JFS E: Food Engineering and Physical Properties

Effects of Drying Temperature and Surface Characteristics of Vegetable on the Survival of Salmonella
N. HAWAREE, N. CHIEWCHAN, AND S. DEVAHASTIN
ABSTRACT: The heat resistance of Salmonella Anatum inoculated on the surface of a model vegetable as affected by hot-air drying temperature (50 to 70 C) and surface characteristics was determined in this study. Cabbage was selected as a model vegetable to demonstrate the effect of topographical feature of vegetable surface on the Salmonella attachment ability. An image analysis technique was developed to monitor the change of cabbage surface during drying and the specific surface characteristics were described in terms of the roughness factor (R). It was found that the water activity of the vegetable decreased while R-value increased with longer drying time and higher drying temperature. However, the changes of both parameters during drying did not show a significant effect on the susceptibility of Salmonella attached on the cabbage surface. Drying temperature was found to be a major factor influencing the heat resistance of Salmonella during drying. Keywords: cabbage, heat resistance, hot-air drying, image analysis, roughness factor, Salmonella, topographical features

E: Food Engineering & Physical Properties

Introduction
almonella is a pathogenic bacterium of serious concern to public health. It is commonly found in natural environment and is frequently reported to contaminate fruits and vegetables (Beuchat 1996; Thunberg and others 2002). In Thailand, the incidence of several Salmonella strains has been reported in vegetables such as cabbage, lettuce, peppermint, and sweet basil (Swetwiwathana and Chungsamanukool 1995). Although Salmonella bacteria do not multiply in an environment with water activity (a w ) below 0.92, they may survive in that environment for a very long period of time (Juven and others 1984). Many dried food products such as cornflour (van Cauwenberg and others 1981) and egg powder (Jung and Beuchat 1999) have also been found to be contaminated with Salmonella. Drying is one of the most common processes used to preserve and improve the quality of many food products including vegetables. The process decreases considerably the water activity of a food material and helps reduce the rate of deterioration reaction, microbiological activity and minimizes physical and chemical changes during storage. In terms of microbial inactivation, dry heat is less effective than moist heat as proteins, which are an important component in maintaining cell viability, are more stable in dry state (Hansen and Riemann 1963). Therefore, a more drastic heat treatment is required to destroy microorganisms during drying. Moreover, cells attached to tissues are more heat resistant than those unattached or dispersed throughout the food or broth (Quintavalla and others 2001; Murphy and others 2002). Chiewchan and others (2007) indeed illustrated the effects of hot-air drying and cell attachment on the heat resistance of Salmonella Krefeld on rawhide
MS 20080580 Submitted 7/30/2008, Accepted 9/29/2008. Authors are with Dept. of Food Engineering, Faculty of Engineering, King Mongkuts Univ. of Technology Thonburi, 126 Phacha u-tid Rd., Tungkru, Bangkok 10140, Thailand. Direct inquiries to author Chiewchan (E-mail: naphaporn. rat@kmutt.ac.th).

surface and found that Salmonella attached on the rawhide exhibited much greater heat resistance than that dispersed in a liquid medium. Although some pretreatments such as washing with sanitizers are generally applied prior to drying, large surface area and topographical features of vegetables can still facilitate entrapment and attachment of microbial cells, which cannot be then eliminated easily (Natl. Advisory Committee on Microbiological Criteria for Foods 1999). Many studies have revealed that bacterial cells are generally distributed on smooth surface of fruits and vegetables and they preferably attach around stomata and especially on damaged or cut surface (Han and others 2000; Hassan and Frank 2003; Palumbo and others 2005; Ells and Hansen 2006). Furthermore, natural topographical surfaces such as the veins of leafy vegetables, stem area, and netted rind surface of some fruits also provide good harborage for bacterial cells (Sapers 2001; Beuchat and Scouten 2004; Ells and Hansen 2006). Once fruits and vegetables are subjected to further processing, pathogenic bacteria may survive. In addition, loss of water from food structure also leads to changes in topographical characteristics, for example, shrinkage, and reduction in the size of the product (Ramos and others 2003), which may enhance the thermal resistance of the bacterial cells even further. To describe the surface and morphological characteristics of food materials, many computerized methods have been developed. For example, Quevedo and Aguilera (2004) developed the glistening point method to describe the surfaces of various fruits. Fern andez and others (2005) analyzed the geometrical features of apple discs during drying using an image analysis technique. Quevedo and others (2002) characterized the texture and microstructure of foods using a fractal analysis technique. Although many studies have focused on the changes of food surface characteristics during processing, there was no report on the effect of food surface characteristics on the heat resistance of bacteria during processing.

