 ± 0.13 c 9.00 ± 0.00 b

c b
FOS 8.79 ± 0.12 8.25 ± 0.06 8.53 ± 0.15 a 8.77 ± 0.09 a

d c
JP 9.09 ± 0.09 8.76 ± 0.12 9.20 ± 0.11 c 9.51 ± 0.02 c

d a
MP 9.07 ± 0.18 7.82 ± 0.15 8.73 ± 0.10 ab 9.64 ± 0.01 c

c b
JC 8.82 ± 0.07 8.39 ± 0.10 8.90 ± 0.11b 8.88 ± 0.03 ab

b a
MC 8.54 ± 0.06 7.91 ± 0.18 8.75 ± 0.17 ab 9.01 ± 0.00 b

cd f e de
pH C 5.35 ± 0.03 5.33 ± 0.01 5.44 ± 0.02 6.09 ± 0.04
cd a a a
GLC 5.28 ± 0.19 3.92 ± 0.04 3.60 ± 0.01 4.47 ± 0.11
b b d c
FOS 5.00 ± 0.00 4.14 ± 0.02 5.13 ± 0.12 5.77 ± 0.03
a a b a
JP 4.76 ± 0.12 3.96 ± 0.02 3.99 ± 0.03 4.55 ± 0.04
bc c c b
MP 5.20 ± 0.03 4.83 ± 0.02 4.93 ± 0.03 5.59 ± 0.17
d e d d
JC 5.45 ± 0.23 5.18 ± 0.04 5.16 ± 0.02 5.97 ± 0.09
e d e e
MC 5.69 ± 0.05 5.12 ± 0.03 5.50 ± 0.02 6.15 ± 0.08

The values are averages. ± indicates the standard deviation of the mean. a–fDifferent lowercase letters in the same column indicate a significant difference (p ≤ 0.05)
between the values based on the Tukey test. C: control; GLC: glucose; FOS: fructooligosaccharide; JP: jerivá pulp; MP: macaúba pulp; JC: jerivá kernel cake; MC:
macaúba kernel cake.

carbohydrate, and fiber content, and the presence of phenolic com-
pounds can stimulate the growth of beneficial bacteria, modulating the
gut microbiota and promoting beneficial health effects.
This study is the first step in the investigation of the functional ef-
fects of these fruits, serving as a basis for further research. Thus, in
addition to in vitro studies, it is important to carry out an in vivo study to
determine the real prebiotic effect of jerivá and macaúba pulps and
kernel cakes, since the intestine is a complex environment with sig-
nificant interactions between various components, including metabo-
lites and microorganisms that have not been studied.

Table 5
Organic acids (g·L−1) produced at time 12 h and total acids at time 0 h and 12 h.
Microorganism Samples Lactic acid Acetic acid Propionic acid Butyric acid TOTAL SCFAs

0h 12 h

d a ab a a
Bifidobacterium lactis C 5.00 ± 0.30 0.57 ± 0.02 2.86 ± 0.27 0.27 ± 0.01 3.57 ± 0.29 8.7 ± 0.49b
GLC 1.33 ± 0.08b 1.43 ± 0.11ab 2.75 ± 0.04ab 0.25 ± 0.02a 3.57 ± 0.06a 5.76 ± 0.12b
FOS 1.52 ± 0.01b 1.62 ± 0.04abc 2.76 ± 0.01ab 0.26 ± 0.00a 3.73 ± 0.05a 6.16 ± 0.04b
JP 0.56 ± 0.01a 3.04 ± 0.94c 2.55 ± 0.16a 0.28 ± 0.02a 3.56 ± 0.08a 6.44 ± 0.79b
MP 6.63 ± 0.18f 1.17 ± 0.16ab 3.29 ± 0.16bc 0.25 ± 0.00a 3.51 ± 0.11a 11.35 ± 0.18b
JC 5.84 ± 0.16e 2.10 ± 0.12bc 3.53 ± 0.09c 0.58 ± 0.00b 4.69 ± 0.41a 12.05 ± 0.19b
MC 3.17 ± 0.09c 0.49 ± 0.03a 3.19 ± 0.27bc 0.30 ± 0.03a 4.40 ± 0.37a 7.69 ± 0.36b

