Food Chemistry 220 (2017) 51–58

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Food Chemistry
journal homepage: www.elsevier.com/locate/foodchem

Industrial processing versus home processing of tomato sauce: Effects

on phenolics, flavonoids and in vitro bioaccessibility of antioxidants
Merve Tomas a,d, Jules Beekwilder b, Robert D. Hall b,c, Osman Sagdic d, Dilek Boyacioglu e, Esra Capanoglu e,⇑
a
Faculty of Engineering and Natural Sciences, Food Engineering Department, Istanbul Sabahattin Zaim University, Halkali 34303, Istanbul, Turkey
b
Wageningen UR, Plant Research International, Bioscience, 6708 PB Wageningen, The Netherlands
c
Wageningen University, Laboratory of Plant Physiology, 6708 PB Wageningen, The Netherlands
d
Faculty of Chemical and Metallurgical Engineering, Food Engineering Department, Yildiz Technical University, 34210 Istanbul, Turkey
e
Faculty of Chemical and Metallurgical Engineering, Food Engineering Department, Istanbul Technical University, Maslak, 34469 Istanbul, Turkey

a r t i c l e i n f o a b s t r a c t

Article history: The effect of industrial and home processing, in vitro gastrointestinal digestion, individual phenolic con-
Received 20 June 2016 tent, and antioxidant capacity of tomato into tomato sauce were investigated. Industrial processing of
Received in revised form 27 September tomato fruit into sauce had an overall positive effect on the total antioxidant capacity (
1.2-fold higher)
2016
compared to tomato fruit whereas home processing of tomato fruit into sauce led to a decrease in these
Accepted 29 September 2016
Available online 29 September 2016
values. Untargeted LC–QTOF-MS analysis revealed 31 compounds in tomato that changed upon process-
ing, of which 18 could be putatively identified. Naringenin chalcone is only detectable in the fruit, while
naringenin is strongly increased in the sauces. Rutin content increased by 36% in the industrial processed
Keywords:
Tomato sauce
sauce whereas decreased by 26% in the home processed sauce when compared to fruit. According to the
Processing results of an in vitro gastrointestinal digestion model, industrial processing may lead to enhanced bioac-
Antioxidant cessibility of antioxidants.
Bioavailability Ó 2016 Elsevier Ltd. All rights reserved.
In vitro gastrointestinal digestion

1. Introduction to the presence of key antioxidants such as lipid-soluble lycopene

In the Western diet, tomatoes are a major source of nourish-
ment for the world’s population due to their large consumption
and versatility. They can be used for direct consumption (fresh/
raw) or as an ingredient in many food recipes (Knockaert et al.,
2012). Tomato is an important fruit in Turkey, with a production
level of 11 million tonnes in 2013 (FAOSTAT, 2013). Most of the
world’s tomato crops are processed each year to produce a variety
of tomato products including canned tomatoes, juices, sauces,
purees, and pastes (Vallverdú-Queralt, Martínez-Huélamo,
Casals-Ribes, & Lamuela-Raventós, 2014; Tulipani et al., 2012).
Tomatoes are rich in lycopene, a carotenoid which is important
because of its health related properties (Knockaert et al., 2012).
Epidemiological evidence suggests an association of phytochemi-
cals such as carotenoids and phenolics to a reduced risk of various
chronic diseases such as cardiovascular disease and certain types
of cancer and especially, prostate cancer (Afrin et al., 2016;
Chiva-Blanch & Visioli, 2012; Forbes-Hernandez et al., 2016;
Forbes-Hernández et al., 2014; Pistollato, Giampieri, & Battino,
2015). These health protective effects have been widely attributed
⇑ Corresponding author.
E-mail address: capanogl@itu.edu.tr (E. Capanoglu).
and b-carotene, as well as water-soluble vitamin C, and com-
pounds of intermediate hydrophobicity such as quercetin glyco-
sides, naringenin chalcone, and chlorogenic acid (Capanoglu,
Beekwilder, Boyacioglu, Hall, & De Vos, 2008). Antioxidants present
in food undergo chemical changes during technological processing.
Domestic and commercial food processing has typically drastic
effects on the structural integrity of fruits and vegetables (Kalt,
2005). Home cooking of tomatoes is very prevalent in Turkey.
Many fruits and vegetables have already been investigated for
changes in their antioxidants as a result of processing including
tomato (Capanoglu et al., 2008), sour cherry (Toydemir et al.,
2013), and black mulberry (Tomas et al., 2015). To our knowledge
there is no report in which the effect of industrial processing and
home processing have been compared.
Bioaccessibility, which is defined as the fraction of the nutrient
that can be released from the food matrix (Colle, Lemmens, Van
Buggenhout, Van Loey, & Hendrickx, 2010), was measured using
an in vitro method. Several studies indicated that cooking may also
enhance digestibility and bioavailability of food nutrients (Van
Boekel et al., 2010). Martínez-Huélamo et al. (2015) showed that
mechanical and thermal treatments during tomato sauce process-
ing may increase the bioaccessibility, extractability and bioavail-
ability of phenolics in tomato.

