Quality attributes of Pleurotus eryngii following gamma irradiation

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Postharvest Biology and Technology 66 (2012) 42–47

Contents lists available at SciVerse ScienceDirect

Postharvest Biology and Technology

journa l h o me pa g e: www.elsev ier .com/ locate /postharvbio

uality attributes of Pleurotus eryngii following gamma irradiation

ashif Akrama, Jae-Jun Ahna, Sung-Ran Yoonb, Gui-Ran Kima, Joong-Ho Kwona,∗

Department of Food Science & Technology & Food and Biotechnology Research Institute, Kyungpook National University, Daegu 702-701, Republic of KoreaDaegu Technopark, BioHealth Convergence Center, Daegu 704-801, Republic of Korea

r t i c l e i n f o

rticle history:eceived 12 August 2011ccepted 4 December 2011

eywords:ushroom

rradiationuality

a b s t r a c t

Quality attributes (appearance, color, texture, weight, and volatile compounds) of irradiated (0, 1, 2, and 3)king oyster (Pleurotus eryngii) mushrooms, packed in polystyrene trays and covered with polyvinylchlo-ride (PVC) film, were evaluated over a storage period of 4 weeks at 5 ± 1 ◦C. Hunter L values (lightness)increased upon irradiation and remained high throughout the storage period in 1 kGy-irradiated sam-ples, whereas a values showed a slight decrease, and b values exhibited an increasing trend followingirradiation. Mushroom texture decreased in firmness with increasing dose, but 1 kGy-irradiated samplesmaintained an overall better texture than all other samples. A similar trend was observed for weight

olorexture analysis-nose analysis

loss during storage. The control samples developed mold, whereas 3 kGy-irradiated mushrooms weresoft at the 3rd week of storage. Scanning electron microscopy showed micro-structural changes in theirradiated samples, which were probably the cause for increased weight loss and poor texture at the high3 kGy dose. A principal component analysis of E-nose data showed dose-dependent differences in volatileprofiles of all samples. Irradiation at 1 kGy was most effective for the extension of postharvest storage

with added advantages.

. Introduction

Mushrooms are extensively used as health food internationallyCheung, 2008), and Pleurotus spp. is ranked third in world mush-oom production (Royse, 2003). Different reports have establishedhat Pleurotus eryngii (king oyster mushroom) is enriched in variousunctional compounds and has higher consumer demand in manyountries (Estrada, 2008; Lo, 2008; Oke and Aslim, 2011). However,ushrooms are very perishable, with a high initial microbial load

nd require effective postharvest technology for safe consumptionnd efficient marketing (Akram and Kwon, 2010).

With the popularity of minimally processed fresh fruit andegetables (Alzamora et al., 2000), different techniques, such asodified atmosphere packaging (Saray et al., 1994; Gonzalez-

andos et al., 2001; Jacxsens et al., 2001) and chemical treatmentsSapers et al., 1994; Brennan et al., 2000) have been tried for various

ushrooms to cope with different challenges such as high micro-ial load, short shelf-life, and overall poor quality (Koorapati et al.,004). Amodio et al. (2003) reported that sliced P. eryngii can main-ain optimum quality characteristics for 3 weeks under controlledtmosphere storage.

The application of improved postharvest technologies such asood irradiation can enhance marketability with increased stor-ge life, and this technology is now widely commercialized. The

∗ Corresponding author. Tel.: +82 53 950 5775; fax: +82 53 950 6772.E-mail address: [email protected] (J.-H. Kwon).

