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LWT 39 (2006) 364371 www.elsevier.com/locate/lwt

Effect of modied atmosphere packaging on the shelf-life of coated, whole and sliced mushrooms
Ki Myong Kima, Jung A Kob, Jin Sil Leec, Hyun Jin Parkb,d, Miford A. Hannaa,
a

Industrial Agricultural Products Center, University of Nebraska, 233 LW Chase Hall Lincoln, NE 68583-0730, USA b Graduate School of Biotechnology, Korea University, Seoul 136-701, Republic of Korea c Department of Food Service Management and Nutrition, Sangmyung University, Seoul 100-743, Republic of Korea d Department of Packaging Science, Clemson University, Clemson, SC 29634-0370, USA Received 6 September 2004; received in revised form 10 February 2005; accepted 15 February 2005

Abstract Whole and sliced fresh mushrooms (Agaricus bisporus) were packaged with PVC wrap or two polyolens (PD-941 and PD-961) lms after coating with CaCl2 and chitosan. Package gas composition, color, weight loss and maturity were measured during storage at 12 1C and 80%RH. For PD-961, the highest in-package concentration occurred during the rst day of storage regardless of treatments, while wrap and PD-941 showed varying degrees in-package concentration with different processes and coatings. The whiteness of whole mushrooms varied signicantly with the type of coating, but not with the type of lms. The extent of darkening was greater in coated whole mushrooms than in sliced ones. Weight loss occurred in all packages and varied from 3 (g/100 g) to about 7 (g/100 g) after 6 days of storage. Due to a lower permeability, PD-961 packages had the lowest weight loss. The type of packaging lms signicantly affected the maturity index, where PD-961 most effectively lowered maturity index for both whole and sliced mushrooms, thus extending the shelf-life. The type of coating did not appear to affect maturity index except for the wrap package where chitosan coating markedly lowered the maturity index of sliced mushrooms. r 2005 Swiss Society of Food Science and Technology. Published by Elsevier Ltd. All rights reserved.
Keywords: Mushroom (Agaricus bisporus); Sliced process; Chitosan; Coating

1. Introduction Due to their thin and porous epidermal structure, the respiration rate of mushrooms is relatively high (200500 mg/kg h at 20 1C) compared to other vegetables and fruits (Kader, 1985; Warwick & Tsureda, 1997). Mushrooms are highly perishable and tend to lose quality right after harvest. Shelf-life of mushrooms is less than 3 days under usual shipping and marketing conditions (Lee, 1999). Therefore, mushrooms need special care to retain freshness. There are several indicators that determine the quality of mushrooms such as whiteness, cap development,
Corresponding author. Tel.: +402 472 1634; fax: +402 472 6338.

E-mail addresses: hjpark@korea.ac.kr (H.J. Park), mhanna@unlnotes.unl.edu (M.A. Hanna).

stripe elongation, number of ripe spores, texture, respiration rate, mannitol content, weight loss and microbial deterioration (Gormley, 1975; Bartley, Beelman, & Winnett, 1991; Lopez-Briones et al., 1992). There are many methods to extend the shelf-life of mushrooms. They include modied atmosphere packaging (MAP) (Roy, Anantheswaran, & Beelman, 1995), controlled atmosphere storage (CA) (Lopez-Briones et al., 1992), coating (Nussinovitch & Kampf, 1993), refrigeration (Gormley, 1975; Mau, Miklus, & Beelman, 1993), cultivating with CaCl2 solution (Miklus & Beelman, 1996) and using sorbitol (Roy et al., 1995). Although CA storage is effective to lower respiration rate and increases shelf-life of fruits and vegetables, it is not appropriate for vegetables, as mushrooms, which have extremely high respiration rates (Roy et al., 1995). MAP is the most simple, economical, and effective way of

0023-6438/$30.00 r 2005 Swiss Society of Food Science and Technology. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.lwt.2005.02.015