http://dx.doi.org/10.1016/j.foodchem.2016.09.201
0308-8146/Ó 2016 Elsevier Ltd. All rights reserved.
52 M. Tomas et al. / Food Chemistry 220 (2017) 51–58
The effects of industrial processing on the antioxidants of toma-
toes have been extensively studied. However, little is known about
the impact of different processing methods on tomato and tomato
sauce. Therefore, in this study the aim was to compare the effect of
industrial-scale preparation and home cooking on tomato antioxi-
dants during sauce production. Using an untargeted LC–MS analy-
sis, a number of phenolic compounds were monitored and
identified in tomato and different processed tomato sauces. More-
over, an in vitro simulated gastrointestinal digestion model was
used to determine the effect of these different processing tech-
niques on the bioaccessibility of tomato antioxidants.
2. Materials and methods
2.1. Tomato sauce material
A commercial tomato variety (Lycopersicum esculentum var.
Advance harvested from a greenhouse in Manisa, Turkey in
2015), suitable for tomato sauce preparation, was used for the
study. The tomato sauce was prepared by two different processing
methods (industrial and home processing) using the same fresh
tomatoes (4.5 °Brix, 4.3 pH) according to the flow sheet repre-
sented in Fig. 1. Processing of each sauce has been repeated three
times as three independent experimental units (EU), and three
technical replicates were analyzed from each EU.
Industrial processed sauce: Tomatoes were processed into sauce
in a factory (Döhler, Balıkesir, Turkey) in 2015. The processing
steps included washing, cold breaking (73 °C, 10 min), evaporating
(11 °Brix, 73 °C), and pasteurization (110 °C, 90 s) to generate the
standard commercial product. The final sauce had 11 °Brix with a
pH of 4.4. The final sauce contains the seed and the skin fractions
as they are not removed during the process.
Home processed sauce: Home processing was performed follow-
ing a typical Turkish recipe. Tomatoes were washed, chopped
(
10 cm3) and crushed with a home type blender. The mixture
was cooked for 60 min at 100 °C. The final sauce had a °Brix of
14. The final sauce contains the seed and the skin fractions as they
are not removed during the process. Both for home processing and
industrial processing, three independent processing events were
Fig. 1. Flowchart of tomato sauce processing (⁄, samples taken for analysis).
sampled. Therefore, the analysis included three independent fruit
samples, three independent home-processing sauce samples and
three independent industrial processing sauce samples (Fig. 1).
For spectrophotometric methods and HPLC analysis each indepen-
dent sample was analyzed in triplicate (technical replicates)
(n = 9). Only for the LC–MS analysis each EU was analyzed only
once (n = 3). All samples were ground to a fine powder in liquid
nitrogen using a pre-cooled grinder (IKA A11, Germany), and
stored at 80 °C before analysis.
2.2. Moisture content analysis
The moisture contents of samples were determined according
to the guidelines of the official Turkish Standard 1129-ISO 1026
method at 70 °C for 6 h using a vacuum oven (Gallenkamp, London,
UK). All samples were analyzed in triplicate and mean values were
reported.
2.3. Extraction method
Tomato samples (2.0 g) were homogenized with 5 mL of 75%
aqueous methanol containing 0.1% formic acid following a proce-
dure described previously by Capanoglu et al. (2008). The samples
were then sonicated for 15 min and centrifuged (2700 rpm at 4 °C)
for 10 min and the supernatants were collected. This extraction
procedure was repeated twice, and three supernatants were
pooled. These extracts were stored at 20 °C until analysis.
Individual black mulberry phenolics were identified and quan-
tified by using targeted HPLC and untargeted LC–QTOF-MS mea-
surements. For these, the samples were prepared by the
extraction of 400 mg freeze-dried material with 3.0 mL of 75%
aqueous methanol with 0.1% formic acid. After the steps of sonica-
tion for 15 min and centrifugation at 2500 rpm for 10 min; the
extracts were filtered through 0.45 lm filters (Minisart SRP4, Bio-
tech GmbH, Germany).
2.4. Spectrophotometric assays
Total antioxidant capacity (TAC) assays were performed using a
spectrophotometer. TAC was estimated using four different assays,
and in all assays, the results were expressed in mg of Trolox equiv-
alent (TE) per 100 g DW. The ABTS (2,2-azinobis 3-ethylbenzothia
zoline-6-sulphonic acid), FRAP (ferric reducing antioxidant power),
CUPRAC (copper reducing antioxidant capacity), and DPPH (1,1-
diphenyl-2-picrylhydrazyl) assays were performed according to
Miller and Rice-Evans (1997), Benzie and Strain (1996), Apak,
Güçlü, Özyürek, and Karademir (2004), and Kumaran and
Karunakaran (2006), respectively.
2.5. Untargeted LC–MS based identification
An LC-PDA-FTMS system was used to investigate the untargeted
analysis of tomato samples. Chromatographic and mass spectro-
metric conditions were as described by Moco et al. (2006). Briefly,
a Luna C18(2) pre-column (2.0  4 mm) and an analytical column
(2.0  150 mm, 100 nm, particle size 3 lm) from Phenomenex
(Torrance, CA, USA) were used for chromatographic separation.
UV absorbance was performed with a Waters 2996 PDA (range
from 240 to 600 nm) and metabolites were detected using a LTQ-
Orbitrap XL hybrid MS system (Waters) operating in negative elec-
trospray ionization mode heated at 300 °C with a source voltage of
4.5 kV for full-scan LC–MS in the m/z range 100–1500.
Compounds naringenin, naringenin chalcone, quercetin, dihy-
drokaempferol, a-tomatine, coumaroyl quinic acid and iso-
quercetin were obtained from Extrasynthese (Genay, France), and
analyzed as reference compounds.
 M. Tomas et al. / Food Chemistry 220 (2017) 51–58
Acquisition and visualization of the LC-FTMS data were per-
formed using Xcalibur software. The MetAlign software package
(www.metAlign.nl) (Lommen, 2009) was used for baseline correc-
tion, noise estimation, and spectral alignment. Aligned masses
were directly used for further analysis. Comparison and visualiza-
tion of the main features of the LC–MS data were performed by
loading the data matrix into GeneMaths XT 1.6 software (www.ap-
