Research Article

Received: 28 July 2010 Revised: 19 October 2010 Accepted: 17 November 2010 Published online in Wiley Online Library: 6 January 2011

(wileyonlinelibrary.com) DOI 10.1002/jsfa.4260

Effects of high hydrostatic pressure

on enzymes, phenolic compounds,
anthocyanins, polymeric color
and color of strawberry pulps
Xiamin Cao, Yan Zhang, Fusheng Zhang, Yongtao Wang, Jianyong Yi
and Xiaojun Liao∗

Abstract
BACKGROUND: Changes in activity of polyphenol oxidase (PPO), peroxidase (POD) and β-glucosidase, individual phenolic
compounds other than anthocyanins, total phenols, monomeric anthocyanins, polymeric color and instrumental color of
strawberry pulps were assessed after high hydrostatic pressure (HHP) (400–600 MPa 5–25 min−1 ) at room temperature.

RESULTS: β-Glucosidase was activated by 4.7–16.6% at 400 MPa 5–25 min−1 and inactivated by 8.0–41.4% at 500 or 600 MPa.
PPO and POD were inactivated at all pressures, the largest reduction in activity being 41.4%, 51.5% and 74.6%, respectively.
The individual phenolic compounds and total phenols decreased at 400 MPa, but total phenols increased at 500 or 600 MPa.
However, the monomeric anthocyanins, polymeric color and redness (a∗ ) exhibited no change. HHP induced a decrease in
lightness (L∗ ) and an increase in yellowness (b∗ ) at 400 MPa, but no significant alteration in L∗ value and b∗ value at 500 or
600 MPa was observed; this was attributed to higher residual activity of PPO, POD and β-glucosidase at 400 MPa. Total color
difference (E) was ≥5 at 400 MPa and ≤3 at 500 or 600 MPa.

CONCLUSION: HHP effectively retained anthocyanins, phenolic compounds and color of strawberry pulps, and partly inactivated
enzymes.

c 2011 Society of Chemical Industry

Keywords: high hydrostatic pressure; strawberry pulps; enzymes; individual phenolic compounds; anthocyanins; polymeric color

INTRODUCTION enzymes.4 – 7 The primary enzyme responsible for the browning

Attractive color is one of the most important quality attributes reaction is PPO,4 as well as POD, since diphenols may function as
of strawberries and strongly affects their consumer acceptance substrates in its reaction. Oxidative products of phenolics, such as
and preference. This is mainly due to the presence of phenolic 4-methylcatechol, resulting from PPO activity could accelerate
compounds, especially anthocyanins, a group of water-soluble anthocyanidin degradation, resulting in enzymatic browning and
pigments with antioxidant properties. The content of anthocyanins the formation of polymeric brown pigments.7 Additionally, the
varies from 200 to 600 mg kg−1 in fresh strawberry.1 Strawberries products of anthocyanin degradation during processing are
possess two types of anthocyanidin pigments: derivatives of easily oxidized by PPO to form browning compounds, and the
bright red pelargonidin and dark red cyanidin, mainly including degradation of anthocyanins in processed berry products also has
pelargonidin-3-glucoside (Pg-3-glu), pelargonidin-3-rutoside (Pg- been reported to arise as a result of indirect oxidation by phenolic
3-rut) and cyanidin-3-glucoside (Cy-3-glu).2 quinones generated by PPO. Regarding POD, involvement in
Strawberries are seasonally available and widely consumed browning is reported by many researchers,4,8 although it is
as jams, juices and pulps. The color of strawberry products is limited by the availability of electron acceptor compounds such
unstable and susceptible to degradation. After a few weeks or as superoxide radicals, hydrogen peroxide and lipid peroxides.
even days of storage, the red color is replaced by a dull, brownish
color. According to the literature, a key role in color degradation
is attributed to enzymatic browning of phenolic compounds, ∗ Correspondence to: Xiaojun Liao, Engineering Research Center for Fruit and
degradation of anthocyanins and products of the Maillard Vegetable Processing, Ministry of Education, Beijing 100083, China.
reaction during or after processing.3 Browning of damaged E-mail: [email protected]
tissues of fresh fruits and vegetables mainly occurs from the
College of Food Science and Nutritional Engineering, China Agricultural
oxidation of phenolic compounds and contributes significantly
University, China; Key Laboratory of Fruit and Vegetable Processing, Ministry
to quality loss.4 polyphenol oxidase (PPO), peroxidase (POD) of Agriculture, China; Engineering Research Center for Fruit and Vegetable
877

and β-glucosidase have been demonstrated to be color-related Processing, Ministry of Education, Beijing 100083, China

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c 2011 Society of Chemical Industry
 www.soci.org X Cao et al.

