effects of high pressure processing on antioxidant activity, and total carotenoid content and...

Technologies xx (2007) xxx–xxx

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INNFOO-00434; No of Pages 6

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Innovative Food Science and Emerging

Effects of high pressure processing on antioxidant activity, and totalcarotenoid content and availability, in vegetables

Jennifer K. McInerney a,c, Cathryn A. Seccafien a,c,Cynthia M. Stewart b,c,1, Anthony R. Bird a,c,⁎

a CSIRO Human Nutrition, Kintore Avenue, Adelaide, South Australia, 5000 Australiab Food Science Australia, PO Box 52, North Ryde NSW 1670, Australia

c CSIRO Food Futures National Research Flagship

Received 14 March 2007; accepted 7 April 2007

Abstract

High pressure processing (HPP) is a relatively new food preservation processing technology that enhances food safety and shelf-life withoutcompromising organoleptic qualities. There has been little research on the impact of HPP on the nutritional and health-promoting properties of foods todate andmost of it has focused on juices and purees of fruit such as oranges and tomatoes. The objective of this studywas to determine the effects of HPPtreatment at two pressure levels (400 MPa; 600 MPa) on antioxidant activity, total carotenoid content and carotenoid availability in vitro, of threecommonly consumed vegetables. Antioxidant capacity and total carotenoid content differed between vegetables but were unaffected by HPP treatment.In vitro availability of specific carotenoids also varied greatly between vegetables (3–35%). HPP altered availability of carotenoids according to the typeof vegetable treated and processing pressure applied, however the magnitude of the responses was minor.© 2007 Elsevier Ltd. All rights reserved.

Keywords: High pressure processing; Antioxidant capacity; Carotenoids; Lutein; Vegetables

Industrial relevance: This study provides further scientific evidence of the benefits of high pressure processing in retaining the nutritionalattributes of fresh foods. Antioxidant activity and levels of carotenoids before and after exposure to high pressures (up to 600 MPa for 2 min) wereessentially no different. Also, the data suggest that micronutrients and phytochemicals in certain vegetables may be made more bioavailable byhigh pressure treatment. From a nutritional perspective, high pressure processing is an attractive food preservation technology and clearly offersopportunities for horticultural and food processing industries to meet the growing demand from consumers for healthier food products.

1. Introduction

Fruits and vegetables are important components of a healthydiet and their intake is widely promoted by government agenciesand health professionalsworldwide.Despitewidespread consumerawareness of the nutritional value of these foods and their role inhealth maintenance, dietary intakes are well below recommendedlevels in Australia (Magarey, Daniels, & Smith, 2001; Mathers,

⁎ Corresponding author. CSIRO Human Nutrition, Kintore Avenue, Adelaide,South Australia, 5000 Australia. Tel.: +61 8303 8902; fax: +61 8 8303 8899.

E-mail address: [email protected] (A.R. Bird).1 Present address: The National Center for Food Safety & Technology, 6502 S.

Archer Rd., Summit-Argo, IL 60501 USA.

1466-8564/$ - see front matter © 2007 Elsevier Ltd. All rights reserved.doi:10.1016/j.ifset.2007.04.005

Please cite this article as: McInerney, J. K. et al. Effects of high pressure procesvegetables. Innovative Food Science and Emerging Technologies (2007), doi:10.1

Vos, Stevenson, & Begg, 2001) and other industrialised countries(van het Hof et al., 1999; Lock, Pomerleau, Causer, Altmann, &McKee, 2005). Indeed, in certain cohorts, fruit and vegetableconsumption appears to have declined in recent years (Magareyet al., 2001).

