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Food Texture Differences affect Energy Metabolism in Rats

¹ Department of Pediatric Dentistry, Kyushu University Faculty of Dental Science, 3-1-1 Maidashi, Higashi-ku, Fukuoka, 812-8582, Japan;
² Section of Pediatric Dentistry, Division of Oral Health, Growth & Development, Faculty of Dental Science, Kyushu University;
³ Department of Internal Medicine I, School of Medicine, Oita Medical University, Japan; and
⁴ Department of Nutrition Sciences, Graduate School of Health and Nutrition Science, Nakamura Gakuen University, Japan;

*corresponding author, okak{at}dent.kyushu-u.ac.jp

	ABSTRACT

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Dietary factors such as taste and nutrients are known to affect satiety and energy balance. We hypothesized that food texture might contribute to the regulation of energy metabolism through the process of mastication in the oral cavity as well. The effects of long-term feeding of different-textured pellets on body weight gain, adiposity, and thermogenesis were assessed. From weaning at 4 wks, rats were divided into 2 groups fed on either standard (controls) or soft pellets (soft-fed) that required less chewing with the same nutritional composition. At 26 wks, the soft-fed rats showed greater adiposity than did the controls. Daily food intake did not differ between the 2 groups. The increase in body temperature following feeding was significantly lower in the soft-fed rats. These results suggested that food texture affected energy metabolism by changing post-prandial thermogenesis. The long-term deficiency of thermogenesis associated with soft foods resulted in a greater tendency toward obesity.

KEY WORDS: mastication • soft diets • body fat • metabolism • and post-prandial thermogenesis

	INTRODUCTION

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The oral cavity is not only the site of the first stage in digestion but also the brain’s source of much sensory information about food, such as taste, smell, and texture. It is known that changing this sensory information alters the process of digestion and the sense of satiation (Fujise et al., 1993).

During feeding, several physical responses are activated, including non-shivering heat production, called post-prandial thermogenesis. Post-prandial thermogenesis is reduced in both humans and dogs when oral sensations are eliminated by gastric-tube feeding (Diamond et al., 1985; LeBlanc and Brondel, 1985). Long-term tube feeding causes a large increase in body weight and percentage of body fat in both rats and humans (LeBlanc and Brondel, 1985; LeBlanc and Diamond, 1986; Yamashita et al., 1993). These results suggest that taste may regulate not only satiety but also energy metabolism by producing thermogenesis during feeding. However, taste is not the only oral sensation; there is also proprioception from masseter muscle spindles and exteroception from the periodontal ligaments during mastication. The present study aimed to determine whether the amount of masticatory effort plays a role in regulating metabolic energy by comparing body weight gain, adiposity, and thermogenic response during feeding in growing rats fed either a hard or a soft diet.

	MATERIALS & METHODS

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General Procedure
    Animals
Mature male Wistar King A rats were used after being weaned at 4 wks. They were housed in a soundproof room under controlled environmental conditions (21 ± 1°C, 55 ± 5% humidity) and with a 12:12-hour light-dark cycle (light on at 0800 hrs). All studies were conducted in accordance with the Kyushu University Guidelines based on the NIH Guide for the Care and Use of Laboratory Animals.

    Foods
The rats were allowed free access to either standard control pellets or soft pellets. Both kinds of pellets (Oriental #MF Tokyo, Japan) had the same nutritional components, were of the same size and shape, and had the same water content. We gave the soft pellets a lower density (3.5 g for hard pellets, 2.5 g for soft pellets) by increasing their air content. The average yield forces of control and soft pellets were calibrated at the factory to 85.5 N and 41.8 N, respectively.

Experimental Procedure
    Measurement of Body Weight, Food Intake, and Body Composition
Twenty rats were divided into 2 weight-matched groups (n = 10) at weaning (4 wks) and were fed either the control or the soft diet until they reached 26 wks of age. The rats were allowed free access to the pellets and tap water. Body weight was measured weekly, and 24-hour food intake was measured every 2 wks, starting when the rats were 8 wks old. One week before the end of the experimental period, each rat was housed individually in a cage. Body weight and 24-hour food intake were measured daily for each rat throughout the following 7 days. All rats were killed, and trunk blood was collected for glucose, insulin, free fatty acid (FFA), triglyceride (TG), and leptin determinations; the white adipose tissue (WAT) deposits (abdominal white adipose tissue: perirenal, epididymal, and mesenteric) were dissected and weighed.

