JFS E: Food Engineering and Physical Properties
Effect of Time, Temperature, and Slicing on Respiration Rate of Mushrooms T. IQBAL, F. A. S. RODRIGUES, P. V. MAHAJAN, AND J. P. KERRY
E: Food Engineering & Physical Properties
ABSTRACT: Respiration rate measurement considering the effects of cutting, temperature, and storage time are important for the shelf life study and modified atmosphere-packaging design of fresh-cut produce. This study investigates in the respiration rate of fresh whole and sliced mushrooms at 0, 4, 8, 12, 16, and 20 ◦ C under ambient atmosphere and different storage times. The O 2 consumption rate increased with temperature and ranged from 22.13 to 102.41 mL/(kg.h) and 28.87 to 143.22 mL/(kg.h) for whole and sliced mushrooms, respectively, in the temperature range tested. Similar trend was observed for CO 2 production rate. Slicing of mushrooms increased the respiration rate by 30% at 0 ◦ C and 40% at 20 ◦ C indicating that the mushrooms are not as sensitive to the stress caused by cutting as other fresh produce. Storage time affected both respiration rate of whole and sliced mushrooms and this effect was prominent at higher temperatures. The respiration rates increased initially for some time, then decreased and reached steady state value at 12, 16, and 20 ◦ C. A 2nd-order polynomial equation was used to fit the respiration rate data as a function of time at each temperature tested. Keywords: fruits and vegetables, mathematical modeling, minimal processing, modified atmosphere packaging, postharvest
T
Introduction
he global mushroom industry is growing in size and popularity. Higher returns from mushrooms cultivation are noted for all world markets. In Ireland, the output value of the horticultural sector in 2004 was estimated at €269 million and out of that, €110 million was contributed by mushrooms alone (Ireland Dept. of Agriculture and Food 2004). Mushrooms are highly perishable due to their high moisture content and very high respiration rate, as a result their freshness and quality decreases quickly. Therefore, shelf life of mushrooms is shorter as compared to other products and they require more attention in the postharvest chain. Mushroom quality and packaging need to be significantly improved, to reach farther markets. Minimal processing, for example, slicing, further reduces its shelf life; therefore, special care is needed for mushrooms. Respiration rate (RR) measurement of fresh and fresh-cut produce is essential in their shelf life study, using modified atmosphere packaging (MAP). Reduction in RR inside the package is favorable for increasing the shelf life of fresh produce. Product type and variety, production conditions, maturity stage at harvest, ageing (time), temperature, gas composition, and cutting (mechanical damage) are the main internal and external factors affecting fresh produce respiration rate. Temperature control is probably a key factor for maintaining the quality as low temperatures decrease respiration rate, enzymatic, and microbial activity. Respiration rate of fresh produce measurement and mathematical modeling is essential for the engineering design of modified atmosphere packages (MAP). Uchino and others (2004) developed a mathematical model for dependence of respiration rate of fresh produce on temperature and time. However, few
MS 20090003 Submitted 1/2/2009, Accepted 4/10/2009. Authors Iqbal, Rodrigues, and Mahajan are with Dept. of Process & Chemical Engineering and author Kerry is with Dept. of Food & Nutritional Sciences, Univ. College Cork, Ireland. Direct inquiries to author Mahajan (E-mail:
[email protected]).
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researchers considered the effect of time on the RR of fresh produce and very limited data is available in the literature (Yang and Chinnan 1988; Budu and others 2001; Kim and others 2004; Uchino and others 2004; Rocculi and others 2006). Kim and others (2004) reported that the respiration rate of intact and fresh-cut salad savoy (white and violet) were initially increased and then decreased with storage time of 24 h at 5 ◦ C. Respiration rates (CO 2 evolution) of the intact and fresh-cut white salad savoy ranged from 0.8 to 1.1 mmol/kg/h and 0.9 to 1.5 mmol/kg/h, respectively during 24 h at 5 ◦ C. Respiration rates of the intact and fresh-cut violet salad savoy ranged from 0.6 to 0.8 mmol/kg/h and 1.1 to 1.4 mmol/kg/h, respectively. Both white and violet fresh-cut salad savoy had respiration rates higher than intact samples. Fresh-cut produce are different from intact fruit and vegetables in terms of their physiology, handling, and storage requirements. Their processing results in tissue and cell integrity disruption, with a concomitant increase in enzymatic, respiratory, and microbiological activity and therefore, reduced shelf life (Lamikanra 2002). This effect might be minimized by the use of adequate temperature management and MAP. The increase in respiration rate of fresh-cut produce is due to the physiological response to wounding and the increasing surface area. Most of the studies reported in the literature consider the respiration rate to be independent of time. Some researchers have, however, reported that this is not the case, particularly for fresh-cut produce, and these changes may have a major impact in the gas composition achieved in MAP (Fonseca and others 2002). The objective of this study was to investigate the changes of respiration rate of whole and sliced mushrooms stored under ambient air over time at different temperatures, and to develop a predictive mathematical model accounting for the effect of both time and temperature.