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2008 Institute of Food Technologists R doi: 10.1111/j.1750-3841.2008.01010.x

Further reproduction without permission is prohibited

Survival of Salmonella . . .
The objective of this study was to determine the effects of hotair drying temperature (50 to 70 C) and surface characteristics of vegetable (cabbage) on the heat resistance of Salmonella. An image analysis technique was developed to study quantitatively the surface characteristics of vegetable during drying. remaining edible leaves of cabbage were washed with tap water for 2 min and cut into sizes of 20 20 mm. The average thickness of the cabbages after cutting it in to a desired size was approximately 1.5 0.3 mm.

Materials and Methods

Bacterial culture and preparation
Salmonella Anatum DMST 19600 isolated from cabbage (Dept. of Medical Science, Thailand) was used in this study. The bacterium was maintained in tryptic soy agar (TSA, Difco, Franklin Lakes, N.J., U.S.A.) slants and incubated at 37 C for 24 h. Then, S. Anatum was maintained in TSA slopes at 4 C and subcultured every month to refresh the organism. For the preparation of microorganism for each experiment, culture was first set at room temperature for 30 min to 1 h. One loopful was transferred to 100 mL of tryptic soy broth (TSB, Difco) in a 250-mL Erlenmeyer flask. The content was then shaken continuously in a rotary shaker (New Brunswick Scientific, Innova 4230, N.J., U.S.A.) at 200 rpm at 37 C for 18 h. The culture was diluted in 0.1% peptone water to obtain the bacterial cells in their stationary phase (approximately 107 CFU/mL).

Inoculation of bacterial cells

Cabbage was submerged in the inoculum solution for 5 min and then incubated at room temperature for 1 min while shaking at 200 rpm by a shaker incubator (New Brunswick Scientific). Then, cabbage contaminated with S. Anatum was packed in a sterile bag and stored at 4 C for 24 h to maintain the bacterial culture. The contaminated material of S. Anatum (1 106 CFU/g) was then obtained.

Moisture content (kg/kg dry basis)

Drying experiments were conducted using a hot air oven (Memmert Model ULM600/II, Schwabach, Germany) at temperatures of 50, 60, and 70 C. Three trays, each containing approximately 400 g of contaminated cabbage, were prepared for each batch of experiments. Approximately 30 g of cabbage was taken at time intervals to determine its moisture content using an oven method (AOAC, 2000); water activity was also determined using a water activity meSample preparation ter (Novasina Model TH2/RTD33, Zurich, Switzerland). The numWhite cabbage (Brassica oleracea var. capitata) was obtained ber of Salmonella survivors was enumerated by diluting the sample from a local supermarket. 2 or 3 outer leaves were removed. The in 0.1% peptone water; 0.1 mL aliquot was spread in duplicate on TSA plates. Viable number was estimated from colony count after an incubation time of 48 h at 37 C. The surface characteristics of the samples undergoing drying were determined by taking images A 20 of the sample surfaces using a scanning electron microscope; image analysis was then performed to process the obtained scanning electron microscopic images. 15

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Figure 2 --- Evolution of (A) water activity and (B) surface Figure 1 --- Drying curves of cabbage undergoing drying at temperature of cabbage during drying at 50 ( r), 60 ( ), 50 ( r), 60 ( ), and 70 C ( ). and 70 C ( ). Vol. 74, Nr. 1, 2009JOURNAL OF FOOD SCIENCE E17