925-5214/$ – see front matter © 2011 Elsevier B.V. All rights reserved.oi:10.1016/j.postharvbio.2011.12.001

© 2011 Elsevier B.V. All rights reserved.

technological applicability and nutritional safety of irradiated foodhas been well studied (Farkas and Mohácsi-Farkas, 2011) and safetyof this technology has been endorsed by major health authori-ties (WHO, 1981, 1999). Low dose irradiation for fresh producecan confer hygienic safety and effect different physiological pro-cesses (enzyme activity and respiration), which result in substantialimprovement in postharvest storage life (Arvanitoyannis, 2010).Considering the effectiveness of this technology, many countrieshave permitted the use of irradiation for fresh (1–3 kGy) and dried(1–10 kGy) mushrooms, aimed at different technological objectives(Akram and Kwon, 2010). Various studies have evaluated the effec-tiveness of irradiation to improve mushroom quality and shelf-life,particularly of Agaricus bisporus (Byun et al., 1990; Beaulieu et al.,2002; Akram and Kwon, 2010) and Lentinus edodes (Jiang et al.,2010). However, to the best of our knowledge, no study has shownthe effect of irradiation on the quality characteristics of P. eryngii.

The objective of this study was to investigate the effect ofgamma irradiation on different quality attributes, such as color,texture, weight loss and volatile profiles of P. eryngii. Scanningelectron microscopy (SEM) was also conducted to evaluate themicro-structural changes in mushrooms following irradiation.

2. Materials and methods

2.1. Mushroom samples

Fresh king oyster (P. eryngii) mushrooms, cultivated in awell-controlled environment and harvested when fully mature

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mushroom cap and margins flat), were purchased from a localushroom farm in Daegu, South Korea. The mushrooms were

uickly pre-cooled to 4 ◦C in a refrigerator on site. Samplesf good commercial quality (uniform color and free of blem-shes) were transferred to the laboratory, packed in polystyrenerays and wrapped with food grade PVC film (oxygen per-

eability: 20,000 cm3/m2/24 h; water–vapour transmission rate00 g/m2/24 h). 48 packs (each 300 ± 10 g) were used for each treat-ent.

.2. Irradiation, and storage

The following day, the mushroom samples were irradiated (0,, 2, and 3 kGy) using a Co-60 gamma-ray source (AECL, IR-79,DS Nordion International Co. Ltd., Ottawa, ON, Canada) at the

orean Atomic Energy Research Institute in Jeongeup, Korea, atoom temperature with a dose rate of 2.1 kGy/h. Absorbed dosesere confirmed by alanine dosimeters with a diameter of 5 mm

Bruker Instruments, Rheinstetten, Germany), and the free-radicalignals were analyzed using a Bruker EMS 104 EPR analyzer (Brukernstruments). All samples were stored at 5 ± 1 ◦C for 4 weeks. After2 h and then weekly, samples were randomly selected in triplicaterom each treatment group and analyzed.

.3. Color evaluation during storage

The stem and cap surface color changes of control and treatedamples were measured using a chromameter (Model CR-200,inolta Camera Co., Osaka, Japan). L* representing lightness,

* redness to greenness, and b* yellowness to blueness wereecorded for each sample (n = 9). The total color difference (�E)alues with respect to a control group were also calculated√

�L2 + �a2 + �b2).

.4. Textural changes and weight loss during storage

Textural changes in the control and irradiated samples duringtorage were evaluated using a Sun rheometer (Compac-100, Suncientific Co., Ltd., Tokyo, Japan) provided with blade geometry

able 1olor changes in the stem region of gamma-irradiated Pleurotus eryngii during storage.

Hunter parametera Storage (day) Irradiation dose (kGy)

0

L* 0 92.28 ± 1.47 ax

7 91.12 ± 1.70 abwx

14 89.66 ± 2.45 bx

21 86.46 ± 2.17 cx

28 84.70 ± 3.06 cx

a* 0 −0.76 ± 0.17 aw

7 −0.87 ± 0.13 abw

14 −0.96 ± 0.24 abx

21 −1.1 ± 0.12 bx

28 −1.1 ± 0.21 bx

b* 0 8.75 ± 1.22 bw

7 8.77 ± 0.57 bx

14 9.04 ± 0.45 bx

21 9.15 ± 0.92 by

28 11.38 ± 0.79 ay

�E 0 0.00 ± 0.00 dx

7 1.16 ± 0.63 dw

14 2.79 ± 1.46 cx

21 5.42 ± 1.15 bx

28 7.82 ± 1.28 axy

ean values (n = 9) within the same column with different letters (a–e) are significantly dean values (n = 9) within the same row with different letters (w–z) are significantly diffa L* represents lightness, a* redness to greenness, b* yellowness to blueness and �E to

d Technology 66 (2012) 42–47 43

(no. 10). Samples were penetrated to a 10 mm depth at a speed of2.0 mm/s. Data were recorded with the Rheology data system (ver-sion 1.0) software. Weight loss was investigated by weighing themushrooms weekly during the storage period. Results are reportedas percentage weight loss with respect to the initial weight.