Lactobacillus casei C 5.59 ± 0.34a 0.69 ± 0.04a 3.06 ± 0.16a 0.25 ± 0.03a 4.25 ± 0.12a 9.59 ± 0.57b
GLC 33.19 ± 0.04e 0.62 ± 0.01a 3.38 ± 0.00bc 0.27 ± 0.01a 6.00 ± 0.00a 37.46 ± 0.06b
FOS 8.04 ± 0.09b 0.85 ± 0.00b 3.54 ± 0.13c 0.29 ± 0.01a 6.77 ± 0.01a 12.71 ± 0.23b
JP 21.69 ± 0.80d 0.88 ± 0.02bc 3.17 ± 0.00ab 0.27 ± 0.00a 6.35 ± 0.11a 26.00 ± 0.82b
MP 9.77 ± 0.24c 0.98 ± 0.01c 3.68 ± 0.02c 0.29 ± 0.00a 8.60 ± 0.00a 14.72 ± 0.21b
JC 9.86 ± 0.11c 1.30 ± 0.06e 4.28 ± 0.01d 0.35 ± 0.00b 8.38 ± 0.08a 15.79 ± 0.03b
MC 8.23 ± 0.24b 1.12 ± 0.00d 4.27 ± 0.02d 0.35 ± 0.00b 7.63 ± 0.19a 13.97 ± 0.26b

Lactobacillus acidophilus C 5.97 ± 0.01a 0.27 ± 0.01a 2.97 ± 0.01a 0.27 ± 0.01ab 4.38 ± 0.06a 9.48 ± 0.00b
GLC 19.85 ± 0.37d 0.62 ± 0.02b 2.83 ± 0.08a 0.25 ± 0.01a 5.30 ± 0.03a 23.55 ± 0.43b
FOS 16.23 ± 0.10c 0.76 ± 0.00bc 2.90 ± 0.12a 0.26 ± 0.01ab 5.21 ± 0.22a 20.15 ± 0.23b
JP 21.61 ± 1.58d 0.96 ± 0.01cde 3.09 ± 0.05a 0.26 ± 0.00ab 4.72 ± 0.01a 25.92 ± 1.61b
MP 9.47 ± 0.06b 0.84 ± 0.03 cd 3.16 ± 0.01a 0.27 ± 0.01ab 6.86 ± 0.15a 13.75 ± 0.01b
JC 9.88 ± 0.06b 1.05 ± 0.12de 2.77 ± 0.14a 0.27 ± 0.03ab 7.72 ± 0.14a 13.96 ± 0.34b
MC 9.84 ± 0.15b 1.10 ± 0.02e 3.78 ± 0.20b 0.31 ± 0.01b 8.32 ± 0.13a 15.04 ± 0.38b

Microorganism Samples Lactic acid Acetic acid Propionic acid Butyric acid TOTAL SCFAs

0h 12 h

Escherichia coli C 0.00 ± 0.00a 0.65 ± 0.03a 6.39 ± 0.41a 0.04 ± 0.00a 18.27 ± 1.13b 7.08 ± 0.44a
GLC 4.83 ± 0.36c 0.87 ± 0.02ab 6.81 ± 0.24a 0.04 ± 0.00a 12.85 ± 0.07a 12.55 ± 0.57a
FOS 0.03 ± 0.00a 0.81 ± 0.01ab 6.71 ± ± 0.04a 0.05 ± 0.00ab 9.36 ± 0.38b 7.59 ± 0.05a
JP 2.98 ± 0.12b 1.26 ± 0.18c 6.68 ± 0.20a 0.06 ± 0.00bc 13.53 ± 0.31b 10.97 ± 0.26a
MP 0.49 ± 0.04a 0.95 ± 0.03ab 7.48 ± 0.56ab 0.26 ± 0.00d 13.81 ± 0.15b 9.19 ± 0.63a
JC 0.03 ± 0.01a 1.00 ± 0.03bc 9.84 ± 0.33c 0.07 ± 0.00c 13.36 ± 0.44b 10.93 ± 0.28a
MC 0.00 ± 0.00a 0.88 ± 0.04ab 8.72 ± 0.36bc 0.05 ± 0.00ab 16.80 ± 0.82b 9.64 ± 0.31a