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extending shelf-life of fresh mushrooms. Nichols and Hammond (1973) reported that over-wrapping with polyvinyl chloride (PVC) lm increased the shelf-life of mushrooms by retarding cap opening, discoloration, and reducing weight loss. Roy et al. (1995) determined the proper O2 and CO2 concentrations for MAP of mushrooms. They found that 6% O2 was effective in reducing cap development. Sveine, Klougart, and Rasmussen, (1967) reported that 0.1% O2 and 5% CO2 were optimum conditions for prolonging shelf-life of mushrooms. Low O2 reduced respiration rate and retarded cap development, reduced aerobic deterioration and weight loss. Also, low O2 decreased tyrosinase activity reducing enzymatic browning. Although a low concentration of O2 may have many advantages, less than 2% could cause anaerobic microbial growth signicantly, such as Clostridium botulinum (Herr, 1991) and Staphylococcus aureus (Martin & Beelman, 1996). Coating vegetables and fruits with semi-permeable lm has the benecial effect of delaying ripening and prolonging the storage life of fresh produce (El Ghaouth, Ponnampalam, Castaigne, & Arul, 1992a; Park, Bunn, Vergano, & Testin, 1994). Chitosan appears to be an ideal preservative coating for fresh produce because of antifungal activity and lm foaming property (Hirano & Nagao, 1989). Chitosan coating has been used to extend the shelf-life of tomatoes, cucumbers, bell peppers, and strawberries (El Ghaouth et al., 1992a; El Ghaouth, Arul, & Ponnampalam, 1992b; Zhang & Quantick, 1997). Alginate and calcium-alginate lms were used as coating materials for mushrooms by Nussinovitch and Kampf (1993) and Hershko and Nussinovitch (1998), but there has been no research on chitosan as a mushroom coating. Recently consumers have been more interested in readily available fruits and vegetables. For the food service industry in particular, there are some advantages of using minimally processed food to save cost and labor (Hoover, 1997). It can be assumed that if sliced mushrooms can be preserved as long as fresh mushrooms, the market share of sliced mushroom will increase. The objectives of this study were to determine the suitable commercial MAP lm and the effect of chitosan coating on the quality of sliced mushrooms (Agaricus bisporus), determining CO2/O2 concentrations, color, weight loss and maturity as indicators of mushrooms quality.

laboratory within 1 h after harvest. Mushrooms with pileus (cap) size of 3040 mm and a maturity index of stage 1 were selected and refrigerated at 4 1C before slicing. The lms for mushroom packaging were PVC wrap (Lucky Co, Naju, Korea), and polyolen PD-941 and PD-961 (Cryovac Division, Sealed Air Corp, Duncan, SC, USA). Chitosan was purchased from Biotech Co. (Mokpo, Korea). It was prepared from red crab shell and had viscosity of 5 cP with deacetylation degree above 95%. Three grams of chitosan was dissolved in 1000 ml of lactic acid solution (5 ml lactic acid/1000 ml distilled water). The pH was adjusted to 5.2 with NaOH solution (40 g/1000 ml distilled water). Mushrooms were sliced to a thickness of 5 mm. Sliced and whole mushrooms were spray-coated with solution of chitosan and CaCl2 (2 g per 100 ml deionized water). The surface was then allowed to dry at room temperature using a fan to shorten drying time. 2.2. Modied atmosphere packaging Coated and uncoated mushrooms were divided into three package groups, PVC wraps, PD-941 and PD-961. Each plastic container (12 17 5 cm) having 150 g of mushrooms was inserted into a bag and heat-sealed. Packages were stored at 12 1C and 80% relative humidity in an incubator (Sugong Tech., Co., Ltd., Seoul, Korea) under static conditions (Roy et al., 1995). The CO2 and O2 concentrations in packages were monitored daily for 6 days using a gas chromatograph (TCD-GC, Hitachi, model 163; column, CTR-I, 50 1C; injector, 50 1C; detector, 150 1C; carrier gas, He; ow rate, 20 1C/min,). A 0.5-ml sample of the package headspace was removed using a hypodermic syringe. The syringe needle was inserted through a septum that was attached on the surface of the package for sampling. The headspace gas sample was injected into a 0.25-ml sample loop of the GC to ensure adequate ow. 2.3. Maturity index The maturity index was assigned to mushrooms based on the extent of cap opening on a 7 point-scales ((1) veil intact tightly; (2) veil intact stretched; (3) veil partially broken (ohalf); (4) veil partially broken (4half); (5) veil completely broken; (6) cap open and gills well exposed; and (7) cap open and gill surface at) (Roy et al., 1995). Ten pieces of sliced mushrooms were selected randomly and measured for maturity based on the 7-point scale. 2.4. Color

2. Materials and methods 2.1. Materials and sample treatment Fresh mushrooms (Agaricus bisporus) were purchased from a local farmer in Seoul, Korea and brought to the The surface color of mushrooms was measured using a Hunter-Lab Chroma Meter CR-300 (Minolta Corporation, Instrument Systems, Ramsey, NJ). Four

