Electromyography of Eating Apples: Influences of Cooking, Cutting, and Peeling

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1 JFS S: Sensory and Nutritive Qualities of Food Electraphy of Eating Apples: Influences of Cooking, Cutting, and Peeling KAOR ORU KOHY OHYAMA AMA, YUK UKO NAKA AKAYAMA AMA,, HIR IROTAKA WATANABE ANABE, AND TOMOK OMOKO SASAKI ABSTRACT CT: The mastication of 7 differently ently prepar epared ed apple samples (raw pieces peeled and unpeeled, sliced, grated, cooked pieces with and without peel, and half-cooked pieces,, 10 g each) was evaluated using elec- tromy ography (EMG). Elev leven en subjects participated in the EMG recor ecording of both sides of the masseter and temporal muscles while eating samples normally mally.. Only the grated sample reduced the number of chewing strokes and muscle activity before e swallowing. wing. In contrast, the thin apple slices produced significantly shorter contraction duration and cycle cle time only during the 1st 5 chewing strokes okes. The EMG duration and cycle cle in subsequent chews,, as well as the other parameters ameters,, did not significantly differ between een slices and pieces. Cooked apples exhibited significantly lower EMG amplitude and muscle activity per chew than their raw counterparts; ts; howev ever er,, there e was no evidence of reduced total muscle activity requir equired ed for swallowing. wing. Raw and cooked apples with peel yielded significantly greater EMG amplitude and longer duration than those without peel. These findings suggest that appropr opriate prepar eparation ation is necessary for people with var arious masti- cation abilities: grated for ver ery low ability,, cooked for those with weak chewing force ce,, and unpeeled for mas- tication training. Keywor eywords: apples,, cooking, sample size,, mastication, electromy ography MS Submitted 8/12/04, Revised 10/29/04, Accepted 12/30/04. Author Kohyama, Nakayama, and Sasaki are with Natl. Food Research Inst., Kannondai, Tsukuba , Japan. Author Watanabe is with Aomori Prefectural Local Food Research Center, Agricultural Products Processing Center, Aomori, Japan. Direct inquiries to author Kohyama ( kaoruk@nfri.affrc.go.jp) Institute of Food Technologists Further reproduction without permission is prohibited Introduction Apples are a common fruit that is often eaten with the skin intact, although people sometimes peel the skin and cut the flesh into appropriate sizes for eating. Apples are often served to persons with weak mastication, such as patients, infants, and the elderly, because apples are rich in dietary fiber and vitamins (Holdsworth 1979; Marlett 1992; Gheyas and others 1997). The dietary fiber produces the texture of the apple flesh through interactions of the pectin with hemicellulose, cellulose, pentosans, and hexosans (Holdsworth 1979). People with low mastication ability find eating apples difficult because a raw apple is somewhat hard (Peleg 1993; Millwood and Heath 2000; Sheiham and Steele 2001; Allen and McMillan 2002). The objective of this study was to present better apple preparation methods for people with different mastication abilities. Food preparation methods used to aid eating generally include cutting and mashing to make big pieces smaller, skinning or peeling to remove the harder parts, and stewing or cooking for long periods to soften the food (Millwood and Heath 2000). These apple preparation methods were applied in this study. The apple skin protects the fleshy tissue from mechanical stimuli, and the skin resists force during chewing. The major effect of heating apple flesh is a breakdown of the structural integrity, resulting in a mushy texture (Holdsworth 1979). We previously measured the bite force of raw and cooked apple specimens during the 1st bite with human incisors and also performed wedge penetration tests to compare them with the human bite measurements (Dan and others 2003a). The effort required for 1 bite could not be determined from the instrumental tests. Therefore, we adopted a mastication recording due to the existence of parameters only measurable by human tests and the difficulty in evaluating the effects of size or peeling using mechanical tests. Mastication following the 1st bite was difficult to measure by the sheet sensor used in our previous studies because the food samples broke and were displaced from the sensor during the 1st bite (Kohyama and others 2001a, 2001b; Dan and others 2003a, 2003b). Moreover, this study involved grated apple samples with fluid that could not be put on the sheet