Population studies demonstrate a strong association betweenincreased consumption of plant foods, or their biologicallyactive components, and reduced risk of major chronic healthproblems, such as cardiovascular disease (Hu, 2003; Scalbert,Johnson, & Saltmarsh, 2005) and certain cancers (Steinmetz &Potter, 1996; Tamimi et al., 2005; Nkondjock, Ghadirian,Johnson, & Krewski, 2005). Dietary patterns comprising greaterproportions of fruit and vegetables also may be useful forcombating the rising prevalence of overweight and obesity

sing on antioxidant activity, and total carotenoid content and availability, in016/j.ifset.2007.04.005

mailto:[email protected]

http://dx.doi.org/10.1016/j.ifset.2007.04.005


2 J.K. McInerney et al. / Innovative Food Science and Emerging Technologies xx (2007) xxx–xxx

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occurring in many countries (Tohill, Seymour, Serdula, Kettel-Kahn, & Rolls, 2004).

Fresh vegetables are rich sources of a wide range of essentialmicronutrients and biologically active phytochemicals, includ-ing carotenoids and polyphenols, many of which have pur-ported health benefits (Kris-Etherton et al., 2002; Tamimi et al.,2005). Evidence is emerging from animal studies thatphytochemicals might offer greater protection against chronicdiseases when acting in combination rather than individually(Canene-Adams, Campbell, Zaripheh, Jeffery, & Erdman, 2005;Lui, 2004).

High pressure processing (HPP) is an innovative, emergingtechnologywith potential for optimising intake of nutrient and non-nutrient phytochemicals in human foods. Retention of organolepticattributes and other characteristics of freshness, combined withincreased convenience and extended shelf life, will no doubtincrease the appeal of foods preserved using HPP to consumers(Deliza, Rosenthal, Abadio, Silva, & Castillo, 2005).

The purpose of this study was to assess the impact of differentHPP regimens on the nutritional value and in vitro antioxidantactivity of a selection of commonly consumed vegetables thatvaried widely in physical or plant matrix characteristics as wellas nutrient composition. Carrots were chosen as they are a staplehard root crop vegetable and have a high carotenoid contentwhereas broccoli was selected because it is a rich source ofhydrophilic antioxidants. Green beans were included owing totheir relatively low carotenoid content and softer texture.

Although nutrients and nonnutrient phytochemicals may bepresent in abundance, this may not necessarily reflect their bio-availability and physiological functionality once consumed. So, inaddition to quantifying concentrations of important phytochemicalsin the three vegetables, we also determined the effect of HPPtreatment on their antioxidant capacity using the ferric reducingantioxidant power (FRAP) assay, and in vitro availability of re-levant carotenoids, as assessed by simulated gastrointestinaldigestion.

2. Materials and methods

2.1. Chemicals

2,4,6-tripyridyl-s-triazine (TPTZ), porcine bile extract, pan-creatin and pepsin were purchased from Sigma Aldrich (St.Louis, MO). All other chemicals and solvents were obtainedfrom BDH (Poole, England).

2.2. Vegetable samples

The vegetables used (carrots, green beans and broccoli) wereeach purchased fresh on three separate occasions from a localsupermarket on the day of processing. Edible portions (N900 g) ofeach vegetable were divided equally into three samples andvacuum packed immediately at Food Science Australia, NorthRyde. Two of the samples were subjected to HPP at either600MPa or 400MPa for 2minwhereas the third sample remaineduntreated. All samples were stored overnight at 1 °C and trans-ported toCSIROHealth Sciences andNutrition inAdelaide on ice


the following day. The samples were then stored at 4 °C untilanalysis, which was within 48 h of arrival. On the day of analysis,samples were finely chopped in a kitchen food processor immedi-ately prior to analysis.

2.3. High pressure treatments

A2-L processing unit (Flow International Corporation, Seattle,WA, USA) was used to pressurize the vacuum packed vegetablesamples to either 400 MPa or 600 MPa for a period of 2 min. Thepressure fluidwaswater. The time to reach the designated pressurewas less than 10 s, and depressurization was less than 5 s. Pres-surization was carried out at ambient temperature.