plied-maths.com). Metabolite intensities were normalized using
log 2 transformation and standardized using range scaling
(autoscaling normalization). Principal component analysis (PCA)
was performed for unsupervised comparison of samples.
2.6. Targeted HPLC analysis of phenolics
Samples from the tomato fruit and the two different processing
methods for producing tomato sauce were prepared each from
three independent processing events. All samples were freeze-
dried and equal amounts of dry-weight were extracted using 75%
methanol, in order to extract semipolar compounds. Major pheno-
lic compounds were determined following the method of
Capanoglu et al. (2008). Samples were passed through 0.45 lm-
membrane filters and injected into a Waters 2695 HPLC (Waters
Co., Milford, MA, USA) coupled with photodiode array (PDA) detec-
tor (Waters 2996). Compounds were separated using a Luna C18
column (150  4.6 mm, 3 l; Phenomenex, Torrance, CA, USA) and
quantification was performed at 312 nm for phenolic acids, and
at 360 nm for flavonols.
2.7. In vitro digestion procedure
In vitro simulated digestion was performed according to
Minekus et al. (2014) with slight modifications. Release of phyto-
chemicals from fruit and different processed sauce matrices was
analyzed at different stages of digestion. These stages represented
the aliquots from oral phase (fraction of released from matrix in
mouth), from stomach phase (fraction of released from matrix in
stomach), and intestinal phase (fraction of released from matrix
by the small intestine) samples that were collected during the
digestion procedure. A simulated saliva fluid (SSF), simulated gas-
tric fluid (SGF), and simulated intestinal fluid (SIF) were prepared
as described previously (Minekus et al., 2014). Briefly, five grams
of samples were weighed into centrifuge tubes and mixed with
3.5 mL of SSF, then human salivary a-amylase solution (1500 U/
mL, Sigma-Aldrich A1031) was added into the sample tubes. The
mixture was then adjusted to pH 7 and incubated at 37 °C in a sha-
ker at 100 rpm for 2 min. For oral phase, 2 mL aliquots were col-
lected for each sample. Afterwards, oral bolus was mixed with
7.5 mL of SGF. Later porcine pepsin solution (25,000 U/mL,
Sigma-Aldrich P7012) was added. The mixture was then adjusted
to pH 3 and incubated at 37 °C in a shaker at 100 rpm for 2 h.
For stomach phase, 2 mL aliquots were collected for each sample.
Finally, 20 mL of gastric cyme is mixed with 11 mL of SIF solution,
Table 1
Changes in the levels of moisture content and total antioxidant capacity.a
Samples Moisture content (%)
Tomato Fruit 93.3 ± 0.7a
Industrial processed sauce 89.0 ± 0.8c
Home processed sauce 91.0 ± 0.8b
a
Data represent average quantities ± standard deviation of nine replications for each sample (n = 9). Different letters in the columns represent statistically significant
differences (p < 0.05).
b
CUPRAC, Copper Reducing Antioxidant Capacity, expressed in mg TE (trolox equivalent)/100 g dry weight.
c
DPPH, 1,1-diphenyl-2-picrylhydrazyl, expressed in mg TE (trolox equivalent)/100 g dry weight.
d
ABTS, 2,20 -azinobis-(3-ethylbenzthiazoline-6-sulphonic acid, expressed in mg TE (trolox equivalent)/100 g dry weight.
e
FRAP, Ferric Reducing Antioxidant Capacity, expressed in mg TE (trolox equivalent)/100 g dry weight.
53
pancreatin solution (800 U/mL, Sigma-Aldrich P7545), and bile
solution (160 mM), respectively. pH adjustment to 7.0, and the
samples were incubated at 37 °C in a shaker at 100 rpm for 2 h.
After the intestinal phase, again samples were collected. These
samples were stored at 20 °C until further analysis.
2.8. Statistical analysis
The results were expressed as means ± standard deviation (SD).
The significance of the results was analyzed using SPSS 20.0 soft-
ware for the analysis of variance (ANOVA). Duncan’s new multiple
range test was used to analyze differences between treatments. To
test LC–QTOF-MS data for significant differences in relative mass
signal intensities different processing, Student’s t-test was used.
Moreover, Pearson’s correlation analysis between four different
antioxidant capacity methods of tomato sauce processing samples
was performed. P values of <0.05 were considered statistically
significant.
3. Results
3.1. Moisture content
In tomato fruit samples, the moisture content was found to be
93.3 ± 0.7%. Martínez-Valverde, Periago, Provan, and Chesson
(2002) have observed that the moisture content varied from
93.21 to 94.73% in nine commercial varieties of tomato. It is possi-
ble to have different moisture contents because of different cli-
mate, growing conditions and harvesting time. Processing of
tomato fruit into the industrial and home processed sauces
resulted in a decrease in the moisture content of approximately
4% and 2%, respectively (p < 0.05) (Table 1).
3.2. Spectrophotometric methods
To correct for any differences in moisture content, all spec-
trophotometric data were compared on a dry-weight (DW) basis.
The antioxidant capacity of samples was determined using four
different assays including ABTS, DPPH, FRAP, and CUPRAC as repre-
sented in Table 1. The results indicated that the total antioxidant
capacity assays showed the same tendency among four different
methods giving the highest correlation coefficients between the
DPPH and FRAP methods (r = 0.9893), whereas the CUPRAC and
ABTS methods had the lowest correlations (r = 0.4362). The mean
values of total antioxidant capacity of tomato fruit samples ana-
lyzed by FRAP, CUPRAC, ABTS and DPPH methods were 8937.4,
1636.8, 991.5, and 635.9 mg TE/100 g dry weight, respectively. By
the industrial processing of tomato sauce a
1.2-fold increase in
TAC values was determined by CUPRAC, DPPH, and FRAP methods,
respectively when compared to the tomato fruit. In contrast, ABTS
method showed that total antioxidant capacity of tomato fruit
decreased 3% (p > 0.05) when industrially processed into sauce
CUPRACb DPPHc ABTSd FRAPe
1636.8 ± 64.9b 635.9 ± 29.6b 991.5 ± 26.6a 8937.4 ± 97.4b
2038.5 ± 24.6a 732.5 ± 12.5a 961.7 ± 44.5a 10657.5 ± 47.2a
1489.5 ± 40.6b 419.2 ± 2.5c 576.4 ± 9.9b 6363.7 ± 13.7c
54 M. Tomas et al. / Food Chemistry 220 (2017) 51–58