Materials and Methods Sample preparation Fresh mushrooms (Agaricus bisporus) were obtained from Walsh Mushrooms Ltd. (Athlone, Co. Westmeath, Ireland) and were stored R Institute of Food Technologists doi: 10.1111/j.1750-3841.2009.01198.x
C 2009
Further reproduction without permission is prohibited
Effect of time, temperature, and slicing on respiration rate. . . at the desired temperatures for 30 to 60 min to equilibrate to Jacxsens and others 2000; Hong and Kim 2001; Lencki 2004). After test temperatures. Mushrooms were sliced approximately 8 mm in preparing the samples, temperature effect was evaluated as 0.2 kg thickness using a sharp knife. of mushrooms were stored in airtight glass jars (1.9 × 10−3 m3 ) at the set temperature under ambient atmosphere over a period of Respiration rate measurement (3 to 4 h) time. A rubber septum was attached on the center of the Respiration rate was measured using the closed system method- lid of glass jar for gas sampling. To ensure complete air tightness, ology as largely reported in the literature (Ratti and others 1996; vaseline (white petroleum jelly, Lever Faberge Gmbh, Buxtehude,
25
Figure 1 --- Decrease of O 2 and increase of CO 2 concentration inside the glass jars for whole and sliced mushrooms at 20 ◦ C.
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E: Food Engineering & Physical Properties
O2, CO2 (%)
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Figure 2 --- Effect of temperature on the respiration rate of whole and sliced mushrooms under ambient atmosphere. (a) RO 2 for whole and sliced mushrooms, (b) RCO 2 for whole and sliced mushrooms.
LnRO 2 ml/(kg.h)
5 4.5 whlole
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3 2.5 2 0.0034 0.00345 0.0035 0.00355 0.0036 0.00365 0.0037 1/T (k)
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Effect of time, temperature, and slicing on respiration rate. . . rate increased with temperature and ranged from 22.13 ± 1.66 to 102.41 ± 2.13 mL/(kg.h) and 28.87 ± 0.31 to 143.22 ± 1.08 mL/(kg.h) for whole and sliced mushrooms, respectively, in the temperature range tested. The CO 2 production rate followed a similar pattern as it increased from 20.21 ± 1.67 to 97.02 ± 2.51 mL/(kg.h) for whole and 23.67 ± 1.01 to 131.67 ± 4 mL/(kg.h) for sliced mushrooms, respectively. This showed that RO 2 and RCO 2 increased by up to 5 fold. The average RQ was found to be 0.89 for both whole and sliced mushrooms, which was within the normal range of 0.7 to 1.3 (Figure 3). Nei and others 2006 reported that the higher the (1) temperature, the higher the RR in shredded cabbage. This showed the importance of temperature control for the shelf life of mushrooms. The effect of temperature was described by an Arrheniustype equation (Eq. 3) (Hong and Kim 2001, Van De Velde and others (2) 2002; Uchino and others 2004; Nei and others 2006) as shown in Figure 2.
Germany) was placed between lid and jar for glass jars. Gas samples were taken at constant intervals, with the help of a needle inserted through a rubber septum on the center of the lid. The needle was connected to a CO 2 /O 2 gas analyzer (PBI Dansensor Checkmate, 9900, Denmark), to measure the gas composition, O 2 and CO 2 volumetric fraction with time (Thiele and others 2006). O 2 consumption (RO 2 ) and CO 2 production (RCO 2 ) rates were measured by the difference in O 2 and CO 2 concentrations at different time intervals using Eq. 1 and 2 (Figure 1). yO2 = yOi 2 −
i + yCO2 = yCO 2
RO2 .W . (t − ti ) Vf RCO2 .W . (t − ti ) Vf
R R = Rre f × e
− ERac × T1 − T 1
Data analysis The constants of the model developed to describe the influence of time and temperature on respiration rate were estimated by fitting this model to the experimental data by nonlinear regression using the Statistica software (release 5.1, 97 edition, Statsoft, Tulsa, Okla., U.S.A.).