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measurements were taken at random locations on the sliced site of the cap and compared to the ideal mushroom color values of L 97, a 2, b 0 using DE as described by the following equation (Ajlouni, 1991): DE L 972 a 22 b2 1=2 , where DE indicates the degree of overall color change in comparison to color values of an ideal mushroom. Color was measured on day 0 and day 6 of storage. 2.5. Weight loss Weight was measured on day 0 and day 6 of storage. Weight loss was determined by dividing the weight change during storage by the original weight. Weight loss g=100 g W 0 W f =W 0 100, where W 0 is the weight on the rst day and W f the weight on nal storage day. 2.6. Statistical analysis Data on CO2 and O2 in-package concentrations, maturity index, color and weight loss of the mushrooms were subjected to analysis of variance (ANOVA). The General Linear Model Procedure developed by Statistical Analysis System (SAS Institute, Inc., 1996) was used to perform ANOVA and to compare treatment means on day 0 and day 6 of storage.

3. Results and discussion 3.1. In-package CO2 and O2 concentration The patterns of changes in the CO2 concentration in both whole and sliced mushrooms during storage were similar for the three lms. Two patterns of changes in the CO2 concentration were observed, namely, a transitional state characterized by a peak of CO2 concentration and a steady state where the CO2 concentration remained relatively constant. The CO2 concentration in containers with whole mushrooms increased sharply within 24 h except for the wrap packaging (Fig. 1). The peak in 24 h is believed to be a result of a sharp rise in post harvest respiration that occurs with fruits and vegetables (Eskin, Henderson, & Townsend, 1971). Because mushrooms have a high rate of respiration relative to most vegetables, the modication of the package headspace readily occurred according to the gas permeability properties of lms. Classically, modication of internal atmosphere shows a decrease of O2 partial pressure and increase

of CO2 partial pressure at initial phase, but a high O2 transmission rate (OTR) of the wrap lm (13,650 ml m2 day1 atm1) prevented depletion of O2 (Barron, Varoquaux, Guilbert, Gontard, & Gouble, 2002). Despite different CO2 permeances between PD-941 (36,000 ml m2 day1 atm1) and PD-961 (19,00022,000 ml m2 day1 atm1) lms, the patterns of changes in the CO2 concentration were not different. This can be explained by the fact that PD-941 and PD961 lms were both effective in blocking passage of the CO2 gas from inside the package to the outside. Changes in gas components were in agreement with the results of Lopez-Briones et al. (1992) and Roy et al. (1995) who reported that the CO2 concentration sharply increased after a few hours in MAP. Changes in O2 concentration, however, displayed different patterns with coating materials and lms in whole mushrooms. Whole mushrooms in wrap depleted O2 in the package and modied atmosphere was achieved in 2 days of storage. Both PD941 and PD-961 packages showed peak concentrations of CO2 within a day. Coating materials did not change the pattern of respiration of CO2 in either the PD-941 or the PD-961 package, but affected O2 consumption in PD-941. High OTR of PD-941 (16,500 ml m2 day1 atm1) increased the O2 concentration in the container again on the second day of storage. There seemed to be no respiration after the second day of storage in all packages regardless of coating in view of the lack of CO2 expiration. The low OTR (7,000 ml m2 day1 atm1) and CTR (21,500 ml m2 day1 atm1, carbon dioxide transmission rate) of PD961 helped maintain anaerobic conditions even after the rst day of storage. After peaks at day 1, sliced mushroom packages except for wrap sustained higher CO2 and lower O2 concentrations than whole mushroom ones (Fig. 2). It appeared that the respiration of the mushrooms was increased by increased surface area. Modication of the package atmosphere can be attributed primarily to the consumption of O2 and generation of CO2 during respiration by mushrooms. The rates of O2 depletion and CO2 production by mushroom were much greater than the permeation rates of these gases through the PD-941 and PD-961. On the other hand, the CO2 concentration decreased after 24 h and gas components were controlled by CTR and OTR of the lm. The free volume in MAP of fresh produce is known to affect the time required to equilibrate the inpackage atmosphere that is governed by the lm permeability and produce respiration (Kang, Park, & Lee, 2000). Wrap and PD-941 packaging showed the increasing O2 concentration after a sharp decrease in the concentration of modied atmosphere. Modied atmosphere seemed to be changeable according to the CO2/ O2 equilibrium at nal state. If MA is not equilibrated to expected composition of CO2 and O2, it may either increase or decrease.

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14 12 10 8 6 4 2 0 0 CO2 concentration (%) 14 12 10 8 6 4 2 0 0 14 12 10 8 6 4 2 0 0 1 2 3 4 5 6 0 1 Storage time (day) 2 3 4 1 2 3 4 5 6 0 1 2 3 4 1 2 3 4 5 6 0 1 2 3 4 25 20 15 10 5 Wrap 0 5 PD-941 20 15 10 5 0 5 PD-961 6 25 20 15 10 5 0 5 6 6 25 O2 concentration (%)

367

Fig. 1. Changes in CO2 and O2 concentrations of whole mushrooms after coating with water, chitosan and CaCl2 in wrap, PD-941 and PD-961 packages during storage (J, control; K, water; , chitosan; m, CaCl2).