2.4. Ferric reducing antioxidant power (FRAP) assay

The FRAP value was determined according to the method ofBenzie and Strain (1996) using a Cobas Bio centrifugal analyser(Roche Diagnostics Systems, Branchburg, NJ). Duplicate sam-ples (10 g) were extracted with 15–20 ml of high purity water,and after centrifugation (2000 ×g at 4 °C for 10 min) andappropriate dilution of the supernatant the sample was analysedby the FRAP assay. Briefly,10 ul of sample was added to 300 ulof FRAP reagent and the absorbance at 593 nm recorded after a4 min incubation at 37 °C.The FRAP value was obtained bycomparing the change in absorbance of the test mixture to thatof Fe2+ standard solutions. The results were expressed in umolof Fe2+ equivalents per kg fresh weight (FW).

2.5. Total carotenoid analysis

Extractionswere preformed in conditions of restricted lighting.Duplicate samples were extracted exhaustively with tetrahydro-furan (THF) based on the method described by Bushway (1985)and adapted for use in our laboratory. Ascorbic acid (10 ml of a1% w/v solution) was added to a 5-g sample and thenhomogenised using a Polytron high speed blender (Kinematica,Switzerland) for 1 min. A 10 ml aliquot of MeOH/THF (9:1) wasadded and the sample homogenised for a further 1 min, centri-fuged at 2000 ×g at 4 °C for 10 min, and the supernatant trans-ferred to a 100-ml volumetric flask. The extraction procedure wasrepeated with 10 ml volumes of THF until no further colour wasextracted. The combined supernatants were made to volume withTHF.Aliquots (2ml) were back extractedwith an equal volume ofhexane following the addition of 200 ul NaCl (10% w/v,aqueous). The hexane was evaporated to dryness under a streamof nitrogen and stored at−20 °C. Samples were reconstitutedwithmobile phase immediately prior to analysis by HPLC. Carote-noids were separated on a Microsorb-MV 100-5 C18 column(250 mm×4.6 mm; Varian) using a Shimadzu SCL 10A liquidchromatograph equipped with a SPD-M10Avp photodiode arraydetector and refrigerated sample compartment (Shimadzu SIL10A, Shimadzu Corporation, Kyoto, Japan). The mobile phaseconsisted of acetonitrile (55%), methanol (22%), dichloro-methane (11.5%) and hexane (11.5%). Ammonium acetate wasadded at 0.02% to stabilise carotenoids. Flow rate was 1 ml/min.Carotenoids were detected at 450 nm and 472 nm and



Table 2Effect of high pressure processing on total carotenoids (ug/g veg (fresh weight))in vegetables1

Pressure(MPa)

Carrots Green beans Broccoli

α Carotene β Carotene Lutein Lutein β Carotene

0 28.5±1.57 57.7±5.7 8.95±2.30 9.62±1.34 6.02±0.89400 28.2±2.09 57.9±5.50 8.78±1.92 9.74±1.77 5.70±1.01600 28.5±1.84 57.1±5.70 8.93±2.07 8.65±1.41 5.03±0.811Values are means±standard error, n=3 for green beans and broccoli, n=4 forcarrots. There were no significant differences between treatments.

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identification achieved by comparing sample retention times andvisible spectra with those for α- and β-carotene and lutein. Forgreen beans and broccoli, saponification with methanolic KOH(2 h at room temperature) was necessary in order to maximisecarotenoid extraction. Carotenoid content was expressed as ug/gFW.

2.6. Carotenoid availability

Samples were subjected to simulated human gastric and pan-creatic digestion based on the method described by Miller,Schricker, Rasmussen, and Van Campen (1981), with modifica-tions to optimise carotenoid availability as described by Garrett,Failla and Sarama (1999). Briefly, to 1 g of finely chopped vege-table sample was added 200 ul ascorbic acid (150 mM) and 9.8 mlsaline (0.9%) and the pH adjusted to 2.0 with 5 M HCl. One ml ofpepsin solution (20 mg/ml in 0.1 M HCl) was then added and thesample tubes filled with nitrogen and incubated at 37 °C for 60minwith gentle shaking. The pHwas then adjusted to about 5 with 1MNaHCO3 followed by the addition of bile/pancreatin solution (3ml,containing 50 mg pancreatin and 300 mg bile in 35 ml 0.1 MNaHCO3). The pH was adjusted to 7.0 and the sample tubes werefilled with nitrogen and incubated as before for 2 h.