2.5. Scanning electron microscopy

Small pieces of the mushroom stem surface, cap surface, andcentral (internal) tissue were prepared with a surgical blade. Afterfreeze-drying (Bondiro, Ilsin Bio Base, Yangju, Kyunggido, Korea),the samples were prepared (gold-coated) using a Struers Discotom-2 (Struers Co., Willich, Germany) sample preparation unit. Thesamples were viewed in a Hitachi scanning electron microscope(Model S-570, Tokyo, Japan) at 15 kV and 400× magnifications.Three samples were prepared for each treatment and the controls.

2.6. Evaluation of sensory properties and volatile compounds

Sensory evaluation was conducted by graduate students (10panelists) from the Department Food Science and Technology,Kyungpook National University, Korea. The samples were scoredusing a 5-point hedonic scale (5 = like very much; 1 = dislike verymuch for odor and overall acceptability).

A zNose (Electronic Sensor Technology, Newbury Park, CA,USA), equipped with a surface acoustic wave (SAW) sensor andVaporPrintTM (Misrosense 4.88) software, was used to evaluatechanges in volatile compounds. A 2 g sample was added to a 40 mLvial (Supelco, Bellefonte, PA, USA) fitted with a Teflon septum(PTFE/silicone septa, Supelco), sealed, and placed at room tem-perature for 4 h to obtain headspace equilibrium. The equipment

was operated at a SAW sensor temperature of 30 ◦C; column, 60 ◦C;valve, 120 ◦C; inlet, 150 ◦C; and trap, 220 ◦C. Principal componentanalysis (PCA) was used to identify the trends in the numerical data(Keshri et al., 2003).

1 2 3

93.54 ± 1.06 awx 94.36 ± 1.07 aw 91.94 ± 1.50 ax92.52 ± 1.03 aw 90.07 ± 1.76 bw 88.31 ± 1.48 bx92.18 ± 1.41 aw 88.4 ± 1.46 cx 75.3 ± 2.97 cy90.21 ± 0.94 bw 88.26 ± 2.16 dx 74.1 ± 2.32 dy88.10 ± 2.63 bw 84.81 ± 2.39 dx 68.98 ± 2.28 ey

−0.87 ± 0.26 aw −1.04 ± 0.14 abx −1.25 ± 0.32 bcy−1.02 ± 0.21 abw −1.36 ± 0.13 cx −1.33 ± 0.28 cx−1.05 ± 0.23 abx −1.31 ± 0.409 cy −0.58 ± 1.01 abw−1.19 ± 0.27 bx −1.14 ± 0.32 bx −0.49 ± 1.16 aw−1.1 ± 0.17 bx −0.92 ± 0.37 ax 0.10 ± 0.77 aw

8.90 ± 1.06 cw 9.38 ± 1.41 cw 9.46 ± 1.66 cw10.05 ± 0.92 cw 9.28 ± 1.25 cwx 8.62 ± 1.09 cx11.65 ± 0.79 bx 10.57 ± 1.07 cx 15.16 ± 1.45 bw12.89 ± 0.87 abx 13.5 ± 0.83 bx 15.91 ± 2.04 bw13.94 ± 1.21 ax 15.72 ± 1.91 ax 23.47 ± 3.75 aw

1.27 ± 1.52 dwx 2.19 ± 0.72 dw 0.88 ± 0.76 dx1.33 ± 0.78 cdw 1.26 ± 0.70 dw 4.00 ± 5.30 dw2.92 ± 1.10 bcx 3.45 ± 1.27 cx 13.62 ± 3.59 cw4.32 ± 1.04 bx 6.23 ± 1.46 bx 19.73 ± 3.30 bw5.52 ± 2.08 ay 8.86 ± 2.27 ax 27.57 ± 3.09 aw

ifferent at � < 0.05.erent at � < 0.05.tal difference with respect to a control group.