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Drying experiments

Survival of Salmonella . . .
Scanning electron microscopy
A cabbage sample (size of 3 mm2 ) was treated with 2.5% (w/v) glutaldehyde in 0.1 M phosphate buffer at pH 7.2 and left in a refrigerator (4 to 8 C) overnight. The treated sample was then washed 2 times with phosphate buffer and dehydrated sequentially for 10 min in aliquots of 30%, 50%, 70%, 90%, and 100% (v/v) of ethanol. The sample was then dehydrated in liquid CO 2 using a critical point dryer (Tousimis Model Samdri 780-A, Rockville, Md., U.S.A.). The dehydrated sample was coated with gold in a sputter coater (Structure Probe, West Chester, Pa., U.S.A.). Finally, an image of each sample was obtained using a scanning electron microscope (Jeol Model JSM-540LV, Tokyo, Japan) at 350 magnification level to study the surface changes during drying and at 5000 magnification level to study the bacterial attachment on the cabbage surface. was between 0.35 and 0.60. If the grayscale value of a particular pixel was higher than the threshold value, the pixel was counted. On the other hand, if the grayscale value of a particular pixel was lower than the threshold value, the pixel was not counted. The frequency of counted pixels was then recorded. The surface characteristics of the cabbage samples were determined in terms of the roughness factor (R), which is defined as (F t F 0 )/F 0 where F t is the frequency of the counted pixels at drying time t and F 0 is the frequency of the counted pixels at the beginning of the drying process (time = 0 h).

Data and statistical analysis

All experiments were performed in triplicate and the results were expressed as mean values with standard deviations. Experimental survival curves were fitted to the Weibull model (Peleg, 2000), log S = bt n , where log S is the log 10 of the survival ratio at time t and b and n are the scale and shape parameters, respectively. An estimation of the heat resistance is shown in terms of the time to obtain 3-log 10 reduction in Salmonella numbers. All statistical analyses were performed using MinitabTM program version 14 (Minitab Inc., State College, Pa., U.S.A.).

E: Food Engineering & Physical Properties

Image analysis

An original image obtained from a scanning electron microscope with image sizes of 520 520 pixels (resolution of 20 pixels/inch) or 0.23 0.23 mm in real size scale was stored as a bitmap file (.bmp). The image was then transformed from an index format to a black and white format prior to image processing. Image processing was performed using MatlabTM version 6.5 Results and Discussion (The MathWorks, Natick, Mass., U.S.A.). First, an image was filtered with a rotationally symmetric Gaussian low-pass filter to diminish Evolutions of cabbage moisture content, water noise. The details of each image were converted into grayscale val- activity, and surface temperature during drying ues (0 to 255). The values of the intensity, in terms of the grayscale Fresh cabbage with an initial moisture content of approximately values, were subsequently converted into binary values based on 17 kg/kg dry basis (or 94% wet basis) was dried until reaching an appropriate threshold; a suitable threshold used in this study its equilibrium moisture content of approximately 0.13 kg/kg dry

Figure 3 --- SEM images (350) of cabbage surface during drying at 60 C at (A) 0, (B) 4, (C) 8, (D) 12, (E) 16, and (F) 20 h.

Figure 4 --- Representative SEM images (350) of cabbage surface during drying at (A) 50, (B) 60, and (C) 70 C after 12 h of drying.

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Survival of Salmonella . . .
basis (or 11.30% wet basis). The drying kinetics of cabbage undergoing hot-air drying are shown in Figure 1a and 1b. As expected, higher drying temperatures resulted in higher drying rates. Cabbage reached its equilibrium moisture content after 16, 12, and 7 h of drying when drying air temperatures of 50, 60, and 70 C were used, respectively. The moisture content decreased more rapidly during the first 5 h of drying due to larger moisture gradients within the sample, leading to a faster movement of moisture. After that period, the moisture content decreased at a much slower rate until reaching the equilibrium moisture content. The effect of drying temperature on the water activity of cabbage is shown in Figure 2a. The water activity also decreased almost

