LWT - Food Science and Technology 135 (2021) 110053

Contents lists available at ScienceDirect

LWT
journal homepage: www.elsevier.com/locate/lwt

Bioactive compounds and antioxidant capacity of grape pomace flours

Gean Charles Monteiro a, b, Igor Otavio Minatel b, *, Adilson Pimentel Junior a,
Hector Alonzo Gomez-Gomez c, João Pedro Corrêa de Camargo b, Marla Silvia Diamante a, b,
Letícia Silva Pereira Basílio a, b, Marco Antonio Tecchio a, Giuseppina Pace Pereira Lima b
a
Department of Horticulture, School of Agriculture, São Paulo State University, Botucatu, São Paulo, Brazil
b
Department of Chemistry and Biochemistry, Institute of Bioscience, São Paulo State University, 18.618-689, Botucatu, São Paulo, Brazil
c
Department of Food Technology, Universidad Nacional de Agricultura, Barrio El Espino, Catacamas, Honduras

A R T I C L E I N F O A B S T R A C T

Keywords: Grape pomace is the main residue from juice and wine industries, and their derived products such as flours, can
Polyphenols be a rich source of phenolic compounds and antioxidants. The overall objective of this study was to assess the
Amino acids phenolic compounds, antioxidant capacity, biogenic amines, and amino acids in flours obtained from grape
Biogenic amines
pomace. Four cultivars (’Niagara Rosada’, ’Bordo’, ’BRS Violeta’, and ’IAC 138-22 Máximo’) were used, isolated
Residues
Grape by-product
or as blends, for juice production and from the resulting pomace, flours were produced. All flours assessed,
independently of the cultivar or blend, showed valuable potential to addition in new products. The lowest levels
of phenolic compounds and antioxidant capacity were observed in the flour produced entirely from cultivar
’Niagara Rosada’. However, when ’Niagara Rosada’ was incorporated in blends with other cultivars, flours with
increased levels of phenolic compounds and antioxidant capacity were obtained. The flour production gives a
better destination for industrial waste, since these flours can be used for food, cosmetic, and pharmaceutical
industries as additives or supplements to improve the antioxidant and bioactive content of their products.

1. Introduction
Residues from winemaking and the grape juice industry have
attracted attention as potential components for new food products.
Moreover, consumers have become more interested in sustainable in­
dustrial practices. Exploitation of these by-products in the food industry
may promote a set of benefits by reducing industrial waste discharge and
increasing the economic gains by reutilization. Industrial extraction of
grape juices is achieved by hot or cold pressing and the resulting pomace
is usually discarded. This pomace is the main solid waste produced by
the grape juice industry, representing up to 60% of total solid waste and
around 20%–25%, in weight, of the grapes used (Spigno, Marinoni, &
Garrido, 2017). The most common destination, in Europe, for solid
grape residues are land-spreading, incineration, or animal feeding
(Spigno et al., 2017), and a similar situation is observed in Brazil.
Nevertheless, this material contains several compounds with health
benefits that may add value to products from the food, cosmetic or
pharmaceutical industries. In addition, this residue may be used for
other purposes, such as natural dyes, preservatives and/or antioxidants
in food products (Tavares et al., 2019).
The major macronutrients in grape pomace are proteins, lipids, and
carbohydrates (Taşeri et al., 2018), in addition to the micronutrients,
vitamins and phenolic compounds, which have antioxidant activity
against reactive oxygen species. It is recognized that antioxidants have a
direct relationship with antitumor, anti-aging, antimicrobial, and
anti-inflammatory effects (Peixoto et al., 2018; Sies & Jones, 2020),
making grape pomace derived products an attractive addition to the
human diet. However, grape pomace may show variation in metabolite
content according to cultivar, cultivation conditions, climate, and
ripening stage (Peixoto et al., 2018; Taşeri et al., 2018).
Phenolic compounds are the main compounds found in grape
pomace (Taşeri et al., 2018; Tavares et al., 2019) and certain amino
acids (lysine, phenylalanine, tyrosine, arginine, and histidine) and
biogenic amines (putrescine and cadaverine) have been described in
winemaking by-products (Chikwanha, Raffrenato, Muchenje, Musar­
urwa, & Mapiye, 2018; Moncalvo et al., 2016). Biogenic amines are
important markers of food quality, mainly for processed foods or addi­
tives, since they exert allergenic and/or toxic effects (histamine and
tyramine) in consumers (Sánchez-Pérez et al., 2018), and indicate poor
sanitary conditions (undesired microbiological spoilage - cadaverine

* Corresponding author. Institute of Bioscience, Department of Chemistry and Biochemistry, São Paulo State University – UNESP, 18618-689, Botucatu, SP, Brazil.
E-mail address: igorminatel@gmail.com (I.O. Minatel).