In plants, β-glucosidases are involved in different key metabolic Instrument Co., Shanghai, China) and pH was 3.6 ± 0.1 (Orion
events, which can catalyze the hydrolysis of aryl and release 868 pH meter, Thermo Fisher Scientific Inc, MA, USA).
glucoside.9 Zapata et al.10 suggested that removal of the sugar
moiety from anthocyanins to form phenolic aglycones was an Preparation of strawberry pulps
important step before POD acted on the anthocyanins. Therefore,
The frozen strawberries were thawed at 4 ◦ C for 12 h, followed
the inactivation of these enzymes is necessary for better color
by 30 min at room temperature. After thawing, they were pulped
retention by processing steps. Conventional thermal processing
by juice extractor (JY-610, Joyoung Co., Ltd Shandong, China) for
(TP) can inactivate enzymes in foods,5 but it seriously affects the
5 min at room temperature. All the pulps were mixed together and
quality of processed foods such as color and anthocyanin.11,12 kept at 4 ◦ C. 120 g strawberry pulps were placed in plastic cups
High hydrostatic pressure (HHP) is a non-thermal processing (EVOH/PVPP) and sealed for 5 s with a heat sealer (Hongyi Ma-
technique which subjects foods to 100–1000 MPa using water chinery & Electric Co., Guangzhou, China) immediately. The sealed
as a pressure-transmitting medium at room or mild temperature. samples were kept at 4 ◦ C until treated by HHP and TP within 10 h.
Food treated in this way has been shown to keep its original
freshness, flavor, taste and color to the greatest extent,9 since
smaller molecules such as volatile compounds, pigments, vitamins, HHP treatments
and other compounds connected with the sensory, nutritional, and Samples were placed in a high-pressure vessel (15 cm internal
health promoting are unaffected by HHP.13 diameter × 30 cm internal height, Pressure Engineered System,
Investigations into the effects of HHP on strawberries or HHP-650, Baotou Kefa Co., Inner Mongolia, China) filled with water
their products have been carried out, which are implicated and subjected to pressures of 400, 500 or 600 MPa for 5–25 min
in the inactivation of indigenous enzymes,5,14 , the stability of at ambient temperature (∼25 ◦ C).
anthocyanins in whole strawberry fruit during storage,11 changes
in water-soluble vitamins in strawberry,12,15 flavor compounds TP treatments
in strawberry,9,16 total phenolic content12 and instrumental Samples were boiled in water until they achieved a core
color changes6,17 in strawberry purée or juice. However, these temperature of 70 ◦ C and were held at this temperature until they
investigations were based on a different matrix, respectively reached a time–temperature (P70 ≥ 2 min) equivalent to a six log
covering whole strawberry fruit, purée and juice. The quality reduction in numbers of vegetative cells of the target pathogen
indicators were difficult to compare and the relationship between Listeria monocytogenes.12 Samples were then immediately cooled
the indigenous enzymes and quality indicators from different to room temperature in an ice-water bath.
publications was hard to establish since the matrix had an
important impact on the HHP effects. Meanwhile, data showing the
HPLC analysis of individual phenolic compounds
effects of HHP on the enzymes, individual phenolic compounds
other than anthocyanins
and polymeric color of HHP-treated strawberry pulps were still
The extraction of soluble phenolic compounds other than
insufficient. Therefore the purpose of this study was to evaluate
anthocyanins was presented with a few modifications18 within
the inactivation of PPO, POD and β-glucosidase, changes of
24 h after treatment. 30 g strawberry pulps were mixed with
the individual phenolic compounds other than anthocyanins,
60 mL ethyl acetate and stirred with a magnetic stirrer for 30 min,
total phenols, monomeric anthocyanins, polymeric color and
and then the ethyl acetate phase was collected. The extractions
instrumental color in strawberry pulps after HHP treatment.
were performed by repeatedly vigorous vortexing samples with
ethyl acetate (3 × 100 mL). The combined ethyl acetate extracts
were evaporated to dryness at 40 ◦ C with a rotary evaporator
MATERIALS AND METHODS (SENCQ R-501, Shenshun Biotechnology Co., Shanghai, China),
Chemicals then dissolved in 10 mL methanol.
Methanol and formic acid of high-performance liquid chromatog- The separation of individual phenolic compounds other than
raphy (HPLC) grade were purchased from Honeywell Burdick & anthocyanins was as described in Aaby et al.,18 with some mod-
Jackson (SK Chemicals, Seoul, Korea). Catechin, β-hydroxybenzoic ifications. The mobile phases were (A) formic acid–acetonitrile
acid, caffeic acid, ρ-coumaric acid, ellagic acid, ferulic acid, (2.5 : 97.5, v/v) and (B) formic acid–water (2.5 : 97.5, v/v). The
myricetin, quercetin and kaempferol were obtained from Yifang detection was carried out at 280 nm and 320 nm for phenolic
Technology Co. (Tianjin, China). Cyanidin-3-glucoside (Cy-3-glu) compounds in absorbance mode at a flow rate of 1 mL min−1 at
was purchased from Polyphenol Co. (Sandnes, Norway, Fin- 30 ◦ C, and aliquots of 20 µL were injected. The gradient elution
lan). p-Nitrophenyl-β-D-xylopyranoside (PNPG) was obtained from was as follows: 0–5 min, 5% A; 5–15 min, 5–13% A; 15–20 min,
Sigma-Aldrich Chemical Co. (Shanghai, China). Pelargonidin-3- 13–30% A; 20–25 min, 30% A; 25–28 min, 30–45% A; 28–32 min,
glucoside (Pg-3-glu) and pelargonidin-3-rutoside (Pg-3-rut) were 45% B; 32–35 min, 45–90% B; 35–40 min, 90% B; 40–45 min,
prepared by HPLC; their purities were higher than 98% and 90%, re- 90–5% B. Results were expressed as milligrams per kilogram fresh
spectively. Other chemicals were obtained from Beijing Chemicals weight (FW).
Co. (Beijing, China).
Determination of total phenols
Samples Total phenols were determined using the Folin–Ciocalteu method
Strawberries (Tongzi I) grown in Tianyi Bio-engineering Company described by Oszmiajski et al.,19 with some modifications within
in Changping county (Beijing, China) were harvested at commer- 24 h after treatment. 125 µL of 100-fold diluted phenolic com-
cial maturation in March 2009 and frozen at −18 ◦ C until analysis pound extracts were mixed with 2 mL Folin–Ciocalteu reagent
within 8 months. The total soluble solid was 9.3 ± 0.1 ◦ Brix (WAY- (previously diluted 10-fold with distilled water) and set for 1 h
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2S digital Abbe refraction meter, Shanghai Precision and Scientific in the dark at room temperature. After 1.8 mL sodium carbonate