    Measurement of Daily Core Body Temperature
Matched by body weight, another 10 rats were divided equally into 2 groups after being weaned at 4 wks and fed either the control or the soft diet ad libitum. The body weight was significantly different between the 2 groups after 17 wks. At 22 wks, after the soft-fed rats had attained a statistically greater body weight, each rat received an intraperitoneally placed biotelemetry transmitter under intraperitoneal pentobarbital sodium anesthesia. After a recovery period of 1 wk, each rat’s body temperature and locomotor activity were recorded at a rate of 1 sample per min for 3 days, while free access to food and water was allowed in the cages.

Measurement of Post-prandial Thermogenesis
At the end of body-temperature measurement for 3 days, the rats were made to fast for 24 hrs. At 10:00 hrs the next morning, the rats were given their usual soft or control diet, and their body temperatures were recorded at one-minute intervals. All rats started to eat immediately when food was presented. During the first hour after they began eating, we measured feeding duration, food volume, and locomotor activity.

Serum Metabolites
Serum samples from experiment 1 were stored at -20°C until the time of measurement. Serum leptin, glucose, insulin, FFA, and TG levels were measured with the use of commercially available kits (Glucose, Merckauto Glucose, Kanto Chemical Co., Tokyo, Japan; Insulin, Rat insulin [¹²⁵I] assay system, Amersham, Buckinghamshire, England; FFA, NEFA-SS ’Eiken’, Eiken Chemical Co., Ltd., Tokyo, Japan: TG, L Type Wako Triglyceride, Wako Pure Chemical Ltd., Osaka, Japan; Leptin, Leptin Rat ELISA system, Amersham, Buckinghamshire, England.)

Measurements of Core Body Temperature and Locomotor Activity
Core temperature was measured with a biotelemetry transmitter implanted into the peritoneal cavity. A battery-operated biotelemetry device designed to measure body temperature and locomotor activity (Model TA11CTA-F40, Data Sciences International, St. Paul, MN, USA) was implanted into the peritoneal cavity of each rat (Ruf and Heldmaier, 1987). Output was monitored by a mounted antenna placed under each animal’s cage (Model RPC-1, Data Sciences International). The monitor was connected to a computer (Series 3510V5, Compaq Computer Corp., Houston, TX, USA; IBM-compatible). A Dataquest 4 data acquisition system (Data Sciences International) was used for automatic control of data collection and analysis. Body temperature and locomotor activity were monitored and recorded at one-minute intervals.

Statistical Analysis
All data were expressed as means ± SEM (standard error of the mean), and ANOVA for repeated measures was used initially for comparison of inter-group differences in body weights and body temperature. When significant inter-group differences were found, post hoc Bonferroni corrections were carried out at each time point. Differences in WAT weight and serum contents were tested for significance by the Mann-Whitney-U test (p < 0.05).

	RESULTS

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Changes in body weight as the rats grew from 4 to 26 wks are shown in Fig. 1A. Initially, growth was rapid until 9 wks, then the gain in body mass slowed. Initially, body weight of the soft-fed rats did not differ from that of controls. However, after 22 wks, body weight in the soft-fed group was significantly greater. The 24-hour food intake at each week did not differ between the groups (Fig. 1B).

View larger version (14K): [in this window] [in a new window]   Figure 1. The effect of long-term feeding of control or soft pellets on (A) body weight and (B) 24-hour food intake. (A) Body weight of control- and soft-fed rats after being weaned at 4 wks, measured weekly. Initially, growth was rapid until 9 wks, after which the gain in body mass slowed. After 22 wks, body weight in the soft-fed group was significantly greater. (B) 24-hour food intake of control- and soft-fed rats was measured biweekly from 8 wks of age. The volume of food intake at each week was not different between the groups. The results are means ± SEM. n = 10 for both groups. *Significantly different from control group means at equivalent week (p < 0.05).