RQ whole mushrooms
re f (3) The respiration rate was measured at different levels of storage times, storage temperatures for whole and sliced mushrooms. The storage temperature included 6 different levels: 0, 4, 8, 12, 16, and By adjusting Eq. 3 in Eq. 1 and 2, the global mathematical models 20 ◦ C. For the effect of temperature and slicing, full factorial exper- as shown in Eq. 4 and 5 were then developed. imental design with 4 replicates was followed with total number of Eo 48 experiments. W − 2× 1− 1 yo2 = yi o2 − Ro2re f × e Rc T Tre f × (4) × t − ti For assessing the effect of storage time the mushrooms were Vf −3 3 stored (0.2 kg each sample) in the closed glass jars (1.9 × 10 m total volume) for up to 176, 126, 100, 80, and 57 h at 4, 8, 12, 16, and 20 ◦ C, respectively. Respiration rate was measured at the specified A time interval of 8, 6, 5, 4, and 3 h for 4, 8, 12, 16, and 20 ◦ C, respec1.4 tively. For the effect of storage time and temperature, full factorial experimental design was followed with 2 replicates for 18 time in1.2 tervals and a total number of 180 experiments were performed. 1
0.8 0.6 0.4 0.2
Results and Discussion
0 0
Effect of slicing The values of RO 2 , RCO 2 , and RQ for whole and sliced mushrooms are shown in Figure 2 and 3, respectively. Due to slicing of mushrooms, the respiration rate increased at each temperature. RO 2 (RCO 2 ) increased about 30.4% (17.1%) at 0 ◦ C and 39.8% (35.7%) at 20 ◦ C as compared to the values of whole mushrooms. Although slicing increased the mushroom respiration rate significantly, they are not as sensitive as other fresh produce, for example, shredded carrots, Galega kale (Fonseca and others 2002; Iqbal and others 2008). This effect is likely to reduce the shelf life of sliced mushrooms, yet it is not as important as in other fruits and vegetables: 2- to 3-fold respiration rate increases have been reported for shredded kale and for apple slices (Lakakul and others 1999; Fonseca and others 2002; Iqbal and others 2004). Techavuthiporn and others (2008) resulted that cut broccoli has a higher CO 2 production rate than intact broccoli at 10 ◦ C, throughout the 10 d of storage and this is probably caused by cells injured by the cutting effect.
Effect of temperature
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E: Food Engineering & Physical Properties
Experimental conditions
1 0.8 0.6 0.4 0.2 0 0
4
8
12
Temperature (°C)
The effect of temperature on the respiration rate of both whole Figure 3 --- Effect of temperature on the respiratory quoand sliced mushrooms is shown in Figure 2. The O 2 consumption tient (RQ) (A) whole mushrooms, (B) sliced mushrooms. E300
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Effect of time, temperature, and slicing on respiration rate. . . 52 kJ/mol showed that cutting actually did not increase the sensitiv W × t − ti (5) ity of the mushrooms to the temperature. These values were found Vf to be within the normal range (29 to 93 kJ/mol) for common fruits and vegetables stored in air (Exama and others 1993). The RR of not The global mathematical model (Eq. 4 and 5) were then applied only the intact produce but also fresh-cut produce followed Arrheto the experimental data, to predict the respiration rate of whole nius equation (Jacxsens and others 2000). The model fitted well to and sliced mushrooms as a function of time and temperature. The the experimental data and the coefficient of determination (R2 ) was global models were developed to estimate the Arrhenius equain the range of 98.7% to 99.6%. The global models parameter estition parameter directly from the raw experimental data, thus minmates and relevant statistical data is presented in Table 1. imizing errors in parameter estimates. The activation energies of the process and respiration rates at a reference temperature (avEffect of storage time erage temperature in the range tested) were estimated by nonlinFigure 4 shows the effect of storage on RR at 2 extreme temperear regression. The values of activation energy for whole and sliced atures (4 and 20 ◦ C) and at a middle temperature (12 ◦ C) for sliced