Figure 5 --- Intensity map obtained from SEM images of Figure 3. Vol. 74, Nr. 1, 2009JOURNAL OF FOOD SCIENCE E19

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Survival of Salmonella . . .
steadily during the first 5 h of drying and tended to approach a certain value by the end of the drying period; the trend which is similar to that of the drying kinetics. Figure 2b shows the surface temperature of cabbage during hotair drying at 50, 60, and 70 C. The surface temperature of cabbage increased instantly once the sample was exposed to drying air and then increased steadily until reaching the set drying air temperature. tics of the cabbage. Higher grayscale values were obtained when the sample surface shrunk more extensively due to larger loss of moisture during drying. Shrinkage during drying of high moisture foods normally occurs when the viscoelastic matrix contracts into the space previously occupied by the water removed (Aguilera 2005). The changes of surface characteristics of cabbage during drying were described in terms of the roughness factor (R). Figure 6a shows the relationship between R and drying time. It is seen that R increased steadily during an early period of drying and reached a certain value by the end of drying. It was observed that the R-value of approximately 1.45 was obtained for every drying condition when the samples reached their equilibrium moisture contents. The R-values are also plotted against the moisture content (Figure 6b). An almost exponential decay relationship between R and moisture content was noted. In fact, a similar type of relationship has been found between the change of volumetric shrinkage of materials during drying and moisture content (Hernandez and others 2000; Hatamipour and Mowla 2002; Khraisheh and others 2004). These results suggested that the roughness factor could adequately describe the shrinkage characteristics of the vegetable surface during drying.

Characteristics of cabbage surface

The surface changes of cabbage during drying as captured by the scanning electron microscope are shown in Figure 3. It was observed that the surface of fresh cabbage exhibited a clear cell periphery. After drying, the wrinkles on the surface of cabbage were more pronounced and this resulted in a significant change in the surface characteristics. A larger area of light gray or white was clearly observed when the sample shrunk upon drying. Considering the results at the same drying time, it was noted that the surface of the samples undergoing drying at higher temperatures exhibited more wrinkles than those undergoing drying at lower temperatures (Figure 4). The results implied that drying temperature had a significant effect on the shrinkage and the surface Heat resistance of Salmonella Anatum characteristics of the leaf. Figure 5 shows the details of scanning electron microscopic on cabbage surface Figure 7 shows the SEM images of S. Anatum attached on the (SEM) images (from Figure 3) in terms of the grayscale values. These intensity maps, plotted between the gray level and pixel location, cabbage surface. The distribution of Salmonella cells on the cabcould be used to represent very well the overall surface characteris- bage surface appeared to be randomized. Salmonella cells appeared to congregate around stomata and on epidermal cells of cabbage; smooth surface area contained lower number of Salmonella. The similar attachment characteristics of bacteria on A 1.8 vegetable surface were reported by Hassan and Frank (2004) and Ells and Hansen (2006). 1.6 During drying the shrunk surface trapped Salmonella to the epi1.4 dermal cell, so the dense accumulation of bacterial cells was clearly 1.2 seen. The stomata were also destroyed leaving small holes on the 1 leave surface. Longer drying time also caused an increase in shrinkage and the destruction of cabbage surface. 0.8 The survival curves of S. Anatum at the drying temperatures of 0.6 50, 60, and 70 C are shown in Figure 8. An exponential decay of the 0.4 survival Salmonella number was observed. The results showed that Salmonella were destroyed rapidly during the first 4 h of drying but 0.2 were destroyed to a lesser extent during the prolonged drying time. 0 The bacterium was destroyed much more rapidly at 60 and 70 o C. 0 5 10 15 20 25 Weibull equation was used to describe the nonlinear survival Drying time (h) curves and the heat resistance data; the parameters of the equation are shown in Table 1. From the calculation, n values were less B 1.6 than unity indicating that the curves are concave upward. It could 1.4 thus be interpreted that the bacterial population was heteroge1.2 neous with regard to heat resistance (Moats and others 1971). Weak or sensitive members of the population were destroyed at a faster 1 rate leaving behind the cells of higher heat resistance (Peleg 2000). 0.8 Higher drying temperature resulted in the higher destruction rate of bacterial cells. The results were also compared in terms of the 0.6 time required to destroy 3 log 10 of Salmonella. Approximately 20 h 0.4 was required to reduce the Salmonella by 3 log 10 at 50 C while only 4 and 2 h were needed to obtain a similar destruction level at 60 and 0.2 70 C, respectively. 0 The relationships between log S and moisture content as well as 0 5 10 15 20 water activity and roughness factor are shown in Figure 9. The deMoisture content (kg/kg dry basis) struction of Salmonella was from both heat treatment and the loss Figure 6 --- Relationship between (A) roughness factor (R ) of free water, which is important for the survival of the cells. Although it was noted that the roughness increased with the and drying time and (B) roughness factor and moisture content during drying at 50 ( r), 60 ( ), and 70 C ( ). drying time and that the samples dried at higher temperatures
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Roughness factor