View larger version (20K): [in this window] [in a new window]   Figure 2. The changes of core body temperature at every hour. The temperatures shown are averages for 3 experimental days. There was no significant difference in body temperature during the light period between the groups. However, during the dark period, body temperature in the soft-fed rats was significantly lower compared with that in controls at 22:00, 23:00, 02:00, 03:00, and 05:00 hrs. The results are means ± SEM. n = 5 for both groups. *Significantly different from control group means at the equivalent hour (p < 0.05).

View larger version (21K): [in this window] [in a new window]   Figure 3. Changes in body temperature of rats in response to feeding of soft or control pellets. (A) Body temperature immediately increased in both groups after the start of a meal. (B) Differences in body temperature from the basal level at the start of the meal expressed as a percentage above the basal level at 10:00 hrs. Body temperature in the soft-fed rats was significantly lower compared with controls at 47, 48, 49, 55, and 57 min after the start of the meal. The results are means ± SEM. n = 5 for both groups.

	DISCUSSION

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Fat deposition results from an imbalance between energy intake and energy expenditure. Food intake at each age was not significantly different between the groups, suggesting that the total energy intake was the same in both groups. We suspect that the body-weight gain of soft-fed rats results from decreasing energy expenditures that might be reflected in a difference of body temperature or locomotor activity between the groups.

Although the 2 groups’ changes in body temperature during the light period did not differ, the body temperature of the soft-fed rats during the dark period was significantly lower than that of the controls. While behavioral factors such as feeding, drinking, and locomotor activity might be related to less thermogenesis in the dark period, we found that both groups had the same amounts of food and water intake and the same amounts of locomotor activity. Therefore, these behavioral factors cannot explain the lower thermogenic response of the soft-fed rats during the dark period. Instead, the observed differences in body temperature appear to be a response to the actual act of feeding. Body temperature immediately increased in both groups after the start of a meal, but this elevation was attenuated in the soft-fed rats.

Several reports have suggested that taste and smell were the factors controlling post-prandial thermogenesis at the initiation of feeding, and this early thermogenesis has been shown to be independent of the meal size and amount of calorie intake (LeBlanc and Brondel, 1985; LeBlanc and Diamond, 1986; Saito et al., 1989). This was also the case here; the different amounts of post-prandial thermogenesis between the groups occurred within an hour after feeding started, although the food intake and locomotor activity of both groups were similar. Our results suggest that food texture is also an important factor regulating thermogenesis at feeding.

Exactly how the different food textures affected peripheral thermogenesis remains unclear. Food texture does modulate hypothalamic neurotransmitter activities (Fujise et al., 1993; Yang et al., 1997). Proprioceptive and exteroceptive signals from the oral cavity are conveyed to the mesencephalic trigeminal nucleus (Me5) through the trigeminal sensory nerves. We previously reported that turnover of neuronal histamine in the Me5 is elevated during the early phase of feeding and is elevated in the hypothalamus at the later phase. This elevated turnover is abolished by gastric intubation for an isocaloric liquid diet or by an equal volume of water (Fujise et al., 1998). Energy metabolism, including thermogenesis, is regulated through sympathetic activity in the hypothalamus (Perkins et al., 1981; Rothwell and Stock, 1979). The histamine system in the hypothalamus controls body temperatures (Sakata et al., 1997; Yoshimatsu et al., 1999; Masaki et al., 2001); therefore, it is possible that the low masticatory effort with soft foods might reduce post-prandial thermogenesis by down-regulating hypothalamic histaminergic neurons.

In the present study, the thermogenesis of soft-fed rats was lower than that of control-fed rats in the dark period, probably resulting in reduced energy expenditure in the soft-fed rats. For fat deposition to be induced, any imbalance between energy intake and expenditure must last a long time. In this study, 22 wks was long enough to produce obesity in soft-fed rats.

In summary, we demonstrated that long-term feeding of soft pellets induced an increase in body weight and fat deposition, due to lowered post-prandial thermogenesis. Food texture might be as important a factor for preventing obesity as taste or food nutrients.

	ACKNOWLEDGMENTS

 
This work was supported by Grants-in-Aid for Scientific Research (Nos. 13470543 and 13771264) from the Japan Society for the Promotion of Science. We thank Dr. Kenjiro Okamoto and Shuji Hidaka, Department of Internal Medicine I, School of Medicine, Oita Medical University, for their technical assistance.

Received May 17, 2002; Last revision February 20, 2003; Accepted February 28, 2003

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