sensor. We thus used electraphy (EMG) to evaluate mastication of the 7 different apple samples. This technique can be used for many subjects because the EMG electrodes are noninvasively attached on the skin surface of humans subjects and do not restrict normal chewing movement, as reviewed by González and others (2001). Masticatory EMG activity is known to correlate with bite force (Pruim and others 1978; van Eijden and others 1990; Blanksma and others 1992; Lindauer and others 1993; Gay and others 1994; Pröschel and Raum 2001; Proeschel and Morneburg 2002). Materials and Methods Sample prepar eparation ation The apples (Malus domestica Borkh. cv Tsugaru) used in this study were harvested in September 2002 in the South Tsugaru region of Aomori Prefecture, Japan. Fruits with diameters between 75 and 85 mm were selected. Apples were cooked as previously described (Dan and others 2003a). Hand-cored apples were sliced axially into 8 pieces per fruit and vacuum-packed in a plastic bag. The peel was removed from some of the pieces. The bags were sealed using a vacuum packaging machine and were then cooked in a water bath at 90 C for 50 min (cooked) or 25 min (half-cooked), followed by cooling in cold water (15 C, 60 min). All samples used in EMG recordings and mechanical tests were processed at the same time. Both raw and processed apples were stored in a refrigerator at 4 C and kept at room tem- Vol. 70, Nr. 4, 2005 JOURNAL OF FOOD SCIENCE S257 Published on Web 4/15/2005

2 perature (23 C) for 60 min before the tests. All tests were carried out within 10 d. Bite-size pieces of apples (10 g each) were prepared to be ingested and swallowed at 1 time through a preliminary test. As apple fruit is anisotropic (Khan and Vincent 1993; Abbott and Lu 1996), the raw, half-cooked, cooked, raw with peel, and cooked with peel specimens were taken from near the middle part of the 1/8 pieces. About 1-mm-thick sliced samples were hand-sliced from a raw, peeled specimen. The grated samples were prepared from the sliced pieces using a food processor to test the effects of size reduction. Chewing was still required for sliced samples, but only rarely required for the grated apples. was statistically tested with a 1-way analysis of variance (ANOVA) for the mechanical tests and with a repeated-measure ANOVA for the EMG data. A paired t-test was applied to test the cooking effect (raw, half-cooked, and cooked), size effect (grated, sliced, and cubed), and peeling effect (with and without peel for raw and cooked samples) as a post-hoc analysis of the EMG variables. Holm s correction was used to reduce the type I error rate when 3 samples were compared (Holm 1979). Mechanical test Compression tests were performed on peeled samples of the raw, half-cooked, and cooked specimens and the grated samples. Solid samples for mechanical tests were cut into cubes ( mm). Samples with an initial cross-sectional area of 225 mm 2 and a height of 10 mm were compressed in the axial direction of the fruit between 2 flat probes attached to an Instron universal testing machine (Instron 5564, Canton, Mass., U.S.A.) as adopted by Abbott and Lu (1996). The crosshead speed was 5 mm/s (Dan and others 2003a) and final sample deformation was set at 90% of its original height. The grated sample was placed in a petri dish (40-mm inner dia 15-mm height) and compressed with a cylindrical probe (20- mm dia) in the same way. Five measurements were carried out for each sample. Electr lectromy ography measurement ement Eleven subjects (mean age, 28.7 y) voluntarily participated in the study. To reduce individual differences in mouth size and chewing variables, subjects were chosen based on the following criteria: (1) females, (2) aged 20 to 40 y, (3) height of 152 to 167 cm, (4) body mass index of 18.5 to 23.0, (5) no missing teeth except the 3rd molars, and (6) no disorders requiring dental treatment. Informed consent was acquired before the recording session. EMG activities were recorded from both the left and right masseter and anterior belly of the temporal muscles using bipolar surface electrodes (Kohyama and others 2000, 2003b). EMG signals were amplified by 1000 using an MEG-6108 (Nihon Kohden, Tokyo, Japan), with 4 AB- 610J units after eliminating electrical noise at 50 Hz. The data were digitized at 1000 Hz and stored in a personal computer for further analysis using an MP100 system and AcqKowledge ver software (Biopak Systems Inc., Goleta, Calif., U.S.A.). Apple samples (7 kinds with duplicates) were provided in random order and eaten normally. The