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44 K. Akram et al. / Postharvest Biology and Technology 66 (2012) 42–47

Table 2Color changes in the cap region of gamma-irradiated Pleurotus eryngii during storage.

Hunter parametera Storage (day) Irradiation dose (kGy)

0 1 2 3

L* 0 68.20 ± 1.06 bx 69.06 ± 1.40 bx 70.76 ± 1.92 awx 72.37 ± 1.71 aw7 69.83 ± 2.19 abw 71.33 ± 1.56 aw 70.17 ± 2.20 abw 67.17 ± 2.45 bx

14 71.83 ± 1.89 aw 71.28 ± 1.07 awx 70.28 ± 2.56 abx 64.25 ± 2.94 cy21 70.00 ± 1.89 abx 72.77 ± 1.47 aw 70.45 ± 1.49 abx 60.54 ± 3.25 dy28 69.10 ± 2.12 abx 71.91 ± 1.81 aw 71.55 ± 2.65 bx 53.04 ± 4.41 ey

a* 0 3.15 ± 0.34 bcy 3.85 ± 0.25abw 3.62 ± 0.34 ax 3.17 ± 0.26 cy7 3.12 ± 0.29 cx 3.52 ± 0.48 bwx 3.96 ± 1.37 aw 3.46 ± 0.312 cwx

14 3.41 ± 0.37 ay 3.39 ± 0.20 by 4.16 ± 0.20 ax 5.33 ± 0.42 bw21 3.36 ± 0.35 aby 4.25 ± 0.24 ax 4.30 ± 0.43 ax 5.64 ± 1.10 bw28 3.47 ± 0.47 ay 4.34 ± 0.38 ax 4.35 ± 0.58 ax 7.23 ± 1.05 aw

b* 0 12.5 ± 0.59 cx 14.45 ± 0.55 dw 14.62 ± 0.65 dw 14.75 ± 0.51 cw7 12.9 ± 0.38 cz 15.08 ± 0.89 cw 16.37 ± 0.92 cx 17.12 ± 0.70 cy

14 14.97 ± 0.67 by 17.47 ± 1.22 cx 19.46 ± 2.53 bw 18.43 ± 4.47 bx21 15.85 ± 1.73 bx 19.85 ± 1.95 bw 20.05 ± 2.56 abw 19.62 ± 4.46 bw28 16.32 ± 2.16 ay 20.97 ± 1.59 ax 20.85 ± 2.50 ax 23.43 ± 4.65 aw

�E 0 0.00 ± 0.00 abw 2.24 ± 1.70 cw 3.36 ± 1.72 cw 4.74 ± 1.47 dw7 1.68 ± 1.37 by 5.59 ± 1.16 bw 4.42 ± 1.64 bwx 2.80 ± 0.80 dx

14 4.40 ± 1.53 ay 5.85 ± 0.93 bx 7.33 ± 1.23 aw 7.45 ± 1.26 cw21 3.33 ± 1.45 aby 8.73 ± 0.75 ax 7.76 ± 0.84 ax 10.75 ± 1.71 bw28 3.94 ± 1.24 ay 9.33 ± 1.36 ax 8.45 ± 0.79 ax 19.13 ± 2.30 aw

M antly dM ly diff

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ean values (n = 9) within the same column with different letters (a–e) are significean values (n = 9) within the same row with different letters (w–z) are significanta L* represents lightness, a* redness to greenness, b* yellowness to blueness and

.7. Statistical analysis

All experiments were conducted at least in triplicate and theata analysis was performed using Origin 6.0 (Microcal Software

nc., Northampton, MA, USA) and the SAS program (version 9.1, SASnstitute, Cary, NC, USA). Differences between the variables wereeported using one way analysis of variance. Duncan’s multipleange test (p < 0.05) was used to compare the mean values.