mushrooms were 51.84 ± 1.83 kJ/mol for O 2 , 52.03 ± 3.17 kJ/mol mushrooms. RR of sliced mushrooms were in the range of 105.5 ± 4 for CO 2 , 49.77 ± 2.07 kJ/mol for O 2 , and 51.49 ± 2.73 kJ/mol for to 133.8 ± 2 mL/(kg.h), during storage of 57 h at 20 ◦ C and 59.2 ± 3.6 CO 2 . These values were not significantly different; average being to 95.2 ± 3.6 mL/(kg.h), during storage of 100 h at 12 ◦ C. The RR increased initially for some time, then decreased and leveled off at Table 1 --- Global model (Eq. 4 and 5) constant estimates 12, 16, and 20 ◦ C. This might be because of cap opening and gill as a function of temperature for whole and sliced mush- development at higher temperatures, and it is delayed and reduced rooms. at lower storage temperatures. Indeed, there was slight decrease in Type Type of Ea R ref R2 respiration rate from 36 ± 2 to 12.9 ± 1 mL/(kg.h), during storage of of gas mushroom (kJ/mol) (mL/[kg.h]) (%) 176 h at 4 ◦ C (Figure 4). These results are in confirmation with Nei and others (2006), O2 whole 52 ± 2 47 ± 1 99.61 50 ± 2 61 ± 1 99.3 who reported a slight decrease in respiration rate of shredded cabCO 2 sliced 52 ± 3 40 ± 1 98.9 bage with storage time at 5 ◦ C. Although fresh-cut produce should 52 ± 3 55 ± 1 98.7 be stored at low temperatures, monitoring of the distribution chain
A
−
E co2 Rc
× T1 − T 1 re f
×
B
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RCO2 ml/(kg.hr)
RO2 ml/(kg.hr)
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Figure 4 --- Effect of storage time on the respiration rate of whole and sliced mushrooms. The symbols represent the experimental respiration rates at each time interval at different temperatures and the lines the models: (A) O 2 consumption rate for whole mushrooms; (B) CO 2 production rate for whole mushrooms; (C) O 2 consumption rate for sliced mushrooms; (D) CO 2 production rate for sliced mushrooms. Vol. 74, Nr. 6, 2009—JOURNAL OF FOOD SCIENCE
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yco2 = yi co2 + Rco2re f × e
Effect of time, temperature, and slicing on respiration rate. . . Table 2 --- Model (Eq. 6) constants for whole and sliced mushrooms at 3 temperatures. Temperature, ◦ C 20
Type of gas
Mushroom
a (mL/[kg.h])
O2
whole sliced whole sliced whole sliced whole sliced whole sliced whole sliced
135.3 ± 7.7 151.3 ± 5.5 109 ± 3.5 125.1 ± 3.2 68.3 ± 3.2 74.5 ± 2.9 50.1 ± 2.1 58.2 ± 2.1 25.3 ± 1 31.1 ± 1.1 15.9 ± 0.6 22.7 ± 1.6
CO 2 12
O2 CO 2
4
O2 CO 2
E: Food Engineering & Physical Properties
has shown that in some countries temperature abuse is not uncommon. Temperature around 20 ◦ C has been observed and in that case the respiration rate would increase sharply after approximately 20 h from around 90 to 130 mL of CO 2 /(kg.h), which would have a major impact on the product shelf life. A correct MAP design should take this effect into account. Slicing increased the RR of mushrooms as compared to the whole mushrooms; however, the effect of storage time was similar at all temperatures tested (Figure 4). Iqbal and others (2005) reported the increase in respiration rate of shredded carrots with storage time and this effect was described by Weibull model. Yang and Chinnan (1988) developed a respiration model considering time using quadratic equations. Budu and others (2001) also used a quadratic model for respiration rate of pineapple fruit. Gong and Corey (1994) found that best fit function for O 2 consumption is a polynomial of 2nd order equation. A polynomial equation of 2nd-order (Eq. 6) was used for modeling the effect of storage time on RR of both whole and sliced mushrooms at each temperature tested. The model constants are presented in Table 2. The model fitted well to the experimental data and predicted the RR of both whole and sliced mushrooms as a function of time at each temperature. R R = a + b(t) + c(t)2
Eo 2 Rc RCO 2 RCO 2ref RO 2 RO 2ref RQ RR R ref T t ti T ref Vf W yco 2 y i co 2
(6)
For both whole and sliced mushrooms, constants a and b decreased with the decrease in temperature from 20 to 4 ◦ C, while constant c slightly increased with decrease in temperature (Table 2).