recording session lasted for 40 min. Parameters were obtained from the EMG data illustrated in Figure 1 and previously described (Kohyama and others 2000). The number of chewing strokes and masticatory time were read directly from the chart. The amplitude, muscle activity or time-integrated EMG signal, duration, and cycle time in each chewing stroke (Figure 2) were obtained for 4 muscles and were averaged because the signals from 4 jaw-closing muscles appeared almost at the same time (Figure 1). Those parameters were then averaged for all the chewing cycles. The mean values of the 1st 5 chewing cycles, from the 6th to 10th, the middle 5 cycles, and the last 5 cycles just before swallowing, were also calculated for those parameters to test the slicing and peeling effects. The sum of the muscle activity and the sum of the duration before swallowing were also analyzed. Statistical treatment An SPSS package ver. 11.0J (for Windows) (SPSS, Chicago, Ill., U.S.A.) was used for the statistical analysis. The effect of the sample Figure 1 Example of electraphy (EMG) chart while eating apple. A subject ate 10 g of raw apple cube without peel. From the upper line, EMG signals of right and left masseter, right and left temporal muscles. Figure 2 Schematic drawing of electraphy (EMG) data S258 JOURNAL OF FOOD SCIENCE Vol. 70, Nr. 4, 2005 URLs and addresses are active links at

3 Table 1 Mechanical characteristics of apple samples a Parameter F-ratio Grated Raw Half-cooked Cooked Rupture stress (kpa) 7.9 ** Not determined 266 ± 10 b 258 ± 11 b 219 ± 28 a Rupture strain 31.2 *** Not determined 0.36 ± 0.03 a 0.52 ± 0.04 c 0.46 ± 0.03 b Stress at 0.05 strain (kpa) 61.9 *** 0.6 ± 0.2 a 12.8 ± 3.4 b 1.2 ± 0.3 a 0.9 ± 0.3 a Stress at 0.3 strain (kpa) *** 5.0 ± 0.5 a ± 17.2 d 64.7 ± 22.2 b 98.0 ± 17.2 c Stress at 0.6 strain (kpa) 28.1 *** 7.3 ± 0.5 a ± 27.0 bc ± 63.7 c ± 22.5 b Stress at 0.9 strain (kpa) 32.4 *** 17.7 ± 11.3 a ± 20.9 b ± b ± 15.6 b a Peeled cubes ( mm) for raw, half-cooked, and cooked samples. F-ratios and statistical probabilities in ANOVA. ** = P < 0.01; *** = P < Mean and standard deviation values for 5 replicates. Values followed by different alphabetical letters within a row differed significantly (P < 0.05). Results and Discussion Mechanical testing Figure 3 displays typical compression curves for grated, cooked, half-cooked, and raw apples without peel. The stress-strain relationship for raw apples was generally linear up to the critical stress, at which time the sample broke and the stress decreased and then increased again, as reported previously (Abbott and Lu 1996). Cooked apples revealed similar stress-strain curves; however, they exhibited a less steep slope until rupture and lower rupture stress at a higher strain than the raw samples, as previously observed in wedge-penetration tests (Dan and others 2003a). Half-cooked apple samples exhibited greater rupture strain than cooked samples, with the rupture stress between that of the raw and the cooked samples. Grated samples showed extremely low stress values over the entire range of strain, and no clear rupture point was observed. The statistical data for the 4 samples is provided in Table 1. Mastication analysis The failure stress of apple flesh was greater during vertical compression than that in a radial or tangential direction, as reported by Abbott and Lu (1996). Our specimen had the smallest dimension in the vertical direction (10 mm), and the subjects bit the specimens vertically because it was difficult to bite thicker specimens between their molars (Kohyama and others 2004). The mechanical test was suitable for describing the 1st bite. However, it was difficult to clarify the differences between peeled and unpeeled samples, or cubed and sliced samples, which evidently differed in textural assessments during eating. It was not necessary to consider anisotropy after the 2nd and subsequent chewing strokes because the flesh orientation Figure 3 Stress-strain curves for 4 apple samples. Samples were compressed at 23 C and a constant rate (5 mm/s) by an Instron universal testing machine. URLs and addresses are active links at was irregularly scattered after fracture during the 1st bite. Therefore, we measured EMGs for 7 different apple samples. The chewing response to different textures varies from person to person (Wilkinson and others 2000; Kemsley and others 2003), although the intra-individual reproducibility is considerable. The EMG data obtained in this study were characteristic for each individual, although a general