Table 2
Metabolites observed through LC–QTOF-MS analysis which differed significantly due to home processing (HS) and/or industrial processing (IS) of tomato.a

Masses over-represented in unprocessed tomato fruit

Rt (min) Observed Elemental formula Expected mass Ratio Ratio Tentative identity Identity
mass [MH] Fruit/IS Fruit/HS confirmedc
15.64 337.092 C16H18O8 337.093 2.55 2.73 Coumaroyl quinic acid Yes
16.07 491.176 0.53 2.66
19.09 392.080 11.73 14.48
22.89 760.823 2.79 12.21
23.89 1112.547 4.57 15.96
26.08 1152.542 3.02 10.58
26.71 839.330 1.49 2.36
27.68 463.120 C21H20O12 463.087 2.22 2.04 Isoquercetin Yes
28.04 515.119 C25H24O12 515.119 2.32 4.07 Dicaffeoylquinic acid I
30.48 1078.542 C50H83NO21 + HCOOH 1078.543 1.10 2.39 Alpha tomatin + FA Yes
30.52 433.113 C21H22O10 433.114 2.03 3.48 Naringenin chalcone-hexoside I
30.61 1136.547 C52H85NO23 + HCOOH 1136.549 1.90 11.73 Acetoxy-tomatine + FA
31.04 433.113 C21H22O10 433.113 28.70 23.34 Naringenin chalcone-hexoside II
32.01 677.282 C34H46O14 677.282 2.26 2.53 N713b
32.24 411.202 1.17 2.88
36.49 1127.547 6.56 0.39
36.89 677.150 C34H30O15 177.151 2.68 3.69 Tricaffeoylquinic acid
40.39 271.061 C15H12O5 271.061 16.64 182.67 Naringenin chalcone Yes
Masses under-represented in unprocessed tomato fruit
Rt (min) Observed Elemental formula Expected mass Ratio Ratio Putative identity
mass [MH] Fruit/IS Fruit/HS
7.14 342.087 0.15 0.24
12.96 309.118 C12H22O9 309.1196 0.21 0.55
13.43 179.035 0.42 0.30
13.66 351.129 0.36 0.80
14.58 399.099 C20H16O9 399.072 0.32 0.40 3,30 ,40 ,5,6,7,8-Heptahydroxyflavone; 30 ,40 :6,7-Bis
(methylene), 3,5,8-tri-Me ether
16.36 1272.584 C56H93NO28 + HCOOH 1272.587 0.15 0.091 Esculeoside B1.1
18.91 1272.584 C56H93NO28 + HCOOH 1272.587 0.23 0.17 Esculeoside B1.2
19.34 1272.584 C56H93NO28 + HCOOH 1272.587 0.34 0.39 Esculeoside B1.3
21.27 699.234 0.063 1.03
27.09 415.197 C20H32O9 415.197 0.27 0.25 2-Methyl-6-methylene-2-octene-1,8-diol, 8-O-(2,6-
Diacetyl-glucopyranoside)
33.57 287.055 C15H12O6 287.056 0.36 0.43 Dihydrokaempferol Yes
35.05 301.035 C15H10O7 301.035 0.14 0.17 Quercetin Yes
39.89 271.061 C15H12O5 271.061 0.14 0.091 Naringenin Yes
a
Identified metabolites detected by LC–QTOF-MS that were significantly different (Student’s t-test, p < 0.05) between Original Fruit and Final Sauces.
b
http://webs2.kazusa.or.jp/.
c
Identity was confirmed by comparison of retention time and mass spectrum to an original standard.