3.2. Color There were signicant differences (Po0:05) in color values between the control and coated mushrooms. Coated mushrooms had lower L value (Table 1) than the control but there were not signicant differences (P40:05) between coated whole and sliced mushrooms. Mushrooms with L values of higher than 80 would be acceptable to wholesalers. Those with L values of less than 70 would be rejected by consumers (Lopez-Briones et al., 1992). L values of the whole controls were still acceptable after 6 days. For the whole controls, there were no signicant differences among package lms, but the sliced control, packed with PD-961 lm, had the best color in terms of L value. The coating treatment had a negative effect on the color of both whole and sliced mushrooms. There were signicant differences in the color difference (DE ) among coating treatments, but no differences among lms. Value differences were less in sliced mushrooms than in whole ones, but coating treatment still showed higher DE than uncoated mushrooms. Chitosan showed higher DE values than other coating treatments in sliced mushrooms. CaCl2 irriga-

tion studies designed to improve post-harvest quality were based on the results of mushroom washing experiments. Guthrie (1983) found that washing mushrooms in hard water led to improved post-harvest quality presumably because of Ca ions in the hard water. Water treatment created additional stress and did not have a positive effect on the color. 3.3. Weight loss Weight loss occurred in all packages and the weight loss varied from 3 g/100 g to about 7 g/100 g after 6 days of storage (Fig. 3). These were almost the same values that were reported with a weight loss of 57 g/100 g after 5 days at 18 1C (Nichols & Hammond, 1973) and higher than those of Roy et al. (1995). In both whole and sliced mushrooms, PD-961 packages displayed the lowest weight losses. Even though surface areas increased in sliced mushrooms, the lowest weight loss percentage occurred in PD-961 packages. Coating did not signicantly (P40:05) reduce the weight loss in sliced mushrooms packed in PD-941 lm. The PD-961 lm packaging prevented mushrooms from losing weight.

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14 12 10 8 6 4 2 0 0 CO2 concentration (%) 14 12 10 8 6 4 2 0 0 14 12 10 8 6 4 2 0 0 1 2 3 4 5 6 0 1 2 3 4 1 2 3 4 5 6 0 1 2 3 4 1 2 3 4 5 6 0 1 2 3 4

25 20 15 10 5 Wrap 5 6 25 PD-941 20 15 10 5 0 5 6 25 PD-961 20 15 10 5 0 5 6 O2 concentration (%)


Chitosan 39.0b 45.2b 43.2b 41.8a 40.6a 38.2a

Storage time (day)


Fig. 2. Changes in CO2 and O2 concentrations of sliced mushrooms after coating with water, chitosan and CaCl2 in wrap, PD-941 and PD-961 packages during storage (J, control; K, water; , chitosan; m, CaCl2).

Table 1 Color changes of sliced and whole mushrooms, with and without coating, in different types of plastic lms packaging L Control Whole mushroom WrapA 76.7a PD-941A 78.8a PD-961A 78.4a Sliced mushroom 68.1a WrapB B PD-941 66.8a,b PD-961A 78.2a Water 63.6c 62.8c 62.8c 66.1a,b 68.6a 68.8b Chitosan 71.1b 63.3c 66.0b 61.6b 62.5b 68.4b CaCl2 69.6b 70.3b 66.6b 64.3a,b 62.5b 71.6b DE Control 32.8c 30.1d 31.3c 36.2b 35.7a 31.7b Water 46.6a 48.0a 46.2a 38.1a,b 38.4a 36.6a CaCl2 40.1b 40.3c 42.5b 39.3a,b 39.0a 36.1a

A,B,C Different superscripts within a column indicate signicant differences between packaging materials (Po0:05).a,b,cDifferent superscripts within a row indicate signicant differences between coating materials (Po0:05).

Weight loss from the mushroom surface is caused by loss of water from the package to the surrounding atmosphere, due to vapor pressure difference across the packaging lm, and to the loss of carbon upon

formation of CO2 during respiration. Mushrooms lack a protective epidermal structure to prevent excessive moisture loss and, therefore, have a very high transpiration rate.