https://doi.org/10.1016/j.lwt.2020.110053
Received 26 April 2020; Received in revised form 8 August 2020; Accepted 10 August 2020
Available online 15 August 2020
0023-6438/© 2020 Elsevier Ltd. This article is made available under the Elsevier license (http://www.elsevier.com/open-access/userlicense/1.0/).
G.C. Monteiro et al.
and putrescine) (Papageorgiou et al., 2018). However, few studies
report the content of biogenic amines in by-products from grape juice
production.
In Brazil, grape juices are mainly prepared from hybrid grapes, such
as the cultivars ’Bordo’, ’Máximo’, and ’Violeta’ (Gomez-Gomez et al.,
2018). Of the table grapes produced for fresh consumption, the cultivar
’Niagara Rosada’ is the most commonly consumed and is distinguished
by its high productivity. However, there is surplus production and,
recently, the industry has also used this cultivar for juice extraction. The
’Niagara Rosada’ is less pigmented than other grapes and requires
blending to obtain a juice that satisfies the consumers demands (Cruz
et al., 2018). The Brazilian and world grape juice markets have
increased in recent years and alternative means of residues disposal
could reduce environmental contamination and provide a better desti­
nation for a low-cost waste with nutritional and functional properties
(Beres et al., 2017). In the literature, there is little or no information
regarding the bioactive compounds and antioxidant capacity of grape
pomace flours (GPF) obtained after grape juice extraction, especially
from hybrid cultivars. In this context, the aim of this study was to
evaluate the profile of phenolic compounds and bioactive amines, and
the antioxidant capacity of the GPF obtained from different grape blends
used for juice production. The correlations between antioxidant capac­
ity, total phenolic content (TPC), and total anthocyanins content (TAC)
were also assessed.
2. Material and methods
2.1. Chemicals
Anhydrous sodium acetate, acetic acid, hydrochloric acid, ethyl
alcohol, Folin-Ciocalteu reagent, potassium chloride, sodium carbonate,
potassium persulfate, and iron chloride were purchased from Dinâmica
(Dinâmica Química, São Paulo, Brazil). 6-hydroxy-2,5,7,8-tetramethyl­
chroman-2-carboxylic acid (Trolox), 2,2-diphenyl-1-picrylhydrazyl
(DPPH), 2,2′ -azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) dia­
mmonium salt (ABTS), 2,4,6-tris(2-pyridyl)-s-triazine (TPTZ), dansyl
chloride, L-proline, potassium carbonate, toluene, perchloric acid,
phosphoric acid, acetonitrile, methanol, sodium acetate trihydrate, and
all phenolic and biogenic amines standards were acquired from Sigma-
Aldrich (Sigma-Aldrich, St. Louis, MO).
2.2. Grape cultivars and harvest conditions
Four red hybrid grape cultivars were used: ’Niagara Rosada’ – a
result of a somatic mutation of ’Niagara Branca’ (’Concord’ × ’Cas­
sady’); ’Máximo’ - ’IAC 138-22 Máximo’ (’Seibel 11342’ × ’Syrah’);
’Bordo’ – a result of ’Hartford’ seed selection (’Isabella’ × ’V. labrusca’)
and ’Violeta’; and - ’BRS Violeta’ (’Traviu’ × ’Rubea’). The grapes were
harvested in December 2017, when they reached maturity, i.e. the
average soluble solids content ranged from 17 to 20 ◦ Brix and titratable
acidity ranged from 0.7% to 1.3% of tartaric acid. After harvest, grapes
were immediately transported to the Sao Paulo State University
(UNESP) beverage laboratory and kept in cold storage (~4 ◦ C) for 1 day
prior to juice production.
2.3. Juice extraction and flour production
Whole juices from cultivars ’Niagara Rosada’, ’Máximo’, ’Bordo’,
and ’Violeta’, and blends of 75%, 50%, and 25%, of each cultivar with
cultivar ’Niagara Rosada’ were obtained by hot-pressing (60 ± 2 ◦ C, 1h).
The residual grape pomaces corresponded to approximately 24% of the
original weight of the grapes used for juice extraction and consisted of
seeds (39%), skins (5%), and pulp (56%). The materials was packed in
aluminum foil and oven dried at 50 ◦ C to constant weight (approxi­
mately 48 h). The dried material was milled (TE-650, Tecnal, Piracicaba,
Brazil) using a 0.5 mm sieve to obtain the GPF that were identified as
2
LWT 135 (2021) 110053
follows: 100N (100% ’Niagara Rosada’), 100M (100% ’Máximo’), 100B
(100% ’Bordo’), 100V (100% ’Violeta’), 75M, 50M and 25M (% of
’Máximo’ + ’Niagara Rosada’), 75B, 50B and 25B (% of ’Bordo’ +
’Niagara Rosada’), and 75V, 50V and 25V (% of ’Violeta’ + ’Niagara
Rosada’).
Before analysis sample were packed in dark-polypropylene-bags (0.8
mm thickness) and stored at − 20 ◦ C. The entire drying procedure, flour
preparation and analysis were carried out in the absence of light,
analyzed in triplicate and each repetition consisted of 200 g of GPF.
2.4. Flour extraction
The profile of phenolic compounds, TPC, TAC and antioxidant ca­
pacity using assays DPPH, Ferric Reducing Antioxidant Power (FRAP),
and ABTS, were assessed using the following extract: 1 g of flour was
homogenized with 5 mL of methanol:water:acetic acid (80:19:1 v/v),
followed by 1 h immersion in an ultrasonic bath (Eco-sonics, São Paulo,
Brazil) and centrifugation at 6000 xg for 20 min at 4 ◦ C (Hettich Mik­
ro220R, Tuttlingen, Germany). The supernatant was collected and the
procedure was repeated twice. The supernatants were mixed and
analyzed.
2.5. TPC and TAC analysis
The TPC was determined using Folin-Ciocalteu reagent (Singleton,
Orthofer, & Lamuela-Raventós, 1999). The absorbance was determined
at 725 nm after 30 min of reaction. The results were calculated using a
standard curve and expressed as mg equivalent of gallic acid per kg of
flour (mg kg− 1).
The TAC was calculated using the differential pH method (Giusti &
Wrolstad, 2001), and absorbances were set at 510 nm and 700 nm for
buffer solutions pH 1.0 and 4.5, respectively. Diluted sample absorbance
(A) was calculated using the following formula:
A = (Aλ vis− max(510) – A700 )pH ​ 1.0 – (Aλvis− max(510) – A700 )pH 4.5 (1)
and to calculate the monomeric anthocyanin concentration in the
sample the formula
A × MW ​ × DF × 1000
TAC = (2)
ε × 1
was used, where MW is the molecular weight of cyanidin 3,5-diglucoside
(the major anthocyanin in the samples - 611.5 g mol− 1), DF is the
dilution factor, and ε is the molar absorption coefficient (ε = 30.175).
The content of monomeric anthocyanins was expressed as mg equivalent
of cyanidin 3,5-diglucoside per kg of flour (mg kg− 1).
2.6. Antioxidant capacity
The capacity of the flours to reduce the DPPH radicals was measured
following the method of Brand-Williams, Cuvelier, and Berset (1995).
Absorbance was measured at 517 nm. ABTS radical scavenging activity
was detected using the spectrophotometric method and the reading was
determined at 734 nm (Re et al., 1999). Both DPPH and ABTS results
were expressed as mg of Trolox equivalents (TEAC) per kg of flour (mg
TEAC kg− 1) using the standard curve (DPPH: y = 23.606x + 2.5805, R2
= 0.99 and ABTS: y = 9.389x + 5.5331, R2 = 0.99). The FRAP assay was
carried out according to Benzie and Strain (1996), and the reading was
performed at 594 nm and expressed in mM Fe2 kg− 1 of flour.
2.7. HPLC profile of phenolic compounds
The methanolic extract described in section 2.4 was used to detect
phenolic compounds, carried out according to Natividade, Corrêa,
Souza, Pereira, and Lima (2013), with minor modifications. Briefly, the
extracts were filtered through membrane filters (PTFE, 0.45 μm,
G.C. Monteiro et al. LWT 135 (2021) 110053

Millipore, Burlington, MA) and injected (20 μL) into an HPLC system
(UltiMate 3000RS, Dionex-Thermo Fisher Scientific, San Jose, CA),
coupled to a diode array detector and a C18 column (2.0 × 50 mm,
Luna® C18 HST 2.5 μm; Phenomenex, Torrance, CA), with a flow rate of
0.6 mL min− 1 at 39 ◦ C.
Phenolic compounds were identified by comparing the retention
times and UV spectra with commercial standards, quantified through
standard curves, and the results were expressed as μg (3-hydroxytyrosol)
or mg per kg of GPF dry weight (DW). The phenolic compounds profile
was measured at 280 nm (3-hydroxytyrosol and catechin), 320 nm
(caffeic acid, trans-ferulic acid, and ρ-cumaric acid), 360 nm (rutin and
kaempferol) and 520 nm (anthocyanins).
2.8. Biogenic amines
Amino acids and biogenic amines extraction and analysis were car­
ried out according to the method previously described by Diamante et al.
(2019). Compounds were identified by comparing their retention time
and UV spectrum with commercial standards. Calibration curves were
prepared with commercial standards and the data were expressed in mg
kg− 1 dry weight.
2.9. Statistical analysis
analysis of variance (ANOVA), followed by the Scott-Knott means
comparison test. Correlation analysis, principal components analysis
(PCA) and hierarchical cluster analysis (HCA) were performed using the
statistical software XLSTAT, version 19.4 (Addinsoft, Paris, France). The
P-value <0.05 was considered statistically significant.
3. Results and discussion
The commercial market for natural products has increased and the
use of industrial by-products, such as the grape pomace, could be a way
to satisfy this demand. In recent years the grape pomace utilization has
been inefficient, and the greater part of this by-product has been dis­
carded in land field, causing environmental concerns (Spigno et al.,
2017). There is no official report or legislation in Brazil regarding the
destination of residues from wine or juice industries. However, it is
estimated that 70%–80% of the residues generated by the grape juice
industry are sent to companies preparing compost or animal feed,
whereas, small family businesses typically use their residues to make
compost and fertilize the vineyards. Taking this into account, the pur­
pose of the present study was to produce flours from the pomace
generated from grape juice production. As the intention was to assess all
the bioactive content of the GPF, the whole pomace was used and the
traditional processes of grape seed oil removal was not carried out, since
this oil is a rich source of phenolic compounds (Beres et al., 2017).