(Table 1). On the other hand, home processing resulted in 42%, 34%,
29%, and 9% reduced values determined by ABTS, DPPH, FRAP, and
CUPRAC, respectively compared to the tomato fruit. As a result, the
antioxidant capacity values of industrial processed sauce obtained
by all TAC methods (except for the ABTS method results for tomato
fruit) were found to be the highest in comparison to tomato fruit
and home processed sauce (p < 0.05).

3.3. Untargeted analysis of semipolar compounds

Methanol extracts of fruit, industrial and home processed

sauces were analyzed using LC–MS. A multivariate analysis was
carried out on the LC–MS data to visualize the changes in meta-
bolic composition as a result of the two tomato processing meth-
ods. The results of the multivariate analyses were visualized
using Principle Component Analysis (PCA) plots (Fig. 2). The PCA
indicates that samples group according to their processing method.
The first principal component (X-axis) explained 21% of total vari-
ation in the dataset whereas the second component (Y-axis)
explained 20% of the variation. This spatial distribution shows
the difference in metabolite profiles between fruit, home processed
and industrial processed sauce samples. (Fig. 2). Fig. 2. Principal component analysis of untargeted LC–MS based metabolomics
For identification of compounds that are significantly differing data of Fruit (F), Industrial processed sauce (IS) and Home processed sauce (HS)
in content between the fruit and processed samples, LC–MS data (n = 3).
 M. Tomas et al. / Food Chemistry 220 (2017) 51–58 55

were further processed. In Table 2 and 13 compounds are shown
that were significantly decreased (p < 0.05) by more than 2-fold
in the home-processed and/or the industrially processed samples,
relative to the fruit, and 18 compounds that increased (p < 0.05)
more than 2-fold due to the processing. Compounds were tenta-
tively identified according to their mass and retention time, by
comparison to the MoTo database (Moco et al., 2006), and, where
possible, confirmed by comparison to authentic standards. 13 out
of 31 observed masses could not be associated to a known com-
pound. Among the compounds that decreased upon processing is
naringenin chalcone, confirming the observations made by HPLC.
Other compounds that appear to be vulnerable to both processing
methods include two naringenin chalcone hexosides, isoquercetin,
a tricaffeoyl-quinic acid and a coumaroyl-quinic acid. Also
processing-method specific reductions are observed, for example
for the glycoalkaloids a-tomatine and acetoxy-a tomatine, which
are not significantly affected by industrial processing, but were
affected by the home-processing method. Compounds that increase
due to processing include naringenin (confirming the observations
made in the HPLC analysis), and other phenolic aglycones
(e.g. quercetin, dihydrokaempferol) and isomers of esculeoside B1.
3.4. Targeted analysis of phenolic compounds
A targeted HPLC method was used to quantify a set of four com-
pounds, including rutin, chlorogenic acid, naringenin and narin-
genin chalcone (Table 3; Supplementary Figure). The clearest
trend in these data was that naringenin chalcone is only detectable
in the starting material (the fruit), while naringenin is strongly
increased in the sauces. Notably, the flavonoid naringenin was
Table 3
The content of selected phenolic compounds in tomato fruit, industrial processed
sauce and home processed sauce.
Amount (mg/100 g DW)a
Compound Fresh fruit Industrial processed
sauce
Chlorogenic acid 17.9 ± 3.4a 17.6 ± 2.7a
Rutin 24.8 ± 4.7b 33.8 ± 5.2a
Naringenin chalcone 2.45 ± 0.60 n.d.
Naringenin 0.12 ± 0.10c 2.38 ± 0.42b
a
Data represent average quantities ± standard deviation of nine replications for
each sample (n = 9). Different letters within the same row indicate statistically
significant differences (p < 0.05).
20-fold and 43-fold higher in industrial and home processed
sauces respectively, compared to fruit. Likely this is the conse-
quence of the high temperature at low pH, under which conditions
conversion of naringenin chalcone to naringenin is stimulated
(Capanoglu et al., 2008). The rutin content significantly increased
by 36% in industrial processed sauce (33.8 mg/100 g DW) whereas
it was seen to decrease by 26% in home processed sauce
(19.0 mg/100 g DW) when compared to fruit (24.8 mg/100 g DW).
3.5. Simulated in vitro gastrointestinal (GI) digestion
Results obtained for TAC analysis are given in Table 4. Industrial
processed sauce showed significantly higher levels of antioxidants
in the in vitro oral phase, CUPRAC (2.0-fold higher), DPPH (4.9-fold
higher), ABTS (1.5-fold higher), FRAP (2.3-fold higher) compared to
the tomato fruit (p < 0.05). Similarly, the in vitro oral phase of
industrial processed sauce showed significant increases in CUPRAC,
DPPH, and ABTS (1.6, 2.5, and 1.3-fold, respectively higher than in
home processed sauce (p < 0.05)). Moreover, in the in vitro stomach
phase, the processing of tomato fruit to industrial sauce led to sig-
nificant increases of the TAC (approximately 1.3–2.0-fold higher,
all assays) values. Furthermore, in the in vitro stomach phase,
industrially processed sauce led to significant increases on the
TAC (approximately 1.2–1.8-fold higher) compared to home pro-
cessed sauce (p < 0.05). Moreover, distinctively, the values for
CUPRAC (325.3 mg TE/100 g) assay showed a remarkable increase
in industrially processed sauce in the in vitro intestinal phase
(p < 0.05) compared to the tomato fruit and home processed sauce.
On the other hand, DPPH, FRAP and ABTS assays did not show any
significant effect of processing on the in vitro intestinal phase of
samples. In the in vitro oral, stomach, and intestinal phases of
industrially processed sauce measured by CUPRAC method were
found to be the highest among tomato fruit and home processed
sauce (p < 0.05). Thus, it seems that industrial processing may lead
to enhanced bioaccessibility of antioxidants.
Home processed
sauce
13.3 ± 2.7b
4. Discussion
19.0 ± 3.2c
n.d. 4.1. Effect of industrial and home processing on total antioxidant
5.12 ± 0.83a capacity of tomato fruits
Domestic and commercial food processing typically have major
effects on the structural integrity of fruits and vegetables (Kalt,