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(105.99 g mol−1 ) was added to the mixture and reacted for 15 min, Enzyme assay
the mixture was immediately measured at 765 nm using a spec- The enzymes were extracted within 8 h after treatment. 10 g
trophotometer (UV-726, Shimadzu, Shanghai, China). Results were strawberry pulps were mixed with 20 mL extraction buffer and 4%
expressed as g gallic acid kg−1 FW. polyvinyl polypyrrolidone and continuously stirred for 3 min, then
extracted for 4 h at 4 ◦ C. The mixture was centrifuged at 543 × g
for 10 min at 4 ◦ C, and the supernatant was collected and analyzed
HPLC analysis of monomeric anthocyanins for enzyme activity. The extraction solution was 0.2 mol L−1
Anthocyanins were extracted and measured within 24 h after phosphate buffer pH 6.5 for PPO and POD5 and 0.1 mol L−1
treatment as earlier described,20 with some modifications. 10 g citrate–0.2 mol L−1 phosphate buffer pH 6.0 for β-glucosidase.22
strawberry pulps were mixed with 20 mL of 0.1% HCl in methanol. PPO and POD activity were determined by a spectrophotometric
After standing for 1 h at 4 ◦ C, the mixture was centrifuged at method5 with some modifications. The reaction mixture for PPO
543 × g for 10 min at 4 ◦ C. The supernatant was collected for was 1 mL extract and 2 mL 0.07 mol L−1 catechol(o-diphenol)
further analysis. Anthocyanins were separated using a Shimadzu in 0.5 mol L−1 sodium phosphate buffer (pH 6.5) solution. The
liquid chromatograph (Shimadzu Co., Japan) equipped with a reaction mixture for POD contained 2.2 mL of 1.0% (v/v) guaiacol
Prominence UV-visible detector (SPD-20AV), an auto sampler (SIL- (dissolved in 0.2 mol L−1 phosphate buffer, pH 6.5), 0.2 mL of
20A) and a column oven (CTO-20A). Chromatographic separation 1.5% H2 O2 , and 0.8 mL extract. The increase in absorbance
was performed on a vessuil C18 column (250 mm × 4.6 mm at 420/470 nm for PPO/POD, respectively, was monitored at
i.d., 5 µm particle size) equipped with a 5 µm C18 guard column, intervals of 0.1 s−1 immediately after incubation with a Cary 50
both from Agela Technologies Co. (Tianjin, China). The HPLC spectrophotometer (Varian Co. Ltd, Santa Clara, CA, USA), which
conditions were similar to those of the above-mentioned analysis was equipped with a Peltier thermostatted cell holder, a water
of anthocyanins. Cy-3-glu, Pg-3-glu and Pg-3-rut were quantified pump (Varian) to keep the temperature at 30 ± 0.1 ◦ C and an
as monomeric anthocyanins by external standards, and expressed in-built electromagnetic stirrer to mix the substrate and extracts.
as mg kg−1 FW of strawberry. Prior to measurement, a pre-equilibrium at 30 ◦ C of the substrate
solution as well as the extracts by the Peltier thermostatted cell
holder was obtained. The slope of the very first linear part of
Polymeric color analysis the reaction curve was taken as the PPO/POD specific activity
Polymeric color was determined using the method described (abs. min−1 ). The β-glucosidase assay used PNPG as substrate
by Hager et al.21 within 24 h after treatment. Sample extracts according to Cleemput et al.,23 with slight modifications. The
were diluted with distilled water in order to have an absorbance following reaction mixture was prepared: 0.5 mL of 4 mmol L−1
reading between 0.5 and 1.0 at 520 nm when evaluated by a PNPG, 0.1 mL extract, 0.4 mL of 0.1 mol L−1 citrate and 0.2 mol L−1
spectrophotometer (UV-726, Shimadzu). For analysis, 1 mL of phosphate buffer (pH 6.0). The mixture was incubated at 40 ◦ C
0.90 mol L−1 potassium metabisulfite was added to 3 mL of diluted for 30 min and the reaction was stopped by adding 2 mL of
sample (bisulfite-bleached sample) and 1 mL distilled water was 3 mol L−1 anhydrous sodium carbonate. In the control reactions,
added to 3 mL of diluted sample (non-bleached, control sample). 0.1 mL distilled water was added instead of enzymatic extract. The
After equilibrating for 30 min, but not more than 1 h, samples amount of p-nitrophenol released was determined measuring the
were evaluated at λ = 700, 520, and 420 nm. Color density optical density at 405 nm. The residual activity (RA) of enzymes
(CD) was calculated using the control sample according to the was estimated with the following equation:
following formula: CD = [(A420 − A700 ) + (A512 − A700 )] × dilution
factor. Polymeric color (PC) was determined using the bisulfite- enzyme specific activity after HHP treatment
RA = × 100%
bleached sample using the following formula: PC = [(A420 −A700 )+ enzyme specific activity in control
(A512 − A700 )] × dilution factor. Percent polymeric color (PPC) was
calculated using the formula: PPC = (polymeric color/color density) Statistical analysis
× 100%. The experiment was performed in triplicate. The data were
analyzed using the Statistical Program for Social Sciences (SPSS
12.0, Chicago, IL, USA) software for analysis of variance and
Measurement of instrumental color Duncan’s test. The significance was established at P ≤ 0.05.
Color of strawberry pulps was measured in a cylindrical sample cup
(inner diameter 2 cm and height 1 cm) within 1 h after treatment,
filled with 5 g samples to the top, using a reflection mode on a RESULTS AND DISCUSSION
color difference meter (SC-80C, Kangguang, Beijing, China). The Effects of HHP on PPO, POD and β-glucosidase in strawberry
instrument was calibrated using black and white tiles; a standard pulps
color plate with reflectance values L∗ = 80.55, a∗ = 81.26, The RA of PPO, POD and β-glucosidase in strawberry pulps
b∗ = 79.72 was used as reference. Color was expressed in L∗ , a∗ and after HHP treatments was detected. As shown in Fig. 1, PPO
b∗ values. Three measurements were performed and results were activity gradually decreased with increasing pressure levels and
averaged. In addition, hue angle (H◦ ), chroma (C ∗ ) and total color extending the treatment times; the highest reduction of PPO
difference (E) were calculated using the following equations,6 activity was 51.5% at 600 MPa for 25 min. These data indicate
where L∗ 0 , a∗ 0 , b∗ 0 are the control values for untreated pulps: that PPO in strawberry pulps showed higher resistance to HHP.
However, Garcia-Palazon et al.5 reported that there is a complete
◦
H = arctan(b∗ /a∗ ) inactivation of PPO in strawberry fruits at 600 MPa for 15 min at
2 2 room temperature. Dalmadi et al.22 showed that PPO extracts of
C ∗ = (a∗ + b∗ )1/2 strawberry (pH = 7.0) were quite stable until 500 MPa and there was
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E = [(L∗ − L∗ 0 )]2 + [(a∗ − a∗ 0 )]2 + [(b∗ − b∗ 0 )2 ]1/2 a sharp decrease in the residual activity after 15 min between 500

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 www.soci.org X Cao et al.

80 80

RA of POD in strawberry pulps (%)

RA of PPO in strawberry pulps (%)

70 60

40
60

20
50
400 MPa; 500 MPa; 600 MPa
400 MPa; 500 MPa; 600 MPa
0
40 5 10 15 20 25
5 10 15 20 25 Time (min)
Time (min)
Figure 2. The effects of high hydrostatic pressure on peroxidase activity in
Figure 1. The effects of high hydrostatic pressure on polyphenol oxidase strawberry pulps.
activity in strawberry pulps.