The results of the (at least triplicate) experiments were submitted to

Table 1
1
Profile of phenolic compounds in different GPF (mg kg− DW).
Compound All GPF

100N 100M 75M 50M 25M 100B 75B 50B 25B 100V 75V 50V 25V

Anthocyanins
Cyanidin 3-O- 1.2 ± 0.5 ± 0.6 ± 1.0 ± 1.2 ± 2.5 ± 2.2 ± 2.0 ± 2.0 ± 7.2 ± 5.0 ± 4.0 ± 2.3 ±
glucoside 0.00h* 0.01l 0.01k 0.01j 0.00i 0.02d 0.00f 0.01g 0.04g 0.08a 0.04b 0.04c 0.01e
Cyanidin 3,5- 28.5 ± 29.8 ± 29.4 ± 29.2 ± 29.0 ± 37.4 ± 34.2 ± 32.2 ± 32.2 ± 118.1 ± 106.0 ± 79.5 ± 54.2 ±
diglucoside 0.06h 0.22h 0.07h 0.04h 0.02h 0.35e 0.10f 0.04g 0.04g 2.79a 1.45b 1.12c 0.73d
Peonidin 3-O- 0.7 ± 1.2 ± 1.2 ± 1.1 ± 0.9 ± 1.3 ± 1.1 ± 1.0 ± 1.0 ± 2.4 ± 2.3 ± 1.7 ± 1.3 ±
glucoside 0.00j 0.01e 0.01e 0.00f 0.00i 0.07d 0.04g 0.01h 0.01h 0.01a 0.01a 0.03b 0.01c
Delphinidin 3-O- 18.4 ± 19.5 ± 19.5 ± 19.3 ± 19.1 ± 22.6 ± 21.8 ± 20.3 ± 20.0 ± 34.3 ± 32.8 ± 28.0 ± 22.3 ±
glucoside 0.01l 0.01i 0.01i 0.00j 0.05k 0.10d 0.02f 0.11g 0.05h 0.16a 0.14b 0.26c 0.09e
Malvidin 3-O- Nd 7.1 ± 6.8 ± 6.1 ± 4.6 ± 5.1 ± 4.4 ± 3.8 ± 3.6 ± 5.0 ± 5.0 ± 4.1 ± 3.5 ±
glucoside 0.04a 0.07b 0.07c 0.05f 0.19d 0.04g 0.05i 0.01j 0.14e 0.05e 0.11h 0.01j
Malvidin 3,5- 3.0 ± 24.9 ± 19.8 ± 14.9 ± 10.3 ± 78.2 ± 49.6 ± 36.3 ± 30.5 ± 75.9 ± 73.5 ± 45.1 ± 26.3 ±
diglucoside 0.01m 0.14i 0.14j 0.20k 0.20l 1,54a 0.18c 0.77f 0.29g 0.01b 0.01d 0.52e 0.00h
Flavonol
Rutin 12.2 ± 6.4 ± 8.9 ± 9.2 ± 11.3 ± 4.9 ± 7.1 ± 8.4 ± 11.3 ± 3.7 ± 7.7 ± 7.89 ± 9.04 ±
0.19a 0.01g 0.25c 0.17c 0.25b 0.11h 0.02f 0.22d 0.36b 0.02i 0.15e 0.02e 0.17c
Kaempferol 0.6 ± 2.9 ± 2.0 ± 1.8 ± 1.4 ± 2.9 ± 2.1 ± 1.6 ± 1.0 ± 0.1 ± 0.2 ± 0.18 ± 0.22 ±
0.01h 0.05a 0.01c 0.10d 0.03f 0.15a 0.04b 0.03e 0.02g 0.00j 0.01i 0.01i 0.01i
Phenolic acids
3-hydroxytyrosol 0.6 ± 1.6 ± 1.3 ± 1.3 ± 1.1 ± 5.9 ± 3.7 ± 3.0 ± 2.2 ± 8.3 ± 7.3 ± 5.4 ± 4.9 ±
(μg kg− 1) 0.01k 0.24i 0.10j 0.15j 0.00j 0.35c 0.08f 0.04g 0.01h 0.10a 0.03b 0.04d 0.13e
p-Coumaric 1.3 ± 2.6 ± 2.1 ± 1.8 ± 1.6 ± 3.8 ± 3.4 ± 2.8 ± 1.4 ± 4.0 ± 3.8 ± 2.1 ± 1.4 ±
0.17j 0.02e 0.02f 0.04g 0.04h 0.07b 0.04c 0.08d 0.01i 0.00a 0.04b 0.09f 0.01i
Caffeic 12.3 ± 1.3 ± 2.9 ± 5.9 ± 11.3 ± 9.8 ± 10.2 ± 10.6 ± 12.1 ± 4.4 ± 8.6 ± 10.8 ± 11.6 ±
0.01a 0.01m 0.01l 0.01j 0.13d 0.15h 0.19g 0.15f 0.09b 0.02k 0.04i 0.02e 0.16c
Trans-Ferulic 0.8 ± 1.3 ± 1.2 ± 1.2 ± 1.2 ± 2.8 ± 2.5 ± 2.0 ± 1.4 ± 3.6 ± 3.6 ± 2.8 ± 1.7 ±
0.01h 0.05f 0.02g 0.01g 0.01g 0.05b 0.02c 0.02d 0.02f 0.05a 0.06a 0.01b 0.02e
Flavan-3-ol
Catechin 38.3 ± 32.0 ± 32.8 ± 33.2 ± 36.4 ± 48.4 ± 46.1 ± 44.3 ± 43.8 ± 45.8 ± 44.0 ± 42.7 ± 39.5 ±
0.64f 0.05i 0.00h 0.22h 0.02g 0.20a 0.17b 0.19d 0.00d 0.13c 0.91d 0.25e 0.15f
TIPC 117.4 ± 129.6 127.3 124.9 128.4 219.8 184.8 165.3 160.2 304.5 ± 292.5 ± 228.9 173.6
0.54 ± 0.01 ± 0.58 ± 0.43 ± 0.76 ± 2.41 ± 0.09 ± 1.57 ± 0.17 2.61 2.60 ± 0.09 ± 0.84
TPC (g kg− 1) 23.2 ± 37.9 ± 36.3 ± 32.5 ± 29.5 ± 28.5 ± 26.8 ± 24.8 ± 24.4 ± 49.3 ± 43.6 ± 39.3 ± 31.6 ±
0.29j 0.37d 0.83e 0.61f 0.89g 0.04g 0.43h 0.20i 0.52i 0.86a 0.67a 0.85c 0.60f
TAC (g kg− 1) 1.2 ± 2.5 ± 1.8 ± 1.5 ± 1.3 ± 5.5 ± 3.8 ± 2.8 ± 1.4 ± 7.9 ± 7.3 ± 5.1 ± 2.4 ±
0.04k* 0.09g 0.04h 0.03i 0.04j 0.07c 0.10e 0.08f 0.04i 0.08a 0.04b 0.06d 0.05g

Values represent the mean ± the standard deviation of three repetitions. *Different letters in the same line represents values statistically different by Scott-Knott test (p
< 0.05). Nd: not detected. 100N: 100% ’Niagara Rosada’; 100M: 100% ’Máximo’; 75M: 75% ’Máximo’ + 25% ’Niagara Rosada’; 50M: 50% ’Máximo’ + 50% ’Niagara
Rosada’; 25M: 25% ’Máximo’ + 75% ’Niagara Rosada’; 100B: 100% ’Bordo’; 75B: 75% ’Bordo’ + 25% ’Niagara Rosada’; 50B: 50% ’Bordo’ + 50% ’Niagara Rosada’;
25B: 25% ’Bordo’ + 75% ’Niagara Rosada’; 100V: 100% ’Violeta’; 75V: 75% ’Violeta’ + 25% ’Niagara Rosada’; 50V: 50% 50% ’Violeta’ + 50% ’Niagara Rosada’; 25V:
25% ’Violeta’ + 75% ’Niagara Rosada’. TIPC: total individual phenolic compounds.