The values are the means of duplicate determination. ± indicates the standard deviation of the mean. The a–b Different lowercase letters on the same line indicate a
significant difference (p ≤ 0.05) between values based on the Tukey test. The a – e Different lowercase letters in the same column indicate a significant difference
(p ≤ 0.05) between the values based on the Tukey test C: control; GLC: glucose; FOS: fructooligosaccharide; JP: jerivá pulp; MP: macaúba pulp; JC: jerivá kernel cake;
MC: macaúba kernel cake; SCFA: short-chain fatty acid.

7
A.C. Andrade, et al.
4. Conclusions
The pulp and kernel cake from jerivá and macaúba fruits have nu-
tritional characteristics relevant to human health. Jerivá and macaúba
pulps and kernel cakes presented high levels of dietary fiber, with
20.45% in JP, 37.87% in JC, 19.95% in MP, and 35.81% in MC. These
byproducts also had high antioxidant activity, especially JP, which also
showed the highest values for ABTS (2498.49 µM Trolox·g−1) and
DPPH (96.97gfruit·g−1 DPPH), in addition to a high total phenolic
content (850.62 mg GAE·100 g−1). Also, JP promoted a better growth
of probiotic strains and a more relevant pH reduction when compared
to the commercial prebiotic FOS. However, MP, JC, and MC were also
able to favor the growth of the strains. Probiotic microorganisms were
able to use JP, MP, JC, and MC and produced short-chain fatty acids
such as lactic, propionic, butyric, and acetic acid, capable of promoting
health benefits. Therefore, the byproducts from jerivá and macaúba oil
extraction have characteristics that indicate their prebiotic potential,
and maybe exciting components to increase the nutritional value of
foods.
CRediT authorship contribution statement
Amanda Cristina Andrade: Investigation, Methodology, Writing -
original draft. Júlia Fernanda Urbano Marinho: Investigation,
Methodology. Angélica Cristina Souza: Investigation, Methodology,
Writing - original draft. Talita Sousa Tavares: Investigation,
Methodology. Disney Ribeiro Dias: Formal analysis, Writing - review
& editing. Rosane Freitas Schwan: Formal analysis, Writing - review &
editing. Cleiton Antônio Nunes: Formal analysis, Project administra-
tion, Writing - review & editing. Sabrina Carvalho Bastos: Formal
analysis, Project administration, Writing - review & editing.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgments
The authors are thankful to Fundação de Amparo à Pesquisa do
Estado de Minas Gerais (FAPEMIG) and Conselho Nacional de
Desenvolvimento Científico e Tecnológico (CNPq) for financial support;
to Sacco®Brasil for providing the probiotics; to Laboratório de
Microbiologia de Alimentos (UFLA, Brasil) for providing the patho-
genics train; to Laboratório de Microbiologia das Fermentações (UFLA,
Brasil) for the infrastructure; and to Geraldo de Sousa Cândido and
Maria Aparecida Gomes Souza-Dias for technical support.
Funding
This study was supported by Conselho Nacional de
Desenvolvimento Científico e Tecnológico (CNPq, Brazil) and Fundação
de Amparo à Pesquisa de Minas Gerais (FAPEMIG, Brazil, APQ-00638-
14 and PPM-00498-16).
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