RA of b-glucosidase in strawberry pulps (%)

140
and 700 MPa; only 5% PPO activity was still noticeable at 800 MPa.
Palou et al.24 reported a 95% reduction in PPO activity in banana 120
purée at pH 3.4 after HHP treatment at 689 MPa. The difference
in pressure resistance of various PPOs to HHP was due to product 100
forms, pH, cultivars, HHP conditions, etc. Moreover, the inactivation
kinetics of PPO by HHP in this study conformed to first-order
80
reaction with higher regression coefficient (R2 ≥ 0.952). Dalmadi
et al.22 also reported that the HHP inactivation of strawberry PPO
extracts was adequately described by the first-order model. 60
POD activity was significantly affected after HHP treatments
400 MPa; 500 MPa; 600 MPa
(Fig. 2). At 400 or 500 MPa, POD activity reduced with increasing 40
treatment time; the maximal reduction of POD activity was 56.5%
or 74.6%. Compared with 400 and 500 MPa, the reduction of 5 10 15 20 25
POD activity was different at 600 MPa. The inactivation of POD Time (min)
may be due to the dissociation or modification of the prosthetic
Figure 3. The effects of high hydrostatic pressure on β-glucosidase activity
group and conformational change in the enzyme.25 The POD in strawberry pulps.
activity was reduced to 35.7% at 600 MPa for 5 min, but returned
to 71.9% for 10 min. This recovery effect of POD activity could
be related to the increase in solubilization by pressure of POD The response of β-glucosidase to HHP was different from that
forms linked to cellular membranes26 or to the pressure-activated of PPO and POD. The β-glucosidase was activated at 400 MPa and
latent form due to conformational changes of the enzyme.25 its activity increased with extending treatment times, the highest
With extension of treatment time to 15–25 min, the residual activity being 116.7% after 25 min (Fig. 3). This finding was in
POD activity was decreased to 54.5–50.0%; this decrease was good agreement with previous studies which reported that β-
possibly due to disruption of intramolecular interactions and/or glucosidase activity was 76% higher in strawberry fruit treated with
interaction between the functional groups of the protein and the 400 MPa for 15 min at 18–22 ◦ C than in unprocessed samples.5
solvent (usually water), which affect the structure, functionality and However, HHP treatments at 500 and 600 MPa effectively reduced
stability of the protein.27 Some similar observations were made in β-glucosidase activity: maximum reduction of β-glucosidase activ-
earlier studies. Cano et al.14 showed that POD activity of strawberry ity was 41.4% at 600 MPa for 25 min. Garcia-Palazon et al.5 reported
purée and orange juice is increasingly inactivated up to 300 MPa that the reduction of β-glucosidase activity in whole strawberry
and 400 MPa at room temperature, and HHP treatments higher fruit at 600 MPa for 15 min was 49% – slightly higher than in this
than these pressures slightly increased POD activity. POD activity of study. This was possibly attributable to the strawberry cultivar.
carrot of 5–8 cm in length decreased to 16% at 350 MPa and 20 ◦ C Compared with HHP, TP induced a complete inactivation of
for 30 min, but an increase in the activity for POD was observed these enzymes in strawberry pulps (data not shown). Similarly,
with increasing pressure to ≥350 MPa25 . However, Garcia-Palazon Chisari et al.28 observed that PPO extracted from ‘Elsanta’
et al.5 reported that there was an 11–35% inactivation of POD strawberries was highly thermolabile, with almost complete
in strawberry fruits at 600 MPa for 5–15 min and no increase of inactivation after 20 min incubation at 60 ◦ C, and POD was
POD activity was observed. The inactivation pattern of POD at completely inactivated at 80 ◦ C for 5 min. Serradell et al.29 also
600 MPa was quite different from PPO and β-glucosidase, which observed almost complete inactivation of crude PPO extract from
was induced by the variety of their structures, pressure resistance ‘Selva’ strawberry in phosphate buffer (pH = 6.0) after 30 min
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and location in plant tissues. treatment at 65 ◦ C.

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c 2011 Society of Chemical Industry J Sci Food Agric 2011; 91: 877–885
 J Sci Food Agric 2011; 91: 877–885
Table 1. Individual phenolic compounds other than anthocyanins (mg kg−1 ) in strawberry pulps treated with high hydrostatic pressure and thermal processinga
ß-Hydroxybenzoic ρ-Coumaric
Treatment Conditions Catechin Ellagic acid acid acid Ferulic acid Caffeic acid Kaempferol Quercetin Myricetin Total

Control 41.6 ± 1.16d 31.9 ± 1.10bc 7.0 ± 0.2ab 5.6 ± 0.1ab 6.6 ± 0.2b 5.3 ± 0.3a 3.6 ± 0.2a 9.5 ± 0.5b 6.4 ± 0.2a 117.5 ± 5.6b
Thermal processing 59.1 ± 1.22e 37.4 ± 1.12d 10.4 ± 0.7c 8.1 ± 0.1d 7.0 ± 0.3bc 6.0 ± 0.2b 3.5 ± 0.1a 10.1 ± 0.3c 8.7 ± 0.3b 150.3 ± 4.8c

400 MPa,5 min 32.8 ± 1.16a 31.7 ± 1.10bc 6.8 ± 0.2a 6.5 ± 0.3bc 5.7 ± 0.2a 5.3 ± 0.2a 3.3 ± 0.1a 8.7 ± 0.2a 6.0 ± 0.3a 106.8 ± 363a
Effects of high hydrostatic pressure on strawberry pulps