3
 G.C. Monteiro et al. LWT 135 (2021) 110053

3.1. Phenolic compounds

Values represent the mean ± the standard deviation of three repetitions. *Different letters in the same line represents values statistically different by Scott-Knott test (p < 0.05). 100N: 100% ’Niagara Rosada’; 100M: 100%

50B: 50% ’Bordo’ + 50% ’Niagara Rosada’; 25B: 25% ’Bordo’ + 75% ’Niagara Rosada’; 100V: 100% ’Violeta’; 75V: 75% ’Violeta’ + 25% ’Niagara Rosada’; 50V: 50% 50% ’Violeta’ + 50% ’Niagara Rosada’; 25V: 25%
’Máximo’; 75M: 75% ’Máximo’ + 25% ’Niagara Rosada’; 50M: 50% ’Máximo’ + 50% ’Niagara Rosada’; 25M: 25% ’Máximo’ + 75% ’Niagara Rosada’; 100B: 100% ’Bordo’; 75B: 75% ’Bordo’ + 25% ’Niagara Rosada’;
153.90 ± 1.37e* 59.13 ± 0.23l 102.17 ± 0.31i 106.09 ± 0.45h 115.40 ± 0.37g 208.73 ± 0.66a 205.37 ± 1.78b 185.73 ± 1.60c 172.99 ± 0.27d 62.37 ± 0.03k 92.98 ± 0.68j 102.77 ± 3.44i 118.32 ± 0.03f
22.24 ± 0.61h 18.69 ± 0.05i 13.54 ± 0.04j 12.90 ± 0.52j 84.89 ± 0.95a 78.38 ± 2.41c 27.05 ± 1.54g 13.37 ± 0.64j 82.97 ± 0.08b 66.58 ± 1.25d 48.65 ± 1.97e 32.88 ± 0.48f

± 0.00h

0.65 ± 0.00h
± 0.02d
± 0.00g

± 0.00g

0.43 ± 0.00g
1.22 ± 0.01e

1.82 ± 0.00c
± 0.02f

0.86 ± 0.00f
Thirteen individual phenolic compounds were detected via HPLC
(Table 1). The highest individual phenolics content (304.5 mg kg− 1) was

2.81
2.84
2.32
0.08
0.06
found in GPF 100V, followed by blends 75V (292.5 mg kg− 1) and 50V
25V

(228.9 mg kg− 1). The lowest levels of these compounds (117.4 mg kg− 1)
were observed in GPF 100N.

0.06 ± 0.00h
4.18 ± 0.10d
7.17 ± 0.05a 5.34 ± 0.01b 3.63 ± 0.09c

3.04 ± 0.01c
5.70 ± 0.10c

1.68 ± 0.03c

1.85 ± 0.13c
0.09 ± 0.00f

0.53 ± 0.01f
0.37 ± 0.01i
Anthocyanins represented the major phenolic compound in GPF
100V, 100B, and 100M, with 79.8%, 67.0%, and 64.1% of the total in­
50V

dividual phenolic compounds, respectively. As expected, due to the low

pigmentation of ’Niagara Rosada’ grapes, the levels of anthocyanins in
0.06b
0.02b
0.10b

10.79 ± 0.00a 7.47 ± 0.07b

2.20 ± 0.15b
0.00e

0.62 ± 0.02e
0.00f

0.19 ± 0.00k 0.31 ± 0.00j

GPF 100N were the lowest, reaching 44.2%. However, blends of culti­
6.08 ±
3.14 ±
7.10 ±
0.09 ±
0.12 ±

vars ’Máximo’, ’Bordo’, or ’Violeta’ with cultivar ’Niagara Rosada’

75V

resulted in GPF with improved levels of anthocyanins and phenolic

compounds, such as rutin and caffeic acid (Table 1). The GPF 100V was
0.11 ± 0.00d
0.19 ± 0.00d
7.00 ± 0.00a
3.42 ± 0.02a
8.92 ± 0.01a

2.41 ± 0.09a
0.70 ± 0.00c
conspicuous compared to other flours as it contained compounds such as
cyanidin 3-O-glucoside, cyanidin 3,5-diglucoside, delphinidin 3-O-
100V

glucoside, peonidin 3-O-glucoside, 3-hydroxytrosol, ρ-cumaric acid,

and trans-ferulic acid (Table 1). Other studies have also detected an­
thocyanins such as malvidin 3,5-diglucoside in ’Bordo’ and ’Máximo’
0.33 ± 0.00h
0.41 ± 0.00g

0.86 ± 0.06g
0.12 ± 0.00e

1.12 ± 0.03e
0.09 ± 0.00f
1.36 ± 0.13i
1.46 ± 0.00i
1.69 ± 0.01i

0.40 ± 0.00j

grapes (da Silva et al., 2019; Lago-Vanzela, Da-Silva, Gomes, Gar­

cía-Romero, & Hermosín-Gutiérrez, 2011), and cyanidin 3,5-digluco­
25B

side, delphinidin 3-O-glucoside, cyanidin 3-O-glucoside, and malvidin

3,5-diglucoside in ’Violeta’ grapes (Natividade et al., 2013), in
0.02h

0.65 ± 0.01d
0.04g

0.74 ± 0.02g
1.11 ± 0.00e

1.38 ± 0.04e
0.00c
0.01c
1.11 ± 0.02f

0.02f

amounts similar to those found in this study. Catechin (32.0–48.4 mg

kg− 1) was the most abundant non-anthocyanin compound in all the GPF.
2.52 ±
2.21 ±
2.16 ±
0.12 ±
0.20 ±

Regarding the blends, flours prepared from ’Máximo’ (75M) showed

50B

the highest content of malvidin 3-O-glucoside (6.8 mg kg− 1), while those
from ’Bordo’ (75B) presented malvidin 3,5-diglucoside (49.6 mg kg− 1),
2.64 ± 0.01d

1.63 ± 0.01d
0.01b
0.00b

0.81 ± 0.00b
0.81 ± 0.00g
0.03e
0.02e
0.03e

0.85 ± 0.01f

kaempferol (2.1 mg kg− 1), and catechin (46.1 mg kg− 1). Flours con­
3.99 ±
2.41 ±
2.61 ±
0.14 ±
0.38 ±

taining 75% ’Violeta’ (75V) had high levels of cyanidin 3-O-glucoside

75B

(5.0 mg kg− 1), cyanidin 3,5-diglucoside (106.0 mg kg− 1), peonidin 3-

O-glucoside (2.3 mg kg− 1), delphinidin 3-O-glucoside (32.8 mg kg− 1),
0.66 ± 0.01h
2.65 ± 0.01d

0.05d
0.01a
0.00a

0.89 ± 0.01a

3-hydroxytyrosol (7.3 μg kg− 1), ρ-cumaric acid (3.8 mg kg− 1), and trans-
0.00e

1.02 ± 0.02e
0.18c

1.84 ± 0.02c

ferulic acid (3.6 mg kg− 1) (Table 1). The presence of diglucoside an­
4.91 ±
2.43 ±
3.65 ±
0.16 ±
0.44 ±
100B

thocyanins identifies the grapes used as hybrids, since varieties of

V. vinifera only synthesize monoglucoside anthocyanins (Wojdyło,
Samoticha, Nowicka, & Chmielewska, 2018). Anthocyanins, other pig­
0.18 ± 0.01h

0.66 ± 0.00h
1.18 ± 0.03d
0.24 ± 0.00k
0.07 ± 0.00g
0.09 ± 0.00f
1.32 ± 0.01i

0.62 ± 0.01l

0.21 ± 0.00l
1.33 ± 0.02j

ments, and phenolic compounds can render GPF more stable and more
resistant to oxidation and heating. However, a predominance of 3,
25M

5-diglucoside anthocyanins is more closely associated with these ef­

fects than monoglucoside anthocyanins (Tavares et al., 2019; Wojdyło
et al., 2018).
0.20 ± 0.01h

0.01h

0.00k

0.25 ± 0.00k
0.00e

1.21 ± 0.01c
0.00f

1.21 ± 0.00f
0.51 ± 0.00i
0.00j

The results of TPC and TAC analysis of 100% flours, i.e. not including
2.54 ±
1.35 ±
0.89 ±
0.10 ±
0.08 ±

blends, showed that the ’Violeta’ flour stands out as having the highest
50M

values (Table 1). When compared to pomace flours from other fruits,
DW) in different GPF.

such as apple (Gorjanović et al., 2020) and orange (Espinosa-Pardo,

0.39 ± 0.02g 0.20 ± 0.01h

0.00h

0.01d

1.38 ± 0.01b
0.00g

0.77 ± 0.03g
0.00e

1.43 ± 0.01e
0.01j

0.28 ± 0.01j

Nakajima, Macedo, Macedo, & Martínez, 2017), the levels of TPC in the
GPF analyzed in this study were 6.1 and 2.2 times higher, respectively.
2.73 ±
1.59 ±
1.05 ±
0.11 ±
0.12 ±
75M