A 15ml-portion of the final digest was centrifuged at 2000 ×gfor 10 min and 2-ml aliquots of the supernatant back extractedinto hexane and evaporated to dryness under nitrogen. Theresidue was dissolved in mobile phase, as described previously,for analysis by HPLC.

Carotenoid availability was expressed as a proportion (%) ofthemaximum amount of carotenoid present in the original sample.

2.7. Statistics

The data are presented as means±SE of 3 observations,unless stated otherwise. Average values of duplicate determina-tions of biochemical and physiological variables were used instatistical analyses. A two-way analysis of variance (ANOVA)was performed using the General Linear Models (GLM) featureof SAS software (version 9.1, Statistical Analytical SystemsInstitute, Cary, NC, USA). The model included processingtreatment (0, 400 and 600 MPa) and day of purchase of eachvegetable (block) as sources of variation. When significantvalues were detected for treatment (F value Pb0.05), differ-ences between individual means were then analysed using theprotected difference option (PDIFF) of SAS. Differences wereconsidered significant at Pb0.05.

Table 1Effect of high pressure processing on antioxidant activity (FRAP values expressedas umol Fe2+/kg veg (fresh weight))1 in vegetable extracts

Pressure (MPa) Carrots2 Green Beans2 Broccoli2

0 571±129a 612±60a 3850±305400 451±140b 768±45b 3260±72600 586±180a 1180±46b 3570±2701 Values are means±standard error, n=3.2 Values in the same row that are followed by a different letter are significantlydifferent (pb0.05).


3. Results

3.1. Effect of HPP on the hydrophilic antioxidant activity asdetermined by the FRAP assay

The hydrophilic antioxidant activity of unprocessed broccoliwas substantially higher than that of carrots and green beans(both Pb0.001). High pressure treatment had differentialeffects on water soluble antioxidant activity depending onvegetable type (Table 1). For broccoli HPP had no effect onantioxidant activity. For carrots there was a modest reduction inantioxidant activity at the lower pressure level (400 MPa),whereas for green beans, water soluble antioxidant activity wasincreased by pressure treatment at both levels (400 & 600 MPa).The between-sample coefficient of variation was noticeablylarger for carrots compared to beans and broccoli.

3.2. Effect of HPP on the total carotenoid levels in vegetables

Of the three vegetables investigated, carrots contained the high-est level of carotenoids, averaging 28 and 58 ug/g FW forα- andβ-carotene, respectively (Table 2). Indeed, the β-carotene level inbroccoli was almost 10-fold less than that found in carrot. Greenbeans and broccoli had comparable concentrations of lutein.

There was no effect of HPP on levels of carotenoids incarrots and green beans (Table 2). Lutein and β-carotene arequantitatively the major carotenoids present in broccoli. Therewas no effect of either pressure treatment (400 or 600 MPa for

Fig. 1. Effect of high pressure processing on carotenoid availability followingsimulated gastrointestinal digestion.




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2 min) on the amount of lutein or β-carotene extracted frombroccoli (Table 2).

3.3. Effect of HPP in carotenoid availability following invitro digestion

The effects of HPP on carotenoid availability in vitro arepresented in Fig. 1. More than 60% of carotenoids in carrots,beans and broccoli remain undigested and, presumably, wouldbe unavailable for absorption in the small bowel. Carrot notonly had the highest concentration of carotenoids (Table 2) butthese were also more readily available than those present in theother vegetables (Fig. 1). Approximately 30% of both α- and β-carotene in carrot was potentially available for intestinal uptake.For green beans, and broccoli in particular, very little of thecarotenoids present was digested in vitro (≤14 and 6%, respec-tively). High pressure treatment had no effect on carotenoidavailability of carrots. Lutein bioavailability in green beans wasincreased by pressure treatment at 600 MPa (Pb0.05) whereasin broccoli β-carotene availability was reduced by pressureprocessing at both 400 or 600 MPa, 2 min.

