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Activity of naturally occurring antioxidants during heat processing of low-salt

fermented shrimp paste

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ABAH BIOFLUX
Animal Biology & Animal Husbandry
International Journal of the Bioflux Society

Activity of naturally occurring antioxidants during

heat processing of low-salt fermented shrimp
paste
1
Ernestina M. Peralta, 2Augusto E. Serrano Jr.
1
Institute of Fish Processing Technology, CFOS, UP Visayas, Miagao Iloilo, Philippines;
2
Institute of Aquaculture, CFOS, UP Visayas, Miagao, Iloilo, Philippines. Corresponding
author: A. E. Serrano Jr., [email protected]

Abstract. The present study intends to assess the activity of naturally occurring antioxidants in salt-
fermented shrimp paste when subjected to thermal processing. Shrimp (Acetes sibugae) was mixed with
a ratio of 1:7 (salt:shrimp) and allowed to ferment for 15 days at room temperature (28 – 32 °C).
Changes in antioxidant activity were measured during fermentation and heat-processed shrimp paste
with added ingredients. Diphenyl-1-picrylhydrazyl (DPPH) free radical and hydrogen peroxide scavenging
activities from day 1 significantly increased at day 5, with minimal increase as fermentation progressed
to day 15 and with no significant differences. DPPH scavenging activity generally increased in the varying
heat processing employed in cooking shrimp paste. On the other hand, although hydrogen peroxide
scavenging activity significantly increased after 10 min heating, activity decreased in the 30 min boiling
and pasteurization except for sample product with no ingredients added. The study showed that the
consequence of processing and preservation procedures on the overall antioxidant activity of shrimp
paste is generally the result of different reactions which probably took place consecutively or
simultaneously. Thus, processing methods may either improve the properties of naturally occurring
antioxidants or induce the formation of new compounds having antioxidant properties.
Key Words: Shrimp paste, low-salt, antioxidant activity, heat processing.

Introduction. Acetes sibugae and Acetes intermedius are two of the species found in the
Visayas sea area (located in the central part of the Philippines) and commonly used in the
production of salt-fermented and dried shrimp products. Traditionally, shrimp is mixed
with a ratio of 1:3 (salt:shrimp) resulting in a salt content of the product of 22 – 25 %.
Fermented fish products contain peptides and amino acids that are known to function as
naturally occurring antioxidants (Guerard et al 2002; Harada et al 2002; Jung et al
2005). Salt-fermented shrimp paste contain strong antioxidant activity when is
fermented for 10 days (Peralta et al 2005) which significantly increased after 60, 180 and
360 days of fermentation (Peralta et al 2007; Peralta 2008; Peralta et al 2008). It
suggests that health benefits can be derived from the consumption of the product.
However, with the changing lifestyle of consumers, preference has shifted to healthy food
such as low-salt, low-fat foods. The change from high to low salt reduces shelf stability of
salt-fermented shrimp, and an additional process of heat treatment is commonly
employed.
Application of heat as processing technique is widely believed to greatly affect the
naturally occurring antioxidants in food. Antioxidants decrease their resistance against
oxidation through interaction with other food components during processing, by
evaporation, formation of pro-oxidants or their liberation from inactive complexes (Nicoli
et al 1997; Pokorny & Schmidt 2001). Astaxanthin extracted from fermented shrimp
byproducts undergoes oxidation when exposed to air and full light (Armenta & Legarreta
2009). On the other hand, antioxidant properties can be enhanced during thermal
heating through the transformation of antioxidants into a more active compound, i.e. the
production of Maillard reaction products (MRPs). Thermal treatment induces the
formation of MRPs with new antioxidant properties (Nicoli et al 1997). Studies have

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shown that during heating of fermented cabbage (Kusznierewicz et al 2008), sugar-tuna
stomach hydrolysate (Martinez-Sumaya et al 2005) and sugar-amino acid model systems
(Benjakul et al 2005; Jing & Kitts 2004; Yoshimura et al 1997), there is concomitant
formation of MRPs with antioxidant capacity. As far as we know, there is no study yet on
the effects of heating on the natural antioxidants in Philippine fermented products. The
present study intends to assess the activity of naturally occurring antioxidants in salt-
fermented shrimp paste subjected to thermal processing.

Material and Method

Preparation of raw material and treatments. Shrimp (A. sibugae), a common

species found in the Central Philippine sea i.e. the Visayan Sea, was purchased from
Tigbauan, Iloilo, cleaned and salted with a ratio of 1:7 (salt:shrimp). The mixture was
allowed to ferment for 15 days at room temperature (30o – 35 oC) with occasional
stirring. Samples from three replicates were withdrawn at days 1, 5, 10 and 15 and were
subjected to antioxidant assays.
Shrimp paste was heat processed (sautéed and boiled) with added ingredients/spices
(Table 1).