In addition to high levels of phenolic compounds, GPF are among the

pomace flours with the highest anthocyanins content.
0.03h

0.00d

1.28 ± 0.01d

1.71 ± 0.02d
0.00b
0.01g

1.73 ± 0.01a
0.12f

0.29 ± 0.01i

3.2. Amino acids and biogenic amines

3.35 ±
1.72 ±
1.80 ±
0.14 ±
0.19 ±
100M
1
Amino acids and biogenic amines (mg kg−

The amino acids tryptophan, 5-hydroxytryptophan and L-dopa were

detected in all GPF, as well as histamine, serotonin, tyramine, trypt­
’Violeta’ + 75% ’Niagara Rosada’.
12.07 ± 0.10j

± 0.03m

0.18 ± 0.00m
0.16 ± 0.01h

± 0.00h

0.60 ± 0.00h
1.17 ± 0.01d
± 0.00k

± 0.00g

0.15 ± 0.01l
± 0.02j

amine, dopamine, putrescine, cadaverine, spermidine, and spermine

(Table 2). Other studies have also detected these compounds in grapes
All GPF

100N

0.96
0.97
0.35
0.08
0.06

and grape-derived beverages (Gomez-Gomez et al., 2020; Gomez-Gomez

et al., 2018; Restuccia, Sicari, Pellicanò, Spizzirri, & Loizzo, 2017),
5-hydroxytryptophan

although not in residues such as GPF.

All GPF contained considerable amounts of amino acids plus
biogenic amines (94.0–312.3 mg kg− 1), but those that stood out were
Monoamines
Tryptophan
Amino acids

Tryptamine

Spermidine
Cadaverine
Compound

Polyamines
Putrescine
Dopamine

Histamine
Serotonin

Tyramine

Spermine
Diamines

100B and 100V (Table 2). The 100B flour contained the highest levels of
Table 2

L-dopa

tryptophan (208.7 mg kg− 1), 5-hydroxytryptophan (84.9 mg kg− 1),

histamine (0.16 mg kg− 1), tyramine (0.44 mg kg− 1), and spermidine

4
G.C. Monteiro et al. LWT 135 (2021) 110053

(0.89 mg kg− 1), while 100V flour contained the highest levels of L-dopa
(7.2 mg kg− 1), serotonin (8.9 mg kg− 1), tryptamine (3.4 mg kg− 1),
dopamine (7.0 mg kg− 1), putrescine (10.8 mg kg− 1) and spermine (2.4
mg kg− 1).
Pearson’s correlation showed good correlation between L-dopa and
DPPH (r = 0.53), ABTS (0.67) and FRAP (r = 0.63), demonstrating the
possible action of this amino acid in the elimination of free radicals.
Higher levels of L-dopa occurred in 100V flour and blends 75V and 50V.
Flours produced entirely from ‘Niagara Rosada’ contained the lowest
levels of 5-hydroxytryptophan and L-dopa. Thus, inclusion of the
cultivar ‘Niagara Rosada’ in the blends induces a decrease in levels of
these amino acids in all samples. L-dopa has attracted attention due to its
action against Parkinson’s disease, as this amino acid can cross the
blood-brain barrier and form dopamine in nervous cells after amino acid
decarboxylation (Kanazawa & Sakakibara, 2000).
High levels of tryptophan and 5-hydroxytryptophan, as observed in
100B flour, are important dietary components, since they are precursors
of serotonin and melatonin. Serotonin is a monoamine neurotransmitter
that is involved in several biological process, such as neuromodulation,
appetite regulation, and, consequently, lipid and glucose metabolism
(Papageorgiou et al., 2018). Melatonin is associated with regulation of
the circadian rhythm and modulation of the immune system, and acts as
a potent hydroxyl radicals scavenger (Salehi et al., 2019). It is worth
mentioning that tryptophan ingestion and bioavailability can induce
serotonin and melatonin biosynthesis in the brain, as this amino acid can
cross the blood-brain barrier (Strasser, Gostner, & Fuchs, 2016). It is
important to emphasize that, in the present study, the levels of trypto­
phan found in the GPF were higher than the levels found in fifteen
different fruits (Islam, Shirakawa, Nguyen, Aso, & Komai, 2016). In this
same study, Islam et al. did not detect tryptamine in grapes, reinforcing
the importance of GPF as a rich source of tryptophan and tryptamine.
High levels of serotonin were observed in ’Violeta’ flours (100V, 75V
and 50V) and the lowest were found in ’Niagara Rosada’ (100N). Similar
results were observed for tryptamine (Table 2), another serotonin pre­
cursor. The serotonin content varied between 0.35 mg kg− 1 (100N) and
8.92 mg kg− 1 (100V), while the levels of tryptamine varied between
0.97 mg kg− 1 (100N) and 3.42 mg kg− 1 (100 V). Pearson’s correlation
analysis of the GPF showed a good correlation between serotonin and
antioxidant capacity (DPPH: r = 0.56; ABTS: r = 0.72; FRAP: r = 0.69).
In addition, the levels of serotonin and tryptamine showed a strong
correlation (r = 0.89). This correlation was also found between seroto­
nin and 5-hydroxytryptophan (r = 0.77), another serotonin precursor
(Strasser et al., 2016).
GPF obtained from ’Niagara Rosada’ contained the lowest level of
monoamines (histamine, tyramine, serotonin, dopamine, and trypt­
amine) (Table 2). Histamine and tyramine are biogenic amines that can
stimulate health disorders when consumed in excess. The amounts
necessary to induce cytotoxicity are 440.6 mg kg− 1 of histamine and
301.8 mg kg− 1 of tyramine (Linares et al., 2016). None of the flours
analyzed exceed the established limits, which indicates a positive effect
in terms of food safety.
Putrescine and cadaverine are sometimes considered to be markers
of contamination by undesirable microorganisms and as agents of
toxicity. However, low levels of both amines were observed in the GPF,
possibly indicating the absence of undesirable microorganism fermen­
tation during juice extraction or flour production. Putrescine and
cadaverine can impair histamine degradation in the intestine by inhib­
iting detoxifying enzymes (diamine oxidase and histamine N-methyl­
transferase) (Papageorgiou et al., 2018), and increasing the histamine
absorption, since they facilitate its passage to the small intestine. The
highest levels of putrescine were found in flour from ’Violeta’ (100V -
10.79 mg kg− 1 and 75V - 7.47 mg kg− 1), while GPF from ’Niagara
Rosada’ contained the lowest levels. Putrescine is considered a growth
factor and a precursor of spermidine and spermine, in addition to being a
biochemical marker of plant stress (Toro-Funes, Bosch-Fuste, Latorre-­
Moratalla, Veciana-Nogués, & Vidal-Carou, 2015). The increase in pu­
trescine levels may be related to its low conversion to the polyamines
spermidine and spermine (Kalač, 2014). The lowest level of cadaverine
was found in ’Violeta’ GPF, whereas the highest levels were found in
GPF 100M, 75M, and 50M. According to the data, the values of both
diamines (putrescine and cadaverine) were below the levels considered
toxic (2000 mg kg− 1) for human consumption (Papageorgiou et al.,
2018).
The levels of spermidine were significant in ’Bordo’ GPF (100B and
75B), while the highest levels of spermine were found in 100V and 75V.
Spermidine and spermine are important constituents of foods, since they
contribute to the elimination of free radicals and are regulators of
several cellular processes, such as cell differentiation and proliferation,
division and death, DNA and protein synthesis (Papageorgiou et al.,
2018). The intake of foods rich in spermidine and spermine is important
to maintain the function of vital organs in elderly people, as levels tend
to decrease with age (Larqué, Sabater-Molina, & Zamora, 2007). On the
other hand, intake should be controlled in people suffering from cancer
or those with familial cases of neoplasia (Cipolla, Havouis, & Moulinoux,
2010), since both spermidine and spermine are involved in the regula­
tion of cell division.
In general the content of amino acids and biogenic amines in the GPF
can be safely incorporated into foods or used as additives in pharma­
cological products. Furthermore, blends containing ’Niagara Rosada’
can result in flours with intermediary levels of tryptophan and reduced
levels of histamine and tyramine.
3.3. Antioxidant capacity, principal component (PCA) and hierarchical
cluster analysis (HCA)
TPC showed a higher correlation with the antioxidant capacity
(DPPH: r = 0.81; ABTS: r = 0.95, and FRAP: r = 0.98), than the TAC
(DPPH: r = 0.59; ABTS: r = 0.69 and FRAP: r = 0.63). Nevertheless, as
observed for 100V GPF, high levels of phenolic acids and polyphenols
were directly associated with improved antioxidant capacity (Table 3),