. Results and discussion

.1. Color changes during storage

The color measurements were obtained on a weekly basis over

period of 4 weeks. Color changes in stem and cap parts are givenn Tables 1 and 2. In the stem region (Table 1), hunter L valueslightness) increased following irradiation in 1 and 2 kGy-irradiatedamples, and a high L value was observed throughout the storage

Fig. 1. Physical appearance of Pleurotus eryngii after gamm

ifferent at � < 0.05.erent at � < 0.05.tal difference with respect to a control group.

period in 1 kGy-irradiated samples. The most drastic changesoccurred in 3 kGy-irradiated samples, and the effect was clearerat the end of storage. A decrease in a values was observed but lit-tle effect was found on b values. At the end of storage, a valueswere similar for the control and 1 kGy-irradiated samples; how-ever, a clear difference was found in samples treated with 3 kGy ofirradiation.

The effect of irradiation was clearer in the colored part (cap)of the mushroom (Table 2). In the cap region, L values slightlyincreased with irradiation, whereas significant changes wereobvious in a- and b-values during storage. Koorapati et al. (2004),studying gamma-irradiated slices of A. bisporus, found that 1 kGy-irradiated samples had higher L values but higher doses (3.1 and5.2 kGy) were inappropriate to preserve color attributes. Color

deterioration in the non-irradiated samples might be due tophysiological changes during the postharvest storage period alongwith microbial action, such as Pseudomonas, the most commonbacterial genus on fresh mushrooms (Simón et al., 2005).

a irradiation (0 d; above) and storage (28 d; below).

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rradiation can effect physiological processes in living systemss well as eliminate microbial populations (Rivera et al., 2011),ut at high doses, irradiation can also produce drastic changes inigmented cells (Moreno et al., 2007). The breakage of membranetructures following irradiation results in watery exudates, asbserved in 3 kGy-irradiated samples (Fig. 1), and this can alsoffect the color properties of irradiated mushrooms.

.2. Physical appearance, textural changes, and weight lossuring storage

No significant difference in physical appearance of any of theamples with respect to the controls was observed following irra-iation (Fig. 1). The 1 kGy-irradiated sample provided the mostromising results, with the best physical appearance (uniform colorith no fungus spoilage and blemishes) at the end of the stor-

ge period. However, 3 kGy-irradiated samples developed wateryxudates, and the non-irradiated samples developed mold at thehird week of storage. Microbial spoilage of the non-irradiated A.isporus slices at the ninth day of storage has also been reportedy Koorapati et al. (2004). Texture is a key quality attributeegarding consumer acceptance of fresh mushrooms (Jiang et al.,010). Gamma-irradiation induced dose-dependent softening inhe mushroom samples (Fig. 2A). All samples softened with thencreasing storage time. The firmness of 1 kGy-irradiated samplesnderwent the least change over the 28 d storage period. The 2 kGy-

rradiated mushrooms were softer at the start but showed similarrends as those of the non-irradiated samples during storage. Atrong softening effect was observed in the 3 kGy-irradiated sam-les. Softening in the non-irradiated samples may be attributed toatural enzymatic breakdown and action of microorganisms duringtorage (Zivanovic et al., 2000). Irradiation can address this problemByun et al., 1990), as 1 kGy-irradiated samples maintained goodrmness over the 28 d storage period. However, at higher doses3 kGy), irradiation induced a drastic effect on sample firmness,nd water exudates were observed at the sample surface due toegradation of structural components. Chitin, the major structuralonstituent of mushrooms, can be depolymerized following irradi-tion (Koorapati et al., 2004). The effect on cell membrane integritylso results in the loss of cell turgidity and overall decreased prod-ct firmness (Beaulieu et al., 2002).

Weight loss was observed in all samples during storage (Fig. 2B).rradiation can alter different physiological processes affecting res-iration rate and water loss (Gautam et al., 1998; Benoit et al., 2000;ivera et al., 2011). This effect was clear in 1 kGy-irradiated sam-les, which had the least weight loss during storage. Weight lossesere high at higher doses (2 and 3 kGy), which might be due to

he irradiation effect on membrane structures and leakage of cellater into intercellular spaces. The physical appearance of 3 kGy-

rradiated mushrooms (Fig. 1), with excess water on the outerurface (watery exudates), at the end of the storage period alsoupported this observation. Our results are consistent with those ofivera et al. (2011) in which watery exudates, weight loss and softexture were observed in 2.5 kGy-irradiated Tuber melanosporumruffles.