Table 1
Ingredients used for each type of shrimp paste product

Sample code Ingredients added Product type

CA oil, garlic Regular
CB oil, garlic, sugar Sweet
CC oil, garlic, sugar, vinegar Traditional
CD none Plain

Shrimp pastes were cooked/boiled for either 10 min or 30 min for water reduction under
heat medium. Product variants were then packed in glass jar and pasteurized under
boiling water for 1 h, cooled and incubated for 15 days. Samples from three replicates of
heating time variable were withdrawn for analysis.

Preparation of 80 % ethanol extract from salt-fermented shrimp paste (raw and

cooked). Shrimp paste (5 g) was homogenized with 5 mL of water and 20 mL of 95 %
ethanol, centrifuged at 1500 rpm for 20 min. The upper layer was recovered and the
process was repeated on the precipitate formed and the combined recovered upper
layers were made up to 50 mL with 95 % ethanol (Peralta et al 2005). When insoluble
materials were observed, the extracted solution was centrifuged again to remove the
insoluble materials. The resulted solution, which contained approximately 80 % ethanol,
was designated as 80 % ethanol sample extract.

Analytical method. Antioxidant activity assay.

A. DPPH radical scavenging activity. This assay involves the use of a free radical, 2,2-
diphenyl-1-picrylhydrazyl (DPPH) which is purple in color that gives a strong maximum
absorption at 517 nm. The color turns from purple to yellow as the molar absorptivity of
DPPH radical is reduced when the odd electron of DPPH radical becomes paired with
hydrogen from free radical scavenging antioxidant to form the reduced DPPH-H.
Appropriate amount of the 80 % ethanol extract was diluted to 3 mg (dry weight) of
shrimp paste mL-1 with 80 % ethanol solution. Each sample (1.0 mL) was incubated with
0.25 mL of 0.1mM DPPH for 20 min at room temperature (Peralta et al 2007). The DPPH
radical scavenging activity (%) was calculated from the decrease of absorbance at 517
nm by the addition of 80 % ethanol extract toward that of the control (without
antioxidant).
B. Measurement of hydrogen peroxide scavenging activity. Being a non-radical oxygen-
containing reactive agent, hydrogen peroxide can form a hydroxyl radical, a known highly
reactive oxygen radical, in the presence of transition metal ions and initiate lipid

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peroxidation by abstracting the hydrogen atom from unsaturated fatty acids (Gutteridge
& Halliwell 1994). Hydrogen peroxide scavenging activity was measured using the
method described by Bahorun et al (1996) with modification. After concentrating the 85
% ethanol extract, an appropriate amount (50 µL) was incubated in 0.45 mL of 0.1 M
phosphate buffer (pH 7.0) containing 89 mM NaCl and 23 µM H2O2 for 10 min at 37 oC.
To the mixture was added 0.5 mL of 0.1 M phosphaste buffer (pH 7.0) containing 0.05
mg HRPO and 0.1 mg phenol red and kept at room temperature for 15 min. Then 50 µL
of 1.33 M NaOH was added to the mixture. Optical density was read at 610 nm after 10
min.

Brown color development. Browning reactions are some of the important phenomena
occurring in food during processing and storage. The reaction is classified as non-
enzymatic browning which involves sugar, amino acids or protein that condense and
progress into a complex reaction products collectively known as Maillard reaction products
(MRPs) (Jing & Kitts 2004). The 80 % ethanol sample extract was diluted to 3.0 mg (dry
weight) sample mL-1 with 80 % ethanol using the method of (Benjakul et al 2005).
Optical density was measured at 420 nm.

Statistical analysis. One-way analysis of variance was used to test for significant
difference among treatment means of DPPH and H2O2 scavenging activities and optical
densities (O.D.) indicating brown color development. If significance was detected, a post
hoc test was done using Duncan’s multiple range test (DMRT) at 0.05 alpha level.

Results

Antioxidant activity assay. Changes in activity during fermentation of low-salt

fermented shrimp paste. DPPH radical scavenging activity was evaluated in salt-
fermented shrimp paste collected every five days (day 1, 5, 10, and 15) for 15 days.
Results showed that the radical scavenging activity of 80 % ethanol extract from shrimp
paste significantly increased with increasing sample concentration during fermentation
(Table 2). Significant increase in activity was observed from day 1 to day 5 which could
be due to the active breakdown of protein to peptides and amino acids by the initial
bacterial load in shrimp paste. The prolonged fermentation from 5 - 15 days resulted in a
slight increase in activity but was not significantly different between treatments.