Table 3
Antioxidant capacity (DPPH, ABTS and FRAP) in different GPF.
Compound All GPF

100N 100M 75M 50M 25M 100B 75B 50B 25B 100V 75V 50V 25V

DPPH (mg 255.4 ± 343.7 ± 339.2 ± 335.6 ± 313.1 ± 332.9 ± 321.9 ± 292.9 ± 278.9 ± 358.0 ± 343.5 ± 334.9 ± 328.3 ±
TEAC kg− 1) 7.41h 1.95b 5.10b 4.86c 5.31e 5.05c 1.34d 1.45f .1,24g 3.54a 0.99b 3.98c 2.64d
ABTS (mg 250.2 ± 401.4 ± 377.7 ± 358.1 ± 296.7 ± 329.3 ± 298.0 ± 273.7 ± 273.3 ± 470.3 ± 425.6 ± 384.9 ± 276.7 ±
TEAC kg− 1) 5.51i 14.41c 11.00d 2.90e 10.52g 8.29f 8.57g 12.20h 8.13h 3.42a 5.23b 5.85d 18.94h
FRAP (mM Fe 109.3 ± 159.4 ± 154.5 ± 146.1 ± 138.8 ± 132.4 ± 126.5 ± 125.2 ± 117.4 ± 180.4 ± 165.6 ± 159.2 ± 141.6 ±
kg− 1) 1.26j 1.17c 1.28d 3.13e 2.77f 3.26g 1.22h 1.70h 2.35i 1.82a 1.94b 2.09c 2.40f

Values represent the mean ± the standard deviation of three repetitions. *Different letters in the same line represents values statistically different by Scott-Knott test (p
< 0.05). 100N: 100% ’Niagara Rosada’; 100M: 100% ’Máximo’; 75M: 75% ’Máximo’ + 25% ’Niagara Rosada’; 50M: 50% ’Máximo’ + 50% ’Niagara Rosada’; 25M:
25% ’Máximo’ + 75% ’Niagara Rosada’; 100B: 100% ’Bordo’; 75B: 75% ’Bordo’ + 25% ’Niagara Rosada’; 50B: 50% ’Bordo’ + 50% ’Niagara Rosada’; 25B: 25%
’Bordo’ + 75% ’Niagara Rosada’; 100V: 100% ’Violeta’; 75V: 75% ’Violeta’ + 25% ’Niagara Rosada’; 50V: 50% 50% ’Violeta’ + 50% ’Niagara Rosada’; 25V: 25%
’Violeta’ + 75% ’Niagara Rosada’.

5
G.C. Monteiro et al. LWT 135 (2021) 110053

Fig. 1. Principal components analysis

(PCA) of the antioxidant capacity, indi­
vidual and total phenolic compounds in
different GPF.
100N: 100% ’Niagara Rosada’; 100M:
100% ’Máximo’; 75M: 75% ’Máximo’ +
25% ’Niagara Rosada’; 50M: 50%
’Máximo’ + 50% ’Niagara Rosada’; 25M:
25% ’Máximo’ + 75% ’Niagara Rosada’;
100B: 100% ’Bordo’; 75B: 75% ’Bordo’ +
25% ’Niagara Rosada’; 50B: 50% ’Bordo’
+ 50% ’Niagara Rosada’; 25B: 25%
’Bordo’ + 75% ’Niagara Rosada’; 100V:
100% ’Violeta’; 75V: 75% ’Violeta’ + 25%
’Niagara Rosada’; 50V: 50% 50% ’Violeta’
+ 50% ’Niagara Rosada’; 25V: 25% ’Vio­
leta’ + 75% ’Niagara Rosada’. TAC: total
anthocyanins; TPC: total phenolic
compounds.

Fig. 2. Principal components analysis (PCA)

of the nitrogen compounds in different GPF.
100N: 100% ’Niagara Rosada’; 100M: 100%
’Máximo’; 75M: 75% ’Máximo’ + 25%
’Niagara Rosada’; 50M: 50% ’Máximo’ + 50%
’Niagara Rosada’; 25M: 25% ’Máximo’ + 75%
’Niagara Rosada’; 100B: 100% ’Bordo’; 75B:
75% ’Bordo’ + 25% ’Niagara Rosada’; 50B:
50% ’Bordo’ + 50% ’Niagara Rosada’; 25B:
25% ’Bordo’ + 75% ’Niagara Rosada’; 100V:
100% ’Violeta’; 75V: 75% ’Violeta’ + 25%
’Niagara Rosada’; 50V: 50% 50% ’Violeta’ +
50% ’Niagara Rosada’; 25V: 25% ’Violeta’ +
75% ’Niagara Rosada’.

and corroborated the results of other studies with grape pomace (Peix­
oto et al., 2018; Taşeri et al., 2018; Tavares et al., 2019). After juice
extraction, the grape pomace retained most of the bioactive compounds
present in the whole grape and, comparing the results obtained in this
study with juices prepared with similar grapes (Lima et al., 2014), it was
possible to observe a higher amount of phenolic compounds and anti­
oxidant capacity in the GPF than in the juices.
The Pearson’s correlation analysis of individual phenolic compounds
with DPPH, ABTS, and FRAP revealed a positive correlation with four
anthocyanins: cyanidin 3,5-diglucoside (r = 0.52, 0.70, and 0.72,
respectively), delphinidin 3-O-glucoside (r = 0.55, 0.72, and 0.71,
respectively), peonidin 3-O-glucoside (r = 0.69, 0.83, and 0.84,
respectively) and malvidin 3-O-glucoside (r = 0.79, 0.62, and 0.63,
respectively). In addition, analyzing the results from Table 1 it is note­
worthy that GPF with up to 25% of ’Niagara Rosada’ maintained high
levels of antioxidants.
In order to establish a descriptive model to group GPF based on
antioxidant activity (DPPH, ABTS, and FRAP), amino acids, profiles of