Conclusions
c Ea Eco 2
yo 2 yi o 2
Model constants b (mL/[kg.h]) 1.8 ± 0.57 0.38 ± 0.45 1.32 ± 0.28 0.125 ± 0.26 0.71 ± 0.15 0.7 ± 0.1 0.5 ± 0.1 0.3 ± 0.09 −0.001 ± 0.02 −0.15 ± 0.02 −0.02 ± 0.01 −0.18 ± 0.04
c (mL/[kg.h]) −0.036 ± 0.009 −0.015 ± 0.007 −0.028 ± 0.004 −0.01 ± 0.004 −0.005 ± 0.001 −0.005 ± 0.001 −0.003 ± 0.0009 −0.001 ± 0.0009 0.00008 ± 0.0001 0.0007 ± 0.0001 0.00008 ± 0.00008 0.0008 ± 0.0002
Constant of Eq. 6 dimensionless Activation energy kJ/mol Arrhenius equation activation energy constant for CO 2 kJ/mol Arrhenius equation activation energy constant for O 2 kJ/mol Universal gas constant (0.008314 kJ/[mol.K]) CO 2 production rate mL/(kg.h) Reference CO 2 consumption rate mL/(kg.h) O 2 consumption rate mL/(kg.h) Reference O 2 consumption rate mL/(kg.h) Respiratory quotient dimensionless Respiration rate mL/(kg.h) Reference respiration rate mL/(kg.h) Temperature K Storage time h Initial time h Reference temperature 283.15 K Free volume inside the container m3 Produce weight kg Volumetric concentration of CO 2 at time t %, v/v Initial volumetric concentration of CO 2 inside the container at time t i %, v/v Volumetric concentration of O 2 at time t %, v/v Initial volumetric concentration of O 2 inside the container at time t i %, v/v
Acknowledgments
Funding for this research was provided under the Irish Natl. Delicing increased the respiration rate of mushrooms but mush- velopment Plan, through the Food Institutional Research Measure, rooms are not as sensitive to the stress caused by cutting as administered by the Dept. of Agriculture, Fisheries & Food, Ireland. some other products; however, refrigeration had vital influence on respiration rate and should be managed and considered in modified atmosphere packaging design. Storage time affected the resReferences piration rate of both whole and sliced mushrooms and this effect Budu AS, Joyce DC, Aked J, Thompson AK. 2001. Respiration of intact and minimally processed pineapple fruit. Trop Sci 41:119–25. was higher at high temperatures. Respiration rate increased initially Exama JP, Arul J, Lencki RW, Lee LZ, Toupin C. 1993. Suitability of plastic films for with time, then decreased and leveled off at 12, 16, and 20 ◦ C. At low modified atmosphere packaging of fruits and vegetables. J Food Sci 58(6):1365–70. temperatures (4 and 8 ◦ C), it slightly decreased with storage time as Fonseca SC, Oliveira FAR, Frias JM, Brecht JK, Chau KV. 2002. Modelling respiration rate of shredded Galega kale for development of modified atmosphere packaging. J compared to the initial respiration rate at time zero. The RQ was Food Eng 54(4):299–307. constant during storage at each test temperature. The temperature Gong S, Corey KA. 1994. Predicting steady state oxygen concentrations in modified atmosphere packages of tomatoes. J Am Soc Hortic Sci 119:546–50. dependence of the respiration rates followed an Arrhenius-type reHong S, Kim D. 2001. Influence of oxygen concentration and temperature on respiralationship and fitted well to the experimental data. A polynomial tory characteristics of fresh-cut green onion. Int J Food Sci Technol 36(3):283–9. model of 2nd order described well the influence of time on the res- Iqbal T, Oliveira FAR, Kerry JP. 2004. Effect of temperature and cutting on the respiration rate of mushrooms. Institute of Food Technologist annual meeting; 2004 Jul piration rate of mushrooms. 12–16; Las Vegas, Nev.: 95–9.
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