Table 2
Changes in DPPH radical and hydrogen peroxide (H2O2) scavenging activity of 80 %
ethanol extract from salt-ferment shrimp paste during fermentation

DPPH radical scavenging activity (%) H2O2 scavenging activity (%)

Sample
7.5 mg* 10 mg* 3.0 mg*
Day 1 13.87 + 2.48a 20.21 + 1.86a 0.83a
Day 5 20.84 + 2.84b 31.56 + 4.05b na
b
Day 10 22.17 + 1.75 33.69 + 4.17b 7.3b
b
Day 15 24.0 + 2.75 34.47 + 1.30b 8.1b
*amount of sample used expressed as dry weight calculated from their moisture content. The moisture content
was determined by oven method at 105 oC. Results are mean + SD for n=3. Values in the same column with
different letters are significantly different (p<0.05), na – not analyzed.

Similar to DPPH scavenging activity, hydrogen peroxide scavenging activity significantly

increased from day 1 to day 10 but did not significantly change at day 15 (Table 2).

Activity in heat processed salt-fermented shrimp paste. The initial DPPH free
radical and hydrogen peroxide scavenging activity of 80 % ethanol extract (3 mg) of
uncooked salt-fermented shrimp was 10.3 % and 8.1 %, respectively. Results showed
that heat treatment of all samples (10 min) resulted in a significant increase in DPPH
radical scavenging activity. In contrast, scavenging activity in samples treated with

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extended heating time resulted in a marked decrease although not significantly different
from each other. Hydrogen peroxide scavenging activity of the samples significantly
increased after heat treatment, but significantly decreased when heating was prolonged
(Table 3).

Table 3
DPPH radical and hydrogen peroxide (H2O2) scavenging activity of 80 % ethanol extract
(3 mg*) of heat processed salt-ferment shrimp paste

DPPH free radical scavenging activity H2O2 scavenging activity

Sample (%) (%)
code Time (min)
10 30 90** 10 30 90**
CA 15.2 13.0 21.8 10.1 11.0 8.5
CB 17.0 13.0 18.1 20.4 8.6 3.9
CC 21.5 17.5 21.4 19.9 7.2 3.5
CD 18.6 18.1 24.4 19.8 6.3 1.0
*amount of sample used expressed as dry weight calculated from their moisture content. The moisture
content was determined by oven method at 105 oC, **shrimp paste sautéed, packed in bottled and
pasteurized.

Spices and ingredients e.g. garlic are known to exhibit antioxidant activity. However, in
the present study, product CA exhibited lower activity than did product CD where no
ingredients or oil was added. It was possible that the added ingredients did not
contribute to the observed increase in scavenging activity. Extended heating (30 min)
showed slight decreased in activity. However, when samples were bottled and heat-
pasteurized, activity between samples significantly increased and was relatively similar
with each other.

Brown color development in shrimp paste. Optical density of shrimp paste during
heat processing as an index of brown color formation was variable. A marked increase in
optical density was recorded when samples were further processed into bottled product.
The observed increase in DPPH radical scavenging activity after bottle-processing (Table
4) could probably be due to the development of reaction products induced by heat.

Table 4
Optical density (brown color indicator) of extracts (15 mg*)

Brown color (O.D.)

Sample code Time of heating (min)
10 30 90**
CA 013 016 022
CB 014 016 022
CC 018 015 017
CD 024 017 032
*amount of sample used expressed as dry weight calculated from their moisture content. The moisture
content was determined by oven method at 105 oC, **shrimp paste sautéed, packed in bottled and
pasteurized.

Discussion. Naturally occurring antioxidants are found in most plants and animal
tissues. Majority of natural antioxidants are phenolic compounds and the most important
groups are the tocopherols, flavonoids and phenolic acids. Shrimps are rich in protein and
other essential nutrients as well as natural antioxidants (Rosenzweig & Babbit 1991;
Seymour et al 1996).
Antioxidants are substances which significantly inhibit or delay oxidative processes
such as lipid peroxidation even at low concentrations. For instance, polyunsaturated fatty
acids (PUFAs) between salted (1:3) and unsalted ferments are similar in shrimp paste
produced in Bolinao, Pangasinan, Philippines (Montano et al 2001). Salt-fermented