6
G.C. Monteiro et al.
Fig. 3. The hierarchical cluster analysis dendrogram of GPF by the contents of
bioactive compounds and antioxidant capacity.
100N: 100% ’Niagara Rosada’; 100M: 100% ’Máximo’; 75M: 75% ’Máximo’ +
25% ’Niagara Rosada’; 50M: 50% ’Máximo’ + 50% ’Niagara Rosada’; 25M:
25% ’Máximo’ + 75% ’Niagara Rosada’; 100B: 100% ’Bordo’; 75B: 75%
’Bordo’ + 25% ’Niagara Rosada’; 50B: 50% ’Bordo’ + 50% ’Niagara Rosada’;
25B: 25% ’Bordo’ + 75% ’Niagara Rosada’; 100V: 100% ’Violeta’; 75V: 75%
’Violeta’ + 25% ’Niagara Rosada’; 50V: 50% 50% ’Violeta’ + 50% ’Niagara
Rosada’; 25V: 25% ’Violeta’ + 75% ’Niagara Rosada’.
biogenic amines and phenolic compounds, and total phenols, both PCA
and HCA were conducted (Figs. 1 and 2). The results for antioxidant
capacity and phenolic compounds profile showed that PC1 and PC2
accounted for 84.15% of the data variance (Fig. 1). There was a clear
separation between flours containing high levels of ’Niagara Rosada’
(PC1-). All flours from ’Máximo’ and some flours from ’Bordo’ (75B and
50B) were grouped in PC1-: in this grouping, the flours presented the
highest rutin content and the lowest level of anthocyanins (Table 1). The
GPF from cultivar ’Máximo’ showed the highest content of kaempferol
and malvidin 3-O-glucoside (Table 1) and were grouped in PC2- (Fig. 1).
The PCA of amino acids and biogenic amines (Fig. 2) explained
87.12% (PC1: 63.78% and PC2: 23.34%) of the variance and explained a
grouping of flours with the highest levels of ’Violeta’ (100V, 75V and
50V) and ’Bordo’ (100B and 75B) in the PC1+. These flours contain the
lowest levels of cadaverine (Table 2).
Hierarchical cluster analysis using similarity (Pearson’s correlation
coefficient) (Fig. 3) revealed the separation of three distinct groups (A′ ,
B′ , and C′ ), reflecting Tables 1 and 3 and Fig. 1. The dendrogram pro­
duced showed the separation of a group with flours from ’Bordo’ (25B,
50B, 75B and 100B) and ’Niagara Rosada’ (100N) (A′ ). This separation
may be attributed to the levels of tryptophan (153.9–208.7 mg kg− 1)
found in flour from ’Bordo’ and ’Niagara Rosada’, which is distinct from
other flours. Flours from ’Violeta’ (50V, 75V and 100V) were grouped in
B′ , which differed from other flours, mainly due to the highest content of
some polyphenols, such as cyanidin 3-O-glucoside, cyanidin 3,5-diglu­
coside, delphinidin 3-O-glucoside, peonidin 3-O-glucoside, and trans-
ferulic acid, in addition to total anthocyanins, total phenolics, antioxi­
dant capacity (DPPH, ABTS, and FRAP), and nitrogenous compounds (L-
dopa, serotonin, tryptamine, dopamine, putrescine, and spermine).
Cluster C′ , formed by flours from ’Máximo’ (25M, 50M, 75M and 100M)
and 25% ’Violeta’ (25V), was connected by similar levels of rutin, total
anthocyanins, total phenolics, and dopamine content.
4. Conclusion
This study demonstrated that GPF (a low cost ingredient from the
wine and grape juice industry) shows promise as an additive in the food
and pharmaceutical industries. The profile of the phenolic compounds
and some nitrogen compounds, besides the antioxidant capacity, varied
depending on the grape cultivar and the blend used to produce the flour.
Bioactive compounds and antioxidant capacity were lower in ’Niagara
Rosada’ GPF than in flours from other cultivars. However, the addition
7
LWT 135 (2021) 110053
of ’Niagara Rosada’ in blends with other cultivars resulted in GPF that
retained high levels of bioactive compounds and antioxidant capacity.
Blends containing up to 25% of ’Niagara Rosada’ seemed to be
optimal in order to obtain GPF with low levels of allergenics and to
improve the supplementation of rutin and caffeic acid, without
compromising antioxidant capacity. Red grapes (’Máximo’, ’Bordo’, and
’Violeta’) have higher anthocyanin content, making them a good source
for food additives with good antioxidant capacity. These findings indi­
cate that GPF are rich sources of bioactive compounds, are safe for use as
foods or additives, and can be incorporated into industrial processes to
reduce waste discharge.
CRediT authorship contribution statement
Gean Charles Monteiro: Conducted experiments, Methodology,
Investigation, Writing - original draft. Igor Otavio Minatel: Method­
ology, Investigation, Writing - review & editing. Adilson Pimentel
Junior: Conducted experiments, Methodology, Investigation. Hector
Alonzo Gomez-Gomez: Conducted experiments, Methodology, Inves­
tigation. João Pedro Corrêa de Camargo: Conducted experiments,
Methodology, Investigation. Marla Silvia Diamante: Conducted ex­
periments, Methodology, Investigation. Letícia Silva Pereira Basílio:
Conducted experiments, Methodology, Investigation. Marco Antonio
Tecchio: Methodology, Investigation, Writing - original draft. Giu­
seppina Pace Pereira Lima: Writing - review & editing, Supervision,
Funding acquisition.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
The authors gratefully acknowledge the financial support of Sao
Paulo Research Foundation (FAPESP) (grant number 2016/22665-2),
National Council for Scientific and Technological Development (CNPq,
Brazil) (grant number 305177/2015-0 and 307571/2019-0) and Bra­
zilian Federal Agency for Support and Evaluation of Graduate Education
(CAPES) for the first author (G.C. Monteiro) fellowship (88882.433043/
2019-01).
References
Benzie, I. F. F., & Strain, J. J. (1996). The ferric reducing ability of plasma (FRAP) as a
measure of “antioxidant power”: The FRAP assay. Analytical Biochemistry, 239,
70–76. https://doi.org/10.1006/abio.1996.0292.
Beres, C., Costa, G. N. S., Cabezudo, I., Silva-James, N. K., Teles, A. S. C., Cruz, A. P. G.,
et al. (2017). Towards integral utilization of grape pomace from winemaking
process: A review. Waste Management, 68, 581–594. https://doi.org/10.1016/j.
wasman.2017.07.017.
Brand-Williams, W., Cuvelier, M. E., & Berset, C. (1995). Use of a free radical method to
evaluate antioxidant activity. Lebensmittel-Wissenschaft und -Technologie- Food Science
and Technology, 28, 25–30. https://doi.org/10.1016/S0023-6438(95)80008-5.
Chikwanha, O. C., Raffrenato, E., Muchenje, V., Musarurwa, H. T., & Mapiye, C. (2018).
Varietal differences in nutrient, amino acid and mineral composition and in vitro
rumen digestibility of grape (Vitis vinifera) pomace from the Cape Winelands
vineyards in South Africa and impact of preservation techniques. Industrial Crops and
Products, 118, 30–37. https://doi.org/10.1016/j.indcrop.2018.03.026.
Cipolla, B. G., Havouis, R., & Moulinoux, J.-P. (2010). Polyamine reduced diet (PRD)
nutrition therapy in hormone refractory prostate cancer patients. Biomedicine &
Pharmacotherapy, 64, 363–368. https://doi.org/10.1016/j.biopha.2009.09.022.
Cruz, M., Carvalho, D., Colombo, R., Yokota, L., Silva, A., Neto, H., et al. (2018).
Exploratory analysis of the sensory attributes of american grape juice blends.
Agronomy Science and Biotechnology, 4, 79–85. https://doi.org/10.33158/
ASB.2018v4i2p79.
Diamante, M. S., Borges, C. V., Silva, M. B., Minatel, I. O., Corrêa, C. R., Gomez-Gomez,
et al. (2019). Bioactive amines screening in four genotypes of thermally processed
cauliflower. Antioxidants, 8, 311–325. https://doi.org/10.3390/antiox8080311.
Espinosa-Pardo, F. A., Nakajima, V. M., Macedo, G. A., Macedo, J. A., & Martínez, J.
(2017). Extraction of phenolic compounds from dry and fermented orange pomace
G.C. Monteiro et al.
using supercritical CO2 and cosolvents. Food and Bioproducts Processing, 101, 1–10.
https://doi.org/10.1016/j.fbp.2016.10.002.
Giusti, M. M., & Wrolstad, R. E. (2001). Characterization and measurement of