400 MPa,10 min 31.9 ± 1.7a 32.4 ± 1.08bc 6.7 ± 0.3a 5.8 ± 0.2ab 6.3 ± 0.1ab 5.2 ± 0.1a 3.4 ± 0.1a 8.4 ± 0.3a 5.9 ± 0.2a 106.0 ± 3.92a
400 MPa,15 min 35.6 ± 1.1b 32.2 ± 1.10bc 6.6 ± 0.1a 5.8 ± 0.1ab 6.2 ± 0.1ab 5.2 ± 0.3a 3.5 ± 0.1a 9.3 ± 0.3b 6.1 ± 0.3a 110.5 ± 3.76ab
400 MPa,20 min 32.1 ± 1.5a 30.0 ± 1.09a 7.0 ± 0.2ab 6.5 ± 0.1bc 6.5 ± 0.2b 5.1 ± 0.1a 3.6 ± 0.1a 9.5 ± 0.4b 6.2 ± 0.3a 106.5 ± 3.74a
400 MPa,25 min 38.6 ± 1.10c 31.4 ± 1.05ab 7.3 ± 0.4b 6.3 ± 0.2b 6.4 ± 0.1b 5.3 ± 0.1a 3.6 ± 0.1a 9.4 ± 0.5b 6.2 ± 0.3a 114.5 ± 4.66b
500 MPa,5 min 34.7 ± 1.4b 30.8 ± 1.09a 7.2 ± 0.3b 5.4 ± 0.3a 6.4 ± 0.4b 5.2 ± 0.2a 3.5 ± 0.1a 9.6 ± 0.4b 5.8 ± 0.2a 110.6 ± 4.51ab
500 MPa,10 min 35.6 ± 1.1b 32.0 ± 1.12bc 6.6 ± 0.2a 6.1 ± 0.1b 6.6 ± 0.3b 5.4 ± 0.2a 3.6 ± 0.1a 9.5 ± 0.3b 6. ± 0.3a 111.4 ± 2.65ab
500 MPa,15 min 38.8 ± 1.3c 32.3 ± 1.11bc 6.5 ± 0.2a 6.0 ± 0.1b 6.7 ± 0.5b 5.4 ± 0.1a 3.4 ± 0.1a 9.9 ± 0.1bc 5.9 ± 0.2a 114.9 ± 3.74b
500 MPa,20 min 40.8 ± 1.4d 30.3 ± 1.09a 6.5 ± 0.1a 6.3 ± 0.1b 6.6 ± 0.2b 5.2 ± 0.1a 3.5 ± 0.1a 10.1 ± 0.5c 5.8 ± 0.3a 115.1 ± 3.67b
500 MPa,25 min 42.6 ± 1.1de 31.1 ± 1.07b 7.3 ± 0.4b 6.4 ± 0.2bc 6.8 ± 0.2b 5.6 ± 0.3a 3.4 ± 0.1a 9.8 ± 0.3b 6.1 ± 0.3a 119.1 ± 3.65b
600 MPa,5 min 40.0 ± 1.1cd 32.4 ± 1.14bc 7.2 ± 0.3b 5.2 ± 0.1a 6.4 ± 0.1b 5.3 ± 0.3a 3.3 ± 0.1a 10.0 ± 0.3c 6.1 ± 0.2a 115.9 ± 4.43b

c 2011 Society of Chemical Industry

600 MPa,10 min 41.5 ± 1.5d 30.2 ± 1.15a 7.7 ± 0.3b 6.3 ± 0.1b 6.4 ± 0.3b 5.4 ± 0.4a 3.3 ± 0.1a 9.3 ± 0.2b 6.0 ± 0.5a 116.1 ± 3.32b
600 MPa,15 min 42.1 ± 1.6de 31.0 ± 1.11ab 7.1 ± 0.2ab 6.4 ± 0.2bc 6.6 ± 0.1b 5.3 ± 0.2a 3.4 ± 0.1a 9.5 ± 0.4b 6.2 ± 0.4a 117.6 ± 4.61b
600 MPa,20 min 42.3 ± 1.4de 29.9 ± 1.06a 7.2 ± 0.2b 5.9 ± 0.3ab 6.8 ± 0.1b 5.5 ± 0.2a 3.5 ± 0.2a 10.0 ± 0.3c 6.2 ± 0.5a 117.3 ± 3.55b
600 MPa,25 min 41.9 ± 1.1de 30.5 ± 1.05a 7.6 ± 0.4b 6.2 ± 0.1b 6.8 ± 0.2b 5.8 ± 0.1ab 3.4 ± 0.1a 9.8 ± 0.3bc 6.3 ± 0.3a 118.3 ± 3.68b
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a
Data are presented as the means ± standard deviations (n = 6). Values with different letters within one column are significantly different (P ≤ 0.05).

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5 5min; 10min; 15min phenolic compounds in the achenes into pulp during thermal
20min; 25min processing.
4
Effects of HHP on monomeric anthocyanins and polymeric
Equal to g GAE kg-1