Table 4
Changes in TAC of tomato fruit and processed sauce during in vitro gastrointestinal digestion.a

Analysis Initial Oral Phase Stomach Phase Intestinal Phase

CUPRACb
Tomato fruit 109.3 ± 4.8b 52.2 ± 3b 76.8 ± 13b 182.1 ± 31b
Industrial Processed Sauce 213.3 ± 0.8a 102.8 ± 20a 165 ± 4a 325.3 ± 33a
Home Processed Sauce 130.4 ± 2.0b 64 ± 5b 90.3 ± 6b 203.4 ± 23b
DPPHb
Tomato fruit 43.0 ± 1.7b 6.4 ± 2.6b 13.4 ± 1.7b 8.9 ± 4.2a
Industrial Processed Sauce 78.6 ± 4.6a 31.2 ± 1.9a 31 ± 2.6a 19.4 ± 9.2a
Home Processed Sauce 35.1 ± 1.1b 12.5 ± 6b 19.6 ± 8.6b 19.7 ± 5.2a
ABTSb
Tomato fruit 66.8 ± 2.0b 20.0 ± 2b 52.8 ± 9b 253.7 ± 14a
Industrial Processed Sauce 105.8 ± 4.9a 29.1 ± 1a 70.9 ± 5a 268.0 ± 5a
Home Processed Sauce 51.9 ± 0.9c 22.5 ± 1b 57.5 ± 4b 266.9 ± 29a
FRAPb
Tomato fruit 435.4 ± 17.3b 5.1 ± 0.3b 13.9 ± 0.9b 15.5 ± 0.1a
Industrial Processed Sauce 1144.5 ± 17.9a 11.8 ± 0.4a 25.3 ± 2.0a 14.7 ± 0.3a
Home Processed Sauce 557.9 ± 5.2b 12.0 ± 0.5a 16.4 ± 1.9a 18.9 ± 6.1a
a
Data represent average quantities ± standard deviation of nine replications for each sample (n = 9). Different letters in the columns represent statistically significant
differences (p < 0.05).
b
TAC, Total Antioxidant Capacity, expressed in mg TE (trolox equivalent)/100 g fresh weight.
56 M. Tomas et al. / Food Chemistry 220 (2017) 51–58
2005). Technological processing often includes many thermal and
hydrothermal processes. These processes can have both negative
and positive effects on the food materials. Benefits of thermal pro-
cessing include inactivation of enzymes, food-borne pathogens,
prolongation of shelf-life, improved digestibility and bioavailabil-
ity of nutrients, including augmented antioxidants. In contrast,
thermal processing can also bring some unintentional and unde-
sired consequences, such as loss of certain desirable nutrients
(Van Boekel et al., 2010). In our study, the industrial processing
of tomato fruit into tomato sauce resulted in significant increases
in all TAC values, except for the ABTS assay, (
1.2-fold increase
with CUPRAC, DPPH, and FRAP assays) (Table 1 (p < 0.05)). Similar
results have also been reported by Dewanto, Wu, Adom, and Liu
(2002) who found that the antioxidant activity of raw tomatoes
was 4.13 lmol of vitamin C equiv/g of tomato. Following heat
treatment at 88 °C for 30 min, the total antioxidant activity signif-
icantly increased to 6.70 lmol of vitamin C equiv/g of tomato. Con-
sistent with these results, Chanforan, Loonis, Mora, Caris-Veyrat,
and Dufour (2012) also reported that the impact of industrial pro-
cessing of fresh tomato into paste had an overall positive effect on
the content of phenolic compounds. It is therefore, apparent that
heat treatment may result in changes in the extractability of phe-
nolics due to the disruption of plant cell wall and thus result in an
easier release of (bound) polyphenolic compounds (Dewanto et al.,
2002). The increase or retention of antioxidant activities in pro-
cessed foods could be linked to the formation of Maillard products
with relatively higher antioxidant capacities (Nicoli, Anese, &
Parpinel, 1999) and/or could be due to the additive or synergistic
effects of phytochemicals released from the matrix during process-
ing (Dewanto et al., 2002). In addition, it has been reported that
polymerization due to heating or concentration during processing
may also increase the polyphenol content of food materials. Some
polyphenolic compounds are reported to exhibit a strong tendency
to be subject to polymerization reactions that promote important
structural changes and, as a consequence, variations in their radical
scavenging activity (Pinelo, Manzocco, Nuñez, & Nicoli, 2004). Data
presented by Hagerman et al. (1998) suggest that polymeric
polyphenolics may be much more potent antioxidants than their
simple monomeric counterparts. On the other hand, heat treat-
ments can also deactivate endogenous oxidative enzymes. There-
fore, increased levels of antioxidants might also be explained by
the deactivation of endogenous oxidative enzymes, which may
degrade antioxidative compounds (Nicoli et al., 1999). In contrast,
according to our study, during home processing, all assays showed
that the total antioxidant capacity of tomato fruit was decreased
from 42% to 9% when processed into sauce.
It is known that industrial processing can be much better con-
trolled and optimized through the application of kinetic principles
when compared household cooking (Van Boekel et al., 2010). These
results also indicate that different cooking methods can affect the
polyphenol content differently. In the view of available literature,
it is apparent that heating for too long may lead to a rapid decrease
in antioxidant potential of a product due, for example, to melanoi-
din and polyphenol breakdown (Yilmaz & Toledo, 2005). Moreover,
high-temperature processing may lead to thermal destruction of
antioxidants. With respect to this information, in the industry
HTST (high temperature short time) pasteurization applications
are preferred instead of long term applications, in order to protect
antioxidants and other phytochemicals present in the product (Lin