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14 Whole typeA 12 Weight loss (g/100g) 10

369

8 7 6 Maturity Index 5 4 3 2 Whole typeB

8 6 4 2 0 wrapa 8 PD-941a PD-961b

1 0 wrapa PD-941b PD-961c

Minimal typeA

Weight loss (g/100g)

8 7 Maturity Index 6 5 4 3 2 1 0 wrapa PD-941b

Minimal typeA

6 4 2 0 wrapa PD-941b PD-961c

Fig. 3. Changes of weight loss percent of whole and sliced type mushrooms after MA storage for 6 days. A,BDifferent superscripts indicate signicant differences between types (Po0:05). a,b,cDifferent superscripts within a type indicate signicant differences between packaging materials (Po0:05). , Control (no treatment); , water; , chitosan; , CaCl2.

PD-961c

3.4. Maturity index PD-961 maintained a low maturity index value for both whole and sliced mushrooms with no signicant differences among coating materials (Fig. 4). Wrap package was found to be unsuitable for storage of mushrooms, but chitosan coating showed a signicantly (Po0:05) lower maturity index in wrap package of sliced mushrooms. It is not easy to determine the reason for which chitosan showed high maturity index in whole mushrooms across all lms. The coating effect appeared in PD-941 lm packages. Coated mushrooms showed lower maturity indices than both whole and sliced uncoated mushrooms. Maturity index did not increased after the MA formed of decreased O2 and increased CO2, and it is well observed in PD-961 packages. The maturity indices of whole and sliced mushrooms did not correspond to the concentration of CO2, but to O2 on the 6th day of storage (Fig. 2). Other researchers attributed this effect to increased CO2 rather than decreased O2, since CO2 is known to act as a regulator for mycelial growth and mushroom morphogenesis. Lopez-Briones and et al. (1992) reported that CO2

Fig. 4. Maturity index of whole and sliced type mushrooms after MA storage for 6 days. A,BDifferent superscripts indicate signicant differences between types (Po0:05). a,b,cDifferent superscripts within a type indicate signicant differences between packaging materials (Po0:05) , Control (no treatment); , water; , chitosan; CaCl2.

exhibited a marked effect on mushroom development. Mushrooms stored for 7 days at 10 1C under 15% CO2 did not break their veil regardless of the O2 content. But Burton (1998), on the contrary, observed a negligible difference in maturity index between mushrooms stored at 2% CO2 and those stored at 6% CO2 at 18 1C. Murr and Morris (1975) stated that the cap opening of mushrooms in storage at 10 1C was promoted by O2 tension lower than air, and that the stimulatory effect was maximum when mushrooms were stored at 5% O2. The maturity index was affected by lm permeability. High permeabilities of the wrap and PD-941 lms resulted in signicantly greater maturity indices than PD-961 for the uncoated mushrooms (Fig. 4). But with the wrap packaging of sliced mushrooms, chitosan coating reduced maturity index by limiting O2 uptake. In both whole and sliced mushrooms, maturity index was affected by coating treatments to some extent (Figs. 4a and b). Despite severe treatment such as

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Fig. 5. (a) Photograph of whole mushrooms, stored for 6 days with and without coating in wrap, PD-941, and PD-961. (b) Photograph of sliced mushrooms stored for 6 days with and without coating in wrap, PD-941, and PD-961.

slicing, the low-level maturity index indicated that the use of coating material on large areas of the mushroom had sealed its surfaces. Although minimum indices were achieved in PD-961 packages of both whole type and sliced type, O2 concentrations after 6 days of storage was almost zero. Storing mushrooms in such low O2 concentrations could create a favorable micro-atmosphere at the center of mushrooms for growth of anaerobic spores and toxin production (Sugiyama & Yang, 1975) (Fig. 5).

4. Conclusions The gas composition of MAP was highly related to the quality of both whole and sliced mushrooms. PD-

961 provided a successful MAP that extended shelf-life up to 6 days, regardless of coating treatment. Coating treatment could be considered with lms that are moderate gas barriers such as a PD-941 lm. Coating treatment is a parameter, beside temperature, lm permeability and weight of tissue, that affects the gas composition of a package. Coating treatment stimulated respiration of the mushrooms and changed the gas composition. Slicing and coating caused physical stress, resulting in changes in maturity index. But gas concentrations of given volume in container wrapped by PD-941 and PD-961 reached the limit and did not appear to stress the mushrooms. But on the sixth day, compared to the whole type, concentrations of CO2 in each package of sliced types were higher. Conclusively, coating can be a good process for creating additional

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barriers when applied to MAP storage of mushrooms in whole and sliced types.

Acknowledgments Journal Series No. 14614, Agricultural Research Division, Institute of Agriculture and Natural Resources, University of Nebraska-Lincoln. References
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