color in strawberry pulps

3 As shown in Table 2, the content of Pg-3-glu, Pg-3-rut and Cy-3-
glu in strawberry pulps was 230.9 (71.3%), 57.9 (17.9%) and 37.0
(11.4%) mg kg−1 , respectively. Gössinger et al.33 reported that
2
Pg-3-glu and Cy-3-glu constituted 75.1–76.8% and 3.5–4.5% of
total monomeric anthocyanins in strawberry. Aaby et al.34 found
1 that the most abundant anthocyanins in the strawberries were
Pg-3-glu (400 mg kg−1 ), Cy-3-glu (19.0 mg kg−1 ) and Pg-3-rut
(16.3 mg kg−1 ), which contributed 76.1%, 12.5%, and 3.1% of
0 total monomeric anthocyanins.
rol ing Pa Pa Pa
Cont cess 400M 500M 600M The monomeric anthocyanins and total monomeric antho-
rmal-pro
The cyanins exhibited no significant changes after HHP treatments
regardless of the pressures or treatment times, indicating that
Figure 4. The effects of high hydrostatic pressure on total phenols in
strawberry pulps. the monomeric anthocyanins were well retained after HHP treat-
ments (Table 2). Similar observations were reported in previous
studies. Garcia-Palazon et al.5 reported that Pg-3-glu and Pg-3-rut
Effects of HHP on individual phenolic compounds in red raspberry and strawberry are stable after HHP treatment
other than anthocyanins and total phenols in strawberry pulps at 800 MPa and 18–22 ◦ C for 15 min. Patras et al.12 found no
The effects of HHP and TP on individual phenolic compounds other significant changes in Pg-3-glu and Cy-3-glu in strawberry and
than monomeric anthocyanins in strawberry pulps are shown in blackberry purées after HHP treatment. Gimenez et al.6 found that
Table 1 and total phenols in Fig. 4. The quantity of total phenol Pg-3-glu and Pg-3-rut in HHP-treated strawberry jam are higher
in unprocessed strawberry pulps was equal to 3.22 g kg−1 gallic than those in commercial jams and traditional heat-processed
acid equivalents (GAE), which conformed to a previous study. jam. The highest stability of Pg-3-glu and Pg-3-rut was found
Aaby et al.18 reported that the total phenols of strawberry are in when strawberries were treated at 800 MPa and stored at 4 ◦ C.14
the range of 2.30–3.40 g kg−1 . As compared with unprocessed Kouniaki et al.35 also reported that cyanidin-3-rutinoside in HHP-
pulps, the total phenols decreased significantly in HHP-treated treated blackcurrants at 600 MPa is more stable than unprocessed
strawberry pulps at 400 MPa regardless of the treatment times samples, while the lowest loss of delphinidin-3-rutinoside is at
(Fig. 4); some individual phenols such as catechin also exhibited a 800 MPa and stored at 5 ◦ C. In general, these results showed a
similar trend, decreasing from 41.6 to 31.9–38.6 mg kg−1 . This high stability of the monomeric anthocyanins in strawberry pulps
may be due to higher residual activity of PPO and POD in to HHP treatments. Moreover, the monomeric anthocyanins in
HHP-treated strawberry pulps at 400 MPa, since these enzymes HHP-treated strawberry pulps exhibited an increasing tendency
catalyzed the oxidation of the phenols. POD and PPO are compared with the unprocessed pulps. HHP treatments aided
considered to be the main enzymes responsible for phenol decay the extraction of monomeric anthocyanins from strawberry pulps.
in processed strawberries and their derived foods.30 Strawberry The extractability of colored pigments in food components was
POD and PPO are capable of oxidizing (+)-catechin, inducing (+)- increased at extreme pressures.12 Anthocyanins are located in the
catechin degradation and brown polymer formation.30 However, vacuoles in plants, and HHP processing is known to affect the mem-
HHP treatments at 500 or 600 MPa for 5–25 min showed no branes in vegetable cells, as well as the vacuole membrane, and
significant effect on individual phenols, while total phenols in to enhance cell permeability owing to its aptitude to deprotonate
HHP-treated strawberry pulps significantly increased at 500 or charged groups and disrupt salt bridges and hydrophobic bonds in
600 MPa apart from at 5 min. Patras et al.12 found a 8.3–9.8% cell membranes.36 Thus HHP made the extraction of anthocyanins
increase in the total phenols of strawberry purée after HHP from strawberry pulps more accessible. Recently, an optimization
treatment at 500 or 600 MPa. Corrales et al.31 also reported an of anthocyanin extraction from red grape skins assisted by HHP
increase in the total phenols of grape by-products following HHP was reported by Corrales et al.,37 which demonstrated it to be an
treatment. This increase in total phenols may be related to an effective technology for extraction purposes.
increased extractability of some antioxidant components such as However, the stability of three monomeric anthocyanins was
anthocyanins, amino acids and protein with phenolic hydroxyl significantly different in the case of TP. There was a significant
group after HHP treatment, since the molybdenum (Mo6+ ) and decrease of three monomeric anthocyanins when strawberry
wolfram (W6+ ) were reduced to Mo2+ or W2+ by these oxidizing pulps were subjected to TP, and the total monomeric anthocyanins
substances in the Folin–Ciocalteu method. The total phenols decreased to 254.1 mg kg−1 . Gössinger et al.33 reported that there
in TP-treated strawberry pulps increased to 4.32 g kg−1 and was a 40% degradation of Pg-3-glu in strawberry purée pasteurized
total individual phenols increased from 117.5 to 150.3 mg kg−1 . at 85 ◦ C for 10 min. Sadilova et al.38 showed that Pg-3-glu purified
The result was different from previous studies. Klopotek et al.32 from strawberry considerably decreased after heating at 95 ◦ C,
reported that a 14.1–50% decrease of total phenols occurred in and suggested that the first step in anthocyanin degradation is
strawberry juice, nectar, wine, and purée processed at 85 ◦ C for the opening of the pyrylium ring; de-glycosylation then occurs.
5 min, but Patras et al.12 detected no significant changes in total The cleavage products of Pg-3-glu are phloroglucinaldehyde and
phenols after thermal processing in strawberry purée. In this study, 4-hydroxybenzoic acid, and the former is the substrate of PPO.
the increase of individual phenols and total phenols induced The effects of HHP and TP on the polymeric color in strawberry
882

by thermal processing was possibly due to easier extraction of pulps are shown in Table 2. The PPC in the unprocessed strawberry

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Table 2. Monomeric anthocyanins (mg kg−1 ) and polymeric color in strawberry pulps treated by high hydrostatic pressure and thermal processinga
Total
Treatment conditions Cy-3-glu Pg-3-glu Pg-3-rut monomer PC CD PPC%