& Chen, 2005). Consequently, mild hydrothermal processing
(<100 °C) are usually advantageous (Grajek & Olejnik, 2010). In
our study, home processing of tomato fruit into sauce in which
tomatoes were cooked for 60 min at 100 °C, revealed significant
decreases in TAC. Similar results were also reported by
Vallverdú-Queralt, Regueiro, Rinaldi de Alvarenga, Torrado, &
Lamuela-Raventos (2014)who found that longer cooking periods,
of up to 60 min, resulted in a greater decrease in the levels of
polyphenols and antioxidants, with the exceptions of caffeic acid
and tyrosol. Another reason for decreased levels of antioxidants
could be linked to the formation of novel compounds having pro-
oxidant activity (Nicoli et al., 1999). In addition to the above find-
ings, differences in TAC results might be attributed to the fact that
current antioxidant tests are incapable of analyzing all the antiox-
idants available in the tissues, and different methods may repre-
sent several advantages and/or disadvantages over each other.
The reactions for the radical formations or the solubility of radicals
in different solvent systems also differ in each method (Arnao,
2000; Niki, 2011). Therefore, it has been recommended, as we have
done here, to apply several test procedures to evaluate antioxidant
activities of plant tissues. It is noteworthy that according to our
results the industrial processed sauce had the highest TAC com-
pared to the tomato fruit and home processed sauce. In view of
the available literature, it is apparent that heat treatment of foods
needs to be optimized in order to promote beneficial effects and to
counteract undesired effects. This may be achieved more effec-
tively/sustainably by consistent fine-tuning of technological pro-
cesses but would be more difficult within ordinary household
cooking conditions (Van Boekel et al., 2010).
4.2. Changes in individual phenolics during sauce processing
The phenolic compounds identified in tomato fruit and pro-
cessed sauces are shown in Table 2, and the contents of the main
quantified phenolics are listed in Table 3. Four major phenolic
compounds were detected in the analyzed samples, namely rutin,
chlorogenic acid, naringenin and naringenin chalcone. Processing
mainly affected naringenin chalcone, which appears to be con-
verted by a cyclization event to naringenin in the processed sauces
(Tables 2 and 3). These results are in agreement with Capanoglu
et al. (2008) who found that at the end of a tomato paste-making
procedure, this chalcone was undetectable in paste samples. Simi-
larly, Martínez-Huélamo et al. (2015) observed naringenin to be 7-
fold higher in sauces than raw tomatoes. Also, native chalcone gly-
cosides tend to transform to flavanone glycosides during extraction
(Tomás-Barberán & Clifford, 2000). Indeed, we also observed a
decrease of naringenin chalcone hexoside during processing
(Table 2). Since naringenin is trapped in the cutin matrix of the
cuticle of the ripe fruit where it strongly interacts with insoluble
polyesters, which are constituents of tomato peel fibre (Tulipani
et al., 2012), mechanical and thermal processing could facilitate
the release of the compound from the matrix breaking the interac-
tions and thus increasing its bioaccessibility (Bugianesi et al., 2004;
Kamiloglu, Boyacioglu, & Capanoglu, 2013; Martínez-Huélamo
et al., 2015). Another change in flavonoids was that the rutin con-
centration increased from 24.8 to 33.8 mg/100 g DW, after indus-
trial processing of tomato fruit into sauce (Table 3). Our results
are in accordance with Vallverdú-Queralt, Medina-Remón,
Andres-Lacueva, and Lamuela-Raventos (2011) who observed that
rutin increased by 35% when tomato dices were subjected to a heat
treatment. Industrial-scale processing of tomatoes, involving heat
treatments, may increase the levels of some unbound antioxidants
(Vallverdú-Queralt, Regueiro et al., 2014). Moreover, heat and
mechanical treatments applied during a tomato sauce-making pro-
cess may induce biochemical changes in the food matrix, positively
affecting the bioaccessibility of phenolics in the processed prod-
ucts (Tulipani et al., 2012). Industrial and home processed sauces
contained 7.1-fold and 5.8-fold higher levels of quercetin com-
pared to the fruit, respectively (Table 2). Similarly, such apparent
increase in the quercetin content was also observed during onion
baking and sauteing (7–25%) as compared to raw onion
(Lombard, Peffley, Geoffriau, Thompson, & Herring, 2005). One
explanation could be that processing into the end product can
 M. Tomas et al. / Food Chemistry 220 (2017) 51–58
increase the content of free quercetin, a change that may be
brought about by enzymatic hydrolysis of rutin and other querce-
tin conjugates during pasteurization and processing procedures
(Stewart et al., 2000). Moreover, quercetin is more susceptible to
degradation than rutin. In the case of rutin, the 3-
hydroxyfunction at the C-ring is blocked by a sugar moiety,
whereas in quercetin it remains unoccupied, thus explaining the
higher stability of rutin towards oxidation (Vallverdú-Queralt, Ma