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shrimp paste is also observed to maintain large amounts of EPA and DHA, which are not
greatly affected during prolonged fermentation, regardless of the level of salt and
temperature of fermentation (Peralta 2008; Peralta et al 2007). These observations could
be attributed to the presence of naturally occurring antioxidants as well as substances
with antioxidant properties produced during fermentation.
Fermentation involves the transformation of organic substances to simpler
compounds such as peptides, amino acids and other nitrogenous compounds by bacterial
or endogenous enzymes. While they are important contributors to the flavor and aroma
of fermented products (Mackie et al 1971; Raksakulthai & Haard 1992), some exhibit
antioxidant capacity (Kitts & Weiler 2003). Hydrolysate of shrimp processing byproduct
contain high amount of hydrophobic amino acids (40.4 %) that may contribute to the
high antioxidant activity (Zhao et al 2011). The amino acid content in salt-fermented
shrimp paste (mostly taurine, alanine and lysine) increases from 886 to 1392 mg 100g-1
after 10 day of fermentation (Peralta et al 2005). Amino acids such as tryptophan and
histidine (Houlihan & Ho 1985), glycine and alanine (Hui-Chun et al 2003) exhibit
antioxidative property. Tyrosine and lysine are generally accepted to be antioxidants
(Wang & Gonzalez de Mejia 2005).
Amino compounds such as amino acids and peptides can function as primary
antioxidants and can also interact with other substances to form Maillard reaction
products (MRPs) (Kitts & Weiler 2003). They are non-enzymatic browning reactions that
occur in foods. Lysine, as one of the major amino acid in salt-fermented shrimp paste,
could have reacted with other substance thus reflecting an increase in activity. Sugar –
lysine (Jing & Kitts 2004; Wijewickreme et al 1999), glucose-glycine (Yoshimura et al
1997) and sugar-protein (Benjakul et al 2005) model systems have been shown to
exhibit antioxidant activity.
Heating results in oxidation reactions occurring rapidly (Pokorny & Schmidt 2001).
In some cases, oxidation reactions show opposite effects on the antioxidant properties of
foods. Partially oxidized polyphenols, for instance, exhibit higher antioxidant activity than
that of non-oxidized phenols. Jeong et al (2004) observe that antioxidant activities in
citrus peel extracts increase as heating temperature increases. Antioxidant activity in
shrimp hydrolysate is stable when heated up to 100 oC (Zhao et al 2011). In the present
study, heat treatment for 10 min significantly enhanced antioxidant activity. However,
extending heating to 30 min resulted in a slight decrease in activity. During boiling,
antioxidant activity of peptides and amino acids probably was affected by way of
denaturation, chemical interaction with other substances or evaporation of some volatile
antioxidants (Pokorny & Schmidt 2001). It is a commonly accepted observation that to
minimize natural antioxidant degradation due to prolonged heating and evaporation, it is
necessary to reduce residence time of food at high temperature and employ optimal
evaporation methods such as rapid rate of heat transfer or low temperature operations.
Thermal processing at elevated temperature, e.g. pasteurization, probably
influence the transformation of antioxidants into a more active and resistant compound
such as MRPs. Antioxidant efficiency of MRPs is influenced by factors such as ratio and
type of amino acid compounds and sugar involved, temperature, pH and water activity
(Manzocco et al 2001). MRPs from sugar-tuna stomach hydrolysate heated at 95 oC and
115 oC increases the DPPH radical scavenging activity (Martinez-Sumaya et al 2005).
MRPs from glucose-glycine heated for 1 h inhibits more than 90 % of active oxygen
species existing in the form of hydroxyl radicals in the sample (Yoshimura et al 1997).
Although the concentration of natural antioxidant is significantly reduced as a
consequence of thermal treatments, the overall antioxidant properties of tomato
derivatives and coffee are maintained or even enhanced by the development of MRPs
(Nicoli et al 1997).

Conclusions. The present study showed that antioxidant activity in low-salt fermented
shrimp paste was enhanced when subjected to thermal treatments probably due to either
the increased resistance of natural antioxidants or its transformation into a more active
compound or the formation of novel compounds such as MRPs or any combination of
these three occurrences. Thus, the overall effect of thermal processing of low-salt

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fermented shrimp was favorable where it converted the product into a shelf-stable
commodity as well as increased its antioxidant capabilities which is known to have health
benefits.

Acknowledgements. The authors are deeply grateful to the University of the Philippines
Visayas through the Office of the Vice Chancellor for Research and Extension for the
financial support given to the study. Profound gratitude is also extended to the Institute
of Fish Processing Technology and its staff for assistance.

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Received: 21 December 2013. Accepted: 16 January 2014. Published online: 23 January 2014.
Authors:
Ernestina Mateo Peralta, University of the Philippines Visayas, College of Fisheries and Ocean Sciences, Institute
of Fish Processing Technology, Philippines, Miagao, Iloilo 5023, e-mail: [email protected]
Augusto Erum Serrano Jr., University of the Philippines Visayas, College of Fisheries and Ocean Sciences,
Institute of Aquaculture, Philippines, Miagao, Iloilo 5023, e-mail: [email protected]
This is an open-access article distributed under the terms of the Creative Commons Attribution License, which
permits unrestricted use, distribution and reproduction in any medium, provided the original author and source
are credited.
How to cite this article:
Peralta E. M., Serrano Jr. A. E., 2014 Activity of naturally occurring antioxidants during heat processing of low-
salt fermented shrimp paste. ABAH Bioflux 6(1):27-33.

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