anthocyanins by UV-Visible spectroscopy. In R. E. Wrolstad (Ed.), Current protocols in
food analytical chemistry (pp. F1.2.1–F1.2.13). New York: John Wiley & Sons.
https://doi.org/10.1002/0471142913.faf0102s00.
Gomez-Gomez, H. A. G., Marques, M. O. M., Borges, C. V., Minatel, I. O., Monteiro, G. C.,
Ritschel, P. S., et al. (2020). Biogenic amines and the antioxidant capacity of juice
and wine from Brazilian hybrid grapevines. Plant Foods for Human Nutrition, 75,
258–264. https://doi.org/10.1007/s11130-020-00811-5.
Gomez-Gomez, H. A., Minatel, I. O., Borges, C. V., Marques, M. O. M., Silva, E. T. da,
Monteiro, G. C., et al. (2018). Phenolic compounds and polyamines in grape-derived
beverages. Journal of Agricultural Science, 10, 65–77. https://doi.org/10.5539/jas.
v10n12p65.
Gorjanović, S., Micić, D., Pastor, F., Tosti, T., Kalušević, A., Ristić, S., et al. (2020).
Evaluation of apple pomace flour obtained industrially by dehydration as a source of
biomolecules with antioxidant, antidiabetic and antiobesity effects. Antioxidants, 9,
1–19. https://doi.org/10.3390/antiox9050413.
Islam, J., Shirakawa, H., Nguyen, T. K., Aso, H., & Komai, M. (2016). Simultaneous
analysis of serotonin, tryptophan and tryptamine levels in common fresh fruits and
vegetables in Japan using fluorescence HPLC. Food Bioscience, 13, 56–59. https://
doi.org/10.1016/j.fbio.2015.12.006.
Kalač, P. (2014). Health effects and occurrence of dietary polyamines: A review for the
period 2005-mid 2013. Food Chemistry, 161, 27–39. https://doi.org/10.1016/j.
foodchem.2014.03.102.
Kanazawa, K., & Sakakibara, H. (2000). High content of dopamine, a strong antioxidant,
in Cavendish banana. Journal of Agricultural and Food Chemistry, 48, 844–848.
https://doi.org/10.1021/jf9909860.
Lago-Vanzela, E. S., Da-Silva, R., Gomes, E., García-Romero, E., & Hermosín-Gutiérrez, I.
(2011). Phenolic composition of the edible parts (flesh and skin) of Bordô grape
(Vitis labrusca) using HPLC-DAD-ESI-MS/MS. Journal of Agricultural and Food
Chemistry, 59, 13136–13146. https://doi.org/10.1021/jf203679n.
Larqué, E., Sabater-Molina, M., & Zamora, S. (2007). Biological significance of dietary
polyamines. Nutrition, 23, 87–95. https://doi.org/10.1016/j.nut.2006.09.006.
Lima, M. D. S., Silani, I. D. S. V., Toaldo, I. M., Corrêa, L. C., Biasoto, A. C. T.,
Pereira, G. E., et al. (2014). Phenolic compounds, organic acids and antioxidant
activity of grape juices produced from new Brazilian varieties planted in the
Northeast Region of Brazil. Food Chemistry, 161, 94–103. https://doi.org/10.1016/j.
foodchem.2014.03.109.
Linares, D. M., del Rio, B., Redruello, B., Ladero, V., Martin, M. C., Fernandez, M., et al.
(2016). Comparative analysis of the in vitro cytotoxicity of the dietary biogenic
amines tyramine and histamine. Food Chemistry, 197, 658–663. https://doi.org/
10.1016/j.foodchem.2015.11.013.
Moncalvo, A., Marinoni, L., Dordoni, R., Duserm Garrido, G., Lavelli, V., & Spigno, G.
(2016). Waste grape skins: Evaluation of safety aspects for the production of
functional powders and extracts for the food sector. Food Additives & Contaminants:
Part A, 33, 1116–1126. https://doi.org/10.1080/19440049.2016.1191320.
Natividade, M. M. P., Corrêa, L. C., Souza, S. V. C. de, Pereira, G. E., & Lima, L. C. de O.
(2013). Simultaneous analysis of 25 phenolic compounds in grape juice for HPLC:
Method validation and characterization of São Francisco Valley samples.
Microchemical Journal, 110, 665–674. https://doi.org/10.1016/j.
microc.2013.08.010.
Papageorgiou, M., Lambropoulou, D., Morrison, C., Kłodzińska, E., Namieśnik, J., &
Płotka-Wasylka, J. (2018). Literature update of analytical methods for biogenic
amines determination in food and beverages. TRAC Trends in Analytical Chemistry,
98, 128–142. https://doi.org/10.1016/j.trac.2017.11.001.
LWT 135 (2021) 110053
Peixoto, C. M., Dias, M. I., Alves, M. J., Calhelha, R. C., Barros, L., Pinho, S. P., et al.
(2018). Grape pomace as a source of phenolic compounds and diverse bioactive
properties. Food Chemistry, 253, 132–138. https://doi.org/10.1016/j.
foodchem.2018.01.163.
Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., & Rice-Evans, C. (1999).
Antioxidant activity applying an improved ABTS radical cation decolorization assay.
Free Radical Biology and Medicine, 26, 1231–1237. https://doi.org/10.1016/S0891-
5849(98)00315-3.
Restuccia, D., Sicari, V., Pellicanò, T. M., Spizzirri, U. G., & Loizzo, M. R. (2017). The
impact of cultivar on polyphenol and biogenic amine profiles in Calabrian red grapes
during winemaking. Food Research International, 102, 303–312. https://doi.org/
10.1016/j.foodres.2017.10.012.
Salehi, B., Sharopov, F., Fokou, P. V. T., Kobylinska, A., de Jonge, L., Tadio, K., et al.
(2019). Melatonin in medicinal and food plants: Occurrence, bioavailability, and
health potential for humans. Cells, 8, 681–703. https://doi.org/10.3390/
cells8070681.
Sánchez-Pérez, S., Comas-Basté, O., Rabell-González, J., Veciana-Nogués, M., Latorre-
Moratalla, M., & Vidal-Carou, M. (2018). Biogenic amines in plant-origin foods: Are
they frequently underestimated in low-histamine diets? Foods, 7, 205–221. https://
doi.org/10.3390/foods7120205.
Sies, H., & Jones, D. P. (2020). Reactive oxygen species (ROS) as pleiotropic
physiological signalling agents. Nature Reviews Molecular Cell Biology, 21, 363–383.
https://doi.org/10.1038/s41580-020-0230-3.
da Silva, M. J. R., Padilha, C. V. S., Lima, M. S., Pereira, G. E., Filho, W. G. V.,
Moura, M. F., et al. (2019). Grape juices produced from new hybrid varieties grown
on Brazilian rootstocks – bioactive compounds, organic acids and antioxidant
capacity. Food Chemistry, 289, 714–722. https://doi.org/10.1016/j.
foodchem.2019.03.060.
Singleton, V. L., Orthofer, R., & Lamuela-Raventós, R. M. (1999). Analysis of total
phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu
reagent. Methods in Enzymology, 299, 152–178. https://doi.org/10.1016/S0076-
6879(99)99017-1.
Spigno, G., Marinoni, L., & Garrido, G. D. (2017). State of the art in grape processing by-
products. In C. M. Galanakis (Ed.), Handbook of grape processing by-products:
Sustainable solutions (pp. 1–28). London, UK: Academic Press. https://doi.org/
10.1016/B978-0-12-809870-7.00001-6.
Strasser, B., Gostner, J. M., & Fuchs, D. (2016). Mood, food, and cognition. Current
Opinion in Clinical Nutrition and Metabolic Care, 19, 55–61. https://doi.org/10.1097/
MCO.0000000000000237.
Taşeri, L., Aktaş, M., Şevik, S., Gülcü, M., Uysal Seçkin, G., & Aktekeli, B. (2018).
Determination of drying kinetics and quality parameters of grape pomace dried with
a heat pump dryer. Food Chemistry, 260, 152–159. https://doi.org/10.1016/j.
foodchem.2018.03.122.
Tavares, I. M. de C., de Castilhos, M. B. M., Mauro, M. A., Ramos, A. M., de Souza, R. T.,
Gómez-Alonso, S., et al. (2019). BRS Violeta (BRS Rúbea × IAC 1398-21) grape juice
powder produced by foam mat drying. Part I: Effect of drying temperature on
phenolic compounds and antioxidant activity. Food Chemistry, 298, 1–11. https://
doi.org/10.1016/j.foodchem.2019.124971.
Toro-Funes, N., Bosch-Fuste, J., Latorre-Moratalla, M. L., Veciana-Nogués, M. T., & Vidal-
Carou, M. C. (2015). Biologically active amines in fermented and non-fermented
commercial soybean products from the Spanish market. Food Chemistry, 173,
1119–1124. https://doi.org/10.1016/j.foodchem.2014.10.118.
Wojdyło, A., Samoticha, J., Nowicka, P., & Chmielewska, J. (2018). Characterisation of
(poly)phenolic constituents of two interspecific red hybrids of Rondo and Regent
(Vitis vinifera) by LC–PDA–ESI-MS QTof. Food Chemistry, 239, 94–101. https://doi.
org/10.1016/j.foodchem.2017.06.077.