Roughness factor

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Survival of Salmonella . . .
possessed more rough surfaces than those dried at lower temperatures, no direct relationship between these 2 parameters was observed in this study. Drying temperature was found to be a major factor influencing the heat resistance of Salmonella on cabbage surface. It is possible that the cabbage leaves were very thin and the bacterial cells on the vegetable surface received the heat directly from hot air. The microbial destruction rate occurred rapidly once the vegetable samples were exposed to the drying air. Therefore, the majority of Salmonella cells were destroyed even before shrinkage of the leaves took place. Although the roughness increased with the drying time, the temperature of vegetable surface also increased and favored the bacterial elimination. Therefore, the effect of roughness was not clearly seen in the present study. cabbage surface. Drying temperature was found to be a major factor influencing the heat resistance of Salmonella during drying. Nevertheless, it was found that the R-value could be used to represent the change of vegetable surface characteristics during drying

0 0 -1 5 10 15 20 25

-2

log S
-3

his study investigated the changes in cabbage leaf surface -4 during drying using an image analysis technique. Using the technique developed in this study, the specific surface characteristics were described in terms of the roughness factor (R). The -5 water activity of the vegetable decreased while R-value increased Drying time (h) with longer drying time and higher drying temperature. However, the changes of both parameters during drying did not show a Figure 8 --- Survival curves of Salmonella Anatum at 50 significant effect on the strength of Salmonella attachment to the ( r), 60 ( ), and 70 C ( ).

Figure 7 --- SEM images (5000) of S . Anatum attachment on (A, B) fresh cabbage; (C, D) cabbage dried at 50 C for 4 h and (E, F) cabbage dried at 50 C 8 h. (A, C, and E show S . Anatum attachment on epidermal cell and B, D, and F show S . Anatum attachment on the stomata.)

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Conclusions

Survival of Salmonella . . .
very well. This technique may also be useful in monitoring the surface changes of other food materials during processing. More research should be done on the study of the changes of surface characteristics of different natural surfaces of fruits and vegetables
Table 1 --- Heat resistance parameters of S. Anatum at drying temperatures of 50, 60, and 70 C. Temperature ( C) 50 60 70
a

to investigate the pattern of surface changes or shrinkage during processing. The data obtained would be useful in predicting the appearance of final products, which can be related to the quality acceptance.

Acknowledgments
The authors express their sincere appreciation to the Thailand Research Fund (TRF) for supporting this study financially.

ba

na

Time to obtain 3-log 10 reduction in cell number (min)a 1186.27 1.26 265.83 0.66 133.88 0.93

R2

References

0.80 0.07 0.43 0.03 0.68 0.04 0.91 0.03 1.61 0.06 0.96 0.08

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The means of 3 replications with standard deviations.

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Figure 9 --- Relationship between log S and (A) moisture content, (B) water activity, and (C) roughness factor during drying at 50 ( r), 60 ( ), and 70 C ( ).

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