tendency was observed associated with the sample as well as the bite force (Dan and others 2003a). The average values for 11 subjects are displayed in Table 2. We found significant sample differences in the number of chewing strokes, mastication time, EMG amplitude, muscle activity, cycle time, sum of the muscle activity, and sum of the duration, whereas there were similar durations per chew. Effect of cooking We 1st focused on the EMG parameters from raw, half-cooked, and cooked samples to discuss the cooking effect. Cooked apples exhibited a significantly lower EMG amplitude and muscle activity per chew than their raw counterparts. The amplitude and muscle activity per chew, expressed as the maximum force during 1 chew, were less for cooked apples than for raw apples, as was the rupture stress. Our previous EMG study involving raw apples for elderly and young subjects revealed that young people were able to produce greater EMG amplitude according to food hardness, whereas elderly people, particularly those with few remaining teeth, had difficulty changing the maximum EMG voltages adapted to food texture (Kohyama and others 2002, 2003a; Kohyama and Mioche 2004). No significant statistical differences were found between half-cooked and cooked apples. This suggests that cooking apples considerably reduces the required chewing force, even if the apples are heated for only a short time. Cooking apples for a short time helps to prevent vitamin loss caused by heat treatment and appears to be a better preparation method for people with low mastication ability. Overcooked vegetables have been suggested for elderly people (Millwood and Heath 2000); however, smaller rupture stress does not always indicate that a significantly less mastication effort is required. The area under the mechanical compression curve was significantly decreased with cooking time, as indicated in Figure 3. Our previous study of bite force between incisors also revealed that the maximum bite force significantly decreased after cooking (Dan and others 2003a). The muscle activity per chew was also less for cooked samples, as noted in the mechanical test and bite force results. The cooked samples exhibited more resistance against compression than raw apples, and thus the effort required for 1 bite of a cooked apple was not significantly reduced compared with that for raw apples (Dan and others 2003a). The area under the stress-strain curve represents the effort required for sample compression. Figure 3 indicates that raw apples required greater rupture work than cooked or half-cooked samples. The number of chewing strokes, mastication time, EMG dura- Vol. 70, Nr. 4, 2005 JOURNAL OF FOOD SCIENCE S259

4 Table 2 Electraphy (EMG) parameters while eating apple samples a Cooked EMG Raw without Raw with Half- without Cooked parameter F-ratio Grated Sliced peel peel cooked peel with peel Number of 30.6*** 8.1 ± ± ± ± ± ± ± 9.1 chewing strokes Mastication 26.2*** 6.0 ± ± ± ± ± ± ± 4.9 time (s) Amplitude (mv) 6.3** ± ± ± ± ± ± ± Burst 2.0 NS ± ± ± ± ± ± ± duration (s) Muscle 11.7*** ± ± ± ± ± ± ± activity (mv.s) Cycle time (s) 11.0** ± ± ± ± ± ± ± Total burst 32.2*** 2.24 ± ± ± ± ± ± ± 1.88 duration (s) Total muscle 14.0** ± ± ± ± ± ± ± activity (mv.s) a F-ratios and statistical probabilities in the repeated-measure ANOVA. NS = not significant (P > 0.05); ** = significantly different at P < 0.01; *** = P < Mean and standard deviations for the 11 subjects. tion, and cycle time, and therefore the total muscle activity and total EMG duration, did not significantly differ between the 3 preparation methods with different heating times. These elements are related to the mastication rhythm and time. Cooking vegetables and fruit causes an initial loss of firmness due to membrane disruption and the associated loss of turgor. Cells are more able to deform before they fail when they lose turgor pressure, resulting in a tender and rubbery texture (Thiel and Donald 2000; Lillford 2001). Apples contain cellulose and pectin as dietary fibers (Marlett 1992). The cellulose does not change through heat treatment, although the pectin component becomes soluble with heating (Holdsworth 1979). The cellulose component that remains in cooked apples most likely keeps the mastication requirement the same as that for raw apples. Effect of piece size Reducing the size of the apple flesh by cutting it into small pieces may influence the mastication for raw apples. Bite-size cubes, sliced, and grated raw apples were compared for this investigation. As indicated in Table 