.3. Scanning electron microscopy

Ultra-structural examination of the mushrooms provided valu-ble information for understanding radiation-induced physicalhanges. Three kinds of mushroom tissue samples (stem sur-ace, cap surface, and central tissue) were examined. Fig. 3 shows

hat all irradiated samples developed enlarged intercellular spacesepending upon the applied dose, and the results were moreronounced in 3 kGy-irradiated samples. At higher doses, celltructures can collapse due to the effect on cell membranes

Fig. 2. Effect of gamma irradiation on firmness (above) and weight (below) of Pleu-rotus eryngii during 28 d of storage.

(Beaulieu et al., 2002). The collapsed cells may produce enlargedspaces (Evered and Burton, 1995), as was evident in the3 kGy-irradiated sample. The 1 kGy-irradiated sample showedcomparable micro-structure to that of the control. The changeswere similar in different tissue samples; however, the irradiationeffect was clearer in the cap surface samples with a collapsedfibrous structure and a loss of shape (Fig. 3). The SEM results were ingood agreement with the texture, physical appearance, and weightloss observations, in which the samples irradiated at higher dosesshowed detrimental quality characteristics. Similar results werealso reported by Moreno et al. (2007) in electron-beam irradiatedblueberries.

3.4. Sensory properties and volatile compounds

Sensory panelists were unable to characterize a significantdifference between non-irradiated control and irradiated sam-ples (data not shown). Different researchers have also reportedsimilar sensory scores for non-irradiated control and irradiated

mushrooms due the low threshold of key flavor compounds inmushrooms (Lai et al., 1994; Mau et al., 2006).

An E-nose analysis was employed to precisely analyze the effectof irradiation on volatile compounds of mushrooms. Data were

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46 K. Akram et al. / Postharvest Biology and Technology 66 (2012) 42–47

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ig. 3. Scanning electron microscopy (above: stem surface; middle: internal tissuleurotus eryngii.

nalyzed using PCA to reduce the dimensionality of the numeri-al data set and to understand the trend in the sample populationKeshri et al., 2003). The PCA results of the control and irradi-ted samples projected onto the first two PCs are given in Fig. 4.istinct groups (circled in Fig. 4) corresponding to control and

rradiated samples could easily be distinguished. These groups inCA plots showed different E-nose responses for the control andach treatment group, demonstrating the clear effect of irradiationn volatile profiles of mushrooms. The E-nose analysis proved itsotential to characterize irradiated mushrooms in which responsesere dependent on applied doses. Researchers have reported the

pplicability of E-nose analysis to discriminate irradiated tomatoesWinquist et al., 1995), anchovy sauce (Kim et al., 2004), red pep-

er powder (Lee et al., 2005) and ground pork (Kim et al., 2008)rom non-irradiated samples. Keshri et al. (2003) characterized theolatile production profile of different Agaricus species using E-nosenalysis.

ig. 4. Principal component analysis (E-nose evaluation) showing different dose-ependent patterns (circled) of volatile profiles of irradiated Pleurotus eryngii.

ow: cap surface) revealing the effect of gamma irradiation on micro-structure of

4. Conclusion

The 1 kGy-irradiated samples gave overall superior results com-pared to those of other samples studied. Color changes were moreapparent in the cap region because of the bleaching effect of irra-diation on colored parts. High-dose irradiation (3 kGy) resultedin detrimental quality changes in color, texture, weight loss, andoverall appearance of the sample. SEM analysis leads to a bet-ter understanding of the results by providing a clear view ofmicro-structural changes following irradiation. The E-nose analysiseffectively characterized the dose-dependent effect of irradiationon volatile profiles of mushrooms.

Acknowledgement

This research was supported by Technology DevelopmentProgram for Food, Ministry for Food, Agriculture, Forestry and Fish-eries, Republic of Korea.

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