rtínez-Huélamo, et al., 2014). In contrast, isoquercetin is signifi-
cantly decreased (p < 0.05) more than 2-fold in the home-
processed and/or the industrially processed samples compared to
the fruit. This decrease is possibly due to the chemical or thermal
degradation and/or leaching action of the cooking water (Aherne
& O’Brien, 2002).
4.3. Changes in simulated GI digestion during sauce processing
The bioaccessibility of tomato antioxidants using an in vitro
model simulating gastro-intestinal conditions has been investi-
gated for tomato fruit and sauce processed by different methods.
The major finding of this work (Table 4) was that with the CUPRAC
method, in the in vitro intestinal phase of the industrial processing
of tomato fruit to tomato sauce gave rise to approximately a 1.8-
fold higher (p < 0.05) value than for tomato fruit; whereas in the
in vitro intestinal phase of the industrial processing of tomato fruit
to tomato sauce resulted in a 1.6- fold increase (p < 0.05) than
home processed tomato sauce. Our findings are comparable to
results noted by Bugianesi et al. (2004) who determined that the
cooking of cherry tomatoes at 100 °C for 15 min significantly
increased the plasma concentrations of naringenin and chlorogenic
acid after ingestion. In tomatoes, naringenin is especially associ-
ated with the cutin of the outer waxy surface and binds to insol-
uble polyesters, and thus, even mild heating affecting the outer
layers could have pronounced effects (Bohn, 2014). In another
study that Martínez-Huélamo et al. (2015) found that the plasma
concentration and urinary excretion of naringenin glucuronide
were both significantly higher after the consumption of tomato
sauce compared to raw tomatoes. In addition, Kamiloglu et al.
(2014) revealed that paste processing and drying significantly
increased the bioaccessible total antioxidant capacity (6.3- and
8.0-fold for the DPPH assay, 26- and 33-fold for the CUPRAC assay,
respectively) compared to fresh tomatoes after in vitro digestion.
These results suggest that the mechanical and thermal treatments
during tomato sauce manufacture may help to deliver these poten-
tially bioactive phenolics from the food matrix more effectively,
thus increasing their bioavailability (Martínez-Huélamo et al.,
2015). The observed increase of TAC after the in vitro model repre-
senting the oral, stomach, and intestinal phase could be explained
by the effect of intestinal digestive enzymes (amylase, pepsin, pan-
creatin) on the complex food matrix, facilitating the release of
bound phenolics. The concentration and composition of enzymes
are also very important factors (Bouayed, Hoffmann, & Bohn,
2011). Typically, higher enzyme concentrations accelerate diges-
tion or degradation of food components, so it is important to use
physiologically relevant levels (Hur, Lim, Decker, & McClements,
2011). Moreover, particle size reduction enhances enzyme access
during subsequent stages of digestion through enlargement of
the surface area of the digest (Bohn, 2014). Industrial processed
sauce may have even smaller particle size in comparison to home
processing as a result of more severe mechanical treatments. It has
been already reported in the literature that small particle size may
enhance the extractability and bioaccessibility of active com-
pounds (Li et al., 2008; Wang & Weller, 2006). On the other hand,
in the stomach, polyphenols are exposed to strong acidic condi-
tions, which also might influence their stability. Some studies indi-
cate that phenolic derivatives could be absorbed in the stomach
57
(Passamonti, Vrhovsek, Vanzo, & Mattivi, 2003). Our results
showed that, in the in vitro stomach phase the amount of bioacces-
sible TAC was higher following industrial processing of tomato into
sauce compared to tomato fruit and home processed sauce
(p < 0.05). In vitro digestion models as also used in our study pro-
vide a useful alternative to animal and human models by rapidly
screening food ingredients (Hur et al., 2011). However, further
studies are needed to understand better the effect of other factors
relevant to these in vitro methods as compared to human interven-
tion studies (in vivo studies).
5. Conclusion
The current study has shown that industrial processing may
contribute to obtaining tomato sauces with higher antioxidant
content compared to tomato and home processed tomato sauces.
Moreover, industrial processing may lead to enhanced bioaccessi-
bility of antioxidants. In further studies, we are planning to focus
on bioavailability of tomato polyphenols using cellular models
such as Caco-2 and in vivo feeding trials in order to compare with
the findings of the present study.
Acknowledgements
We thank TUBITAK, the Scientific and Technological Council of
Turkey (2211-D Industrial Ph.D. Scholarship Program,
1649B031501886), and Istanbul Technical University, Scientific
Research Projects Unit (BAP) for financial support. The authors
thank to Harrie Verhoeven and Bert Schipper for their technical
support.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.foodchem.2016.
09.201.
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