Control 37.0 ± 0.5bc 230.9 ± 5.2b 57.9 ± 2.3bc 323.8 ± 7.2b 0.28 ± 0.02ab 1.06 ± 0.02b 26.41 ± 1.24c
Thermal processing 30.7 ± 0.11a 177.7 ± 0.49a 45.7 ± 0.19a 254.1 ± 3.79a 0.31 ± 0.01c 1.06 ± 0.01b 29.25 ± 1.27d
400 MPa, 5 min 39.1 ± 1.5cd 233.4 ± 0.70b 57.9 ± 2.3bc 330.4 ± 1.08bc 0.26 ± 0.01ab 1.11 ± 0.02bcd 23.42 ± 1.17abc
400 MPa, 10 min 39.5 ± 1.3bc 230.6 ± 2.96b 54.4 ± 1.21c 328.1 ± 4.3bc 0.28 ± 0.02ab 1.09 ± 0.01b 25.69 ± 1.04bc
400 MPa, 15 min 35.7 ± 0.8cd 232 ± 3.47b 58.4 ± 1.12c 320.7 ± 4.67bc 0.26 ± 0.01ab 1.00 ± 0.01a 26.00 ± 0.84bc
400 MPa, 20 min 37.1 ± 0.10bcd 233.5 ± 3.39b 57.9 ± 2.10bc 320.5 ± 3.58bc 0.28 ± 0.02b 1.11 ± 0.02bcd 25.23 ± 1.03bc
400 MPa, 25 min 37.2 ± 0.8bc 227.9 ± 2.41b 56.8 ± 1.0bc 321.9 ± 3.59bc 0.26 ± 0.01ab 1.08 ± 0.02b 24.08 ± 0.65abc
500 MPa, 5 min 37.8 ± 1.12bcd 230.1 ± 3.89b 55.3 ± 1.19bc 323.1 ± 3.21bc 0.29 ± 0.02b 1.11 ± 0.02bcd 26.13 ± 1.16c
500 MPa, 10 min 38.9 ± 1.14bcd 234.5 ± 2.87b 56.7 ± 2.17bc 330.0 ± 4.17bc 0.28 ± 0.02b 1.15 ± 0.04f 24.35 ± 1.46bc
500 MPa, 15 min 40.2 ± 1.11d 234.7 ± 2.55b 58.3 ± 0.91c 333.2 ± 3.87bc 0.26 ± 0.01ab 1.15 ± 0.03cd 22.61 ± 0.76abc
500 MPa, 20 min 40.1 ± 2.12d 233.8 ± 3.79b 59.2 ± 1.18c 333.1 ± 4.09bc 0.25 ± 0.01a 1.11 ± 0.04bcd 22.52 ± 0.68ab
500 MPa, 25 min 38.9 ± 1.11bcd 238.1 ± 3.15b 57.5 ± 2.32bc 334.5 ± 5.59bc 0.28 ± 0.01a 1.10 ± 0.06bc 25.45 ± 0.87a
600 MPa, 5 min 37.9 ± 1.12bcd 239.0 ± 2.47b 58.1 ± 1.12bc 335.0 ± 5.71bc 0.26 ± 0.01a 1.07 ± 0.01b 24.30 ± 0.70abc
600 MPa, 10 min 36.3 ± 2.10b 232.5 ± 2.50b 57.0 ± 1.10bc 325.7 ± 4.70bc 0.26 ± 0.01ab 1.08 ± 0.01b 24.07 ± 0.46abc
600 MPa, 15 min 36.8 ± 2.07bc 236.5 ± 3.49b 58.1 ± 1.15bc 330.1 ± 3.72bc 0.28 ± 0.02ab 1.09 ± 0.01b 25.69 ± 1.24bc
600 MPa, 20 min 37.0 ± 1.11bc 238.9 ± 2.46b 56.8 ± 1.20bc 334.0 ± 4.76bc 0.27 ± 0.02ab 1.10 ± 0.01bc 24.55 ± 1.31abc
600 MPa, 25 min 38.6 ± 1.15bcd 239.7 ± 2.40b 58.7 ± 2.39c 337.0 ± 3.95bc 0.26 ± 0.02ab 1.15 ± 0.05bcd 22.61 ± 1.66abc
a Data are presented as the means ± standard deviations (n = 6). Values with different letters within one column are significantly different (P ≤ 0.05).

pulps was 26% in this study. PPC in individual quick-frozen bonds, hydrophobic bonds and ionic bonds.13 Moreover, the
strawberries was 7.2%39 and in blackberries 10.5%.21 It was hydrogen bonds may be destroyed by acidified methanol during
reported that PPC increases from 8.6% in fresh black raspberry the extraction process.
to 21%21 and from 1% in fresh blueberry to 22% in berries canned TP led to a 12.0% increase in PC of strawberry pulps, which was
in water.40 Higher PPC in frozen strawberry in this study was indicative of condensation reactions of anthocyanins with other
possibly due to browning reactions induced by the activity of phenolics to form colored polymer pigments.41 Anthocyanin losses
PPO and POD, as well as condensation reactions of anthocyanins were accompanied by increased PPC in raspberry pulp stored at
with other phenolics during longer freezing and thawing. Larger different temperatures.39
ice crystals in the vacuoles possibly formed compared to shock
freezing with liquid nitrogen, which may partly destroy the
vacuole walls, and enzymes may thus come into contact with Effects of HHP on instrumental color parameters of strawberry
phenolic compounds. This could also create better conditions for pulps
co-pigmentation formation.33 Moreover, condensation reactions The color parameters of strawberry pulps subjected to HHP and
of anthocyanins with other phenolics including flavan-3-ols or TP are shown in Table 3. HHP at 400 MPa induced a significant
polyflavan-3-ols naturally occurred.41 Phenolic acids such as decrease in the L∗ of strawberry pulps regardless of treatment
ferulic and syringic acids have also been shown to complex time, which characterized the presence of the browning reaction
with anthocyanins in strawberry and raspberry juices.41 Natural in strawberry pulps. This was related to higher residual activity
polymeric anthocyanins such as 5-carboxypyranopelargonidin-3- of PPO, POD and β-glucosidase at 400 MPa. The L∗ of strawberry
glucoside were also detected in strawberry.42 However, peaks in pulps at 500 or 600 MPa exhibited no significant reduction. Butz
the HPLC chromatograms indicative of degradation compounds et al.43 observed that HHP induced discoloration in mushrooms
or the formation of pyranoanthocyanins in this study were not and onions because of the residual activity of PPO responsible
observed, which was possibly caused by breakage of hydrogen for browning. The a∗ parameter of strawberry pulps showed no
bonds during elution when detected by HPLC. Another reason change after HHP treatments. Rodrigo et al.36 described a high
was that condensation products between anthocyanins and other retention of strawberry red color after HHP treatment. The b∗
phenolics were of larger molecular weight and were either not parameter did not change at 500 MPa and 600 MPa, and showed
separated on the reverse-phase C18 column or possibly removed a significant increase with increasing HHP treatment time at
by the filtering step prior to HPLC analysis.21 400 MPa apart from at 5 min. Similar to b∗ , H◦ and C ∗ significantly
The CD and PC exhibited no significant difference after HHP increased at 400 MPa apart from at 5 min, while no significant
treatment. An insignificant increase of CD in HHP-treated pulps changes occurred at 500 and 600 MPa. Moreover, higher E (≥5)
was consistent with the change of monomeric anthocyanin. was observed at 400 MPa, whereas lower E (≤3) was attained at
The decrease tendency in PC in HHP-treated strawberry pulps 500 and 600 MPa and reduced with increasing pressure, regardless
was accompanied by an increase tendency in monomeric of treatment times.
anthocyanins. The PC contributed by monomeric anthocyanins TP induced a significant decrease in L∗ , and significant increases
bound to macromolecules such as protein, flavan-3-ols and in the a∗ , b∗ , H◦ and C ∗ of the strawberry pulps. The highest
phenolic acids through hydrogen bonds may be destroyed during E = 10 of the strawberry pulps indicated that a significant
HHP treatment due to the breakage of weak hydrogen bonds, since non-enzymatic browning reaction was present, since PPO and
883

HHP is known to affect non-covalent bonds such as hydrogen POD were totally inactivated during TP. The significant changes in

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 www.soci.org X Cao et al.