4. Discussion

4.1. Effect of HPP on the hydrophilic antioxidant activity asdetermined by the FRAP assay

Free radical-induced oxidative damage is strongly implicated inthe development of a number of common chronic disease states(Gutteridge & Halliwell, 2000; Diplock et al., 1998; Halliwell,1997; Ames, Gold, &Willet, 1995) andmany of the health benefitsassociated with consumption of vegetables and fruits have beenlinked to their potent antioxidant properties (Halliwell, Rafter, &Jenner, 2005). For the three vegetables investigated in this study,high pressure treatment essentially preserved their hydrophilicantioxidant capacity as measured in vitro. The lack of an effect ofHPP on antioxidant activity is consistent with the findings of otherstudies (Fernandez Garcia, Butz, & Tauscher, 2001; Butz et al.,2003; Butz et al., 2002; Sanchez-Moreno, Plaza, De Ancos, &Cano, 2003). In the case of green beans, brief exposure to highhydrostatic pressures actually increased their antioxidant activity(see Table 1). It is possible that changes to the tissuematrix inducedby high hydrostatic pressures, for example disruption of plant cellwalls, resulted in the release into the extracellular environment ofcompounds with antioxidant actions. That HPP increased thefraction of lutein released by simulated gastric and pancreaticdigestion is consistent with this notion (see later).

The FRAP assay, as developed by Benzie and Strain (1996), isbased on a different chemical (redox) reaction for measuringantioxidant capacity to that employed by more direct methods,such as the ORAC (oxygen radical absorbance capacity) andTEAC (trolox equivalent antioxidant capacity) assays. The FRAPassay, due to its low cost, speed and technical simplicity, is auseful tool for estimating total reducing/antioxidant power ofaqueous vegetable extracts. It has been shown to yield valueswhich correlate closely to those obtained by the TEAC assay for arange of fruits and vegetables (Pellegrini et al., 2003; Proteggente


et al., 2002) and the ORAC assay for some vegetables, includingcarrots and broccoli (Ou, Huang, Hampsch-Woodill, Flanlgan, &Deemer, 2002), and fruits (Aaby, Skrede, & Wrolstad, 2005).However, the limitations of using a simple in vitro assay system topredict the complex in vivo functionality of antioxidant rich foodsmust be acknowledged (Collins, 2005).

4.2. Effect of HPP on the total carotenoid levels in vegetables

High pressure treatment of foods in not expected to have anadverse effect on low molecular weight components, such asflavouring agents, pigments and vitamins, because covalentbonds are not disrupted by the level of pressure that is normallyused (Tauscher, 1995). Research on the effects of high pressuretreatment on carotenoids in fruits and vegetables has focussed ontomatoes and tomato products, orange juice and persimmons(Fernandez Garcia et al., 2001; de Ancos, Gonzalez, & Cano,2000; Krebbers et al., 2003; Butz et al., 2002). There are no knownreports of HPP having detrimental effects on concentrations ofindividual or total carotenoids in vegetables or fruits, althoughsome studies found an increase in total carotenoid concentrationafter high pressure treatment (Sanchez-Moreno et al., 2003).

Carrots are a major dietary source of carotenoids and of thecommon fruits and vegetables in developed countries, they are alsothe richest source ofβ-carotene. A prominent role of carotenoids inthe human diet is their ability to serve as a precursor of vitamin A,and of these β-carotene possesses the greatest provitamin Aactivity. In the present study, levels of the most abundant individualcarotenoids present in carrots, green beans and broccoli wereunaffected by high pressure treatment, regardless of the pressurelevel that was employed. Indeed, the magnitude of the difference intotal carotenoid content between the different types of vegetableswas markedly greater than differences between treatments. In thisstudy the total carotenoid concentration in carrots was between 5and 10-fold greater than that of green beans and broccoli.