2, the grated sample differed significantly in all parameters tested. The grated apple reduced the number of chewing strokes and mastication time by 1/3, shortened the EMG duration, decreased the amplitude and muscle activity, and increased the cycle time. EMG bursts almost disappeared for 1 subject. Therefore, the total muscle activity and total EMG duration were minimal. In contrast, a thin-sliced apple had no effect on any EMG parameter, if we took the average values over the whole masticatory process. These findings suggest that we must cut food into very small pieces that can be swallowed without chewing to change the mastication effort by cutting food into pieces. Our previous EMG study on bite-sized and sliced cucumbers revealed that a pile of thinly sliced samples required more mastication than a bite-sized one of the same weight, as indicated by a greater number of chewing strokes, longer mastication time, and higher EMG amplitude per chew (Kohyama and others 2003b). Significant differences in EMG amplitude (sliced > bite size) were found only in the early stages of mastication. This is reasonable because the sample size was reduced by chewing, and the initial piece size does not affect the bolus state after the 1st several chews. Thus, cubed and sliced apples at each stage of mastication were compared. Statistical significance was found in the EMG duration (0.341 s for sliced and s for a cube, P < 0.01) and cycle time (0.685 and s, P < 0.05) of the 1st 5 chewing strokes. These differences were not observed from the 6th chews or in later stages. Raw apples and cucumbers are similar in texture, hard, and brittle, as is common in many raw vegetables and fruits. Bourne (2002) discussed the relationship between chewing rate and power output of the jaw work. When the food toughness is low to moderate, the chewing rate remains constant and the power output increases as toughness increases. Beyond the limit of comfortable power output, the power remains approximately constant, and chewing rate slows down as toughness increases. The power output corresponds to the EMG amplitude and chewing rate is equivalent to the EMG duration and cycle time. Apples are slightly harder than cucumbers, and because raw apple is hard to crush within the limit of power output, the subjects reduced their contraction speed for large pieces of raw apples. This was only required in the beginning because the sample size was sufficiently broken down during those initial chews. Cutting the sample into small pieces affected only the 1st several chews; no subsequent effects were evident, at least for fibrous foods such as apples and cucumbers. With and without peel Another problem with eating apples is the presence of skin. Apple peel is a difficult food for elderly people to eat (Millwood and Heath 2000). Therefore, the influence of apple peel in the mastication of raw and cooked samples was tested. A piece of unpeeled, raw apple yielded significantly greater EMG amplitude and muscle activity per chew than a peeled one. Significant differences were found in all stages of mastication (in the 1st, middle, and last 5 chewing strokes, P < 0.05), unlike the cutting effect described previously. The total muscle activity required until swallowing increased 130% when unpeeled apple was served (Table 2), though the weight of the peel is negligible. The number of chewing strokes, EMG duration, and cycle time did not differ significantly. A similar tendency was found in cooked samples, although to a lesser extent. This evidence suggests that mixing a small amount of a tough component with the food considerably affects the total mastication. S260 JOURNAL OF FOOD SCIENCE Vol. 70, Nr. 4, 2005 URLs and addresses are active links at

5 Conclusions The mastication amount for 7 different apple preparations of a constant weight was quantified using an electraphic technique. Cooking or slicing an apple piece did not reduce the total number of chewing cycles required. These results suggest that grated apple is best for impaired people with very low mastication ability, cooked but not overcooked apple is best for those with weak chewing force, and raw apple with peel is best for healthy subjects capable of more mastication. Acknowledgments This work was supported by the Program for Promotion of Basic Research Activities for Innovative Bioscience (PROBRAIN) and by the Integrated Research on Safety and Physiological Function of Food from the Ministry of Agriculture, Forestry and Fisheries of Japan. We thank S. Fukuda and Y. Kojima of NFRI for helpful data analysis. References Abbott JA, Lu R Anisotropic mechanical properties of apples. Trans ASAE 39: Allen F, McMillan A Food selection and perceptions of chewing ability following provision of implant and conventional prostheses complete denture wearers. Clin Oral Impl Res 13: Blanksma NG, Van Eijden TMGJ, Weijs WA Electraphic heterogeneity in the human masseter muscle. J Dent Res 71: Bourne MC Body-texture interactions. In: Bourne MC, editor. Food texture and viscosity: concept and measurement. 