Table 3. The color characteristics of strawberry pulps treated by high hydrostatic pressure and thermal processinga

Treatment conditions L∗ a∗ b∗ H◦ C∗ E

Control 30.84 ± 1.02e 25.07 ± 1.01abc 12.84 ± 0.68bc 27.14 ± 1.32bcd 28.17 ± 1.04abc –
Thermal processing 22.18 ± 0.48a 27.89 ± 0.42d 17.40 ± 0.65g 31.95 ± 0.69h 32.87 ± 0.67e 10.18
400 MPa, 5 min 25.36 ± 0.48b 25.38 ± 0.81abc 12.84 ± 0.22bc 26.84 ± 0.61bc 28.45 ± 0.78bc 5.49
400 MPa, 10 min 25.35 ± 1.25b 25.76 ± 0.68 abc 14.61 ± 0.43e 29.57 ± 0.97fg 29.62 ± 0.63cd 5.80
400 MPa, 15 min 26.17 ± 0.39b 25.54 ± 0.51 abc 14.19 ± 0.45de 29.06 ± 0.86def 29.22 ± 0.52cd 4.88
400 MPa, 20 min 25.49 ± 0.96b 25.67 ± 0.61 abc 14.49 ± 0.56e 29.45 ± 1.23efg 29.48 ± 0.54cd 5.63
400 MPa, 25 min 25.69 ± 0.75b 26.18 ± 0.85c 15.62 ± 0.66f 30.75 ± 1.38g 30.49 ± 2.07d 5.95
500 MPa, 5 min 29.43 ± 0.67cd 25.40 ± 0.41abc 13.15 ± 0.35bcd 27.36 ± 0.67cd 28.60 ± 0.42bc 1.48
500 MPa, 10 min 28.06 ± 0.34c 25.96 ± 0.69bc 13.57 ± 0.31bcde 27.61 ± 0.66cde 29.29 ± 0.69cd 3.01
500 MPa, 15 min 28.11 ± 0.67c 25.89 ± 0.86 bc 14.01 ± 0.19cde 28.44 ± 0.51cdef 29.44 ± 0.84cd 3.08
500 MPa, 20 min 28.09 ± 0.34c 25.88 ± 0.65 bc 13.64 ± 0.32bcde 27.64 ± 0.82cde 29.34 ± 0.85cd 3.01
500 MPa, 25 min 28.10 ± 0.68c 25.85 ± 0.88bc 14.68 ± 0.54cde 28.45 ± 0.61cdef 29.45 ± 0.98cd 3.08
600 MPa, 5 min 29.89 ± 1.66d 24.32 ± 1.29a 11.47 ± 0.45a 26.91 ± 1.27ab 26.91 ± 1.27a 1.82
600 MPa, 10 min 28.48 ± 0.66c 24.43 ± 0.78ab 12.44 ± 0.69b 27.42 ± 1.01bc 27.42 ± 1.01ab 2.48
600 MPa, 15 min 29.06 ± 1.21cd 25.52 ± 0.47abc 12.82 ± 0.59bc 28.56 ± 0.62bc 28.56 ± 0.62bc 1.84
600 MPa, 20 min 29.43 ± 0.21cd 24.61 ± 0.20abc 12.26 ± 0.96a 27.08 ± 0.59a 27.08 ± 0.59ab 2.17
600 MPa, 25 min 29.07 ± 0.57cd 25.02 ± 0.65abc 12.58 ± 0.27b 27.99 ± 0.69bc 27.99 ± 0.39abc 1.79
a Data are presented as the means ± standard deviations (n = 6). Values with different letters within one column are significantly different (P ≤ 0.05).

color were due to the breakdown of anthocyanins and formation 5 Garcia-Palazon A, Suthanthangjai W, Kajda P and Zabetakis I, The
of Maillard reaction products by intensive TP. Moreover, there effects of high hydrostatic pressure on β-glucosidase, peroxidase
was a 56.5% loss of ascorbic acid in TP-treated pulps. Skrede and polyphenoloxidase in red raspberry (Rubus idaeus) and
strawberry (Fragaria × ananassa). Food Chem 88:7–10 (2004).
et al.44 also reported that most ascorbic acid in strawberries 6 Gimenez J, Kajda P, Margomenou L, Piggott JR and Zabetakis I, A
was destroyed during TP. Ascorbate degradation could also be study on the color and sensory attributes of high-hydrostatic-
significantly involved in the color changes.45 pressure jams as compared with traditional jams. J Sci Food Agric
81:1228–1234 (2000).
7 Jiang YM, Duan XW, Joyce D, Zhang ZQ and Li JR, Advances in un-
derstanding of enzymatic browning in harvested litchi fruit. Food
CONCLUSION Chem 88:443–446 (2004).
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grapevine (Vitis vinifera) cultivars. Fruit Variety J 49:82–84 (1995).
600 MPa, and it reduced with increasing pressures. 11 Zabetakis I, Leclerc D and Kajda P, The effect of high hydrostatic
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ACKNOWLEDGEMENTS 12 Patras A, Brunton NP, Pieve SD and Butler F, Impact of high pressure
processing on total antioxidant activity, phenolic, ascorbic acid,
This project was supported by the National High-Tech 863 anthocyanin content and color of strawberry and blackberry purées.
Program of China (No. 2007AA100405) and the Scientific Research Innov Food Sci Eng Technol 10:308–313 (2009).
Common Program of Beijing Municipal Commission of Science 13 Cheftel JC, Effect of high hydrostatic pressure on food constituents:
and Technology (No. D10110504660000). an overview, in High-Pressure and Biotechnology, ed. by Balny C,
Hayashi R, Hereman K and Masson P. John Libbey Eurotext, London,
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