4.3. Effect of HPP on the carotenoid availability following asimulated gastrointestinal digest

As this and other studies have demonstrated, HPP of vegetableshas little influence on their in vitro antioxidant activity and contentof carotenoids. However, exposure of plant foods to highhydrostatic pressures has been shown to alter plantmatrix structures(Tauscher, 1995) which may impact on the nutritional propertiesand possible protective effects of the food once processed.

Simulated gastric and pancreatic digestion of the threevegetables chosen for the study shows that they differ markedlyin carotenoid availability. More than 26% of the carotenoids incarrots was released by in vitro digestion, and presumably,potentially available for absorption in vivo, whereas very little(b6%) of the total carotenoid content of broccoli was. The presentfindings agree with those from a previous study in men whichhad shown that carotenoids from carrots were more bioavailablethan those from broccoli (Micozzi et al., 1992). Generally, thebioavailability of carotenoids in vegetables and other plant foodsis low (Erdman, 1999). High pressure treatments had very littleimpact on the availability of carotenoids from either carrots or



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broccoli. However, processing green beans at a pressure of600 MPa resulted in a significant increase in lutein availabilitycompared to untreated samples or those processed at the lowerpressure level (400 MPa). Disruption of cellular structures inbeans by exposure to high pressures might have facilitated therelease of lutein within the plant tissue matrix during the in vitrodigestion process. Carrots and broccoli, being substantially firmervegetables than green beans, perhaps require higher processingpressures in order to improve bioavailability of their bioactiveconstituents. It must be acknowledged that the magnitude of thedifference in lutein availability in beans before and after highpressure processing was small. From a human health standpoint,the effect of HPP on lutein bioavailability would be consideredminimal. In addition to food matrix properties, various extrinsicfactors including interactions with other carotenoids as well asdietary components, especially lipids and nonstarch polysacchar-ides, also have a major influence on carotenoid bioavailability(Brown et al., 2004; Castenmiller, West, Linssen, van het Hof, &Voragen, 1999; van het Hof,West,Weststrate, & Hautvast., 2000;Horvitz, Simon, & Tanumihardjo, 2004; Yeum & Russell, 2002).

As with all models of human gastrointestinal digestion, carefulinterpretation of study findings is warranted. A critical factorinfluencing the performance of in vitro digestion assays is samplepreparation, especially particle size (Butz et al., 2002). However,uniform assay conditions were maintained throughout the presentexperiment and therefore the relative differences in carotenoidavailability in vitro between the different vegetables or treatmentregimens that were observed are likely to reflect the in vivosituation.

In conclusion, carotenoid content and total antioxidant activityof commonly consumed vegetables was not influenced greatly byhigh pressure treatment, which is consistent with findings ofprevious studies demonstrating that HPP retains micronutrient andphytochemical properties of fresh plant foods. The present studyalso suggests that HPP may be of benefit for improving bio-availability of certain vegetable carotenoids, as is suggested byincreased in vitro availability of lutein in green beans followingHPP. In this particular case the effect is unlikely to equate to ameaningful increase in lutein consumption owing to the relativelylow lutein content of green beans. However, it suggests that thebioavailability of micronutrients and phytochemicals in certainfresh plant foods may be amenable to HPP and that application ofthis novel technology to foods rich in these bioactive agents mayprove useful for developing healthier food products for consumers.

Acknowledgements

We thank Vicki Eggleston, Barbara Stephens and DimitriaGoicoechea, Food Science Australia, North Ryde, Australia, fortheir assistance with vegetable preparation and high pressureprocessing of the samples.

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effects of high pressure processing on antioxidant activity, and total carotenoid content and...

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