2nd ed. San Diego: Academic Press. p Dan H, Watanabe H, Dan I, Kohyama K. 2003a. Effects of textural changes in cooked apples on the human bite and instrumental tests. J Texture Stud 34: Dan H, Watanabe H, Kohyama K. 2003b. Effects of sample thickness on bite force of apples. J Texture Stud 34: Gay T, Rendell J, Majoureau A, Maloney FT Estimating human incisal bite forces from the electram/bite-force function. Arch Oral Biol 39: Gheyas F, Blankenship SM, Young E, McFeeters R Dietary fiber content of thirteen apple cultivars. J Sci Food Agric 75: González R, Montoya I, Cárcel J Review: the use of electraphy on food texture assessment. Food Sci Tech Int 7: Holdsworth SD Fruits. In: Priestley RJ, editor. Effects of heating on foodstuffs. London: Applied Science Publishers. p Holm SA A simple sequentially rejective Bonferroni test procedure. Scand J Stat 6:71 6. Kemsley EK, Defernez M, Sprunt JC, Smith AC Electromographic responses to prescribed mastication. J Electr Kinesiol 13: Khan AA, Vincent JFV Anisotropy in the fracture properties of apple flesh as investigated by crack-opening tests. J Mater Sci 28: Kohyama K, Mioche L Chewing behavior observed at different stage of mastication for six foods studied by electraphy and jaw kinematics in young and elderly subjects. J. Texture Stud 35: Kohyama K, Hatakeyama E, Sasaki T, Azuma T, Karita K Effect of sample thickness on bite force studied with a multiple-point sheet sensor. J Oral Rehab 31: Kohyama K, Kobayashi S, Hatakeyama E, Suzuki T Electraphic study of mastication of kelp snack. J Texture Stud 31: Kohyama K, Mioche L, Bourdiol P. 2003a. Influence of age and dental status on chewing behavior studied by EMG recordings during consumption of various food samples. Gerodontology 20: Kohyama K, Mioche L, Martin JF Chewing patterns of various texture foods studied by electraphy in young and elderly populations. J Texture Stud 33: Kohyama K, Nakayama Y, Fukuda S, Dan H, Sasaki T. 2003b. Thinly sliced cucumber requires more mastication. Nippon Shokuhin Kagakukogaku Kaishi (Japanese) 50: Kohyama K, Sakai T, Azuma T. 2001a. Patterns of the first chew of foods with various textures. Food Sci Technol Res 7: Kohyama K, Sakai T, Azuma T, Mizuguchi T, Kimura I. 2001b. Pressure distribution measurement in biting surimi gels with molars using a multiple-point sheet sensor. Biosci Biotechnol Biochem 65: Lillford PJ Mechanisms of fracture in foods. J Texture Stud 32: Lindauer SJ, Gay T, Rendell J Effect of jaw opening on masticatory muscle EMG-force characteristics. J Dent Res 72:51 5. Marlett JA Content and composition of dietary fiber in 117 frequently consumed foods. J Am Diet Assoc 92: Millwood J, Heath MR Food choice by older people: the use of semi-structured interviews with open and closed questions. Gerodontlogy 17: Peleg M Tailoring texture for the elderly: theoretical aspects and technological opinions. Crit Rev Food Sci Nutr 33: Proeschel PA, Morneburg T Task-dependence of activity/bite force relations and its impact on estimation of chewing force from EMG. J Dent Res 81: Pröschel PA, Raum J Preconditions for estimation of masticatory forces from dynamic EMG and isometric bite force-activity relations of elevator muscles. Int J Prosthodont 14: Prium GJ, Ten Bosch JJ, de Jongh HJ Jaw muscle EMG-activity and static loading of the mandible. J Biomech 11: Sheiham A, Steele J Does the condition of the mouth and teeth affect the ability to eat certain foods, nutrient and dietary intake and nutritional status among older people? Public Health Nutr 4: Thiel BL, Donald AM Microstructural failure mechanisms in cooked and aged carrots. J Texture Stud 31: Van Eijden TMGJ, Brugman P, Weijs WA, Oosting J Coactivation of jaw muscles: recruitment order and level as a function of bite force direction and magnitude. J Biomech 23: Wilkinson C, Dijksterhuis GB, Minekus M From food structure to texture. Trends Food Sci Technol 11: URLs and addresses are active links at Vol. 70, Nr. 4, 2005 JOURNAL OF FOOD SCIENCE S261

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